Advertisement

The Origin and Early Evolution of Adaptive Immune Systems

  • Masayuki HiranoEmail author
Chapter
First Online:

Abstract

Two forms of recombinatorial adaptive immune systems arose in vertebrates about 480 million years ago. The repertoire of immunoglobulin domain-based T and B cell antigen receptors in jawed vertebrates is diversified primarily through the rearrangement of V(D)J (variable, diversity, and/or joining) gene segments and somatic hypermutation, but none of the major recognition elements in jawed vertebrates have been found in jawless vertebrates. Instead, the adaptive immune systems of jawless vertebrates are based on variable lymphocyte receptors (VLRs) that are generated through recombinatorial usage of a large panel of greatly diverse leucine rich repeat sequences. Whereas the emergence of transposon-like, recombination-activating genes (RAGs) contributed uniquely to the origin of the adaptive immune systems in jawed vertebrates, the use of activation-induced cytidine deaminase (AICDA) for receptor diversification is common to both the jawed and jawless vertebrates. Despite these differences in anticipatory receptor structure, the basic design of adaptive immune system featuring two cooperating T and B lymphocyte arms apparently evolved in an ancestor of jawed and jawless vertebrates within the context of established innate immunity and has been sustained due to powerful and durable selection, mostly for pathogen defense commitments.

Keywords

Adaptive immune system Adaptive immunity Innate immunity Lymphocyte Innate immune cell Vertebrate Jawed vertebrate Jawless vertebrate Invertebrate Variable lymphocyte receptor (VLR) T cell B cell Lamprey Hagfish Gene assembly Evolution 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The author thanks Prof. Edwin L. Cooper for suggestions and critical reading of the manuscript. The author also thanks Dr. Yoichi Sutoh for the figure illustrations. This work is supported by the National Science Foundation.

References

  1. Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751PubMedGoogle Scholar
  2. Alder MN, Rogozin IB, Iyer LM, Glazko GV et al (2005) Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970–1973PubMedGoogle Scholar
  3. Alder MN, Herrin BR, Sadlonova A, Stockard CR et al (2008) Antibody responses of variable lymphocyte receptors in the lamprey. Nat Immunol 9:319–327PubMedGoogle Scholar
  4. Azumi K, De Santis R, De Tomaso A, Rigoutsos I et al (2003) Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: “waiting for Godot”. Immunogenetics 55:570–581PubMedGoogle Scholar
  5. Bajoghli B, Guo P, Aghaallaei N, Hirano M et al (2011) A thymus candidate in lampreys. Nature 470:90–94PubMedGoogle Scholar
  6. Basu U, Franklin A, Schwer B, Cheng HL et al (2009) Regulation of activation-induced cytidine deaminase DNA deamination activity in B-cells by Ser38 phosphorylation. Biochem Soc Trans 37:561–568PubMedPubMedCentralGoogle Scholar
  7. Baulcombe DC (1996) Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8:1833–1844PubMedPubMedCentralGoogle Scholar
  8. Bell JJ, Bhandoola A (2008) The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452:764–767PubMedGoogle Scholar
  9. Bergstrom CT, Antia R (2006) How do adaptive immune systems control pathogens while avoiding autoimmunity? Trends Ecol Evol 21:22–28PubMedGoogle Scholar
  10. Beutler B (2004) Innate immunity: an overview. Mol Immunol 40:845–859PubMedGoogle Scholar
  11. Bilej M, Rossmann P, Sinkora M, Hanusova R et al (1998) Cellular expression of the cytolytic factor in earthworms Eisenia foetida. Immunol Lett 60:23–29PubMedPubMedCentralGoogle Scholar
  12. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS et al (1987) The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329:512–518PubMedGoogle Scholar
  13. Boehm T, Hirano M, Holland SJ, Das S et al (2018) Evolution of alternative adaptive immune systems in vertebrates. Annu Rev Immunol 36:19–42PubMedGoogle Scholar
