Advertisement

Ecotoxicology

, Volume 20, Issue 2, pp 305–319 | Cite as

The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review

  • Sylvain Milla
  • Sophie Depiereux
  • Patrick Kestemont
Article

Abstract

During the last decade, a number of studies have shown that, in addition to their classically described reproductive function, estrogens and androgens also regulate the immune system in teleosts. Today, several molecules are known to interfere with the sex-steroid signaling. These chemicals are often referred to as endocrine disrupting contaminants (EDCs). We review the growing evidence that these compounds interfere with the fish immune system. These studies encompass a broad range of approaches from field studies to those at the molecular level. This integrative overview improves our understanding of the various endocrine-disrupting processes triggered by these chemicals. Furthermore, the research also explains why fish that have been exposed to EDCs are more sensitive to pathogens during gametogenesis. In this review, we first discuss the primary actions of sex-steroid-like endocrine disruptors in fish and the specificity of the fish immune system in comparison to mammals. Then, we review the known interactions between the immune system and EDCs and interpret the primary effects of sex steroids (estrogens and androgens) and their related endocrine disruptors on immune modulation. The recent literature suggests that immune parameters may be used as biomarkers of contamination by EDCs. However, caution should be used in the assessment of such immunotoxicity. In particular, more attention should be paid to the specificity of these biomarkers, the external/internal factors influencing the response, and the transduction pathways induced by these molecules in fish. The use of the well-known mammalian models provides a useful guide for future research in fish.

Keywords

Fish Immunity Endocrine disruptors Sex-steroids 

Notes

Acknowledgments

S.M. was supported by the Belgian National Funds for Scientific Research (FNRS), contract 2. 4570. 06.

References

  1. Aluru N, Jorgensen EH, Maule AG, Vijayan MM (2004) PCB disruption of the hypothalamus-pituitary-interrenal axis involves brain glucocorticoid receptor downregulation in anadromous Arctic charr. Am J Physiol Regul Integr Comp Physiol 287:R787–R793Google Scholar
  2. Ankley GT, Jensen KM, Makynen EA, Kahl MD, Korte JJ, Hornung MW, Henry TR, Denny JS, Leino RL, Wilson VS, Cardon MC, Hartig PC, Earl Gray L (2003) Effects of the androgenic growth promoter 17-β-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environ Toxicol Chem 22:1350–1360CrossRefGoogle Scholar
  3. Ankley GT, Defoe DL, Kahl MD, Jensen KM, Makynen EA, Miracle A, Hartig P, Gray LE, Cardon M, Wilson V (2004) Evaluation of the model anti-androgen flutamide for assessing the mechanistic basis of responses to an androgen in the fathead minnow (Pimephales promelas). Environ Sci Technol 38:6322–6327CrossRefGoogle Scholar
  4. Ankley GT, Jensen KM, Durhan EJ, Makynen EA, Butterworth BC, Kahl MD, Villeneuve DL, Linnum A, Gray LE, Cardon M, Wilson VS (2005) Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fathead minnow (Pimephales promelas). Toxicol Sci 86:300–308CrossRefGoogle Scholar
  5. Aoki T, Takano T, Santos MD, Kondo H, Hirono I (2008) Molecular innate immunity in teleost fish: review and future perspectives. In: Tsukamoto K, Kawamura T, Takeuchi T, Beard Jr. TD, Kaiser MJ (Eds) Fisheries for global welfare and environment. 5th World Fisheries Congress 263–276Google Scholar
  6. Arukwe A (2001) Cellular and molecular responses to endocrine-modulators and the impact on fish reproduction. Mar Pollut Bull 42:643–655CrossRefGoogle Scholar
  7. Baldwin WS, Roling JA, Peterson S, Chapman LM (2005) Effects of nonylphenol on hepatic testosterone metabolism and the expression of acute phase proteins in winter flounder (Pleuronectes americanus): comparison to the effects of Saint John’s Wort. Comp Biochem Physiol C Toxicol Pharmacol 140:87–96CrossRefGoogle Scholar
  8. Baron D, Houlgatte R, Fostier A, Guiguen Y (2008) Expression profiling of candidate genes during ovary-to-testis trans-differenciation in rainbow trout masculinized by androgens. Gen Comp Endocrinol 156:369–378CrossRefGoogle Scholar
  9. Benninghoff AD, Williams DE (2008) Identification of a transcriptional fingerprint of estrogen exposure in rainbow trout liver. Toxicol Sci 101:65–80CrossRefGoogle Scholar
  10. Binuramesh C, Prabakaran M, Steinhagen D, Dinakaran M (2006) Effect of sex ratio on the immune system of Oreochromis mossambicus (Peters). Brain behav immun 20:300–308CrossRefGoogle Scholar
  11. Bols NC, Brubacher JL, Ganassin RC, Lee LEJ (2001) Ecotoxicology and innate immunity in fish. Dev Comp Immunol 25:853–873CrossRefGoogle Scholar
  12. Bowden TJ, Thompson KD, Morgan AL, Gratacap RML, Nikoskelainen S (2007) Seasonal variation and the immune response: a fish perspective. Fish Shellfish Immunol 22:695–706CrossRefGoogle Scholar
  13. Browser PR, Munson AD (1986) Seasonal variation in channel catfish virus antibody titers in adult channel catfish. Progress Fish Cult 48:198–199CrossRefGoogle Scholar
