Abstract
Teleosts and elasmobranchs are the lowest vertebrates that possess adaptive immunity akin to mammalian ones. However, the fish immune system is different from that of mammals, that is, a lack of bone marrow, lymph nodes and germinal center. Their immune system is also characterized by the fact that their surface is covered by live cells with mucus in direct contact with environmental water and the fact that the immune response is greatly affected by temperature.
In this review we will describe the current understanding of the teleost immune system from a comparative viewpoint. We will also discuss the regulation of immune response by internal and external factors, since fish aquaculture is growing enormously worldwide, and understanding of the immune system is important for the development of immunological control of fish diseases.
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References
Abelli L, Baldassini R, Mastrolia L, Scapigliati G (1999) Immunodetection of lymphocyte subpopulations involved in allograft rejection in a teleost, Dicentrarchus labrax (L.). Cell Immunol 191:152–160
Ackerman PA, Forsyth RB, Mazur CF, Iwama GK (2000) Stress hormones and the cellular stress response in salmonids. Fish Physiol Biochem 23:327–336
Ainsworth AJ, Dexiang C, Waterstrat PR, Greenway T (1991) Effect of temperature on the immune system of channel catfish (Ictalurus punctatus)-I. Leucocyte distribution and phagocyte function in the anterior kidney at 10°C. Comp Biochem Physiol 100A:907–912
Alejo A, Tafalla C (2011) Chemokines in teleost fish species. Dev Comp Immunol 35:1215–1222
Altmann SM, Mellon MT, Distel DL, Kim CH (2003) Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J Virol 77:1992–2002
Anastasiou V, Mikrou A, Papanastasiou AD et al (2011) The molecular identification of factor H and factor I molecules in rainbow trout provides insights into complement C3 regulation. Fish Shellfish Immunol 31(3):491–499
Anderson DP (1996) Environmental factors in fish health: immunological aspects. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, San Diego, pp 289–310
Anderson DP, Dixon OW, Bodammer JE, Lizzio EF (1989) Suppression of antibody-producing cells in rainbow trout spleen sections exposed to copper in vitro. J Aquat Anim Health 1:57–61
Ank N, West H, Paludan SR (2006) IFN-λ: novel antiviral cytokines. J Interf Cytokine Res 26:373–379
Ao J, Ding Y, Chen Y et al (2015) Molecular characterization and biological effects of a C-type lectin-like receptor in large yellow croaker (Larimichthys crocea). Int J Mol Sci 16(12):29631–29642
Aoki T, Hikima J, Hwang SD et al (2013) Innate immunity of finfish: primordial conservation and function of viral RNA sensors in teleosts. Fish Shellfish Immunol 35:1689–1702
Arts JA, Tijhaar EJ, Chadzinska M, Savelkoul HF, Verburg-van Kemenade BM (2010) Functional analysis of carp interferon-γ: evolutionary conservation of classical phagocyte activation. Fish Shellfish Immunol 229:793–802
Awad E, Awaad A (2017) Role of medicinal plants on growth performance and immune status in fish. Fish Shellfish Immunol 67:40–54
Bacon K, Baggiolini M, Broxmeyer H, Horuk R, Lindley I, Mantovani A et al (2002) Chemokine/chemokine receptor nomenclature. J Interf Cytokine Res 22:1067–1068
Ball JN, Hawkins EF (1976) Adrenocortical (interrenal) responses to hypophysectomy and adenohypophysial hormones in the teleost Poecilia latipinna. Gen Comp Endocrinol 28:59–70
Balm PHM (1997) Immune-endocrine interactions. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 195–221
Barron MG (1986) Endocrine control of smoltification in anadromous salmonids. J Endocrinol 108:313–319
Barros-Becker F, Romero J, Pulgar A, Feijóo CG (2012) Persistent oxytetracycline exposure induces an inflammatory process that improves regenerative capacity in zebrafish larvae. PLoS One 7. https://doi.org/10.1371/journal.pone.0036827
Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26
Barton BA, Schreck CB, Ewing RD, Hemmingsen AR, Patiño R (1985) Changes in plasma cortisol during stress and smoltification in coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 59:468–471
Bassity E, Clark TG (2012) Functional identification of dendritic cells in the teleost model, rainbow trout (Oncorhynchus mykiss). PLoS One 7(3):e33196
Basu N, Nakano T, Grau EG, Iwama GK (2001) The effects of cortisol on heat shock protein 70 levels in two fish species. Gen Comp Endocrinol 124:97–105
Bayne CJ, Levy S (1991a) Modulation of the oxidative burst in trout myeloid cells by adrenocorticotropic hormone and catecholamines: mechanisms and action. J Leukoc Biol 50:554–560
Bayne CJ, Levy S (1991b) The respiratory burst of rainbow trout, Oncorhynchus mykiss (Walbaum), phagocytes is modulated by sympathetic neurotransmitters and the ‘neuro’ peptide ACTH. J Fish Biol 38:609–619
Bengtén E, Quiniou SM, Stuge TB, Katagiri T, Miller NW, Clem LW et al (2002) The IgH locus of the channel catfish, Ictalurus punctatus, contains multiple constant region gene sequences: different genes encode heavy chains of membrane and secreted IgD. J Immunol 169:2488–2497
Bengtén E, Quiniou S, Hikima J, Waldbieser G, Warr GW, Miller NW, Wilson M (2006) Structure of the catfish IGH locus: analysis of the region including the single functional IGHM gene. Immunogenetics 58:831–844
Bentley PJ (1998) Comparative vertebrate endocrinology, 3rd. edn. Cambridge University Press, Cambridge
Bernier NJ, Flik G, Klaren PHM (2009) Regulation and contribution of the corticotropic, melanotropic and thyrotropic axes to the stress response in fishes. In: Bernier NJ, Van Der Kraak G, Farrell AP, Brauner CJ (eds) Fish neuroendocrinology. Academic Press, San Diego, pp 235–311
Betoulle S, Troutaud D, Khan N, Deschaux R (1995) Résponse anticorps, cortisolémie et prolactinémie chez la truite arc-en-ciel. CR Acad Sci Paris 318:677–681. (in French with English abstract)
Biacchesi S, LeBerre M, Lamoureux A et al (2009) Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J Virol 83:7815–7827
Bird S, Tafalla C (2015) Teleost chemokines and their receptors. Biology (Basel) 4:756–784
Bird S, Zou J, Kono T, Sakai M, Dijkstra JM, Secombes C (2005) Characterisation and expression analysis of interleukin 2 (IL-2) and IL-21 homologues in the Japanese pufferfish, Fugu rubripes, following their discovery by synteny. Immunogenetics 56:909–923
Biswas G, Bilen S, Kono T et al (2016) Inflammatory immune response by lipopolysaccharide-responsive nucleotide binding oligomerization domain (NOD)-like receptors in the Japanese pufferfish (Takifugu rubripes). Dev Comp Immunol 55:21–31
Blázquez M, Bosma PT, Fraser EJ, Van Look KJW, Trudeau VL (1998) Fish as models for the neuroendocrine regulation of reproduction and growth. Comp Biochem Physiol 119C:345–364
Bly JE, Clem LW (1992) Temperature and teleost immune functions. Fish Shellfish Immunol 2:159–171
Bodmer JL, Schneider P, Tschopp J (2002) The molecular architecture of the TNF superfamily. Trends Biochem Sci 27:19–26
Brown DJA, Sadler K (1989) Fish survival in acid waters. In: Morris R, Taylor EW, Brown DJA, Brown JA (eds) Acid toxicity and aquatic animals. Cambridge University Press, Cambridge, pp 31–44
Burreson EM, Frizzell LJ (1986) The seasonal antibody response in juvenile summer flounder (Paralichthys dentatus) to the haemoflagellate (Trypanoplasma bullocki). Vet Immunol Immunopathol 12:395–402
Cai Z, Gao C, Zhang Y, Xing K (2009) Functional characterization of the ELR motif in piscine ELR+CXC-like chemokine. Mar Biotechnol (NY) 11:505–512
Calduch-Giner JA, Sitjà-Bobadilla A, Alvarez-Pellitero P, Prérez-Sánchez J (1997) Growth hormone as an in vitro phagocyte-activating factor in the gilthead sea bream (Sparus aurata). Cell Tissue Res 287:535–540
Callewaert L, Michiels CW (2010) Lysozymes in the animal kingdom. J Biosci 35:127–160
Casanova-Nakayama A, Wenger M, Burki R, Eppler E, Krasnov A, Segner H (2011) Endocrine disrupting compounds: can they target the immune system of fish? Mar Pollut Bull 63:412–416
Castellana B, Iliev DB, Sepulcre MP, MacKenzie S, Goetz FW, Mulero V, Planas JV (2008) Molecular characterization of interleukin-6 in the gilthead seabream (Sparus aurata). Mol Immunol 45:3363–3370
Castillo J, Teles M, Mackenzie S, Tort L (2009) Stress-related hormones modulate cytokine expression in the head kidney of gilthead seabream (Sparus aurata). Fish Shellfish Immunol 27:493–499
Castro R, Abós B, González L et al (2017) Expansion and differentiation of IgM (+) B cells in the rainbow trout peritoneal cavity in response to different antigens. Dev Comp Immunol 70:119–127
Chang CI, Pleguezuelos O, Zhang YA et al (2005) Identification of a novel cathelicidin gene in the rainbow trout, Oncorhynchus mykiss. Infect Immun 73(8):5053–5064
Chen K, Xu W, Wilson M, He B, Miller NW, Bengtén E et al (2009) Immunoglobulin D enhances immune surveillance by activating antimicrobial, proinflammatory and B cell-stimulating programs in basophils. Nat Immunol 10(8):889–898
Chen W, Jia Z, Zhang T, Zhang N, Lin C, Gao F, Wang L, Li X, Jiang Y et al (2010) MHC class I presentation and regulation by IFN in bony fish determined by molecular analysis of the class I locus in grass carp. J Immunol 185:2209–2221
Choi K, Cope WG, Harms CA, Law JM (2013) Rapid decreases in salinity, but not increases, lead to immune dysregulation in Nile tilapia, Oreochromis niloticus (L.). J Fish Dis 36:389–399
Cioffi CC, Middleton DL, Wilson MR, Miller NW, Clem LW, Warr GW (2001) An IgH enhancer that drives transcription through basic helix–loop–helix and Oct transcription factor binding motifs. Functional analysis of the Eμ3’ enhancer of the catfish. J Biol Chem 276:27825–27830
Cole AM, Weis P, Diamond G (1997) Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder. J Biol Chem 272:12008–12013
Collazos ME, Ortega E, Barriga C (1994) Effect of temperature on the immune system of a cyprinid fish (Tinca tinca, L). Blood phagocyte function at low temperature. Fish Shellfish Immunol 4:231–238
Cuesta A, Esteban MA, Meseguer J (2008a) The expression profile of TLR9 mRNA and CpG ODNs immunostimulatory actions in the teleost gilthead seabream points to a major role of lymphocytes. Cell Mol Life Sci 65:2091–2104
Cuesta A, Meseguer J, Esteban MA (2008b) The antimicrobial peptide hepcidin exerts an important role in the innate immunity against bacteria in the bony fish gilthead seabream. Mol Immunol 45:2333–2342
Dalmo RA, Bøgwald J (2008) Beta-glucans as conductors of immune symphonies. Fish Shellfish Immunol 25:384–396
Danilova N, Bussmann J, Jekosch K, Steiner LA (2005) The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z. Nat Immunol 6:295–302