  14. Bosch TC, David CN (1984) Growth regulation in Hydra: relationship between epithelial cell cycle length and growth rate. Dev Biol 104:161–171PubMedGoogle Scholar
  15. Bronkhorst AW, van Cleef KW, Vodovar N, Ince IA et al (2012) The DNA virus invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery. Proc Natl Acad Sci U S A 109:E3604–E3613PubMedPubMedCentralGoogle Scholar
  16. Buchanan SG, Gay NJ (1996) Structural and functional diversity in the leucine-rich repeat family of proteins. Prog Biophys Mol Biol 65:1–44PubMedGoogle Scholar
  17. Bucy RP, Coltey M, Chen CI, Char D et al (1989) Cytoplasmic CD3+ surface CD8+ lymphocytes develop as a thymus-independent lineage in chick-quail chimeras. Eur J Immunol 19:1449–1455PubMedGoogle Scholar
  18. Burnet FM (1968) Evolution of the immune process in vertebrates. Nature 218:426–430PubMedGoogle Scholar
  19. Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3:1200–1207PubMedGoogle Scholar
  20. Cannon JP, Haire RN, Magis AT, Eason DD et al (2008) A bony fish immunological receptor of the NITR multigene family mediates allogeneic recognition. Immunity 29:228–237PubMedPubMedCentralGoogle Scholar
  21. Chaudhuri J, Basu U, Zarrin A, Yan C et al (2007) Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol 94:157–214PubMedGoogle Scholar
  22. Cheng TC, Streisfeld SD (1963) Innate phagocytosis in the trematodes Megalodiscus temperatus and Haematoloechus sp. J Morphol 113:375–380PubMedGoogle Scholar
  23. Cohen IR (2007) Biomarkers, self-antigens and the immunological homunculus. J Autoimmun 29:246–249PubMedGoogle Scholar
  24. Cooper EL (1971) New observations on lymph gland (LM1) and thymus activity in larval bullfrogs, Rana catesbeiana. In: Lindahl-Kiessling K, Alm G, Hanna MG Jr (eds) Morphological and functional aspects of immunity. Springer, New York, pp 1–10Google Scholar
  25. Cooper EL (1976) Immunity mechanisms. In: Lofts B (ed) Physiology of the Amphibia. Academic Press, New York, pp 163–272Google Scholar
  26. Cooper EL (2006) Comparative immunology. Integr Zool 1:32–43PubMedGoogle Scholar
  27. Cooper EL (2010) Evolution of immune systems from self/not self to danger to artificial immune systems (AIS). Phys Life Rev 7:55–78PubMedPubMedCentralGoogle Scholar
  28. Cooper EL, Overstreet N (2014) Diversity, evolution, and therapeutic applications of small RNAs in prokaryotic and eukaryotic immune systems. Phys Life Rev 11:113–134PubMedGoogle Scholar
  29. Cooper MD, Peterson RD, Good RA (1965) Delineation of the thymic and bursal lymphoid systems in the chicken. Nature 205:143–146PubMedGoogle Scholar
  30. Cooper EL, Cossarizza A, Kauschke E, Franceschi C (1999) Cell adhesion and the immune system: a case study using earthworms. Microsc Res Tech 44:237–253PubMedGoogle Scholar
  31. Cooper EL, Kauschke E, Cossarizza A (2002) Digging for innate immunity since Darwin and Metchnikoff. BioEssays 24:319–333PubMedGoogle Scholar
  32. Deveau H, Garneau JE, Moineau S (2010) CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64:475–493PubMedGoogle Scholar
  33. Dudley DD, Chaudhuri J, Bassing CH, Alt FW (2005) Mechanism and control of V(D)J recombination versus class switch recombination: similarities and differences. Adv Immunol 86:43–112PubMedGoogle Scholar
  34. Fange R, Pulsford A (1983) Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L. Cell Tissue Res 230:337–351PubMedGoogle Scholar
  35. Finstad J, Good RA (1964) The evolution of the immune response. 3. Immunologic responses in the lamprey. J Exp Med 120:1151–1168PubMedPubMedCentralGoogle Scholar
  36. Fire A, Xu S, Montgomery MK, Kostas SA et al (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811PubMedGoogle Scholar
  37. Flajnik MF (2002) Comparative analyses of immunoglobulin genes: surprises and portents. Nat Rev Immunol 2:688–698PubMedGoogle Scholar
  38. Flajnik MF, Kasahara M (2010) Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 11:47–59PubMedGoogle Scholar