  14. Chaves-Pozo E, Liarte S, Fernández-Alacid L, Abellán E, Meseguer J, Mulero V, García-Ayala A (2008) Pattern of expression of immune-relevant genes in the gonad of a teleost, the gilthead seabream (Sparus aurata L.). Mol Immunol 45:2998–3011CrossRefGoogle Scholar
  15. Cheshenko K, Pakdel F, Segner H, Kah O, Eggen RI (2008) Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity, and consequences for reproduction of teleost fish. Gen Comp Endocrinol 155:31–62CrossRefGoogle Scholar
  16. Christiansen LB, Pedersen KL, Korsgaard B, Bjerregaard P (1998) Estrogenicity of xenobiotics in rainbow trout (Oncorhynchus mykiss) using in vivo synthesis of vitellogenin as a biomarker. Marine Environ Res 46:137–140CrossRefGoogle Scholar
  17. Cook J (1994) The effects of stress, background colour and steroid hormones on the lymphocytes of rainbow trout (Oncorhynchus mykiss). Ph.D. Thesis, University of SheffieldGoogle Scholar
  18. Cosnefroy A, Brion F, Guillet B, Laville N, Porcher JM, Balaguer P, Aït-Aïssa S (2009) A stable fish reporter cell line to study estrogen receptor transactivation by environmental (xeno)estrogens. Toxicol In Vitro 23:1450–1454CrossRefGoogle Scholar
  19. Craig PM, Hogstrand C, Wood CM, McClelland GB (2009) Gene expression endpoints following chronic waterborne copper exposure in a genomic model organism, the zebrafish, Danio rerio. Physiol Genomics 40:23–33CrossRefGoogle Scholar
  20. Cuesta A, Vargas-Chacoff L, García-López A, Arjona FJ, Martínez-Rodríguez G, Meseguer J, Mancera JM, Esteban MA (2007) Effect of sex-steroid hormones, testosterone and estradiol, on humoral immune parameters of gilthead seabream. Fish Shellfish Immunol 23:693–700CrossRefGoogle Scholar
  21. Cuesta A, Meseguer J, Esteban MA (2008) Effects of the organochlorines p, p′-DDE and lindane on gilthead seabream leucocyte immune parameters and gene expression. Fish Shellfish Immunol 25:682–688CrossRefGoogle Scholar
  22. Cutolo M, Sulli A, Capellino S, Villagio B, Montagna P, Seriolo B, Straub RH (2004) Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus 13:635–638CrossRefGoogle Scholar
  23. Cutolo M, Capellino S, Montagna P, Ghiorzo P, Sulli A, Villagio B (2005) Sex hormone modulation of cell growth and apoptosis of the human monocytic/macrophage cell line. Arthritis Res Ther 7:1124–1132CrossRefGoogle Scholar
  24. Cutolo M, Capellino S, Sulli A, Serioli A, Secchi ME, Villaggio B, Straub RH (2006) Estrogens and autoimmune diseases. Ann NY Acad Sci 1089:538–545CrossRefGoogle Scholar
  25. Cutolo M, Montagna P, Brizzolara R, Sulli A, Seriolo B, Villagio B, Triolo P, Clerico P, Soldano S (2009) Sex hormones modulate the effects of leflunomide on cytokine production by cultures of differentiated monocyte/macrophages and synovial macrophages from rheumatoid arthritis patients. J Autoimmunity 32:254–260CrossRefGoogle Scholar
  26. Deane EE, Li J, Woo NY (2001) Hormonal status and phagocytic activity in sea bream infected with vibriosis. Comp Biochem Physiol B Mol Biol 129:687–693CrossRefGoogle Scholar
  27. Dorts J, Catherine A, Wright-Osment MK, Richter CA, Ellersieck MR, Carter BJ, Tillitt DE (2009) The genomic transcriptional response of female fathead minnows (Pimephales promelas) to an acute exposure to the androgen, 17beta-trenbolone. Aquat Toxicol 91:44–53CrossRefGoogle Scholar
  28. Duffy E, Carlson EA, Li Y, Prophete C, Zelikoff JT (2003) Age-related differences in the sensitivity of the fish immune response to a coplanar PCB. Ecotoxicology 12:251–259CrossRefGoogle Scholar
  29. Dunier M, Siwicki K (1993) Effects of pesticides and other organic pollutants in the aquatic environment on immunity of fish: a review. Fish Shellfish Immunol 8:423–438CrossRefGoogle Scholar
  30. Erlandsson MC, Ohlsson C, Gustafsson JA, Carlsten H (2001) Role of estrogen receptors alpha and beta in immune organ development and in estrogen-mediated effects on thymus. Immunology 103:17–25CrossRefGoogle Scholar
  31. Esteban A, Rodriguez A, Ayala AG, Meseguer J (2004) Effects of high doses of cortisol on innate cellular immune response of seabream (Sparus aurata L.). Gen Comp Endocrinol 137:89–98CrossRefGoogle Scholar
  32. Falk HF, Negele RD, Goerlich R (1990) Phagocytosis activity as an in vitro test for the effects of chronic exposure of rainbow trout to Linuron, a herbicide. J Appl Ichthyol 6:231–236CrossRefGoogle Scholar
  33. Farkas I, Varju P, Szabo E, Hrabovszky E, Okada N, Okada H, Liposits Z (2008) Estrogen enhances expression of the complement C5a receptor and the C5a-agonist evoked calcium influx in hormone secreting neurons of the hypothalamus. Neurochem Int 52:846–856CrossRefGoogle Scholar
  34. Fenske M, van Aerle R, Brack S, Tyler CR, Segner H (2001) Development and validation of a homologous zebrafish (Danio rerio) vitellogenin enzyme-linked immunosorbent assay (ELISA) and its application for studies on estrogenic chemicals. Comp Biochem Physiol C Toxicol Pharmacol 129:217–232CrossRefGoogle Scholar