Dautigny A, Prager EM, Pham-Dinh D et al (1991) cDNA and amino acid sequences of rainbow trout (Oncorhynchus mykiss) lysozymes and their implications for the evolution of lysozyme and lactalbumin. J Mol Evol 32:187–198
De Guerra A, Charlemagne J (1997) Genomic organization of the TcR β-chain diversity (Dβ) and joining (Jβ) segments in the rainbow trout: Presence of many repeated sequences. Mol Immunol 34(8–9):653–662
de Oliveira S, Reyes-Aldasoro CC, Candel S et al (2013) Cxcl8 (IL-8) mediates neutrophil recruitment and behavior in the zebrafish inflammatory response. J Immunol 190(8):4349–4359
de Rosa M, Zacarias S, Athanasiadis A (2013) Structural basis for Z-DNA binding and stabilization by the zebrafish Z-DNA dependent protein kinase PKZ. Nucleic Acids Res 41(21):9924–9933
de Souza KB, Jutfelt F, Kling P, Förlin L, Sturve J (2014) Effects of increased CO2 on fish gill and plasma proteome. PLoS One 9:e102901
Deane EE, Kelly SP, Lo CK, Woo NY (1999) Effects of GH, prolactin and cortisol on hepatic heat shock protein 70 expression in a marine teleost Sparus sarba. J Endocrinol 161:413–421
DeVries ME, Kelvin AA, Xu L, Ran L, Robinson J, Kelvin DJ (2006) Defining the origins and evolution of the chemokine/chemokine receptor system. J Immunol 176:401–415
Dexiang C, Ainsworth AJ (1991) Effect of temperature on the immune system of channel catfish (Ictalurus punctatus)-II. Adaptation of anterior kidney phagocytes to 10°C. Comp Biochem Physiol 100A:913–918
Diaz M, Greenberg A, Flajnik M (1998) Somatic hypermutation of the new antigen receptor gene (NAR) in the nurse shark does not generate the repertoire: possible role in antigen-driven reactions in the absence of germinal centers. Proc Natl Acad Sci U S A 95:14343–14348
Díaz-Resendiz KJG, Toledo-Ibarra GA, Girón-Pérez MI (2015) Modulation of immune response by organophosphorus pesticides: fishes as a potential model in immunotoxicology. J Immunol Res 2015:213836. https://doi.org/10.1155/2015/213836
Dickhoff WW, Beckman BR, Larsen DA, Duan C, Moriyama S (1997) The role of growth in endocrine regulation of salmon smoltification. Fish Physiol Biochem 17:231–236
Ding Y, Ai C, Mu Y, Ao J, Chen X (2016) Molecular characterization and evolution analysis of five interleukin-17 receptor genes in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol 58:332–339
Dorshkind K, Horseman ND (2000) The roles of prolactin, growth hormone, insulin-like growth factor-I, and thyroid hormones in lymphocyte development and function: insights from genetic models of hormone and hormone receptor deficiency. Endocr Rev 21(3):292–312
Douglas SE, Gallant JW, Gong Z et al (2001) Cloning and developmental expression of a family of pleurocidin-like antimicrobial peptides from winter flounder, Pleuronectes americanus (Walbaum). Dev Comp Immunol 25(2):137–147
Du L, Qin L, Wang X, Zhang A, Wei H, Zhou H (2014) Characterization of grass carp (Ctenopharyngodon idella) IL-17D: molecular cloning, functional implication and signal transduction. Dev Comp Immunol 42(2):220–228
Du L, Feng S, Yin L, Wang X, Zhang A, Yang K, Zhou H (2015) Identification and functional characterization of grass carp IL-17A/F1: an evaluation of the immunoregulatory role of teleost IL-17A/F1. Dev Comp Immunol 51(1):202–211
Edholm E-S, Stafford JL, Quiniou SM, Waldbieser G, Miller NW, Bengtén E, Wilson M (2007) Channel catfish, Ictalurus punctatus, CD4-like molecules. Dev Comp Immunol 31(2):172–187
Edholm ES, Bengtén E, Stafford JL, Sahoo M, Taylor EB, Miller NW, Wilson M (2010) Identification of two IgD+ B cell populations in channel catfish, Ictalurus punctatus. J Immunol 185:4082–4094
Edholm ES, Bengten E, Wilson M (2011) Insights into the function of IgD. Dev Comp Immunol 35:1309–1316
Eimon PM, Kratz E, Varfolomeev E, Hymowitz SG, Stern H, Zha J et al (2006) Delineation of the cell-extrinsic apoptosis pathway in the zebrafish. Cell Death Differ 13:1619–1630
Ellis AE (2001) Innate host defense mechanisms of fish against viruses and bacteria. Dev Comp Immunol 25:827–839
Elsasser MS, Roberson BS, Hetrick FM (1986) Effects of metals on the chemiluminescent response of rainbow trout (Salmo gairdneri) phagocytes. Vet Immunol Immunopathol 12:243–250
Endo Y, Takahashi M, Nakao M et al (1998) Two lineages of mannose-binding lectin-associated serin protease (MASP) in vertebrates. J Immunol 161:4924–4930
Engelsma MY, Huising MO, van Muiswinkel WB, Flik G, Kwang J, Savelkoul HFJ, Verburg-van Kemenede BML (2002) Neuroendocrine-immune interactions in fish: a role for interleukin-1. Vet Immunol Immunopathol 87:467–479
Evans DL, Jaso-Friedmann L (1992) Nonspecific cytotoxic cells of effectors of immunity of fish. Annu Rev Fish Dis 2:109–121
Evans DL, Leary JH 3rd, Jaso-Friedmann L (1998) Nonspecific cytotoxic cell receptor protein-1: a novel (predicted) type III membrane receptor on the teleost equivalent of natural killer cells recognizes conventional antigen. Cell Immunol 187:19–26
Fernández-Trujillo MA, Porta J, Manchado M et al (2008) c-Lysozyme from Senegalese sole (Solea senegalensis): cDNA cloning and expression pattern. Fish Shellfish Immunol 25:697–700
Fischer U, Koppang EO, Nakanishi T (2013) Teleost T and NK cell immunity. Fish Shellfish Immunol 35:197–206
Fraser J, de Mello LV, Ward D, Rees HH, Williams DR, Fang Y, Brass A, Gracey AY, Cossins AR (2006) Hypoxia-inducible myoglobin expression in nonmuscle tissues. Proc Natl Acad Sci U S A 103:2977–2981
Fries CR (1986) Effects of environmental stressors and immunosuppressants on immunity in Fundulus heteroclitus. Am Zool 26:271–282
Gambón-Deza F, Sánchez-Espinel C, Magadán-Mompó S (2010) Presence of an unique IgT on the IGH locus in three-spined stickleback fish (Gasterosteus aculeatus) and the very recent generation of a repertoire of VH genes. Dev Comp Immunol 34:114–122
Gao C, Fu Q, Zhou S, Song L, Ren Y, Dong X, Su B, Li C (2016) The mucosal expression signatures of g-type lysozyme in turbot (Scophthalmus maximus) following bacterial challenge. Fish Shellfish Immunol 54:612–619
Gao XM et al (2012) A novel function of murine B1 cells: active phagocytic and microbicidal abilities. Eur J Immunol 42:982–992
Gasser S, Zhang WYL, Tan NYJ et al (2017) Sensing of dangerous DNA. Mech Ageing Dev 165(PtA):33–46
Geeraerts C, Belpaire C (2010) The effects of contaminants in European eel: a review. Ecotoxicology 19:239–266
Gercken J, Renwrantz L (1994) A new mannan-binding lectin from the serum of the eel (Anguilla anguilla L.): isolation, characterization and comparison with the fucose-specific serum lectin. Comp Biochem Physiol Biochem Mol Biol 108B:449–461
Gerwick L, Demers NE, Bayne CJ (1999) Modulation of stress hormones in rainbow trout by means of anesthesia, sensory deprivation and receptor blockade. Comp Biochem Physiol 124A:329–334
Ghoneum M, Faisal M, Peters G et al (1988) Supression of natural cytotoxic cell activity of social aggressiveness in tilapia. Dev Comp Immunol 12:595–602
Gorissen M, Flik G (2016) The endocrinology of the stress response in fish. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Biology of stress in fish. Academic Press, San Diego, pp 75–111
Graham S, Secombes CJ (1990) Do fish lymphocytes secrete interferon-γ? J Fish Biol 36:563–573
Granja AG, Leal E, Pignatelli J et al (2015) Identification of teleost skin CD8α+ dendritic-like cells, representing a potential common ancestor for mammalian cross-presenting dendritic cells. J Immunol 195:1825–1837
Grayfer L, Hodgkinson JW, Belosevic M (2014) Antimicrobial responses of teleost phagocytes and innate immune evasion strategies of intracellular bacteria. Dev Comp Immunol 43:223–242
Grimholt U (2016) MHC and evolution in Teleosts. Biology (Basel) 5(1):E6. https://doi.org/10.3390/biology5010006
Gunimaladevi I, Savan R, Sato K, Yamaguchi R, Sakai M (2007) Characterization of an interleukin-15 like (IL-15L) gene from zebrafish (Danio rerio). Fish Shellfish Immunol 22:351–362
Gushiken Y, Watanuki H, Sakai M (2002) In vitro effect of carp phagocytic cells by bisphenol A and nonylphenol. Fish Sci 68:178–183
Haedo MR, Gerez J, Fuertes M, Giacomini D, Páez-Pereda M, Labeur M, Renner U, Stalla GK, Arzt E (2009) Regulation of pituitary function by cytokines. Horm Res Paediatr 72:266–274
Han Q, Das S, Hirano M, Holland SJ, McCurley N, Guo P, Rosenberg CS, Boehm T, Cooper MD (2015) Characterization of lamprey IL-17 family members and their receptors. J Immunol 195:5440–5451
Han J, Wang Y, Chu Q et al (2016) The evolution and functional characterization of miiuy croaker cytosolic gene LGP2 involved in immune response. Fish Shellfish Immunol 58:193–202
Hansen JD, Landis ED, Phillips RB (2005) Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish. Proc Natl Acad Sci U S A 102:6919–6924
Harris J, Bird DJ (1997) The effects of α-MSH and MCH on the proliferation of rainbow trout (Oncorhynchus mykiss) lymphocytes in vitro. In: Kawashima S, Kikuyama S (eds) Advances in comparative endocrinology. Monduzzi Editore, Bologna, pp 1023–1026
Harris J, Bird DJ (1998) Alpha-melanocyte stimulating hormone (α-MSH) and melanin-concentrating hormone (MCH) stimulate phagocytosis by head kidney leucocytes of rainbow trout (Oncorhynchus mykiss) in vitro. Fish Shellfish Immunol 8:631–638
Harris J, Bird DJ (2000a) Modulation of the fish immune system by hormones. Vet Immunol Immunopathol 77:163–176
Harris J, Bird DJ (2000b) Supernatants from leucocytes treated with melanin-concentrating hormone (MCH) and α-melanocyte stimulating hormone (α-MSH) have a stimulatory effect on rainbow trout (Oncorhynchus mykiss) phagocytes in vitro. Vet Immunol Immunopathol 76:117–124
Harris J, Bird DJ, Yeatman LA (1998) Melanin-concentrating hormone (MCH) stimulates the activity of rainbow trout (Oncorhynchus mykiss) head kidney phagocytes in vitro. Fish Shellfish Immunol 8:639–642
Haugarvoll ED, Bjerkås I, Nowak BF, Hordvik I, Koppang EO (2008) Identification and characterization of a novel intraepithelial lymphoid tissue in the gills of Atlantic salmon. J Anat 213:202–209
Heath AG (1987) Water pollution and fish physiology. CRC Press, Boca Raton
Hikima J, Hirono I, Aoki T (1997) Characterization and expression of c-type lysozyme cDNA from Japanese flounder (Paralichthys olivaceus). Mol Mar Biol Biotechnol 6:339–344
Hikima J, Hirono I, Aoki T (2000) Molecular cloning and novel repeated sequences of a c-type lysozyme gene in Japanese flounder (Paralichthys olivaceus). Mar Biotechnol 2:241–247
Hikima J, Jung TS, Aoki T (2011) Immunoglobulin genes and their transcriptional control in teleosts. Dev Comp Immunol 35:924–936
