Reptilia: Cellular Immunity in Reptiles: Perspective on Elements of Evolution

  • Soma Mondal GhoraiEmail author
  • Manisha Priyam


To understand the evolution of the immune system and its related genes, studies on reptiles are essential because they occupy a key phylogenetic position as a sister group to both birds and mammals. Reptiles comprise diverse groups presenting vast differences in morphology, reproductive, and developmental characteristics among its clades. They form the link between anamniotic amphibians and amniotic birds and are the first terrestrial animals to encounter full-blown land pathogens. Though much is known on the innate immunity of reptiles, the cellular components and cell-mediated immunity are largely unknown. Thus, the study of cellular immunity in nonavian reptiles will fill an important gap in reconstructing the evolutionary history of amniote vertebrates, which to date has been poorly represented. This chapter aims to annotate the missing links in reptilian immunology.


Reptiles Ontogeny B lymphocytes T lymphocytes NK cells Major histocompatibility complex genes Genomics Transcriptomics Cellular immunity Evolution 



This chapter was inspired by Edwin L. Cooper, PhD, ScD, highly distinguished professor, Laboratory of Comparative Immunology, Department of Neurobiology, David Geffen School of Medicine, UCLA, and founding editor in chief of DCI (1977), eCAM (2004), and JECM (2009). I am highly indebted to him for his faith in our potential for contributing a chapter on cellular immunity in reptiles.


  1. Alföldi J, di Palma F, Grabherr M, Williams C, Kong L, Mauceli E, Russell P, Lowe CB, Glor RE, Jaffe JD, Ray DA, Boissinot S, Shedlock AM, Botka C, Castoe TA, Colbourne JK, Fujita MK, Moreno RG, Hallers ten BF, Haussler D, Heger A, Heiman D, Janes DE, Johnson J, de Jong PJ, Koriabine MY, Lara M, Novick PA, Organ CL, Peach SE, Poe S, Pollock DD, de Queiroz K, Sanger T, Searle S, Smith JD, Smith Z, Swofford R, Turner-Maier J, Wade J, Young S, Zadissa A, Edwards SV, Glenn TC, Schneider CJ, Losos JB, Lander ES, Breen M, Ponting CP, Lindblad-Toh K (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477(7366):587–591CrossRefPubMedGoogle Scholar
  2. Arakawa H, Saribasak H, Buerstedde JM (2004) Activation-induced cytidine deaminase initiates immunoglobulin gene conversion and hypermutation by a common intermediate. PLoS Biol 2(7):e179CrossRefPubMedGoogle Scholar
  3. Ariel E (2011) Viruses in reptiles. Ariel Vet Res 42:100. CrossRefGoogle Scholar
  4. Bach P, Kamphuis E, Odermatt B, Sutter G, Buchholz CJ, Kalinke U (2007) Vesicular stomatitis virus glycoprotein displaying retrovirus-like particles induce a type I IFN receptor-dependent switch to neutralizing IgG antibodies. J Immunol 178(9):5839–5847CrossRefGoogle Scholar
  5. Bertram EM, Wilkinson RG, Lee BA, Jilbert AR, Kotlarski I (1996) Identification of duck T lymphocytes using an anti-human T cell (CD3) antiserum. Vet Immunol Immunopathol 51(3–4):353–363CrossRefGoogle Scholar
  6. Boehm T (2011) Design principles of adaptive immune systems. Nat Rev Immunol 11(5):307CrossRefGoogle Scholar
  7. Brown DR (2002) Mycoplasmosis and immunity of fish and reptiles. Front Biosci 7:D1338–D1346CrossRefGoogle Scholar
  8. Burnham DK, Keall SN, Nelson NJ, Daugherty CH (2005) T cell function in tuatara (Sphenodon punctatus). Comp Immunol Microbiol Infect Dis 28(3):213–222CrossRefGoogle Scholar
  9. Castoe TA, Poole AW, de Koning AJ, Jones KL, Tomback DF, Oyler-McCance SJ, Fike JA, Lance SL, Streicher JW, Smith EN, Pollock DD (2012) Rapid microsatellite identification from Illumina paired-end genomic sequencing in two birds and a snake. PloS One 7(2):e30953CrossRefPubMedGoogle Scholar
  10. Chen SN, Huang B, Zhang XW, Li Y, Zhao LJ, Li N, Gao Q, Nie P (2013) IFN-γ and its receptors in a reptile reveal the evolutionary conservation of type II IFNs in vertebrates. Dev Comp Immunol 41(4):587–596CrossRefGoogle Scholar
  11. Chong AY, Kojima KK, Jurka J, Ray DA, Smit AFA, Isberg SR, Gongora J (2014) Evolution and gene capture in ancient endogenous retroviruses – insights from the crocodilian genomes. Retrovirology 11:71. CrossRefPubMedCentralPubMedGoogle Scholar