  39. Fujii T, Nakagawa H, Murakawa S (1979a) Immunity in lamprey. I. Production of haemolytic and haemagglutinating antibody to sheep red blood cells in Japanese lampreys. Dev Comp Immunol 3:441–451PubMedGoogle Scholar
  40. Fujii T, Nakagawa H, Murakawa S (1979b) Immunity in lamprey. II. Antigen-binding responses to sheep erythrocytes and hapten in the ammocoete. Dev Comp Immunol 3:609–620PubMedGoogle Scholar
  41. Goodnow CC, Sprent J, Fazekas de St Groth B, Vinuesa CG (2005) Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 435:590–597PubMedGoogle Scholar
  42. Gowans JL, Knight EJ (1964) The route of re-circulation of lymphocytes in the rat. Proc Biol Sci 159:257–282Google Scholar
  43. Greaves MF, Roitt IM, Rose ME (1968) Effect of bursectomy and thymectomy on the responses of chicken peripheral blood lymphocytes to phytohaemagglutinin. Nature 220:293–295PubMedGoogle Scholar
  44. Guo P, Hirano M, Herrin BR, Li J et al (2009) Dual nature of the adaptive immune system in lampreys. Nature 459:796–801PubMedPubMedCentralGoogle Scholar
  45. Hedrick SM, Cohen DI, Nielsen EA, Davis MM (1984) Isolation of cDNA clones encoding T cell-specific membrane-associated proteins. Nature 308:149–153PubMedGoogle Scholar
  46. Herrin BR, Alder MN, Roux KH, Sina C et al (2008) Structure and specificity of lamprey monoclonal antibodies. Proc Natl Acad Sci U S A 105:2040–2045PubMedPubMedCentralGoogle Scholar
  47. Herrin BR, Hirano M, Li J, Das S et al (2015) B cells and antibodies in jawless vertebrates. In: Honjo T, Reth M, Radbruch A, Alt FW (eds) Molecular biology of B cells. 2 ed. Academic Press, London, pp 121–132Google Scholar
  48. Hiom K, Gellert M (1997) A stable RAG1-RAG2-DNA complex that is active in V(D)J cleavage. Cell 88:65–72PubMedGoogle Scholar
  49. Hirano M (2015) Evolution of vertebrate adaptive immunity: immune cells and tissues, and AID/APOBEC cytidine deaminases. BioEssays 37:877–887PubMedGoogle Scholar
  50. Hirano M, Das S, Guo P, Cooper MD (2011) The evolution of adaptive immunity in vertebrates. Adv Immunol 109:125–157PubMedPubMedCentralGoogle Scholar
  51. Hirano M, Guo P, McCurley N, Schorpp M et al (2013) Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501:435–438PubMedPubMedCentralGoogle Scholar
  52. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284:1313–1318PubMedGoogle Scholar
  53. Huang G, Xie X, Han Y, Fan L et al (2007) The identification of lymphocyte-like cells and lymphoid-related genes in amphioxus indicates the twilight for the emergence of adaptive immune system. PLoS One 2:e206PubMedPubMedCentralGoogle Scholar
  54. Jameson SC, Hogquist KA, Bevan MJ (1995) Positive selection of thymocytes. Annu Rev Immunol 13:93–126PubMedGoogle Scholar
  55. Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54:1–13PubMedPubMedCentralGoogle Scholar
  56. Jinek M, Chylinski K, Fonfara I, Hauer M et al (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821PubMedGoogle Scholar
  57. Jung D, Alt FW (2004) Unraveling V(D)J recombination; insights into gene regulation. Cell 16(2):299–311PubMedGoogle Scholar
  58. Kasamatsu J, Sutoh Y, Fugo K, Otsuka N et al (2010) Identification of a third variable lymphocyte receptor in the lamprey. Proc Natl Acad Sci U S A 107:14304–14308PubMedPubMedCentralGoogle Scholar
  59. Kau AL, Ahern PP, Griffin NW, Goodman AL et al (2011) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336PubMedPubMedCentralGoogle Scholar
  60. Kendall MD (1980) Avian thymus glands: a review. Dev Comp Immunol 4:191–209PubMedGoogle Scholar
  61. Klempau AE, Cooper EL (1984) T-lymphocyte and B-lymphocyte dichotomy in anuran amphibians: II. Further investigations on the E-rosetting lymphocyte by using monoclonal antibody azathioprine inhibition and mitogen-induced polyclonal expansion. Dev Comp Immunol 8:323–338PubMedGoogle Scholar
  62. Korn ED, Weisman RA (1967) Phagocytosis of latex beads by Acanthamoeba. II. Electron microscopic study of the initial events. J Cell Biol 34:219–227PubMedPubMedCentralGoogle Scholar
  63. Li J, Barreda DR, Zhang YA, Boshra H et al (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 7:1116–1124PubMedGoogle Scholar