Hikima J, Minagawa S, Hirono I et al (2001) Molecular cloning, expression and evolution of the Japanese flounder goose-type lysozyme gene, and the lytic activity of its recombinant protein. Biochim Biophys Acta 1520:35–44
Hikima J, Hirono I, Aoki T (2002) The lysozyme gene in fish. In: Shimizu N, Aoki T, Hirono I, Takashima F (eds) Aquatic genomics-steps toward a great future. Springer-Verlag, New York, pp 301–309
Hikima J, Cioffi CC, Middleton DL, Wilson MR, Miller NW, Clem LW, Warr GW (2004) Evolution of transcriptional control of the IgH locus: characterization, expression, and function of TF12/HEB homologs of the catfish. J Immunol 173:5476–5484
Hikima J, Lennard ML, Wilson MR, Miller NW, Clem LW, Warr GW (2006a) Conservation and divergence of the E3 enhancer in the IGH locus of teleosts. Immunogenetics 58:226–234
Hikima J, Lennard ML, Wilson MR, Miller NW, Warr GW (2006b) Regulation of the immunoglobulin heavy chain locus expression at the phylogenetic level of a bony fish: transcription factor interaction with two variant octamer motifs. Gene 377:119–129
Hirono I, Uchiyama T, Aoki T (1995) Cloning, nucleotide sequence analysis, and characterization of cDNA for medaka (Oryzias latipes) transferrin. J Mar Biotechnol 2:193–198
Hirono I, Hwang JY, Ono Y et al (2005) Two different types of hepcidins from the Japanese flounder Paralichthys olivaceus. FEBS J 272(20):5257–5264
Hoar WS (1988) The physiology of smolting salmonids. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XI., Part B. Academic Press, San Diego, pp 275–343
Hodgkinson JW, Grayfer L, Belosevic M (2015) Biology of bony fish macrophages. Biology (Basel) 4:881–906
Honma Y, Tamura E (1984) Histological changes in the lymphoid system of fish with respect to age, seasonal and endocrine changes. Dev Comp Immunol 3:239–244
Hoole D (1997) The effects of pollutants on the immune response of fish: implications for helminth parasites. Parassitologia 39:219–225
Howe K, Schiffer PH, Zielinski J et al (2016) Structure and evolutionary history of a large family of NLR proteins in the zebrafish. Open Biol 6:160009
Huising MO, Stet RJM, Savelkoul HFJ, Verburg-van Kemenade BML (2004) The molecular evolution of the interleukin-1 family of cytokines; IL-18 in teleost fish. Dev Comp Immunol 28:395–413
Huising MO, Kruiswijk CP, van Schijndel JE, Savelkoul HF, Flik G, Verburg-van Kemenade BM (2005) Multiple and highly divergent IL-11 genes in teleost fish. Immunogenetics 57:432–443
Huising MO, van Schijndel JE, Kruiswijk CP, Nabuurs SB, Savelkoul HFJ, Flik G, Verburg-van Kemenade BML (2006) The presence of multiple and differentially regulated interleukin-12p40 genes in bony fishes signifies an expansion of the vertebrate heterodimeric cytokine family. Mol Immunol 43:1519–1533
Hwang SD, Asahi T, Kondo H et al (2010) Molecular cloning and expression study on Toll-like receptor 5 paralogs in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 29:630–638
Hwang SD, Fuji K, Takano T et al (2011a) Linkage mapping of toll-like receptors (TLRs) in Japanese flounder, Paralichthys olivaceus. Mar Biotechnol 13:1086–1091
Hwang SD, Kondo H, Hirono I et al (2011b) Molecular cloning and characterization of toll-like receptor 14 in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 30:425–429
Igawa D, Sakai M, Savan R (2006) An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and IL-26 genes have been described for the first time outside mammals. Mol Immunol 43:999–1009
Iida T, Wakabayashi H (1990) Relationship between iron acquisition ability and virulence of Edwardsiella tarda, etiological agent of paracolo disease in Japanese eel, Anguilla japonica. In: Hirano R, Hanyu I (eds) The second Asian fisheries. Asian Fisheries Society, Manila, pp 667–670
Iida T, Takahashi K, Wakabayashi H (1989) Decrease in the bactericidal activity of normal serum during the spawning period of rainbow trout. Bull Jpn Soc Sci Fish 55:463–465
Iida T, Manoppo H, Matsuyama T (2001) Phagocytosis of tilapia inflammatory macrophages isolated from swim bladder. In: Carman O, Sulistiono Aurbayanto A, Suzuki T, Watanabe S, Arimoto T (eds) Proceedings of the JSPS–DGHE international symposium on fisheries science in tropical area, Bogor, pp 261–264
Iliev DB, Castellana B, Mackenzie S, Planas JV, Goetz FW (2007) Cloning and expression analysis of an IL-6 homolog in rainbow trout (Oncorhynchus mykiss). Mol Immunol 44:1803–1807
Iliev DB, Skjæveland I, Jørgensen JB (2013) CpG oligonucleotides bind TLR9 and RRM-containing proteins in Atlantic salmon (Salmo salar). BMC Immunol 14:12
Inagawa H, Kuroda A, Nishizawa T et al (2001) Cloning and characterisation of tandem-repeat type galectin in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 11:217–231
Inui Y, Yamano K, Miwa S (1995) The role of thyroid hormone in tissue development in metamorphosing flounder. Aquaculture 135:87–98
Irwin DM, Gong Z (2003) Molecular evolution of vertebrate goose-type lysozyme genes. J Mol Evol 56:234–242
Ishikawa T, Mano N, Minakami K, Namba A, Kojima T, Hirose H, Nakanish T (2013) Efficacy of high-concentration ascorbic acid supplementation against infectious hematopoietic necrosis in salmonid fish influenced by viral strain and fish size. Fish Pathol 48:113–118
Jamieson A (1990) A survey of transferrins in 87 teleostean species. Anim Genet 21:295–301
Jenkins JA, Ourth DD (1993) Opsonic effect of the alternative complement pathways of channel catfish peripheral blood phagocytes. Vet Immunol Immunopathol 39:447–459
Jiménez-Cantizano RM, Infante C, Martin-Antonio B et al (2008) Molecular characterization, phylogeny, and expression of c-type and g-type lysozymes in brill (Scophthalmus rhombus). Fish Shellfish Immunol 25:57–65
Johnson RW, Arkins S, Dantzer R, Kelley KW (1997) Hormones, lymphohemopoietic cytokines and the neuroimmune axis. Comp Biochem Physiol 116A:183–201
Johnson LL, Anulacion BF, Arkoosh MR, Burrows DG, da Silva DAM et al (2014) Effects of legacy persistent organic pollutants (POPS) in fish – current and future challenges. In: Tierney KB, Farrell AP, Brauner CJ (eds) Fish physiology: organic chemical toxicity of fishes. Academic Press, San Diego, pp 53–140
Jollès P, Jollès J (1984) What's new in lysozyme research? Always a model system, today as yesterday. Mol Cell Biochem 63:165–189
Kaattari SL, Zhang HL, Khor W, Kaattari IM, Shapiro DA (2002) Affinity maturation in trout: clonal dominance of high affinity antibodies late in the immune response. Dev Comp Immunol 26:191–200
Kaiya H, Hosoda H, Kangawa K, Miyazato M (2012) Determination of nonmammalian ghrelin. In: Kojima M, Kangawa K (eds) Ghrelin. Academic Press, San Diego, pp 75–87
Kajita Y, Sakai M, Kobayashi M, Kawauchi H (1992) Enhancement of non-specific cytotoxic activity of leucocytes in rainbow trout Oncorhynchus mykiss injected with growth hormone. Fish Shellfish Immunol 2:155–157
Kamiya H, Muramoto K, Goto R (1988) Purification and properties of agglutinins from conger eel, Conger myriaster (Brevoort), skin mucus. Dev Comp Immunol 12:309–318
Kawai T, Akira S (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34:637–650
Khangarot BS, Rathore RS (1999) Copper exposure reduced the resistance of the catfish Saccobranchus fossilis to Aeromonas hydrophila infection. Bull Environ Contam Toxicol 62:490–495
Kobayashi I, Sekiya M, Moritomo T, Ototake M, Nakanishi T (2006) Demonstration of hematopoietic stem cells in ginbuna carp (Carassius auratus langsdorfii) kidney. Dev Comp Immunol 30:1034–1046
Kobayashi I, Moritomo T, Ototake M, Nakanishi T (2007) Isolation of side population cells from ginbuna carp (Carassius auratus langsdorfii) kidney hematopoietic tissues. Dev Comp Immunol 31:696–707
Kobayashi I, Saito K, Moritomo T, Araki K, Takizawa F, Nakanishi T (2008) Characterization and localization of side population (SP) cells in zebrafish kidney hematopoietic tissue. Blood 111:1131–1137
Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402:656–660
Kono T, Bird S, Sonoda K, Savan R, Secombes CJ, Sakai M (2008) Characterization and expression analysis of an interleukin-7 homologue in the Japanese pufferfish, Takifugu rubripes. FEBS J 275:1213–1226
Kono T, Korenaga H, Sakai M (2011) Genomics of fish IL-17 ligand and receptors: a review. Fish Shellfish Immunol 31:635–643
Kooijman R, Gerlo S, Coppens A, Hooghe-Peters EL (2000) Growth hormone and prolactin expression in the immune system. Ann N Y Acad Sci 917:534–540
Koppang EO, Fischer U, Moore L, Tranulis MA, Dijkstra JM et al (2010) Salmonid T cells assemble in the thymus, spleen and in novel interbranchial lymphoid tissue. J Anat 217:728–739
Krajhanzl A (1990) Egg lectins of invertebrates and lower vertebrates: properties and biological function. Adv Lectin Res 3:83–131
Kurata O, Okamoto N, Suzumura E, Sano N, Ikeda Y (1995) Accommodation of carp natural killer-like cells to environmental temperature. Aquaculture 129:421–424
Kurobe T, Hirono I, Kondo H, Saito-Taki T, Aoki T (2007) Molecular cloning, characterization, expression and functional analysis of Japanese flounder Paralichthys olivaceus Fas ligand. Dev Comp Immunol 31:687–695
Kyomuhendo P, Myrnes B, Nilsen IW (2007) A cold-active salmon goose-type lysozyme with high heat tolerance. Cell Mol Life Sci 64:2841–2847
Laing K, Hansen JD (2011) Fish T cells: recent advances through genomics. Dev Comp Immunol 35:1282–1295
Laing KJ, Purcell MK, Winton JR, Hansen JD (2008) A genomic view of the NOD-like receptor family in teleost fish: identification of a novel NLR subfamily in zebrafish. BMC Evol Biol 8:42
Lam SH, Sin YM, Gong Z, Lam TJ (2005) Effects of thyroid hormone on the development of immune system in zebrafish. Gen Comp Endocrinol 142:325–335
Langenau DM, Zon LI (2005) The zebrafish: a new model of T-cell and thymic development. Nat Rev Immunol 5:307–317
Larsen AN, Solstad T, Svineng G, Seppola M, Jørgensen TØ (2009) Molecular characterisation of a goose-type lysozyme gene in Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol 26:122–132
Lauth X, Shike H, Burns JC, Westerman ME, Ostland VE, Carlberg JM et al (2002) Discovery and characterization of two isoforms of moronecidin, a novel antimicrobial peptide from hybrid striped bass. J Biol Chem 277:5030–5039
Le Guével R, Petit FG, Le Goff P, Métivier R, Valotaire Y, Pakdel F (2000) Inhibition of rainbow trout (Oncorhynchus mykiss) estrogen receptor activity by cadmium. Biol Reprod 63:259–266
Le Morvan C, Troutaud D, Deschaux P (1998) Differential effects of temperature on specific and nonspecific immune defences in fish. J Exp Biol 201:165–168
Lee JY, Tada T, Hirono I, Aoki T (1998) Molecular cloning and evolution of transferrin cDNAs in salmonids. Mol Mar Biol Biotechnol 7:287–293