  35. Fent K, Escher C, Caminada D (2006) Estrogenic activity of pharmaceuticals and pharmaceutical mixtures in a yeast reporter gene system. Reprod Toxicol 22:175–185CrossRefGoogle Scholar
  36. Filby AL, Thorpe KL, Maack G, Tyler CR (2007) Gene expression profiles revealing the mechanisms of anti-androgen- and estrogen-induced feminization in fish. Aquat Toxicol 81:219–231CrossRefGoogle Scholar
  37. Flores-Valverde AM, Horwood J, Hill EM (2010) Disruption of the steroid metabolome in fish caused by exposure to the environmental estrogen 17alpha-ethinylestradiol. Environ Sci Technol 44:3552–3558CrossRefGoogle Scholar
  38. Folmar LC, Hemmer MJ, Denslow ND, Kroll K, Chen J, Cheek A, Richman H, Meredith H, Grau EG (2002) A comparison of the estrogenic potencies of estradiol, ethynylestradiol, diethylstilbestrol, nonylphenol and methoxychlor in vivo and in vitro. Aquat Toxicol 60:101–110CrossRefGoogle Scholar
  39. Folomeev M, Dougados M, Beaune J, Kouyoumdjian JC, Nahoul K, Amor B, Alekberova Z (1992) Plasma sex hormones and aromatase activity in tissues of patients with systemic lupus erythematosus. Lupus 1:191–195CrossRefGoogle Scholar
  40. Förlin L, Anderson T (1984) Influence of biological and environmental factors on hepatic steroid and xenobiotic metabolism in fish: interaction with PCB and ß-naphtoflavone. Marine Environ Res 14:47–58CrossRefGoogle Scholar
  41. Garcia-Reyero N, Villeneuve DL, Kroll KJ, Liu L, Orlando EF, Watanabe KH, Sepúlveda MS, Ankley GT, Denslow ND (2009) Expression signatures for a model androgen and antiandrogen in the fathead minnow (Pimephales promelas) ovary. Environ Sci Technol 43:2614–2619CrossRefGoogle Scholar
  42. Grinwis GCM, Wester PW, Vethaak AD (2009) Histopathological effects of chronic aqueous exposure to bis(tri-n-butyltin)oxide (TBTO) to environmentally relevant concentrations reveal thymus atrophy in European flounder (Platichthys flesus). Environ Pollut 157:2587–2593CrossRefGoogle Scholar
  43. Gushiken Y, Watanuki H, Sakai M (2002) In vitro effect of carp phagocytic cells by bisphenol A and nonylphenol. Fish Sci 68:178–183CrossRefGoogle Scholar
  44. Harford AJ, O’Halloran K, Wright PFA (2005) The effects of in vitro pesticide exposures on the phagocytic function of four native Australian freshwater fish. Aquat Toxicol 75:330–342CrossRefGoogle Scholar
  45. Harford AJ, O’Halloran K, Wright PE (2007) Effect of in vitro and in vivo organotin exposures on the immune functions of murray cod (Maccullochella peelii peelii). Environ Toxicol Chem 26:1649–1656CrossRefGoogle Scholar
  46. Heppell SA, Denslow ND, Folmar LC, Sullivan CV (1995) Universal assay of vitellogenin as a biomarker for environmental estrogens. Environ Health Perspect 103:9–15CrossRefGoogle Scholar
  47. Hill EM, Evans KL, Horwood J, Rostkowski P, Olapado FO, Gibson R, Shears JA, Tyler JC (2010) Profiles and some initial identification of (anti)androgenic compounds in fish exposed to wastewater treatment works effluents. Environ Sci Technol 44:1137–1143CrossRefGoogle Scholar
  48. Hossain MS, Larsson A, Scherbak N, Olsson PE, Orban L (2008) Zebrafish androgen receptor: isolation, molecular, and biochemical characterization. Biol Reprod 78:361–369CrossRefGoogle Scholar
  49. Hou Y, Han XD (2001) Effects of estradiol-17beta on immunocompetence in rainbow trout. Acta Zool Sin 47:285–291Google Scholar
  50. Hou Y, Suzuki Y, Aida K (1999a) Effects of steroids on the antibody producing activity of lymphocytes in rainbow trout. Fish Sci 65:850–855Google Scholar
  51. Hou Y, Suzuki Y, Aida K (1999b) Changes in immunoglobulin producing cells in response to gonadal maturation in rainbow trout. Fish Sci 65:844–849Google Scholar
  52. Hou Y, Suzuki Y, Aida K (1999c) Effects of steroid hormones on immunoglobulin M (IgM) in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 20:155–162CrossRefGoogle Scholar
  53. Islander U, Erlandsson MC, Hasséus B, Jonsson CA, Ohlsson C, Gustafsson JA, Dahlgren U, Carlsten H (2003) Influence of oestrogen receptor alpha and beta on the immune system in aged female mice. Immunology 110:149–157CrossRefGoogle Scholar
  54. Iwanowicz LR, Blazer VS, McCormick SD, Vanveld PA, Ottinger CA (2009) Aroclor 1248 exposure leads to immunomodulation, decreased disease resistance and endocrine disruption in the brown bullhead, Ameiurus nebulosus. Aquat Toxicol 93:70–82CrossRefGoogle Scholar
  55. Janele D, Lang T, Capellino S (2006) Effects of testosterone, 17-beta estradiol, and downstream estrogens on cytokine secretion from human leukocytes in the presence and absence of cortisol. Ann NY Acad Sci 1069:168–182CrossRefGoogle Scholar
  56. Jin Y, Chen R, Sun L, Liu W, Fu Z (2009) Photoperiod and temperature influence endocrine disruptive chemical-mediated effects in male adult zebrafish. Aquat Toxicol 92:38–43CrossRefGoogle Scholar
  57. Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP (1998) Widespread sexual disruption in wild fish. Environ Sci Technol 32:2498–2506CrossRefGoogle Scholar
  58. Katsiadaki I, Scott AP, Hurst MR, Matthiessen P, Mayer I (2002) Detection of environmental Androgens: a novel method based on Enzyme-Linked Immunosorbent Assay of spiggin, the Stickleback (Gasterosteus Aculeatus) glue protein. Environ Toxicol Chem 21:1946–1954Google Scholar