  64. Li J, Das S, Herrin BR, Hirano M et al (2013) Definition of a third VLR gene in hagfish. Proc Natl Acad Sci U S A 110:15013–15018PubMedPubMedCentralGoogle Scholar
  65. Lin W, Zhang H, Beck G (2001) Phylogeny of natural cytotoxicity: cytotoxic activity of coelomocytes of the purple sea urchin, Arbacia punctulata. J Exp Zool 290:741–750PubMedGoogle Scholar
  66. Linthicum DS, Hildemann WH (1970) Immunologic responses of Pacific hagfish. 3. Serum antibodies to cellular antigens. J Immunol 105:912–918PubMedGoogle Scholar
  67. Litman GW, Cannon JP, Rast JP (2005) New insights into alternative mechanisms of immune receptor diversification. Adv Immunol 87:209–236PubMedGoogle Scholar
  68. Litman GW, Rast JP, Fugmann SD (2010) The origins of vertebrate adaptive immunity. Nat Rev Immunol 10:543–553PubMedPubMedCentralGoogle Scholar
  69. Lloyd-Evans P (1993) Development of the lymphomyeloid system in the dogfish, Scyliorhinus canicula. Dev Comp Immunol 17:501–514PubMedGoogle Scholar
  70. Lu R, Maduro M, Li F, Li HW et al (2005) Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436:1040–1043PubMedPubMedCentralGoogle Scholar
  71. Mayer WE, Uinuk-Ool T, Tichy H, Gartland LA et al (2002) Isolation and characterization of lymphocyte-like cells from a lamprey. Proc Natl Acad Sci U S A 99:14350–14355PubMedPubMedCentralGoogle Scholar
  72. McKitrick TR, De Tomaso AW (2010) Molecular mechanisms of allorecognition in a basal chordate. Semin Immunol 22:34–38PubMedGoogle Scholar
  73. Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449:819–826PubMedGoogle Scholar
  74. Metchnikoff E (ed) (1893) Lectures on the comparative pathology of inflammation delivered at Pasteur Institute in 1891. Kegan Paul, LondonGoogle Scholar
  75. Miller JF (1961) Immunological function of the thymus. Lancet 2:748–749PubMedGoogle Scholar
  76. Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447PubMedGoogle Scholar
  77. Moore MA, Owen JJ (1965) Chromosome marker studies on the development of the haemopoietic system in the chick embryo. Nature 208:956. passimPubMedGoogle Scholar
  78. Morita M (1991) Phagocytic response of planarian reticular cells to heat-killed bacteria. Hydrobiologia 227:193–199Google Scholar
  79. Mukaigasa K, Hanasaki A, Maeno M, Fujii H et al (2009) The keratin-related Ouroboros proteins function as immune antigens mediating tail regression in Xenopus metamorphosis. Proc Natl Acad Sci U S A 106:18309–18314PubMedPubMedCentralGoogle Scholar
  80. Nagata T, Suzuki T, Ohta Y, Flajnik MF et al (2002) The leukocyte common antigen (CD45) of the Pacific hagfish, Eptatretus stoutii: implications for the primordial function of CD45. Immunogenetics 54:286–291PubMedGoogle Scholar
  81. Nagawa F, Kishishita N, Shimizu K, Hirose S et al (2007) Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nat Immunol 8:206–213PubMedGoogle Scholar
  82. Najakshin AM, Mechetina LV, Alabyev BY, Taranin AV (1999) Identification of an IL-8 homolog in lamprey (Lampetra fluviatilis): early evolutionary divergence of chemokines. Eur J Immunol 29:375–382PubMedGoogle Scholar
  83. Oettinger MA, Schatz DG, Gorka C, Baltimore D (1990) RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248(4962):1517–1523PubMedGoogle Scholar
  84. Owen JJ, Moore MA, Harrison GA (1965) Chromosome marker studies in the graft-versus-host reaction in the chick embryo. Nature 207:313–315PubMedGoogle Scholar
  85. Pancer Z, Cooper MD (2006) The evolution of adaptive immunity. Annu Rev Immunology 24:497–518Google Scholar
  86. Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J et al (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174–180PubMedPubMedCentralGoogle Scholar
  87. Pancer Z, Saha NR, Kasamatsu J, Suzuki T et al (2005) Variable lymphocyte receptors in hagfish. Proc Natl Acad Sci U S A 102:9224–9229PubMedPubMedCentralGoogle Scholar
  88. Paul WE (2008) Fundamental Immunology, 6th edn. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  89. Paust S, von Andrian UH (2011) Natural killer cell memory. Nat Immunol 12:500–508PubMedGoogle Scholar