Lennard ML, Hikima J, Ross DA, Kruiswijk CP, Wilson MR, Miller NW, Warr GW (2007) Characterization of an Oct1 orthologue in the channel catfish, Ictalurus punctatus: a negative regulator of immunoglobulin gene transcription? BMC Mol Biol 31:8
Li J, Barreda DR, Zhang YA, Boshra H, Gelman AE, Lapatra S, Tort L, Sunyer JO (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 7:1116–1124
Li JH, Shao JZ, Xiang LX, Wen Y (2007) Cloning, characterization and expression analysis of pufferfish interleukin-4 cDNA: the first evidence of Th2-type cytokine in fish. Mol Immunol 44:2078–2086
Li J, Kong L, Gao Y, Wu C, Xu T (2015) Characterization of NLR-A subfamily members in miiuy croaker and comparative genomics revealed NLRX1 underwent duplication and lose in actinopterygii. Fish Shellfish Immunol 47(1):397–406
Li J, Chu Q, Xu T (2016) A genome-wide survey of expansive NLR-C subfamily in miiuy croaker and characterization of the NLR-B30.2 genes. Dev Comp Immunol 61:116–125
Liao Z, Wan Q, Su H, Wu C, Su J (2017) Pattern recognition receptors in grass carp Ctenopharyngodon idella: I. Organization and expression analysis of TLRs and RLRs. Dev Comp Immunol 76:93–104
Lin AF, Xiang LX, Wang QL, Dong WR, Gong YF, Shao JZ (2009) The DC-SIGN of zebrafish: insights into the existence of a CD209 homologue in a lower vertebrate and its involvement in adaptive immunity. J Immunol 183:7398–7410
Liu J, Li J, Xiao J, Chen H, Lu L, Wang X, Tian Y, Feng H (2017) The antiviral signaling mediated by black carp MDA5 is positively regulated by LGP2. Fish Shellfish Immunol 66:360–371
Loo YM Jr, Gale M (2011) Immune signaling by RIG-I-like receptors. Immunity 34:680–692
Lugo-Villarino G, Balla KM, Stachura DL, Bañuelos K, Werneck MB, Traver D (2010) Identification of dendritic antigen-presenting cells in the zebrafish. Proc Natl Acad Sci U S A 107:15850–15855
Lutfalla G, Crollius HR, Stange-thomann N, Jaillon O, Mogensen K, Monneron D (2003) Comparative genomic analysis reveals independent expansion of a lineage-specific gene family in vertebrates: the class II cytokine receptors and their ligands in mammals and fish. BMC Genomics 4:29
Ma HL, Shi YH, Zhang XH, Li MY, Chen J (2016) A transmembrane C-type lectin receptor mediates LECT2 effects on head kidney-derived monocytes/macrophages in a teleost, Plecoglossus altivelis. Fish Shellfish Immunol 51:70–76
Magor BG (2015) Antibody affinity maturation in fishes—our current understanding. Biology 4:512–524
Magor BG, Wilson MR, Miller NW, Clem LW, Middleton DL, Warr GW (1994) An Ig heavy chain enhancer of the channel catfish Ictalurus punctatus: evolutionary conservation of function but not structure. J Immunol 153:5556–5563
Maier VH, Dorn KV, Gudmundsdottir BK, Gudmundsson GH (2008) Characterisation of cathelicidin gene family members in divergent fish species. Mol Immunol 45:3723–3730
Makrinos DL, Bowden TJ (2016) Natural environmental impacts on teleost immune function. Fish Shellfish Immunol 53:50–57
Manning MJ, Nakanishi T (1996) The specific immune system: cellular defenses. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, San Diego, pp 159–205
Mariano G, Stilo R, Terrazzano G, Coccia E, Vito P, Varricchio E, Paolucci M (2012) Effects of recombinant trout leptin in superoxide production and NF-κB/MAPK phosphorylation in blood leukocytes. Peptides 48:59–69
Matsumoto M, Hayashi K, Suetake H, Yamamoto A, Araki K (2016) Identification and functional characterization of multiple interleukin 12 in amberjack (Seriola dumerili). Fish Shellfish Immunol 55:281–292
Matsushita M, Fujita T (2001) Ficolins and the lectin complement pathway. Immunol Rev 180:78–85
Matsuura Y, Yabu T, Shiba H, Moritomo T, Nakanishi T (2014) Identification of a novel fish granzyme involved in cell-mediated immunity. Dev Comp Immunol 46:499–507
Matsuura Y, Yabu T, Shiba H, Moritomo T, Nakanishi T (2016) Purification and characterization of a fish granzymeA involved in cell-mediated immunity. Dev Comp Immunol 60:33–40
Matsuura Y, Takasaki M, Miyazawa R, Nakanishi T (2017) Stimulatory effects of heat-killed enterococcus faecalis on cell-mediated immunity in fish. Dev Comp Immunol 74:1–9
Matsuyama H, Yano T, Yamakawa T, Nakao M (1992) Opsonic effect of the third complement conponent (C3) of carp (Cyprinus carpio) on phagocytosis by neutrophils. Fish Shellfish Immunol 2:69–78
Maule AG, Schreck CB, Kaattari SL (1987) Changes in the immune system of coho salmon (Oncorhynchus kisutch) during the parr-to-smolt transformation and after implantation of cortisol. Can J Fish Aquat Sci 44:161–166
Maule AG, Schrock R, Slater C, Fitzpatrick MS, Schreck CB (1996) Immune and endocrine responses of adult chinook salmon during freshwater migration and sexual maturation. Fish Shellfish Immunol 6:221–233
Mazur CF, Iwama GK (1993) Handling and crowding stress reduces number of plaque-forming cells in Atlantic salmon. J Aquat Anim Health 5:98–101
McCormick SD (1995) Hormonal control of gill Na+, K+-ATPase and chloride cell function. In: Wood CM, Shuttleworth TJ (eds) Cellular and molecular approaches to fish ionic regulation. Academic Press, San Diego, pp 285–315
McDonald G, Milligan L (1997) Ionic, osmotic and acid-base regulation in stress. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 119–144
McLeay DJ (1975) Variations in the pituitary-interrenal axis and the abundance of circulating blood-cell types in juvenile coho salmon, Oncorhynchus kisutch, during stream residence. Can J Zool 53:1882–1891
Mehinto AC, Pruchab MS, Colli-Dulac RC, Kroll KJ (2014) Gene networks and toxicity pathways induced by acute cadmium exposure in adult largemouth bass (Micropterus salmoides). Aquat Toxicol 152:186–194
Melingen GO, Stefansson SO, Berg A, Wergeland HI (1995) Changes in serum protein and IgM concentration during smolting and early post-smolt period in vaccinated and unvaccinated Atlantic salmon (Salmo salar L). Fish Shellfish Immunol 5:211–222
Meloni S, Zarletti G, Benedetti S, Randelli E, Buonocore F, Scapigliati G (2006) Cellular activities during a mixed leucocyte reaction in the teleost sea bass dicentrarchus labrax. Fish Shellfish Immunol 20:739–749
Metz JR, Huising MO, Leon K, Verburg-van Kemenade BM, Flik G (2006) Central and peripheral interleukin-1beta and interleukin-1 receptor I expression and their role in the acute stress response of common carp, Cyprinus carpio L. J Endocrinol 191:25–35
Milla S, Depiereux S, Kestemont P (2011) The effects of estrogenic and androgenic endocrine disrupters on the immune system of fish: a review. Ecotoxicology 20:305–319
Miller NW, Sizemore RC, Clem LW (1985) Phylogeny of lymphocyte heterogeneity: the cellular requirements for in vitro antibody responses of channel catfish leukocytes. J Immunol 134:2884–2888
Miller NW, Deuter A, Clem LW (1986) Phylogeny of lymphocyte heterogeneity: the cellular requirements for the mixed leukocyte reaction with channel catfish. Immunology 59:123–128
Minagawa S, Hikima J, Hirono I, Aoki T, Mori H (2001) Expression of Japanese flounder c-type lysozyme cDNA in insect cells. Dev Comp Immunol 25:439–445
Miwa S, Inui Y (1991) Thyroid hormone stimulates the shift of erythrocyte populations during metamorphosis of the flounder. J Exp Zool 259:222–228
Mola L, Gambarelli A, Pederzoli A, Ottaviani E (2005) ACTH response to LPS in the first stages of development of the fish Dicentrarchus labrax L. Gen Comp Endocrinol 143:99–103
Molle V, Campagna S, Bessin Y, Ebran N, Saint N, Molle G (2008) First evidence of the pore-forming properties of a keratin from skin mucus of rainbow trout (Oncorhynchus mykiss, formerly Salmo gairdneri). Biochem J 411:33–40
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268
Monte MM, Wang T, Holland JW, Zou J, Secombes CJ (2013) Cloning and characterization of rainbow trout interleukin-17A/F2 (IL-17A/F2) and IL-17 receptor A: expression during infection and bioactivity of recombinant IL-17A/F2. Infect Immun 81:340–353
Morcillo P, Meseguer J, Esteban M-Á, Cuesta A (2016) In vitro effects of metals on isolated head-kidney and blood leucocytes of the teleost fish Sparus aurata L. and Dicentrarchus labrax L. Fish Shellfish Immunol 54:77–85
Morimoto T, Biswas G, Kono T, Sakai M, Hikima J (2016) Immune responses in the Japanese pufferfish (Takifugu rubripes) head kidney cells stimulated with particulate silica. Fish Shellfish Immunol 49:84–90
Moritomo T, Iida T, Wakabayashi H (1988) Chemiluninescence of neutrophils isolated from peripheral blood of eel. Fish Pathol 23:49–53
Moss LD, Monette MM, Jaso-Friedmann L, Leary JH 3rd, Dougan ST et al (2009) Identification of phagocytic cells, NK-like cytotoxic cell activity and the production of cellular exudates in the coelomic cavity of adult zebrafish. Dev Comp Immunol 33:1077–1087
Muñoz P, Calduch-Giner JA, Sitjà-Bobadilla A, Alvarez-Pellitero P, Prérez-Sánchez J (1998) Modulation of the respiratory burst activity of Mediteranean sea bass (Dicentrarchus labrax L.) phagocytes by growth hormone and parasitic status. Fish Shellfish Immunol 8:25–36
Muona M, Soivio A (1992) Changes in plasma lysozyme and blood leucocyte levels of hatchery-reared Atlantic salmon (Salmo salar L.) and sea trout (Salmo trutta L.) during parr-smolt transformation. Aquaculture 106:75–87
Muramoto K, Kamiya H (1992) The amino-acid sequence of a lectin from conger eel, Conger myriaster, skin mucus. Biochim Biophys Acta 1116:129–136
Murthy KS, Kiran BR (2013) Review on usage of medicinal plants in fish diseases. Int J Pharm Bio Sci 4:975–986
Nagae M, Fuda H, Ura K, Kawamura H, Adachi S, Hara A, Yamauchi K (1994) The effect of cortisol administration on blood plasma immunoglobulin M (IgM) concentrations in masu salmon (Oncorhynchus masou). Fish Physiol Biochem 13:41–48
Nagae M, Ogawa K, Kawahara A, Yamaguchi M, Nishimura T, Ito F (2001) Effect of acidification stress on endocrine and immune functions in carp, Cyprinus carpio. Water Air Soil Pollut 130:893–898
Nagasawa T, Nakayasu C, Rieger AM, Barreda DR, Somamoto T, Nakao M (2014) Phagocytosis by thrombocytes is a conserved innate immune mechanism in lower vertebrates. Front Immunol 5:445
Nagasawa T, Somamoto T, Nakao M (2015) Carp thrombocyte phagocytosis requires activation factors secreted from other leukocytes. Dev Comp Immunol 52:107–111
Nakai T, Kanno T, Cruz ER, Muroga K (1987) The effect of iron compounds on the virulence of Vibrio anguillarum in Japanese eels and ayu. Fish Pathol 22:185–189
Nakamura H, Shimozawa A (1994) Phagocytotic cells in the fish heart. Arch Histol Cytol 57:415–425
Nakanishi T (1986) Seasonal changes in the humoral immune response and the lymphoid tissues of the marine teleost, Sebastiscus marmoratus. Vet Immunol Immunopathol 12:213–221