  59. Katsiadaki I, Morris S, Squires C, Hurst MR, James JD, Scott AP (2006) Use of the Three-Spined Stickleback (Gasterosteus aculeatus) as a sensitive in vivo test for detection of Environmental Antiandrogens. Environ Health Perspect 114:115–121CrossRefGoogle Scholar
  60. Kausch U, Alberti M, Haind S, Budczies J, Hock B (2008) Biomarkers for exposure to estrogenic compounds: gene expression analysis in Zebrafish (Danio rerio). Environ Toxicol 23:15–24CrossRefGoogle Scholar
  61. Kawano H, Kono T, Watanuki H, Savan R, Sakai M (2003) Analysis of genes expressed in head kidney of common carp Cyprinus carpio L. treated with cortisol. Comp Biochem Physiol B 136:875–886CrossRefGoogle Scholar
  62. Kloas W, Urbatzka R, Opitz R, Würtz S, Behrends T, Hermelink B, Hofmann F, Jagnytsch O, Kroupova H, Lorenz C, Neumann N, Pietsch C, Trubiroha A, Van Ballegooy C, Wiedemann C, Lutz I (2009) Endocrine disruption in aquatic vertebrates. Ann N Y Acad Sci 1163:187–200CrossRefGoogle Scholar
  63. Knudsen FR, Pottinger TG (1999) Interaction of endocrine disrupting chemical, singly and combination, with estrogen-, androgen-, and corticosteroid-binding sites in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 44:159–170CrossRefGoogle Scholar
  64. Korter R, Vainikka A (2008) Seasonality of innate immunity; evolutionary aspects and latest updates. In: Durand M, Morel CV (eds) New research on innate immunity. Nova Science Publishers, New York, pp 13–45Google Scholar
  65. Kortner TM, Rocha E, Arukwe A (2009) Previtellogenic oocyte growth and transcriptional changes of steroidogenic enzyme genes in immature female Atlantic cod (Gadus morhua L.) after exposure to the androgens 11-ketotestosterone and testosterone. Comp Biochem Physiol A Mol Integr Physiol 152:304–313CrossRefGoogle Scholar
  66. Krøvel AV, Søfteland L, Torstensen BE, Olsvik PA (2010) Endosulfan in vitro toxicity in Atlantic salmon hepatocytes obtained from fish fed either fish oil or vegetable oil. Comp Biochem Physiol C Toxicol Pharmacol 151:175–186CrossRefGoogle Scholar
  67. Kumari J, Sahoo PK, Swain T, Sahoo SK, Sahu AK, Mohanty BR (2006) Seasonal variation in the innate immune parameters of the Asian catfish Clarias batrachus. Aquaculture 252:121–127CrossRefGoogle Scholar
  68. Kumari J, Larsen AN, Bogwald J, Dalmo RA (2009) Interleukin-17D in Atlantic salmon (Salmo salar): molecular characterization, 3D modelling and promoter analysis. Fish Shellfish Immunol 27:647–659CrossRefGoogle Scholar
  69. Kurtz J, Kalbe M, Langefors A, Mayer I, Milinski M, Hasselquist D (2007) An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks. Am Nat 170:509–519CrossRefGoogle Scholar
  70. Lamková K, Simková A, Palíková M, Jurajda P, Lojek A (2007) Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitol Res 101:775–789CrossRefGoogle Scholar
  71. Langston WJ, Burt GR, Chesman BS, Vane CH (2005) Partitioning, bioavailability and effects of oestrogens and xeno-estrogens in the aquatic environment. J Mar Biol Assoc UK 85:1–31CrossRefGoogle Scholar
  72. Larsson DGJ, Adolfsson-Erici M, Thomas P (2006) Characterization of putative ligands for a fish gonadal androgen receptor in a pulp mill effluent. Environ Toxicol Chem 25:419–427CrossRefGoogle Scholar
  73. Lavado R, Thibat R, Raldua D, Martin R, Porte C (2004) First evidence of endocrine disruption in feral carp from the Ebro river. Toxicol Appl Pharmacol 196:247–257CrossRefGoogle Scholar
  74. Law WY, Chen WH, Song YL, Dufour S, Chang CF (2001) Differential in vitro suppressive effects of steroids on leukocyte phagocytosis in two teleosts, tilapia and common carp. Gen Comp Endocrinol 121:163–172CrossRefGoogle Scholar
  75. Le Gac F, Thomas J-L, Mourot B, Loir M (2001) In vivo and in vitro effects of prochloraz and nonylphenol ethoxylates on trout spermatogenesis. Aquat toxicol 53:187–200CrossRefGoogle Scholar
  76. Legler J, Zeinstra LM, Schuitemaker F, Lanser PH, Bogerd J, Brouwer A, Vethaak AD, De Voogt P, Murk AJ, Van der Burg B (2002) Comparison of in vivo and in vitro reporter gene assays for short-term screening of estrogenicactivity. Environ Sci and Technol 36:4410–4415CrossRefGoogle Scholar
  77. Lehmann D, Siebold K, Emmons LR, Muller HJ (1988) Androgens inhibit proliferation of human peripheral blood lymphocytes in vitro. Clin Immunol Immunopath 46:122–128CrossRefGoogle Scholar
  78. Liu X, Su H, Zhu P, Zhang Y, Huang J, Lin H (2009) Molecular cloning, characterization and expression pattern of androgen receptor in Spinibarbus denticulatus. Gen Comp Endocrinol 160:93–101CrossRefGoogle Scholar
  79. Lorenzen K (1993) Acquired immunity o infectious diseases in fish: implications for the interpretation of fish disease surveys. In: Braunbeck T, Hanke W, Segner H (eds) Fish: ecotoxicology and ecophysiology. Verlag Chemie, Weinheim/New york, pp 183–196Google Scholar
  80. Lye CM, Frid CLJ, Gill ME, Mc Cormick D (1997) Abnormalities in the reproductive health of flounder Platichthys flesus exposed to effluent from a sewage treatment works. Mar Pollut Bull 34:34–41CrossRefGoogle Scholar