  12. Cook MT, Morrison RN, Wilkinson R, Nowak BF, Hayball PJ, Hayball JD (2001) A screen of mammalian antibodies on snapper (Pagrus auratus, Sparidae) peripheral blood leukocytes reveals cross reactivity of an anti-human CD3 antibody with a population of mIg−cells. Dev Comp Immunol 25(7):553–559CrossRefGoogle Scholar
  13. Cooper MA, Yokoyama WM (2010) Memory-like responses of natural killer cells. Immunol Rev 235(1):297–305CrossRefPubMedGoogle Scholar
  14. Decker T, Müller M, Stockinger S (2005) The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 5(9):675CrossRefGoogle Scholar
  15. Deza F, Espinel CS (2008) IgD in the reptile leopard gecko. Mol Immunol 45(12):3470–3476CrossRefGoogle Scholar
  16. Deza FG, Espinel CS, Beneitez JV (2007) A novel IgA-like immunoglobulin in the reptile Eublepharis macularius. Dev Comp Immunol 31(6):596–605CrossRefGoogle Scholar
  17. Digby MR, Lowenthal JW (1995) Cloning and expression of the chicken interferon-gamma gene. J Interferon Cytokine Res 15:939945CrossRefGoogle Scholar
  18. Du Pasquier L (1992) Origin and evolution of the vertebrate immune system. APMIS: acta pathologica, microbiologica, et immunologica. Scandinavica 100(5):383–392Google Scholar
  19. El Deeb S, Zada S, El Ridi R (1985) Ontogeny of hemopoietic and lymphopoietic tissues in the lizard Chalcides ocellatus (Reptilia, Sauna, Scincidae). J Morphol. CrossRefGoogle Scholar
  20. El Masri M, Saar AH, Mansour MH, Badir N (1995) Seasonal distribution and hormonal modulation of reptilian T cells. Immunobiology 193(1):15–41CrossRefGoogle Scholar
  21. El Ridi R, Badir N, Rouby SE (1981) Effect of seasonal variations on the immune system of the snake, Psammophis schokari. J Exp Zool 216(3):357–365CrossRefGoogle Scholar
  22. El Ridi R, Wahby AF, Saad AH, Soliman MAW (1987) Concanavalin A responsiveness and interleukin 2 production in the snake Spalersophis diadema. Immunobiology 174:177–189CrossRefGoogle Scholar
  23. Farag MA, El Ridi R (1990) Functional markers of the major histocompatibility gene complex of snakes. Eur J Immunol 20:2029–2033CrossRefGoogle Scholar
  24. Gilbert C, Meik JM, Dashevsky D, Card DC, Castoe TA, Schaack S (2014) Endogenous hepadnaviruses, bornaviruses and circoviruses in snakes. Proc R Soc Lond B Biol Sci 281(1791):20141122CrossRefGoogle Scholar
  25. Göbel TW, Meier EL, Du Pasquier L (2000) Biochemical analysis of the Xenopus laevis TCR/CD3 complex supports the “stepwise evolution” model. Eur J Immunol 30(10):2775–2781CrossRefGoogle Scholar
  26. Gouaillard C, Huchenq-Champagne A, Arnaud J, Chen CL, Rubin B (2001) Evolution of T cell receptor (TCR) α β heterodimer assembly with the CD3 complex. Eur J Immunol 31(12):3798–3805CrossRefGoogle Scholar
  27. Green RE et al (2014) Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346(6215):1254449. CrossRefPubMedCentralPubMedGoogle Scholar
  28. Grossberger D, Parham P (1992) Reptilian class I major histocompatibility complex genes reveal conserved elements in class I structure. Immunogenetics 36(3):166–174CrossRefGoogle Scholar
  29. Hareramadas B, Rai U (2005) Mechanism of androgen-induced thymic atrophy in the wall lizard, Hemidactylus Flaviviridis: an in vitro study. Gen Comp Endocrinol 144(1):10–19CrossRefGoogle Scholar
  30. Hareramadas B, Rai U (2006) Cellular mechanism of estrogen-induced thymic involution in wall lizard: caspase-dependent action. J Exp Zool A: Comp Exp Biol 305A(5):396–409CrossRefGoogle Scholar
  31. Hedrick PW, Miller PS (1994) Rare alleles, MHC and captive breeding. In: Conservation genetics. Birkhäuser, Basel, pp 187–204CrossRefGoogle Scholar
  32. Höglund P, Brodin P (2010) Current perspectives of natural killer cell education by MHC class I molecules. Nat Rev Immunol 10(10):724CrossRefGoogle Scholar
  33. Horton TL, Ritchie P, Watson MD, Horton JD (1996) NK-like activity against allogeneic tumour cells demonstrated in the spleen of control and thymectomized Xenopus. Immunol Cell Biol 74(4):365–373CrossRefGoogle Scholar
  34. Hugall AF, Foster R, Lee MS (2007) Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Syst Biol 56(4):543–563CrossRefGoogle Scholar
  35. Jaffredo T, Fellah JS, Dunon D (2005) Immunology of birds and reptiles. In: Encyclopedia of Life Sciences. John Wiley & Sons, Ltd: Chichester. [].