Nakanishi T, Ototake M (1999) The graft-versus-host reaction (GVHR) in the ginbuna crucian carp, Carassius auratus langsdorfii. Dev Comp Immunol 23:15–26
Nakanishi T, Fischer U, Dijkstra JM, Hasegawa S, Somamoto T et al (2002) Cytotoxic T cell function in fish. Dev Comp Immunol 26:131–139
Nakanishi T, Toda H, Shibasaki Y, Somamoto T (2011) Cytotoxic T cells in teleost fish. Dev Comp Immunol 35:1317–1323
Nakanishi T, Shibasaki Y, Matsuura Y (2015) T cells in fish. Biology 4:640–663
Nakano T, Graf T (1991) Goose-type lysozyme gene of the chicken: sequence, genomic organization and expression reveals major differences to chicken-type lysozyme gene. Biochim Biophys Acta 1090:273–276
Nakao M, Tsujikura M, Ichiki S, Vo TK, Somamoto T (2011) The complement system in teleost fish: progress of post-homolog-hunting researches. Dev Comp Immunol 35:1296–1308
Nakashima M, Kinoshita M, Nakashima H, Habu Y, Miyazaki H, Shono S et al (2012) Pivotal advance: characterization of mouse liver phagocytic B cells in innate immunity. J Leukoc Biol 91:537–546
Nam BH, Hirono I, Aoki T (2003) The four TCR genes of teleost fish: the cDNA and genomic DNA analysis of Japanese flounder (Paralichthys olivaceus) TCR alpha-, beta-, gamma-, and delta-chains. J Immunol 170:3081–3090
Narnaware YK, Kelly SP, Woo NYS (1997) Effect of injected growth hormone on phagocytosis in silver sea bream (Sparus sarba) adapted to hyper- and hypo-osmotic salinities. Fish Shellfish Immunol 7:515–517
Nascimento DS, do Vale A, Tomás AM, Zou J, Secombes CJ, dos Santos NMS (2007) Cloning, promoter analysis and expression in response to bacterial exposure of sea bass (Dicentrarchus labrax L.) interleukin-12 p40 and p35 subunits. Mol Immunol 44:2277–2291
Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14
Ndoye A, Troutaud D, Rougier F, Deschaux P (1991) Neuroimmunology in fish. Adv Neuroimmunol 1:242–251
Nevid NJ, Meier AH (1993) A day-night rhythm of immune activity during scale allograft rejection in the gulf killifish, Fundulus grandis. Dev Comp Immunol 17:221–228
Nikolakopoulou K, Zarkadis IK (2006) Molecular cloning and characterisation of two homologues of Mannose-Binding Lectin in rainbow trout. Fish Shellfish Immunol 21:305–314
Nomiyama H, Hieshima K, Osada N, Kato-Unoki Y, Otsuka-Ono K, Takegawa S et al (2008) Extensive expansion and diversification of the chemokine gene family in zebrafish: identification of a novel chemokine subfamily CX. BMC Genomics 9:222
Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58:701–713
Nonaka M, Smith SL (2000) Complement system of bony and cartilaginous fish. Fish Shellfish Immunol 10:213–228
Ohtani M, Hayashi N, Hashimoto K, Nakanishi T, Dijkstra JM (2008) Comprehensive clarification of two paralogous interleukin 4/13 loci in teleost fish. Immunogenetics 60:383–397
Ohtani M, Hikima J, Kondo H, Hirono I, Jung TS, Aoki T (2010) Evolutional conservation of molecular structure and antiviral function of a viral RNA receptor, LGP2, in Japanese flounder, Paralichthys olivaceus. J Immunol 185:7507–7517
Ohtani M, Hikima J, Kondo H, Hirono I, Jung TS, Aoki T (2011) Characterization and antiviral function of a cytosolic sensor gene, MDA5, in Japanese flounder, Paralichthys olivaceus. Dev Comp Immunol 35:554–562
Olavarría VH, Sepulcre MP, Figueroa JE, Mulero V (2010) Prolactin-induced production of reactive oxygen species and IL-1β in leukocytes from the bony fish gilthead seabream involves Jak/Stat and NF-κB signaling pathways. J Immunol 185:3873–3883
Oliva-Teles A (2012) Nutrition and health of aquaculture fish. J Fish Dis 35:83–108
Olsson P-E, Kling P, Petterson C, Silversand C (1995) Interaction of cadmium and oestradiol-17β on metallothionein and vitellogenin synthesis in rainbow trout (Oncorhynchus mykiss). Biochem J 307:197–203
Ortiz NN, Gerdol M, Stocchi V, Marozzi C, Randelli E, Bernini C et al (2014) T cell transcripts and T cell activities in the gills of the teleost fish sea bass (Dicentrarchus labrax). Dev Comp Immunol 47:309–318
Oshiumi H, Tsujita T, Shida K, Matsumoto M, Ikeo K, Seya T (2003) Prediction of the prototype of the human Toll-like receptor gene family from the pufferfish, Fugu rubripes, genome. Immunogenetics 54:791–800
Øvergård AC, Nepstad I, Nerland AH, Patel S (2012) Characterisation and expression analysis of the Atlantic halibut (Hippoglossus hippoglossus L.) cytokines: IL-1β, IL-6, IL-11, IL-12β and IFNγ. Mol Biol Rep 39:2201–2213
Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshw Res 62:1015–1026
Park SB, Hikima J, Suzuki Y, Ohtani M, Nho SW, Cha IS, Jang HB, Kondo H et al (2012) Molecular cloning and functional analysis of nucleotide-binding oligomerization domain 1 (NOD1) in olive flounder, Paralichthys olivaceus. Dev Comp Immunol 36:680–687
Parra D, Rieger AM, Li J, Zhang YA, Randall LM, Hunter CA et al (2012) Pivotal advance: peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells. J Leukoc Biol 91:525–536
Partula S, de Guerra A, Fellah JS, Charlemagne J (1995) Structure and diversity of the T cell antigen receptor beta-chain in a teleost fish. J Immunol 155:699–706
Partula S, de Guerra A, Fellah JS, Charlemagne J (1996) Structure and diversity of the TCR alpha-chain in a teleost fish. J Immunol 157:207–212
Périn JP, Jollés P (1976) Enzymatic properties of a new type of lysozyme isolated from Asterias rubens: comparison with the Nephthys hombergii (annelid) and hen lysozymes. Biochimie 58:657–662
Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202:8–32
Petit J, Wiegertjes GF (2016) Long-lived effects of administering β-glucans: indications for trained immunity in fish. Dev Comp Immunol 64:93–102
Pettersen EF, Ingerslev HC, Stavang V, Egenberg M, Wergeland HI (2008) A highly phagocytic cell line TO from Atlantic salmon is CD83 positive and M-CSFR negative, indicating a dendritic-like cell type. Fish Shellfish Immunol 25:809–819
Pickering AD, Christie P (1980) Sexual differences in the incidence and severity of ectoparasitic infestation of the brown trout, Salmo trutta L. J Fish Biol 16:669–683
Pickering AD, Pottinger TG (1987) Lymphocytopenia and interrenal activity during sexual maturation in the brown trout, Salmo trutta L. J Fish Biol 30:41–50
Pickford GE, Srivastave AK, Slicher AM, Pang PKT (1971) The stress response in the abundance of circulating leucocytes in the killifish, Fundulus heteroclitus. I. The cold-shock sequence and the effects of hypophysectomy. J Exp Zool 177:89–96
Pilstrom L, Warr GW, Strömberg S (2005) Why is the antibody response of Atlantic cod so poor? The search for a genetic explanation. Fish Sci 71:961–971
Poulton LD, Nolan KF, Anastasaki C, Waldmann H, Patton EE (2010) A novel role for glucocorticoid-induced TNF receptor ligand (Gitrl) in early embryonic zebrafish development. Int J Dev Biol 54:815–825
Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306–360
Prunet P, Cairns MT, Winberg S, Pottinger TG (2008) Functional genomics of stress responses in fish. Rev Fish Sci 16(Sup 1):157–166
Pulsford AL, Lamaire-Gony S, Tomlinson M, Cliingwood N, Glynn PJ (1994) Effects of acute stress on the immune system of the dab, Limanda limanda. Comp Biochem Physiol 109C:129–139
Qi Z, Nie P, Secombes CJ, Zou J (2010) Intron-containing type I and type III IFN coexist in amphibians: refuting the concept that a retroposition event gave rise to type I IFNs. J Immunol 184:5038–5046
Qin QW, Ototake M, Nagoya H, Nakanishi T (2002) Graft-versus-host reaction (gvhr) in clonal amago salmon, Oncorhynchus rhodurus. Vet Immunol Immunopathol 89:83–89
Quabius ES, Balm PHM, Wendelaar Bonga SE (1997) Interrenal stress responsiveness of tilapia (Oreochromis mossambicus) is impaired by dietary exposure to PCB126. Gen Comp Endocrinol 108:472–482
Quesada-García A, Encinas P, Valdehita A, Baumann L, Segner H, Coll JM, Navas JM (2016) Thyroid active agents T3 and PTU differentially affect immune gene transcripts in the head kidney of rainbow trout (Oncorynchus mykiss). Aquat Toxicol 174:159–168
Quynh NT, Hikima J, Kim YR, Fagutao FF, Kim MS, Aoki T, Jung TS (2015) The cytosolic sensor, DDX41, activates antiviral and inflammatory immunity in response to stimulation with double-stranded DNA adherent cells of the olive flounder, Paralichthys olivaceus. Fish Shellfish Immunol 44:576–583
Rakers S, Niklasson L, Steinhagen D, Kruse C, Schauber J, Sundell K, Paus R (2013) Antimicrobial peptides (AMPs) from fish epidermis: perspectives for investigative dermatology. J Invest Dermatol 133:1140–1149
Ramirez-Gomez F et al (2012) Discovery and characterization of secretory IgD in rainbow trout: secretory IgD is produced through a novel splicing mechanism. J Immunol 188:1341–1349
Rasquin P (1951) Effects of carp pituitary and mammalian ACTH on the endocrine and lymphoid systems of the teleost Astyanax mexicanus. J Exp Zool 117:317–357
Regala RP, Rice CD, Schwedler TE, Dorociak IR (2001) The effects of tributyltin (TBT) and 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126) mixtures on antibody responses and phagocyte oxidative burst activity in channel catfish, Ictalurus punctatus. Arch Environ Contam Toxicol 40:386–391
Rhodes DA, de Bono B, Trowsdale J (2005) Relationship between SPRY and B30.2 protein domains. Evolution of a component of immune defence? Immunology 116:411–417
Rice CD, Xiang Y (2000) Immune function, hepatic CYP1A, and reproductive biomarker responses in the gulf killifish, Fundulus grandis, during dietary exposures to endocrine disrupters. Mar Environ Res 50:163–168
Rice CD, Banes MM, Ardelt TC (1995) Immunotoxicity in channel catfish, Ictalurus punctatus, following acute exposure to tributyltin. Arch Environ Contam Toxicol 28:464–470
Richards RH, Pickering AD (1978) Frequency and distribution patterns of Saprolegnia infection in wild and hatchery-reared brown trout Salmo trutta L. and char Salvelinus alpinus (L.). J Fish Dis 1:69–82
Richter K, Buchner J (2001) Hsp90: chaperoning signal transduction. J Cell Physiol 188:281–290
Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A (2005) The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A 102:9577–9582
Robertsen B (2006) The interferon system of teleost fish. Fish Shellfish Immunol 20:172–191
Roca FJ, Mulero I, Lopez-Munoz A, Sepulcre MP, Renshaw SA, Meseguer J et al (2008) Evolution of the inflammatory response in vertebrates: fish TNF-alpha is a powerful activator of endothelial cells but hardly activates phagocytes. J Immunol 181:5071–5081
Rombout JH, Joosten PH, Engelsma MY, Vos AP Taverne N, Taverne-Thiele JJ (1998) Indications for a distinct putative Tcell population in mucosal tissue of carp (Cyprinus carpio L.). Dev Comp Immunol 22:63–77