  81. Lynn SG, Birge WJ, Shepherd BS (2008) Molecular characterization and sex-specific tissue expression of estrogen receptor alpha (esr1), estrogen receptor betaa (esr2a) and ovarian aromatase (cyp19a1a) in yellow perch (Perca flavescens). Comp Biochem Physiol B Biochem Mol Biol 149:126–147CrossRefGoogle Scholar
  82. Marchand-Geneste N, Cazaunau M, Carpy AJ, Laguerre M, Porcher JM, Devillers J (2006) Homology model of the rainbow trout estrogen receptor (rtERalpha) and docking of endocrine disrupting chemicals (EDCs). SAR QSAR Environ Res 17:93–105CrossRefGoogle Scholar
  83. Matthews J, Celius T, Halgren R, Zacharewski T (2000) Differential estrogen receptor binding of estrogenic substances: a species comparison. J Steroid Biochem Mol Biol 74:223–234CrossRefGoogle Scholar
  84. Maule AG, Jorgensen EH, Vijayan MM, Killie JEA (2005) Aroclor 1254 exposure reduces disease resistance and innate immune responses in fasted arctic charr. Environ Toxicol Chem 24:117–124CrossRefGoogle Scholar
  85. Milla S, Wang N, Mandiki R, Kestemont P (2009) Corticosteroids: friends or foes of teleost fish reproduction? Comp Biochem Physiol A Mol Integr Physiol. 153:242–251CrossRefGoogle Scholar
  86. Miller LL, Wang F, Palace VP, Hontela A (2007) Effects of acute and subchronic exposures to waterborne selenite on the physiological stress response and oxidative stress indicators in juvenile rainbow trout. Aquat Toxicol 83:263–271CrossRefGoogle Scholar
  87. Misiti S, Stigliano A, Borro M, Gentile G, Michienzi S, Cerquetti L, Bucci B, Argese N, Brunetti E, Simmaco M, Toscano V (2010) Proteomic profiles in hyperandrogenic syndromes. J Endocrinol Invest 33:156–164Google Scholar
  88. Misumi I, Yada T, Leong JA, Schreck CB (2009) The effect of in vitro exposure to tributyltin on the immune competence of chinook Salmon (Oncorhynchus tshawytscha) leukocytes. Arch Environ contamin toxicol 56:229–237CrossRefGoogle Scholar
  89. Moens LN, Van der ven K, Remortel PV, Del-Favero J, De Coen WM (2006) Expression profiling of endocrine-disrupting coumpounds using a customized Cyprinus carpio cDNA microarray. Toxicol Sci 93:298–310CrossRefGoogle Scholar
  90. Moens LN, Soetaert A, van der Ven K, Del-Favero J, De Coen WM (2007) Use of suppression subtractive hybridization PCR for the development of cDNA arrays for the detection of endocrine disruption in carp (Cyprinus carpio). Comp Biochem Physiol D Genomics Proteomics 2:18–33CrossRefGoogle Scholar
  91. Morgan AL, Thompson KD, Auchinachie NA, Migaud H (2008) The effect of seasonality on normal haematological and innate immune parameters of rainbow trout Oncorhynchus mykiss L. Fish Shellfish Immunol 25:791–799CrossRefGoogle Scholar
  92. Mortensen AS, Arukwe A (2008) Estrogenic effect of dioxin-like aryl hydrocarbon receptor (AhR) agonist (PCB congener 126) in salmon hepatocytes. Mar Environ Res 66:119–120CrossRefGoogle Scholar
  93. Mortensen AS, Arukwe A (2009) Effects of tributyltin (TBT) on in vitro hormonal and biotransformation responses in Atlantic salmon (Salmo salar). J Toxicol Environ Health A 72:209–218CrossRefGoogle Scholar
  94. Munkittrick KR, McMaster ME, Portt CB, Van Der Kraak GJ, Smith IR, Dixon DG (1992) Changes in maturity, plasma sex steroid levels, hepatic mixed-function oxygenase activity, and the presence of external lesions in lake whitefish (Coregonus culpeaformis) exposed to bleached kraft mill effluent. Can J Fish Aquat Sci 49:1560–1569CrossRefGoogle Scholar
  95. Munkittrick KR, Servos MR, Van Der Kraak GJ, McMaster ME, Portt CB, Van Den Heuvel MR (1994) Survey of receiving-water environmental impacts associated with discharges from pulp mills. 2. Gonad size, liver size, hepatic EROD activity and plasma sex steroid levels in white sucker. Environ Toxicol Chem 13:1089–1101Google Scholar
  96. Nakayama A, Kurokawa Y, Kawahara E, kitayoshi N, Harino H, Miyadai T, Seikai T, Kawai S (2005) The immunotoxic effects of tributyltin on non-specific biodefense system in rainbow trout (Oncorhynchus mykiss). Jpn J Environ Toxicol 8:23–35Google Scholar
  97. Nakayama A, Kurokawa Y, Harino H, Kawahara E, Miyadai T, Seikai T, Kawai S (2007) Effects of tributyltin on the immune system of Japanese flounder (Paralichthys olivaceus). Aquat Toxicol 83:126–133CrossRefGoogle Scholar
  98. Noaksson E, Linderoth M, Bosveld ATC, Norrgren L, Zebühr Y, Balk L (2003a) Endocrine disruption in brook trout (Salvelinus fontinalis) exposed to leachate from a public refuse dump. Sci Total Environ 305:87–103CrossRefGoogle Scholar
  99. Noaksson E, Linderoth M, Bosveld ATC, Balk L (2003b) Altered steroid metabolism in several teleost species exposed to endocrine disrupting substances in refuse dump leachate. Gen Comp Endocrinol 134:273–284CrossRefGoogle Scholar
  100. Orlando EF, Davis WP, Guillette LJ Jr (2002) Aromatase activity in the ovary and brain of the eastern mosquitofish (Gambusia holbrooki) exposed to paper mill effluent. Environ Health Perspect 110:429–433Google Scholar
  101. Parks LG, Lambright CS, Orlando EF, Guillette LJ Jr, Ankley GT, Gray LE Jr (2001) Masculinization of female mosquitofish in kraft mill effluent-contaminated fenholloway river water is associated with androgen receptor agonist activity. Toxicol Sci 62:257–267CrossRefGoogle Scholar