  36. Jaratlerdsiri W, Isberg SR, Higgins DP, Ho SY, Salomonsen J, Skjodt K, Miles LG, Gongora J (2014) Evolution of MHC class I in the Order Crocodylia. Immunogenetics 66(1):53–65CrossRefGoogle Scholar
  37. Jaratlerdsiri W, Deakin J, Godinez RM, Shan X, Peterson DG, Marthey S, Lyons E, McCarthy FM, Isberg SR, Higgins DP, Chong AY (2014a) Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC. PloS One 9(12):e114631CrossRefPubMedGoogle Scholar
  38. Jones K, Ariel E, Burgess G, Read M (2016) A review of fibropapillomatosis in green turtles (Chelonia mydas). Vet J 212:48–57CrossRefGoogle Scholar
  39. Kanakambika P, Muthukkaruppan VR (1972) The immune response to sheep erythrocytes in the lizard Calotes versicolor. J Immunol 109:415–420Google Scholar
  40. Kaufman J, Milne S, Gobel TW, Walker BA (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401(6756):923CrossRefGoogle Scholar
  41. Keller JM, Kannan K, Taniyasu S, Yamashita N, Day RD, Arendt MD, Segars AL, Kucklick JR (2005a) Perfluorinated compounds in the plasma of loggerhead and Kemp’s ridley sea turtles from the southeastern coast of the United States. Environ Sci Technol 39(23):9101–9108CrossRefGoogle Scholar
  42. Keller JM, McClellan-Green PD, Lee AM, Arendt MD, Maier PP, Segars AL, Whitaker JD, Keil DE, Peden-Adams MM (2005b) Mitogen-induced lymphocyte proliferation in loggerhead sea turtles: comparison of methods and effects of gender, plasma testosterone concentration, and body condition on immunity. Vet Immunol Immunopathol 103:269–281CrossRefGoogle Scholar
  43. Keller JM, McClellan-Green PD, Kucklick JR, Keil DE, PedenAdams MM (2006) Effects of organochlorine contaminants on loggerhead sea turtle immunity: comparison of a correlative field study and in vitro exposure experiments. Environ Health Perspect 114:70–76CrossRefGoogle Scholar
  44. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56(10):683–695CrossRefGoogle Scholar
  45. Klein J (1987) The major histocompatibility complex and protein recognition by T lymphocytes. Adv Exp Med Biol 225:1–10CrossRefGoogle Scholar
  46. Krebs P, Barnes MJ, Lampe K, Whitley K, Bahjat KS, Beutler B, Janssen E, Hoebe K (2009) NK cell–mediated killing of target cells triggers robust antigen-specific T cell–mediated and humoral responses. Blood 113(26):6593–6602CrossRefPubMedGoogle Scholar
  47. Kumar V, McNerney ME (2005) A new self: MHC-class-I-independent natural-killer-cell self-tolerance. Nat Rev Immunol 5(5):363–374CrossRefGoogle Scholar
  48. Kvell K, Cooper EL, Engelmann P, Bovari J, Nemeth P (2007) Blurring borders: innate immunity with adaptive features. Clin Dev Immunol 1–10:83671. CrossRefGoogle Scholar
  49. Leceta J, Zapata A (1985) Seasonal changes in the thymus and spleen of the turtle, Mauremys caspica. A morphometrical, light microscopical study. Dev Comp Immunol 9(4):653–668CrossRefGoogle Scholar
  50. Litman GW, Anderson MK, Jonathan PR (1999) Evolution of antigen binding receptors. Annu Rev Immunol 17(1):109–147CrossRefGoogle Scholar
  51. Loetscher P, Seitz M, Clark-Lewis I, Baggiolini M, Moser B (1994) Both interleukin-8 receptors independently mediate chemotaxis. Jurkat cells transfected with IL-8R1 or IL-8R2 migrate in response to IL-8, GRO alpha and NAP-2. FEBS Lett 21;341(2-3):187–192CrossRefGoogle Scholar