Rombout JH, Huttenhuis HB, Picchietti S, Scapigliati G (2005) Phylogeny and ontogeny of fish leucocytes. Fish Shellfish Immunol 19:441–455
Rombout JH, Abelli L, Picchietti S, Scapigliati G, Kiron V (2010) Teleost intestinal immunology. Fish Shellfish Immunol 31:616–626
Romero A, Manríquez R, Alvarez C, Gajardo C, Vásquez J, Kausel G et al (2012) Prolactin-releasing peptide is a potent mediator of the innate immune response in leukocytes from Salmo salar. Vet Immunol Immunopathol 147:170–179
Rønneseth A, Ghebretnsae DB, Wergeland HI, Haugland GT (2015) Functional characterization of IgM+ B cells and adaptive immunity in lumpfish (Cyclopterus lumpus L.). Dev Comp Immunol 52:132–143
Rothenburg S, Deigendesch N, Dittmar K, Koch-Nolte F, Haag F, Lowenhaupt K, Rich A (2005) A PKR-like eukaryotic initiation factor 2alpha kinase from zebrafish contains Z-DNA binding domains instead of dsRNA binding domains. Proc Natl Acad Sci U S A 102(5):1602–1607
Saha NR, Suetake H, Suzuki Y (2004) Characterization and expression of the immunoglobulin light chain in the fugu: evidence of a solitaire type. Immunogenetics 56:47–55
Sakai M, Kobayashi M, Kawauchi H (1995) Enhancement of chemiluminescent responses of phagocytic cells from rainbow trout, Oncorhynchus mykiss, by injection of growth hormone. Fish Shellfish Immunol 5:375–379
Sakai M, Kobayashi M, Kawauchi H (1996a) In vitro activation of fish phagocytic cells by GH, PRL and somatolactin. J Endocrinol 151:113–118
Sakai M, Kajita Y, Kobayashi M, Kawauchi H (1996b) Increase in haemolytic activity of serum from rainbow trout Oncorhynchus mykiss injected with exogenous growth hormone. Fish Shellfish Immunol 6:615–617
Sakai M, Kobayashi M, Kawauchi H (1996c) Mitogenic effect of growth hormone and prolactin on chum salmon Oncorhynchus keta leukocytes in vitro. Vet Immunol Immunopathol 53:185–189
Sakai M, Yamaguchi T, Watanuki H, Yasuda A, Takahashi A (2001) Modulation of fish phagocytic cells by N-terminal peptides of proopiomelanocortin (NPP). J Exp Zool 290:341–346
Salinas I (2015) The mucosal immune system of teleost fish. Biology (Basel) 4:525–539
Sano T, Nagakura Y (1982) Studies on viral diseases of Japanese fishes. VIII. Interferon induced by RTG-2 cell infected with IHN virus. Fish Pathol 17:179–185. (In Japanese)
Sathiyaa R, Campbell T, Vijayan MM (2001) Cortisol modulates HSP90 mRNA expression in primary cultures of trout hepatocytes. Comp Biochem Physiol 129B:679–685
Saunders HL, Magor BG (2004) Cloning and expression of the AID gene in the channel catfish. Dev Comp Immunol 28:657–663
Saurabh A, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239
Savan R, Aman A, Sakai M (2003) Molecular cloning of G type lysozyme cDNA in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 15:263–268
Savan R, Aman A, Sato K, Yamaguchi R, Sakai M (2005a) Discovery of a new class of immunoglobulin heavy chain from fugu. Eur J Immunol 35:3320–3331
Savan R, Kono T, Igawa D, Sakai M (2005b) A novel tumor necrosis factor (TNF) gene present in tandem with the TNF-alpha gene on the same chromosome in teleosts. Immunogenetics 57:140–150
Schreck CB (1996) Immunomodulation: endogenous factors. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, San Diego, pp 311–337
Schreiber AM (2001) Metamorphosis and early larval development of the flatfishes (Pleuronectiformes): and osmoregulatory perspective. Comp Biochem Physiol 129B:587–595
Secombes CJ (1996) The nonspecific immune system: cellular defenses. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, San Diego, pp 63–103
Secombes CJ, Wang T, Bird S (2011) The interleukins of fish. Dev Comp Immunol 35:1336–1345
Seong SK, Beck BR, Kim D, Park J, Kim J, Kim HD, Ringø E (2014) Prebiotics as immunostimulants in aquaculture: a review. Fish Shellfish Immunol 40:40–48
Sepulcre MP, Alcaraz-Pérez F, López-Muñoz A, Roca FJ, Meseguer J et al (2009) Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-kappaB activation. J Immunol 182:1836–1845
Sha Z, Abernathy JW, Wang S, Li P, Kucuktas H, Liu H, Peatman E, Liu Z (2009) NOD-like subfamily of the nucleotide-binding domain and leucine-rich repeat containing family receptors and their expression in channel catfish. Dev Comp Immunol 33:991–999
Shen L, Stuge TB, Bengtén E, Wilson M, Chinchar VG, Naftel JP et al (2004) Identification and characterization of clonal NK-like cells from channel catfish (Ictalurus punctatus). Dev Comp Immunol 28:139–152
Shiau CE, Monk KR, Joo W, Talbot WS (2013) An anti-inflammatory NOD-like receptor is required for microglia development. Cell Rep 5:1342–1352
Shibasaki Y, Toda H, Kobayashi I, Moritomo T, Nakanishi T (2010) Kinetics of CD4+ and CD8α+ T-cell subsets in Graft-Versus-Host Reaction (GVHR) in ginbuna crucian carp Carassius auratus langsdorfii. Dev Comp Immunol 34:1075–1081
Shibasaki Y, Yabu T, Araki K, Mano N, Shiba H, Moritomo T, Nakanishi T (2014) Peculiar monomeric interferon gammas, IFNγrel 1 and IFNγrel 2, in ginbuna crucian carp. FEBS J 281:1046–1056
Shibasaki Y, Hatanaka C, Matsuura Y, Miyazawa R, Yabu T, Moritomo T, Nakanishi T (2016) Effects of IFNγ administration on allograft rejection in ginbuna crucian carp. Dev Comp Immunol 62:108–115
Shibasaki Y, Matsuura Y, Toda H, Imabayashi N, Nishino T, Uzumaki K, Hatanaka C, Yabu T, Moritomo T, Nakanishi T (2015) Kinetics of lymphocyte subpopulations in allogeneic grafted scales of ginbuna crucian carp. Dev Comp Immunol 52(1):75–80
Shike H, Lauth X, Westerman ME, Ostland VE, Carlberg JM, Van Olst JC et al (2002) Bass hepcidin is a novel antimicrobial peptide induced by bacterial challenge. Eur J Biochem 269:2232–2237
Shu C, Wang S, Xu T (2015) Characterization of the duplicate L-SIGN and DC-SIGN genes in miiuy croaker and evolutionary analysis of L-SIGN in fishes. Dev Comp Immunol 50:19–25
Silphaduang U, Noga EJ (2001) Peptide antibiotics in mast cells of fish. Nature 414(6861):268–269
Silva AB, Palmer DB (2011) Evidence of conserved neuroendocrine interactions in the thymus: intrathymic expression of neuropeptides in mammalian and non-mammalian vertebrates. Neuroimmunomodulation 18:264–270
Simora RM, Ohtani M, Hikima J, Kondo H, Hirono I, Jung TS, Aoki T (2010) Molecular cloning and antiviral activity of IFN-β promoter stimulator-1 (IPS-1) gene in Japanese flounder, Paralichthys olivaceus. Fish Shellfish Immunol 29:979–986
Skjaeveland I, Iliev DB, Zou J, Jørgensen T, Jørgensen JB (2008) A TLR9 homolog that is up-regulated by IFN-gamma in Atlantic salmon (Salmo salar). Dev Comp Immunol 32:603–607
Slicher AM (1961) Endocrinological and hematological studies in Fundulus heteroclitus (Linn.). Bull Bingham Ocean Coll 17:3–55
Sneddon LU, Wolfenden DCC, Thomson JS (2016) Stress management and welfare. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Biology of stress in fish. Academic Press, San Diego, pp 463–539
Somamoto T, Nakanishi T, Okamoto N (2000) Specific cell-mediated cytotoxicity against a virus-infected syngeneic cell line in isogeneic ginbuna crucian carp. Dev Comp Immunol 24:633–640
Somamoto T, Nakanishi T, Okamoto N (2002) Role of specific cell-mediated cytotoxicity in protecting fish from viral infections. Virology 297:120–127
Somamoto T, Kondo M, Nakanishi T, Nakao M (2014) Helper function of cd4(+) lymphocytes in antiviral immunity in ginbuna crucian carp, Carassius auratus langsdorfii. Dev Comp Immunol 44:111–115
Somamoto T, Miura Y, Nakanishi T, Nakao M (2015) Local and systemic adaptive immune responses toward viral infection via gills in ginbuna crucian carp. Dev Comp Immunol 52:81–87
Srisapoome P, Ohira T, Hirono I, Aoki T (2004) Genes of the constant regions of functional immunoglobulin heavy chain of Japanese flounder, Paralichthys olivaceus. Immunogenetics 56:292–300
Stafford JL, Belosevic M (2003) Transferrin and the innate immune response of fish: identification of a novel mechanism of macrophage activation. Dev Comp Immunol 27:539–554
Stafford JL, Wilson EC, Belosevic M (2004) Recombinant transferrin induces nitric oxide response in goldfish and murine macrophages. Fish Shellfish Immunol 17:171–185
Stafford JL, Wilson M, Nayak D, Quiniou SM, Clem LW, Miller NW, Bengtén E (2006) Identification and characterization of a FcR homolog in an ectothermic vertebrate, the channel catfish (Ictalurus punctatus). J Immunol 177:2505–2517
Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrøm M et al (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207–210
Steine NO, Melingen GO, Wergeland HI (2001) Antibodies against Vibrio salmonicida lipopolysaccharide (LPS) and whole bacteria in sera from Atlantic salmon (Salmo salar L.) vaccinated during the smolting and early post-smolt period. Fish Shellfish Immunol 11:39–52
Stenvik J, Jørgensen TO (2000) Immunoglobulin D (IgD) of Atlantic cod has a unique structure. Immunogenetics 51:452–461
Stet RJ, Kruiswijk CP, Dixon B (2003) Major histocompatibility lineages and immune gene function in teleost fishes: the road not taken. Crit Rev Immunol 23:441–471
Stolte EH, Chadzinska M, Przybylska D, Flik G, Savelkoul HFJ, Verburg-van Kemenade BML (2009) The immune response differentially regulates Hsp70 and glucocorticoid receptor expression in vitro and in vivo in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 27:9–16
Strandskog G, Villoing S, Iliev DB, Thim HL, Christie KE, Jørgensen JB (2011) Formulations combining cpg containing oliogonucleotides and poly I:C enhance the magnitude of immune responses and protection against pancreas disease in Atlantic salmon. Dev Comp Immunol 35:1116–1127
Stuge TB, Wilson MR, Zhou H, Barker KS, Bengten E, Chinchar G et al (2000) Development and analysis of various clonal alloantigen-dependent cytotoxic cell lines from channel catfish. J Immunol 164:2971–2977
Sugamata R, Suetake H, Kikuchi K, Suzuki Y (2009) Teleost B7 expressed on monocytes regulates T cell responses. J Immunol 182:6799–6806
Sullivan C, Kim CH (2008) Zebrafish as a model for infectious disease and immune function. Fish Shellfish Immunol 25:341–350
Sumpter JP (1998) Xenoendocrine disrupters – environmental impacts. Toxicol Lett 102-103:337–342
Sumpter JP, Jobling S, Tyler CR (1996) Oestrogenic substances in the aquatic environment and their potential impact on animals, particularly fish. In: Tyler EW (ed) Toxicology of aquatic pollution: physiological, cellular and molecular approaches. Cambridge University Press, Cambridge, pp 205–224
Sunyer JO (2012) Evolutionary and functional relationships of B cells from fish and mammals: insights into their novel roles in phagocytosis and presentation of particulate antigen. Infect Disord Drug Targets 12:200–212