  102. Peters RE, Courtenay SC, Cagampan S, Hewitt ML, MacLatchy DL (2007) Effects on reproductive potential and endocrine status in the mummichog (Fundulus heteroclitus) after exposure to 17alpha-ethynylestradiol in a short-term reproductive bioassay. Aquat Toxicol 85:154–166CrossRefGoogle Scholar
  103. Petit F, Le Goff P, Cravedi JP, Valotaire Y, Pakdel F (1997) Two complementary bioassays for screening the estrogenic potency of xenobiotics: recombinant yeast for trout estrogen receptor and trout hepatocyte cultures. J Mol Endocrinol 19:321–335CrossRefGoogle Scholar
  104. Pietsch C, Neumann N, Knopf K, Wuertz S, Kloas W (2009) Progestogens cause immunosuppression of stimulated carp (Cyprinus carpio L.) leukocytes in vitro. Comp Biochem Physiol C Toxicol Pharmacol 150:16–24CrossRefGoogle Scholar
  105. Plouffe DA, Hanington PC, Walsh JG, Wilson EC, Belosevic M (2005) Comparison of select innate immune mechanisms of fish and mammals. Xenotransplantation 12:266–277CrossRefGoogle Scholar
  106. Powell DB, Palm RC, Skillman A, Godtfredsen K (2003) Immunocompetence of juvenile Chinook salmon against Listonella anguillarum following dietary exposure to Aroclor® 1254. Environ Toxicol Chem 22:285–295Google Scholar
  107. Purdom CE, Hardiman PA, Bye VJ, Eno NC, Tyler CR, Sumpter JP (1994) Estrogenic effects of effluents from sewage treatment works. Chem Ecol 8:275–285CrossRefGoogle Scholar
  108. Rabitto IS, Alves Costa JRM, Silva de Assis HC, Pelletier E, Akaishi FM, Anjos A, Randi MAF, Oliveira Ribeiro CA (2005) Effects of dietary Pb(II) and tributyltin on neotropical fish, Hoplias malabaricus: histopathological and biochemical findings. Ecotox Environ Safe 60:147–156CrossRefGoogle Scholar
  109. 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 40:386–391CrossRefGoogle Scholar
  110. Rhen T, Cidlowski CA (2006) Estrogens and glucocorticoids have opposing effects on the amount and latent activity of complement proteins in the rat uterus. Biol Reprod 74:265–274CrossRefGoogle Scholar
  111. Rice CD, Schlenk D (1995) Immune function and cytochrome P4501A activity after acute exposure to 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) in channel catfish. J Aquat Animal Health 7:195–204CrossRefGoogle Scholar
  112. 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 50:163–168CrossRefGoogle Scholar
  113. Rice CD, Kergosin DH, Adams SM (1996) Innate immune functions as a bioindicator of pollution stress in fish. Ecotoxicol Environ Saf 33:186–192CrossRefGoogle Scholar
  114. Robertson LR, Iwanowicz LR, Marranca JM (2009) Identification of centrarchid hepcidins and evidence that 17β-estradiol disrupts constitutive expression of hepcidin-1 and inducible expression of hepcidin-2 in largemouth bass (Micropterus salmoides). Fish Shellfish Immunol 26:898–907CrossRefGoogle Scholar
  115. Ros AFH, Ferreira C, Serrão Santos R, Oliveira RF (2006) Regulation of immunocompetence by different androgen metabolites in a blenny with alternative reproductive tactics. J Exp Zool 305:986–994CrossRefGoogle Scholar
  116. Routledge EJ, White R, Malcolm G, Sumpter JP (2000) Differencial effects of xenoestrogens on coactivator recruitment by estrogens receptor (ER) a and ERb. J Biol Chem 275:35986–35993CrossRefGoogle Scholar
  117. Roy P, Salminen H, Koskimies P, Simola J, Smeds A, Saukko P, Huhtaniemi IT (2004) Screening of some anti-androgenic endocrine disruptors using a recombinant cell-based in vitro bioassay. J Steroid Biochem Mol Biol 88:157–166CrossRefGoogle Scholar
  118. Ruggeri B, Ubaldi M, Lourdusamy A, Soverchia L, Ciccocioppo R, Hardiman G, Bakere ME, Palermo F, Polzonetti-Magni AM (2008) Variation of the genetic expression pattern after exposure to estradiol-17β and 4-nonylphenol in male zebrafish (Danio rerio). Gen Comp Endocrinol 158:138–144CrossRefGoogle Scholar
  119. Saha NR, Usami T, Suzuki Y (2004) In vitro effects of steroid hormones on IgM-secreting cells and IgM secretion in common carp (Cyprinus carpio). Fish Shellfish Immunol 17:149–158CrossRefGoogle Scholar
  120. Sanchez W, Goin C, Brion F, Olsson PE, Goksøyr A, Porcher JM (2008) A new ELISA for the three-spined stickleback (Gasterosteus aculeatus L.) spiggin, using antibodies against synthetic peptide. Comp Biochem Physiol C Toxicol Pharmacol 147:129–137CrossRefGoogle Scholar
  121. Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aqua Res 39:223–239CrossRefGoogle Scholar
  122. Scholz S, Klüver N (2009) Effects of endocrine disrupters on sexual, gonadal development in fish. Sex Dev 3:136–151CrossRefGoogle Scholar
  123. Schwaiger J, Spieser OH, Bauer C, Ferling H, Mallow U, Kalbfus W, Negele RD (2000) Chronic toxicity of nonylphenol and ethinylestradiol: haematological and histopathological effects in juvenile Common carp (Cyprinus carpio). Aquatic Toxicol 51:69–78CrossRefGoogle Scholar
  124. Shimasaki Y, Kitano T, Oshima Y, Inoue S, Imada N, Honjo T (2003) Tributyltin causes masculinization in fish. Environ Toxicol Chem 22:141–144CrossRefGoogle Scholar