  52. Longenecker BM, Mosmann TR (1981) Structure and properties of the major histocompatibility complex of the chicken. Speculations on the advantages and evolution of polymorphism. Immunogenetics 13(1):1–23CrossRefGoogle Scholar
  53. Madsen T, Ujvari B (2011) The potential demise of a population of adders (Vipera berus) in Smygehuk, Sweden. Beata Ujvari University of New South Wales, Research Article. 72Google Scholar
  54. Madsen T, Ujvari B, Nandakumar KS, Hasselquist D, Holmdahl R (2007) Do “infectious” prey select for high levels of natural antibodies in tropical pythons? Evol Ecol 21(2):271–279CrossRefGoogle Scholar
  55. Manickasundari M, Selvaraj P, Pitchappan RM (1984) Studies on T-cells of the lizard, Calotes versicolor: adherent and non-adherent populations of the spleen. Dev Comp Immunol 8(2):367–374CrossRefGoogle Scholar
  56. Marchalonis JJ, Ealey EH, Diener E (1969) Immune response of the tuatara, Sphenodon punctatum. Aust J Exp Biol Med Sci 47(3):367–380CrossRefGoogle Scholar
  57. Marschang RE, Ihász K, Kugler R, Lengyel G, Fehér E, Marton S, Bányai K, Aqrawi T, Farkas SL (2016) Development of a consensus reverse transcription PCR assay for the specific detection of tortoise picornaviruses. J Vet Diagn Invest 28(3):309–314CrossRefGoogle Scholar
  58. McArthur S, Wilkinson R, Meyer J (2004) Medicine and Surgery of Tortoises and Turtles. ISBN: 978-1-4051-0889-8.Wiley-BlackwellGoogle Scholar
  59. Merchant ME, Roche C, Elsey RM, Prudhomme J (2003) Antibacterial properties of serum from the American alligator (Alligator mississippiensis). Comp Biochem Physiol B: Biochem Mol Biol 136(3):505–513CrossRefGoogle Scholar
  60. Merchant M, Thibodeaux D, Loubser K, Elsey RM (2004) Amoebacidal effects of serum from the American alligator (Alligator mississippiensis). J Parasitol 90(6):1480–1483CrossRefGoogle Scholar
  61. Miller HC, Belov K, Daugherty CH (2005) Characterization of MHC class II genes from an ancient reptile lineage, Sphenodon (tuatara). Immunogenetics 57(11):883–891CrossRefGoogle Scholar
  62. Miller HC, O’Meally D, Ezaz T, Amemiya C, Marshall-Graves JA, Edwards S (2015) Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the Tuatara Sphenodon punctatus. G3: Genes Genomes Genetics 5(7):1439–1451CrossRefGoogle Scholar
  63. Mondal S, Rai U (2001) In vitro effect of temperature on phagocytic and cytotoxic activities of splenic phagocytes of the wall lizard, Hemidactylus flaviviridis. Comp Biochem Physiol A Mol Integr Physiol 129(2):391–398CrossRefGoogle Scholar
  64. Montali RJ (1988) Comparative pathology of inflammation in the higher vertebrates (reptiles, birds and mammals). J Comp Pathol 99(1):1–26CrossRefGoogle Scholar
  65. Muñoz FJ, De la Fuente M (2004) Seasonal changes in lymphoid distribution of the turtle Mauremys caspica. Copeia 2004(1):178–183CrossRefGoogle Scholar
  66. Munoz FA, Estrada-Parra S, Romero-Rojas A, Work TM, Gonzalez-Ballesteros E, Estrada-Garcia I (2009) Identification of CD3+ T lymphocytes in the green turtle Chelonia mydas. Vet Immunol Immunopathol 131:211–217CrossRefGoogle Scholar
  67. Natarajan K, Muthukkaruppan VR (1985) Distribution and ontogeny of B cells in the garden lizard, Calotes versicolor. Distribution and ontogeny of B cells in the garden lizard, Calotes versicolor. Dev Comp Immunol 9(2):01–310. ISSN 0145-305XCrossRefGoogle Scholar
  68. Ochesenbein AF, Zinkernagel RM (2000) Natural antibodies and complement link innate and acquired immunity. Immunol Today 21(12):624–630CrossRefGoogle Scholar