Sunyer JO (2013) Fishing for mammalian paradigms in the teleost immune system. Nat Immunol 14:320–326
Sunyer JO, Lambris JD (1998) Evolution and diversity of the complement system of poikilothermic vertebrates. Immunol Rev 166:39–57
Sures B, Knopf K (2004) Individual and combined effects of cadmium and3,30,4,40,5-pentachlorobiphenyl (PCB 126) on the humoral immune response in European eel (Anguilla anguilla) experimentally infected with larvae of Anguillicola crassus (Nematoda). Parasitology 128:445–454
Sures B, Lutz I, Kloas W (2006) Effects of infection with Anguillicola crassus and simultaneous exposure with Cd and 3,30,4,40,5-pentachlorobiphenyl (PCB 126) on the levels of cortisol and glucose in European eel (Anguilla anguilla). Parasitology 132:281–288
Suzuki Y, Orito M, Iigo M, Kezuka H, Kobayashi M, Aida K (1996) Seasonal changes in blood IgM levels in goldfish, with special reference to water temperature and gonadal maturation. Fish Sci 62:754–759
Suzuki Y, Otaka T, Sato S, Hou YY, Aida K (1997) Reproduction related immunoglobulin changes in rainbow trout. Fish Physiol Biochem 17:415–421
Suzumoto BK, Schreck CB, McIntyre JD (1977) Relative resistances of three transferrin genotypes of coho salmon (Onco-rhynchus kisutch) and their hematological responses to bacterial kidney disease. J Fish Res Board Can 34:1–8
Tafalla C, Novoa B, Alvarez JM, Figueras A (1999) In vivo and in vitro effect of oxytetracycline treatment on the immune response of turbot, Scophthalmus maximus (L.). J Fish Dis 22:271–276
Takahashi A, Ogasawara T, Kawauchi H, Hirano T (1990) Plasma profiles of the N-terminal peptide of proopiomelanocortin in the rainbow trout with reference to stress. Gen Comp Endocrinol 77:98–106
Takahashi A, Takasaka T, Yasuda A, Amemiya Y, Sakai M, Kawauchi H (2000) Identification of carp proopiomelanocortin-related peptides and their effects on phagocytes. Fish Shellfish Immunol 10:273–284
Takahashi M, Iwaki D, Matsushita A, Nakata M, Matsushita M, Endo Y, Fujita T (2006) Cloning and characterization of mannose-binding lectin from lamprey (Agnathans). J Immunol 176:4861–4868
Takano T, Kondo H, Hirono I, Endo M, Saito-Taki T, Aoki T (2007) Molecular cloning and characterization of Toll-like receptor 9 in Japanese flounder, Paralichthys olivaceus. Mol Immunol 44:1845–1853
Takano T, Hwang SD, Kondo H, Hirono I, Aoki T, Sano M (2010) Evidence of molecular Toll-like receptor mechanisms in teleosts. Fish Pathol 45:1–16
Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140:805–820
Takizawa F, Dijkstra JM, Kotterba P, Korytář T, Kock H, Köllner B et al (2011) The expression of CD8alpha discriminates distinct T cell subsets in teleost fish. Dev Comp Immunol 35:752–763
Takizawa F, Magadan S, Parra D, Xu Z, Korytář T, Boudinot P, Oriol Sunyer J (2016) Novel teleost CD4-bearing cell populations provide insights into the evolutionary origins and primordial roles of CD4 lymphocytes and CD4 macrophages. J Immunol 196(11):4522–4535
Tasumi S, Yang WJ, Usami T, Tsutsui S, Ohira T, Kawazoe I, Wilder MN, Aida K, Suzuki Y (2004) Characteristics and primary structure of a galectin in the skin mucus of the Japanese eel, Anguilla japonica. Dev Comp Immunol 28:325–335
Tasumi S, Yamaguchi A, Matsunaga R, Fukushi K, Suzuki Y, Nakamura O et al (2016) Identification and characterization of pufflectin from the grass pufferfish Takifugu niphobles and comparison of its expression with that of Takifugu rubripes. Dev Comp Immunol 59:48–56
Tatner MF (1996) Natural changes in the immune system of fish. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, San Diego, pp 255–287
Toda H, Shibasaki Y, Koike T, Ohtani M, Takizawa F, Ototake M, Moritomo T, Nakanishi T (2009) Allo-antigen specific killing is mediated by CD8 positive T cells in fish. Dev Comp Immunol 33:646–652
Toda H, Araki K, Moritomo T, Nakanishi T (2011a) Perforin-dependent cytotoxic mechanism in killing by CD8 positive T cells in Ginbuna crucian carp, Carassius auratus langsdorfii. Dev Comp Immunol 35:88–93
Toda H, Saito Y, Koike T, Takizawa F, Araki K, Yabu T, Somamoto T et al (2011b) Conservation of characteristics and functions of CD4 positive lymphocytes in a teleost fish. Dev Comp Immunol 35:650–660
Tosi MF (2005) Innate immune responses to infection. J Allergy Clin Immunol 116:241–249
Trede NS, Langenau DM, Traver D, Look AT, Zon LI (2004) The use of zebrafish to understand immunity. Immunity 20:367–379
Trites MJ, Barreda DR (2017) Contributions of transferrin to acute inflammation in the goldfish, C. auratus. Dev Comp Immunol 67:300–309
Tsujita T, Tsukada H, Nakao M, Oshiumi H, Matsumoto M, Seya T (2004) Sensing bacterial flagellin by membrane and soluble orthologs of Toll-like receptor 5 in rainbow trout (Onchorhynchus mikiss). J Biol Chem 279:48588–48597
Turnbell AV, Rivier C (1999) Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev 79:1–71
Unajak S, Santos MD, Hikima J, Jung TS, Kondo H, Hirono I, Aoki T (2011) Molecular characterization, expression and functional analysis of a nuclear oligomerization domain proteins subfamily C (NLRC) in Japanese flounder (Paralichthys olivaceus). Fish Shellfish Immunol 31:202–211
Unniappan S, Peter RE (2005) Structure, distribution and physiological functions of ghrelin in fish. Comp Biochem Physiol 140A:396–408
Uribe E, Steele TJ, Richards RC, Ewart KV (2013) Ligand and pathogen specificity of the Atlantic salmon serum C-type lectin. Biochim Biophys Acta 1830:2129–2138
Utke K, Bergmann S, Lorenzen N, Kollner B, Ototake M, Fischer U (2007) Cell-mediated cytotoxicity in rainbow trout, Oncorhynchus mykiss, infected with viral haemorrhagic septicaemia virus. Fish Shellfish Immunol 22:182–196
van der Marel M, Adamek M, Gonzalez SF, Frost P, Rombout JH, Wiegertjes GF et al (2012) Molecular cloning and expression of two β-defensin and two mucin genes in common carp (Cyprinus carpio L.) and their up-regulation after β-glucan feeding. Fish Shellfish Immunol 32:494–501
van der Sar AM, Appelmelk BJ, Vandenbroucke-Grauls CM, Bitter W (2004) A star with stripes: zebrafish as an infection model. Trends Microbiol 12:451–457
Varma M, Jain S (2016) Immunotoxicity of cadmium in fishes: a review. Adv Pharmacol Toxicol 17:1–8
Vasta GR, Ahmed H, Du S, Henrikson D (2004) Galectins in teleost fish: Zebrafish (Danio rerio) as a model species to address their biological roles in development and innate immunity. Glycoconj J 21:503–521
Venters HD, Dantzer R, Freund GG, Broussard SR, Kelley KW (2001) Growth hormone and insulin-like growth factor as cytokines in the immune system. In: Ader R, Felten DL, Cohen N (eds) Psychoneuroimmunology, vol 1, 3rd edn. Academic Press, San Diego, pp 339–362
Verburg-van Kemenade BM, Stolte EH, Metz JR, Chadzinska M (2009) Neuroendocrine-immune interactions in teleost fish. In: Bernier NJ, Van Der Kraak G, Farrell AP, Brauner CJ (eds) Fish neuroendocrinology. Academic Press, San Diego, pp 313–364
Verrier ER, Langevin C, Benmansour A, Boudinot P (2011) Early antiviral response and virus-induced genes in fish. Dev Comp Immunol 35:1204–1214
Villarroel F, Bastías A, Casado A, Amthauer R, Concha MI (2007) Apolipoprotein A-I, an antimicrobial protein in Oncorhynchus mykiss: evaluation of its expression in primary defence barriers and plasma levels in sick and healthy fish. Fish Shellfish Immunol 23:197–209
Vitved L, Holmskov U, Koch C, Teisner B, Hansen S, Salomonsen J, Skjødt K (2000) The homologue of mannose-binding lectin in the carp family Cyprinidae is expressed athigh level in spleen, and the deduced primary structure predicts affinity for galactose. Immunogenetics 51:955–964
von Ginneken V, Bruijs M, Murk T, Palstra A, van den Thillart G (2009) The effect of PCBs on the spawning migration of European silver eel (Anguilla anguilla L.). In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European eel. Springer, Dordrecht, pp 365–386
Wang T, Secombes CJ (2009) Identification and expression analysis of two fish-specific IL-6 cytokine family members, the ciliary neurotrophic factor (CNTF)-like and M17 genes, in rainbow trout Oncorhynchus mykiss. Mol Immunol 46:2290–2298
Wang HJ, Xiang LX, Shao JZ, Jia S (2006) Molecular cloning, characterization and expression analysis of an IL-21 homologue in Tetraodon nigroviridis. Cytokine 35:126–134
Wang T, Martin SA, Secombes CJ (2010) Two interleukin-17C-like genes exist in rainbow trout Oncorhynchus mykiss that are differentially expressed and modulated. Dev Comp Immunol 34:491–500
Wang T, Diaz-Rosales P, Costa MM, Campbell S, Snow M, Collet B, Martin SAM, Secombes CJ (2011) Functional characterisation of a non-mammalian IL-21: rainbow trout Oncorhynchus mykiss IL-21 up-regulates the expression of the Th cell signature cytokines interferon-γ, IL-10 and IL-22. J Immunol 186:708–721
Wang T, Jiang Y, Wang A, Husain M, Xu Q, Secombes CJ (2015) Identification of the salmonid IL-17A/F1a/b, IL-17A/F2b, IL-17A/F3 and IL-17N genes and analysis of their expression following in vitro stimulation and infection. Immunogenetics 67:395–412
Wedemeyer GA (1997) Effects of rearing conditions on the health and physiological quality of fish in intensive culture. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 35–71
Wen Y, Fang W, Xiang LX, Pan RL, Shao JZ (2011) Identification of Treg-like cells in Tetraodon: insight into the origin of regulatory T subsets during early vertebrate evolution. Cell Mol Life Sci 68:2615–2626
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77(3):591–625
Weyts FAA, Cohen N, Flik G, Verburg-Van Kemenade BML (1999) Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 9:1–20
Whang I, Lee Y, Lee S, Oh MJ, Jung SJ, Choi CY, Lee WS, Kim HS, Kim SJ, Lee J (2011) Characterization and expression analysis of a goose-type lysozyme from the rock bream Oplegnathus fasciatus, and antimicrobial activity of its recombinant protein. Fish Shellfish Immunol 30:532–542
Wick G (1994) Ageing of the immune response. Dev Comp Immunol 18:591
Wiens GD, Glenney GW (2011) Origin and evolution of TNF and TNF receptor superfamilies. Dev Comp Immunol 35:1324–1335
Wilder RL (1995) Neuroendocrine-immune system interactions and autoimmunity. Annu Rev Immunol 13:307–338
Wilmanski JM, Petnicki-Ocwieja T, Kobayashi KS (2008) NLR proteins: integral members of innate immunity and mediators of inflammatory diseases. J Leukoc Biol 83:13–30
Wilson JM (2014) Stress physiology. In: Trischitta F, Takei Y, Sébert P (eds) Eel physiology. CRC Press, Boca Raton, pp 318–358
Wilson M, Hsu E, Marcuz A, Courtet M, du Pasquier L, Steinberg C (1992) What limits affinity maturation of antibodies in Xenopus—the rate of somatic mutation or the ability to select mutants? EMBO J 11:4337–4347