  125. Shved N, Berishvili G, Häusermann E, D’Cotta H, Baroiller JF, Eppler E (2009) Challenge with 17alpha-ethinylestradiol (EE2) during early development persistently impairs growth, differentiation, and local expression of IGF-I and IGF-II in immune organs of tilapia. Fish Shellfish Immunol 26:524–530CrossRefGoogle Scholar
  126. Sieroslawska A, Siwicki AK (2003) In vitro influence of ciprofloxacin on selected functions of rainbow trout (Oncorhynchus mykiss) leucocytes. Pol J Vet Sci 6:47–48Google Scholar
  127. Šimková A, Lafond T, Ondračková M, Jurajda P, Ottová E, Morand S (2008) Parasitism, life history traits and immune defence in cyprinid fish from Central Europe. BMC Evol Biol 8:29CrossRefGoogle Scholar
  128. Slater CH, Schreck CB (1997) Physiological levels of testosterone kill salmonid leukocytes in vitro. Gen Comp Endocrinol 106:113–119CrossRefGoogle Scholar
  129. Slater CH, Fitzpatrick MS, Schreck CB (1995) Characterization of an androgen receptor in salmonid lymphocytes: possible link to androgen-induced immunosuppression. Gen Comp Endocrinol 100:218–225CrossRefGoogle Scholar
  130. Smolinsky AN, Doughman JM, Kratzke LT, Lassiter CS (2010) Zebrafish (Danio rerio) androgen receptor: sequence homology and up-regulation by the fungicide vinclozolin. Comp Biochem Physiol C Toxicol Pharmacol 151:161–166CrossRefGoogle Scholar
  131. Sohoni P, Sumpter JP (1998) Several environmental oestrogens are also anti-androgens. J Endocrinol 158:327–339CrossRefGoogle Scholar
  132. Sone K, Hinago M, Itamoto M, Katsu Y, Watanabe H, Urushitani H, Tooi O, Guillette LJ Jr, Iguchi T (2005) Effects of an androgenic growth promoter 17beta-trenbolone on masculinization of Mosquitofish (Gambusia affinis affinis). Gen Comp Endocrinol 143:151–160CrossRefGoogle Scholar
  133. Steine NO, Melingen GO, Wergeland HI (2001) Antibodies against Vibrio salmonicida lipopolysaccharide (LPS) and wholebacteria in sera from Atlantic salmon (Salmo salar L.) vaccinated during the smolting and early post-smolt period. Fish shellfish immunol 11:39–52CrossRefGoogle Scholar
  134. Sumpter JP (2008) The ecotoxicology of hormonally active micropollutants. Water Sci Technol 57:125–130CrossRefGoogle Scholar
  135. Sunyer JO, Tort L, Lambris JD (1997) Structural C3 diversity in fish: characterization of five forms of C3 in the diploid fish Sparus aurata. J Immunol 158:2813–2821Google Scholar
  136. 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 62:754–759Google Scholar
  137. Suzuki Y, Otaka T, Sato S, Hou YY, Aida K (1997) Reproduction related immunoglobulin changes in rainbow trout. Fish Physiol Biochem 17:415–421CrossRefGoogle Scholar
  138. Swain P, Kayak SK (2009) Role of maternally derived immunity in fish. Fish Shellfish Immunol 24:89–99CrossRefGoogle Scholar
  139. Tavares-Dias (2006) Cytochemical method for staining fish basophils. J Fish Biol 69:312–317CrossRefGoogle Scholar
  140. Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitsev G (2009) Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentration of endosulfan. Fish Shellfish Immunol 27:105–111CrossRefGoogle Scholar
  141. Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Zaitsev G (2010) Endosulfan increases seric interleukin-2 like (IL-2L) factor and immunoglobulin M (IgM) of Nile tilapia (Oreochromis niloticus) challenged with Aeromona hydrophila. Fish Shellfish Immunol 28:401–405CrossRefGoogle Scholar
  142. Thibaut R, Porte C (2004) Effects of endocrine disrupters on sex steroid synthesis and metabolism pathways in fish. J Steroid Biochem Mol Biol 92:485–494CrossRefGoogle Scholar
  143. Thilagam H, Gopalakrishnan S, Bo J, Wang KJ (2009) Effect of 17beta-estradiol on the immunocompetence of Japanese sea bass (Lateolabrax japonicus). Environ Toxicol Chem 28:1722–1731CrossRefGoogle Scholar
  144. Thorpe KI, Hutchinson TH, Hetheridge MJ, Sumpter JP, Tyler CR (2000) Development of an in vivo screening assay for estrogenic chemicals using juvenile rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 19:2812–2820Google Scholar
  145. Todo T, Ikeuchi T, Kobayashi T, Nagahama Y (1999) Fish androgen receptor: cDNA cloning, steroid activation of transcription in transfected mammalian cells, and tissue mRNA levels. Biochem Biophys Res Com 254:378–383CrossRefGoogle Scholar
  146. Tokalov SV, Gutzeit HO (2007) Lectin-binding pattern as tool to identify and enrich specific primary testis cells of the tilapia (Oreochromis niloticus) and medaka (Oryzias latipes). J Exp Zool B Mol Dev Evol 308:127–138CrossRefGoogle Scholar
  147. Tollefsen KE (2007) Binding of alkylphenols and alkylated non-phenolics to the rainbow trout (Oncorhynchus mykiss) plasma sex steroid-binding protein. Ecotoxicol Environ Saf 68:40–48CrossRefGoogle Scholar
  148. Tollefsen KE, Meys JFA, Frydenlund J, Stenersen J (2002) Environmental estrogens interact with and modulate the properties of plasma sex steroid-binding proteins in juvenile Atlantic salmon (Salmo salar). Mar Environ Res 54:697–701CrossRefGoogle Scholar