  69. Ohta Y, Goetz W, Hossain MZ, Nonaka M, Flajnik MF (2006) Ancestral organization of the MHC revealed in the amphibian Xenopus. J Immunol 176(6):3674–3685CrossRefGoogle Scholar
  70. Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H (2003) Major histocompatibility complex and mate choice in sand lizards. Proc R Soc Lond B Biol Sci 270(Suppl 2):S254–S256CrossRefGoogle Scholar
  71. Origgi FC, Klein PA, Mathes K, Blahak S, Marschang RE, Tucker SJ et al (2001) Enzyme-linked immunosorbent assay for detecting herpesvirus exposure in Mediterranean tortoises (spur-thighed tortoise [Testudo graeca] and Hermann’s tortoise [Testuto hermanni]). J Clin Microbiol 39:3156–3163CrossRefPubMedGoogle Scholar
  72. Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202:8–32CrossRefGoogle Scholar
  73. Priyam M, Tripathy M, Rai U, Ghorai SM (2016) Tracing the evolutionary lineage of pattern recognition receptor homologues in vertebrates: An insight into reptilian immunity via de novo sequencing of the wall lizard splenic transcriptome. Vet Immunol Immunopathol 172:26–37CrossRefGoogle Scholar
  74. 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 retro-position event gave rise to type-1 IFNs. J Immunol, ol.0903374.
  75. Radtkey RR, Becker B, Miller RD, Riblet R, Case TJ (1996) Variation and evolution of class I MHC in sexual and parthenogenetic geckos. Proc R Soc Lond B Biol Sci 263(1373):1023–1032CrossRefGoogle Scholar
  76. Saad AH (1989) Sex-associated differences in the mitogenic responsiveness of snake blood lymphocytes. Dev Comp Immuno 13(3):225–229CrossRefGoogle Scholar
  77. Saad AH, El Ridi R (1984) Mixed leukocyte reaction, graft-versus-host reaction and skin allograft rejection in the lizard, Chalcides ocellatus. Immunobiology 166:484CrossRefGoogle Scholar
  78. Saad AH, Zapata A (1992) Reptilian thymus gland: an ultrastructural overview. Thymus 20(3):135Google Scholar
  79. Sacchi R, Capelli E, Scali S, Pellitteri-Rosa D, Ghitti M, Acerbi E, Pingitore E (2014) In vitro temperature dependent activation of T-lymphocytes in 46 Common wall lizards (Podarcis muralis) in response to PHA stimulation. Acta Herpetologica 9(2):131–138.
  80. Sandmeier FC, Tracy RC (2014) The metabolic pace-of-life model: incorporating ectothermic organisms into the theory of vertebrate. Ecoimmunology 54:387–395Google Scholar
  81. Savan R, Ravichandran S, Collins JR, Sakai M, Young HA (2009) Structural conservation of interferon gamma among vertebrates. Cytokine Growth Factor Rev 20(2):115–124CrossRefPubMedGoogle Scholar
  82. Shaffer HB, Minx P, Warren DE, Shedlock AM, Thomson RC, Valenzuela N, Abramyan J, Amemiya CT, Badenhorst D, Biggar KK, Borchert GM (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14(3):R28CrossRefGoogle Scholar
  83. Shaney KJ, Card DC, Schield DR, Ruggiero RP, Pollock DD, Mackessy SP, Castoe TA (2014) Squamate reptile genomics and evolution. In: Toxinology. Springer, Netherlands, pp 1–18Google Scholar
  84. Shen L, Stuge TB, Bengtén E, Wilson M, Chinchar VG, Naftel JP, Bernanke JM, Clem LW, Miller NW (2004) Identification and characterization of clonal NK-like cells from channel catfish (Ictalurus punctatus). Dev Comp Immunol 28(2):139–152CrossRefGoogle Scholar
  85. St John JA, Braun EL, Isberg SR, Miles LG, Chong AY, Gongora J, Dalzell P, Moran C, Bed'Hom B, Abzhanov A, Burgess SC (2012) Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes. Genome Biol 13(1):415CrossRefPubMedGoogle Scholar