Winter GW, Schreck CB, Mcintyre JD (1980) Resistance of different stocks and transferrin genotypes of coho salmon, Oncorhynchus kisutch, and steelhead trout, Salmo gairdneri, to bacterial kidney disease and vibriosis1. Fish Bull 77:795–802
Withler RE, Evelyn TPT (1990) Genetic variation in resistance to bacterial kidney disease \m'thin and between two strains of coho salmon from British Columbia. Trans Am Fish Soc 119:1003–1009
Wittamer V, Bertrand JY, Gutschow PW, Traver D (2011) Characterization of the mononuclear phagocyte system in zebrafish. Blood 117:7126–7135
Wu XM, Hu YW, Xue NN, Ren SS, Chen SN, Nie P, Chang MX (2017) Role of zebrafish NLRC5 in antiviral response and transcriptional regulation of MHC related genes. Dev Comp Immunol 68:58–68
Xiang J, Li X, Chen Y, Lu Y, Yu M, Chen X, Zhang W, Zeng Y, Sun L, Chen S, Sha Z (2015) Complement factor I from flatfish half-smooth tongue (Cynoglossus semilaevis) exhibited anti-microbial activities. Dev Comp Immunol 53:199–209
Xie J, Belosevic M (2018) Characterization and functional assessment of the NLRC3-like molecule of the goldfish (Carassius auratus L.). Dev Comp Immunol 79:1–10
Yada T (2009) Effects of insulin-like growth factor-I on non-specific immune functions in rainbow trout. Zool Sci 26:338–343
Yada T (2012) Effect of gonadotropin-releasing hormone on phagocytic leucocytes of rainbow trout. Comp Biochem Physiol 155C:375–380
Yada T, Nakanishi T (2002) Interaction between endocrine and immune systems in fish. Int Rev Cytol 220:35–92
Yada T, Tort L (2016) Stress and disease resistance: immune system and immunoendocrine interactions. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Biology of stress in fish. Academic Press, San Diego, pp 365–403
Yada T, Nagae M, Moriyama S, Azuma T (1999) Effect of prolactin and growth hormone on plasma immunoglobulin M levels of hypophysectomized rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 115:46–52
Yada T, Azuma T, Takagi Y (2001) Stimulation of non-specific immune functions in seawater-adapted rainbow trout, Oncorhynchus mykiss, with reference to the role of growth hormone. Comp Biochem Physiol 129B:695–701
Yada T, Uchida K, Kajimura S, Azuma T, Hirano T, Grau EG (2002) Immunomodulatory effects of prolactin and growth hormone in the tilapia, Oreochromis mossambicus. J Endocrinol 173:483–492
Yada T, Misumi I, Muto K, Azuma T, Schreck CB (2004) Effects of prolactin and growth hormone on proliferation and survival of cultured trout leucocytes. Gen Comp Endocrinol 136:298–306
Yada T, Kaiya H, Mutoh K, Azuma T, Hyodo S, Kangawa K (2006a) Ghrelin stimulates phagocytosis and superoxide production in fish leucocytes. J Endocrinol 189:57–65
Yada T, Muto K, Azuma T, Fukamachi S, Kaneko T, Hirano T (2006b) Effects of acid water exposure on plasma cortisol, ion balance and immune functions in the“cobalt” variant of rainbow trout. Zool Sci 23:707–713
Yada T, McCormick SD, Hyodo S (2012) Effects of environmental salinity, biopsy, and GH and IGF-I administration on the expression of immune and osmoregulatory genes in the gills of Atlantic salmon (Salmo salar). Aquaculture 362–363:177–183
Yada T, Mekuchi M, Ojima N (2018) Molecular biology and functional genomics of immune-endocrine interactions in the Japanese eel, Anguilla japonica. Gen Comp Endocrinol. 257:272-279
Yamaguchi N, Teshima C, Kurashige S, Saito R, Mitsuhashi S (1980) Seasonal modulation of antibody formation in rainbow trout, Salmo gairdneri. In: Solomon JB (ed) Aspects of developmental and comparative immunology, vol 1. Pergamon Press, Oxford, pp 483–484
Yamaguchi T, Katakura F, Someya K, Dijkstra JM, Moritomo T, Nakanishi T (2013) Clonal growth of carp (Cyprinus carpio) T cells in vitro: long-term proliferation of Th2-like cells. Fish Shellfish Immunol 34:433–442
Yamasaki M, Araki K, Nakanishi T, Nakayasu C, Yoshiura Y et al (2013) Adaptive immune response to Edwardsiella tarda infection in ginbuna crucian carp, Carassius auratus langsdorfii. Vet Immunol Immunopathol 153:83–90
Yamasaki M, Araki K, Nakanishi T, Nakayasu C, Yamamoto A (2014) Role of cd4(+) and cd8 alpha (+) t cells in protective immunity against Edwardsiella tarda infection of ginbuna crucian carp, Carassius auratus langsdorfii. Fish Shellfish Immunol 36:299–304
Yang M, Qiu W, Chen B, Chen J, Liu S, Wu M, Wang K-J (2015) The in vitro immune modulatory effect of bisphenol a on fish macrophages via estrogen receptor α and nuclear factor-κB signaling. Environ Sci Technol 49:1888–1895
Yang Q, Sun Y, Su X, Li T, Xu T (2016) Characterization of six IL-17 family genes in miiuy croaker and evolution analysis of vertebrate IL-17 family. Fish Shellfish Immunol 49:243–251
Yang S, Tang X, Sheng X, Xing J, Zhan W (2017) Development of monoclonal antibodies against IgM of half-smooth tongue sole (Cynoglossus semilaevis) and analysis of phagocytosis of fluorescence microspheres by mIgM+ lymphocytes. Fish Shellfish Immunol 66:280–288
Yano T (1995) The complement systems of fish. Fish Pathol 302:151–158
Yano Y (1996) The non-specific immune system: humoral defense. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, San Diego, pp 105–157
Yazawa R, Hirono I, Aoki T (2006) Transgenic zebrafish expressing chicken lysozyme show resistance against bacterial diseases. Transgenic Res 15:385–391
Ye X, Zhang L, Tian Y, Tan A, Bai J, Li S (2010) Identification and expression analysis of the g-type and c-type lysozymes in grass carp Ctenopharyngodon idellus. Dev Comp Immunol 34:501–509
Ye J, Bromage E, Kaattari I, Kaattari I (2011) Transduction of binding affinity by B lymphocytes: a new dimension in immunological regulation. Dev Comp Immunol 35:982–990
Ye J, Kaattari IM, Ma C, Kaattari S (2013) The teleost humoral immune response. Fish Shellfish Immunol 35:1719–1728
Yeh DW, Liu YL, Lo YC, Yuh CH, Yu GY, Lo JF, Luo Y, Xiang R, Chuang TH (2013) Toll-like receptor 9 and 21 have different ligand recognition profiles and cooperatively mediate activity of CpG-oligodeoxynucleotides in zebrafish. Proc Natl Acad Sci U S A 110:20711–20716
Yin ZX, He JG, Deng WX, Chan SM (2003) Molecular cloning, expression of orange-spotted grouper goose-type lysozyme cDNA, and lytic activity of its recombinant protein. Dis Aquat Org 55:117–123
Yin D-Q, Hu S-Q, Gu Y, Wei L, Liu S-S, Zhang A-Q (2007) Immunotoxicity of bisphenol A to Carassius auratus lymphocytes and macrophages following in vitro exposure. J Environ Sci 19:232–237
Yoon S, Mitra S, Wyse C, Alnabulsi A, Zou J, Weerdenburg EM, van der Sar AM, Wang D, Secombes CJ, Bird S, Fischer U (2015) First demonstration of antigen induced cytokine expression by CD4-1+ lymphocytes in a poikilotherm: studies in zebrafish (Danio rerio). PLoS One 10(6):e0126378
Yoshiura Y, Kiryu I, Fujiwara A, Suetake H, Suzuki Y, Nakanishi T, Ototake M (2003) Identification and characterization of Fugu orthologues of mammalian interleukin-12 subunits. Immunogenetics 55:296–306
Yousif AN, Albright LJ, Evelyn TPT (1994a) In vitro evidence for the antibacterial role of lysozyme in salmonid eggs. Dis Aquat Org 19:15–19
Yousif AN, Albright LJ, Evelyn TPT (1994b) Purification and characterization of a galactose-specific lectin from the eggs of coho salmon Oncorhynchus kisutch and its interaction with bacterial fish pathogens. Dis Aquat Org 20:127–136
Yu Y, Huang Y, Yang Y, Wang S, Yang M, Huang X, Qin Q (2016) Negative regulation of the antiviral response by grouper LGP2 against fish viruses. Fish Shellfish Immunol 56:358–366
Zapata AG, Chiba A, Varas A (1996) Cells and tissues of the immune system of fish. In: Iwama G, Nakanishi K (eds) The fish immune system: organism, pathogen and environment. Academic Press, San Diego, pp 1–62
Zelensky AN, Gready JE (2004) C-type lectin-like domains in Fugu rubripes. BMC Genomics 5:51
Zhang YA, Salinas I, Li J, Parra D, Bjork S, Xu Z, LaPatra SE, Bartholomew J, Sunyer JO (2010) IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol 11:827–835
Zhang YA, Salinas I, Sunyer JO (2011) Recent findings on the structure and function of teleost IgT. Fish Shellfish Immunol 31:627–634
Zhang QM, Zhao X, Li Z, Wu M, Gui JF, Zhang YB (2017a) Alternative splicing transcripts of Zebrafish LGP2 gene differentially contribute to IFN antiviral response. J Immunol. In press. https://doi.org/10.4049/jimmunol.1701388
Zhang XJ, Wang P, Zhang N, Chen DD, Nie P, Li JL, Zhang YA (2017b) B cell functions can be modulated by antimicrobial peptides in rainbow trout Oncorhynchus mykiss: novel insights into the innate nature of B cells in fish. Front Immunol 8:388
Zheng W, Tian C, Chen X (2007) Molecular characterization of goose-type lysozyme homologue of large yellow croaker and its involvement in immune response induced by trivalent bacterial vaccine as an acute-phase protein. Immunol Lett 113:107–116
Zhou H, Stuge TB, Miller NW, Bengten E, Naftel JP, Bernanke JM, Chinchar VG et al (2001) Heterogeneity of channel catfish CTL with respect to target recognition and cytotoxic mechanisms employed. J Immunol 167:1325–1332
Zhu LY, Lin AF, Shao T, Nie L, Dong WR, Xiang LX, Shao JZ (2014) B cells in teleost fish act as pivotal initiating APCs in priming adaptive immunity: an evolutionary perspective on the origin of the B-1 cell subset and B7 molecules. J Immunol 192:2699–2714
Zimmerman LM, Vogel LA, Edwards KA, Bowden RM (2010) Phagocytic B cells in a reptile. Biol Lett 6:270–273
Zoccola E, Delamare-Deboutteville J, Barnes AC (2015) Identification of barramundi (Lates calcarifer) DC-SCRIPT, a specific molecular marker for dendritic cells in fish. PLoS One 10:e0132687
Zou J, Secombes CJ (2016) The function of fish cytokines. Biology (Basel) 5(2):E23
Zou J, Yoshiura Y, Dijkstra JM, Sakai M, Ototake M, Secombes CJ (2004a) Identification of an interferon gamma homologue in Fugu, Takifugu rubripes. Fish Shellfish Immunol 17:403–409
Zou J, Bird S, Truckle J, Bols N, Horne M, Secombes CJ (2004b) Identification and expression analysis of an IL-18 homologue and its alternatively spliced form in rainbow trout Oncorhynchus mykiss. Eur J Biochem 271:1913–1923
Zou J, Mercier C, Koussounadis A, Secombes C (2007a) Discovery of multiple beta-defensin like homologues in teleost fish. Mol Immunol 44:638–647
Zou J, Tafalla C, Truckle J, Secombes CJ (2007b) Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol 179:3859–3871
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Nakanishi, T., Hikima, Ji., Yada, T. (2018). Osteichthyes: Immune Systems of Teleosts (Actinopterygii). In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_19
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