  149. Tollefsen KE, Finne EF, Romstad R, Sandberg C (2006) Effluents from oil production activities contain chemicals that interfere with normal function of intra- and extra-cellular estrogen binding proteins. Mar Environ Res 62:S191–S194CrossRefGoogle Scholar
  150. Tyler CR, van der Eerden B, Jobling S, Panter G, Sumpter JP (1996) Measurement of vitellogenin, a biomarker for exposure to oestrogenic chemicals, in a wide variety of cyprinid fish. J Comp Physiol B 166:418–426CrossRefGoogle Scholar
  151. Vaccaro E, Meucci V, Intorre L, Soldani G, Di Bello D, Longo V, Gervasi PG, Pretti C (2005) Effects of 17beta-estradiol, 4-nonylphenol and PCB 126 on the estrogenic activity and phase 1 and 2 biotransformation enzymes in male sea bass (Dicentrarchus labrax). Aquat Toxicol 75:293–305CrossRefGoogle Scholar
  152. Vainikka A, Jokinen EI, Kortet R, Paukku S, Pirhonen J, Rantala MJ, Taskinen J (2005) Effects of testosterone and b-glucan on immune functions in tench. J Fish Biol 66:348–361CrossRefGoogle Scholar
  153. Van den Belt K, Berckmans P, Vangenechten C, Verheyen R, Witters H (2004) Comparative study on the in vitro/in vivo estrogenic potencies of 17beta-estradiol, estrone, 17alpha-ethynylestradiol and nonylphenol. Aquat Toxicol 66:183–195CrossRefGoogle Scholar
  154. Van Ginneken V, Palstra A, Leonards P, Nieveen M, van den Berg H, Flik G, Spanings T, Niemantsverdriet P, van den Thillart G, Murk A (2009) PCBs and the energy cost of migration in the European eel (Anguilla anguilla L.). Aquat Toxicol 92:213–220CrossRefGoogle Scholar
  155. Vetillard A, Bailhache T (2006) Effects of 4-n-nonylphenol and tamoxifen on sGnRH, estrogen receptor and vitellogenin gene expression in juvenile rainbow trout. Toxicol Scie 92:537–544CrossRefGoogle Scholar
  156. Wang R, Belosevic M (1994) Estradiol increases susceptibility of goldfish to Trypanosoma danilewskyi. Dev Comp Immunol 18:377–387CrossRefGoogle Scholar
  157. Wang KJ, Cai JJ, Cai L, Qu HD, Yang M, Zhang M (2009) Cloning and expression of a hepcidin gene from a marine fish (Pseudosciaena crocea) and the antimicrobial activity of its synthetic peptide. Peptides 30:638–646CrossRefGoogle Scholar
  158. Wang RL, Bencic D, Villeneuve DL, Ankley GT, Lazorchak J, Edwards S (2010) A transcriptomic biological framework for studying mechanisms of endocrine disruption in small fish species. Aquatic toxicol 98:230–234CrossRefGoogle Scholar
  159. Wartman CA, Hogan NS, Hewitt LM, McMaster ME, Landman MJ, Taylor S, Kovacs TG, van den Heuvel MR (2009) Androgenic effects of a Canadian bleached kraft pulp and paper effluent as assessed using threespine stickleback (Gasterosteus aculeatus). Aquat Toxicol 92:131–139CrossRefGoogle Scholar
  160. Watanuki H, Yamaguchi T, Sakai M (2002) Suppression in function of phagocytic cells in common carp Cyprinus carpio L. injected with estradiol, progesterone or 11-ketotestosterone. Comp Biochem Physiol C Toxicol Pharmacol 132:407–413CrossRefGoogle Scholar
  161. Watanuki H, Gushiken Y, Sakai M (2003) In vitro modulation of common carp (Cyprinus carpio L.) phagocytic cells by Di-n-butyl phthalate and Di-2-ethylhexyl phthalate. Aquat Toxicol 63:119–126CrossRefGoogle Scholar
  162. Werner J, Ouellet JD, Cheng CS, Ju YJ, Law RD (2010) Pulp and paper mill effluents induce distinct gene expression changes linked to androgenic and estrogenic responses in the fathead minnow (Pimephales Promelas). Environ Toxicol Chem 29:430–439CrossRefGoogle Scholar
  163. Williams TD, Amer MD, George SG, Sabine V, Chipman JK (2007) Gene expression responses of European flounder (Platichtys flesus) to 17-beta estradiol. Toxicol Lett 168:236–248CrossRefGoogle Scholar
  164. Yamaguchi T, Watanuki H, Sakai M (2001) Effects of estradiol, progesterone and testosterone on the function of carp, Cyprinus carpio, phagocytes in vitro. Comp Biochem Physiol C Toxicol Pharmacol 129:49–55CrossRefGoogle Scholar
  165. Yin DQ, Hu SQ, Gu Y, Wei L, Liu SS, Zhang AQ (2007) Immunotoxicity of bisphenol A to Carassius auratus lymphocytes and macrophages following in vitro exposure. J Environ Sci 19:232–237CrossRefGoogle Scholar
  166. Yu Y, Zhong Q, Li C, Jiang L, Yan F, Wang Z, Zhang Q (2009) Isolation and characterization of Toll-like receptor 9 in half-smooth tongue sole Cynoglossus semilaevis. Fish Shellfish Immunol 26:492–499CrossRefGoogle Scholar
  167. Yum S, Woo S, Kagami Y, Park HS, Ryu JC (2010) Changes in gene expression profile of medaka with acute toxicity of Arochlor 1260, a polychlorinated biphenyl mixture. Comp Biochem Physiol C Toxicol Pharmacol 151:51–56CrossRefGoogle Scholar
  168. Zhang Z, Hu J (2008) Effects of p,p′-DDE exposure on gonadal development and gene expression in Japanese medaka (Oryzias latipes). J Environ Scie 20:347–352CrossRefGoogle Scholar
  169. Zhang X, Hecker M, Park JW, Tompsett AR, Newsted J, Nakayama K, Jones PD, Au D, Kong R, Wu RS, Giesy JP (2008) Real-time PCR array to study effects of chemicals on the Hypothalamic-Pituitary-Gonadal axis of the Japanese medaka. Aquat Toxicol 88:173–182CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Sylvain Milla
    • 1
  • Sophie Depiereux
    • 1
  • Patrick Kestemont
    • 1
  1. 1.University of Namur, URBONamurBelgium

Personalised recommendations