  86. Straub C, Neulen ML, Sperling B, Windau K, Zechmann M, Jansen CA, Viertlboeck BC, Göbel TW (2013) Chicken NK cell receptors. Dev Comp Immunol 41(3):324–333CrossRefGoogle Scholar
  87. Sun JC, Lanier LL (2009) Natural killer cells remember: an evolutionary bridge between innate and adaptive immunity? Eur J Immunol 39(8):2059–2064CrossRefPubMedGoogle Scholar
  88. Sun JC, Joseph C, Joshua N, Lewis B, Lanier L (2009) Adaptive immune features of natural killer cells. Nature 457(7229):557CrossRefPubMedGoogle Scholar
  89. Sypek JP, Borysenko M, Findlay SR (1984) Anti-immunoglobulin induced histamine release from naturally abundant basophils in the snapping turtle, Chelydra serpentina. Dev Comp Immunol 8(2):359–366CrossRefGoogle Scholar
  90. Trinchieri G (2010) Type I interferon: friend or foe? J Exp Med 207(10):2053–2063CrossRefPubMedGoogle Scholar
  91. Turchin A, Hsu E (1996) The generation of antibody diversity in the turtle. J Immunol 156(10):3797–3805Google Scholar
  92. Ulsh BA, Congdon JD, Hinton TG, Whicker FW, Bedford JS (2000) Culture methods for turtle lymphocytes. Methods Cell Sci 22(4):285–297CrossRefGoogle Scholar
  93. Vonk FJ, Casewell NR, Henkel CV, Heimberg AM, Jansen HJ, McCleary RJ, Kerkkamp HM, Vos RA, Guerreiro I, Calvete JJ, Wüster W (2013) The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci 110(51):20651–20656CrossRefGoogle Scholar
  94. Voogdt CG, Bouwman LI, Kik MJ, Wagenaar JA, van Putten JP (2016) Reptile Toll-like receptor 5 unveils adaptive evolution of bacterial flagellin recognition. Sci Rep 6:19046CrossRefPubMedGoogle Scholar
  95. Wang T, Sun Y, Shao W, Cheng G, Li L, Cao Z, Yang Z, Zou H, Zhang W, Han B, Hu Y (2012) Evidence of IgY subclass diversification in snakes: evolutionary implications. J Immunol 189(7):3557–3565CrossRefGoogle Scholar
  96. Warr GW, Magor KE, Higgins DA (1995) IgY: clues to the origins of modern antibodies. Immunol Today 16:392–398. CrossRefGoogle Scholar
  97. Wei Z, Wu Q, Ren L, Hu X, Guo Y, Warr GW, Hammarström L, Li N, Zhao Y (2009) Expression of IgM, IgD, and IgY in a reptile, Anolis carolinensis. J Immunol 183(6):3858–3864. CrossRefGoogle Scholar
  98. Work TM, Balazs GH, Rameyer RA, Chang SP, Berestecky J (2000) Assessing humoral and cell-mediated immune response in Hawaiian green turtles, Chelonia mydas. Vet Immunol Immunopathol 74(3):179–194CrossRefGoogle Scholar
  99. Wu S, Gao J, Dinh QT, Chen C, Fimmel S (2008) IL-8 production and AP-1 transactivation induced by UVA in human keratinocytes: roles of D-alpha-tocopherol. Mol Immunol 45(8):2288–2296. CrossRefGoogle Scholar
  100. Yoder JA (2004) Investigating the morphology, function and genetics of cytotoxic cells in bony fish. Comp Biochem Physiol C Toxicol Pharmacol 138(3):271–280CrossRefGoogle Scholar
  101. Zimmerman LM, Vogel LA, Bowden RM (2010) Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 213:661–671CrossRefPubMedGoogle Scholar
  102. Zou J, Secombes CJ (2011) Teleost fish interferons and their role in immunity. Dev Comp Immunol 35(12):1376–1387CrossRefGoogle Scholar
  103. Zucker K, Lu P, Esquenazi V, Miller J (1992) Cloning of the cDNA for canine interferon-gamma. J Interf Res 12(3):191–194CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Hindu College, University of DelhiDelhiIndia
  2. 2.Department of ZoologyUniversity of DelhiDelhiIndia

Personalised recommendations