  90. Putnam NH, Butts T, Ferrier DE, Furlong RF et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071PubMedGoogle Scholar
  91. Rast JP, Anderson MK, Strong SJ, Luer C et al (1997) Alpha, beta, gamma, and delta T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity 6:1–11PubMedGoogle Scholar
  92. Rast JP, Smith LC, Loza-Coll M, Hibino T et al (2006) Genomic insights into the immune system of the sea urchin. Science 314:952–956PubMedPubMedCentralGoogle Scholar
  93. Rimer J, Cohen IR, Friedman N (2014) Do all creatures possess an acquired immune system of some sort? BioEssays 36:273–281PubMedGoogle Scholar
  94. Rogers SL, Viertlboeck BC, Gobel TW, Kaufman J (2008) Avian NK activities, cells and receptors. Semin Immunol 20:353–360PubMedGoogle Scholar
  95. Rogozin IB, Iyer LM, Liang L, Glazko GV et al (2007) Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat Immunol 8:647–656PubMedGoogle Scholar
  96. Schatz DG, Oettinger MA, Baltimore D (1989) The V(D)J recombination activating gene, RAG-1. Cell 59:1035–1048PubMedGoogle Scholar
  97. Schmid-Hempel P (2008) Parasite immune evasion: a momentous molecular war. Trends Ecol Evol 23:318–326PubMedGoogle Scholar
  98. Sherif M, el Ridi R (1992) Natural cytotoxic cell activity in the snake Psammophis sibilans. Immunobiology 184:348–358PubMedGoogle Scholar
  99. Steinman RM, Inaba K, Turley S, Pierre P et al (1999) Antigen capture, processing, and presentation by dendritic cells: recent cell biological studies. Hum Immunol 60(7):562PubMedGoogle Scholar
  100. Storni T, Bachmann MF (2003) On the role of APC-activation for in vitro versus in vivo T cell priming. Cell Immunol 225:1–11PubMedGoogle Scholar
  101. Sun JC, Lanier LL (2009) Natural killer cells remember: an evolutionary bridge between innate and adaptive immunity? Eur J Immunol 39:2059–2064PubMedPubMedCentralGoogle Scholar
  102. Takahashi K, Naito M, Takeya M (1996) Development and heterogeneity of macrophages and their related cells through their differentiation pathways. Pathol Int 46:473–485PubMedGoogle Scholar
  103. Terebey N (1972) A light microscopic study of the mononuclear cells infiltrating skin homografts in the garter snake, Thamnophis sirtalis (Reptilia: Colubridae). J Morphol 137:149–159PubMedGoogle Scholar
  104. Terszowski G, Muller SM, Bleul CC, Blum C et al (2006) Evidence for a functional second thymus in mice. Science 312:284–287PubMedGoogle Scholar
  105. Tizard I (2001) Comparative Immunology. In: Kreier J (ed) Infection, resistance, and immunity, 2nd edn. CRC Press, London, pp 247–264Google Scholar
  106. Tomonaga S, Yamaguchi K, Ihara K, Awaya K (1986) Mononuclear phagocytic cells (Kupffer cells) in hagfish liver sinusoids. Zool Sci 3:613–620Google Scholar
  107. Tonegawa S (1983) Somatic generation of antibody diversity. Nature 302:575–581PubMedGoogle Scholar
  108. Uinuk-Ool T, Mayer WE, Sato A, Dongak R et al (2002) Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. Proc Natl Acad Sci U S A 99:14356–14361PubMedPubMedCentralGoogle Scholar
  109. Unanue ER (1980) Cooperation between mononuclear phagocytes and lymphocytes in immunity. N Engl J Med 303:977–985PubMedGoogle Scholar
  110. Voinnet O (2001) RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459PubMedGoogle Scholar
  111. von Boehmer H (2004) Selection of the T-cell repertoire: receptor-controlled checkpoints in T-cell development. Adv Immunol 84:201–238Google Scholar
  112. Wada H, Masuda K, Satoh R, Kakugawa K et al (2008) Adult T-cell progenitors retain myeloid potential. Nature 452:768–772PubMedGoogle Scholar
  113. Watanabe K, Horiguchi T, Sasaki F (1985) Scanning electron microscopy of macrophages in the tail musculature of the metamorphosing anuran tadpole, Rana japonica. Cell Tissue Res 241:545–550PubMedGoogle Scholar
  114. Watanabe T, Kamijo A, Narita H, Kitayama K et al (1995) Resident peritoneal cells in red sea bream Pargrus major. Fish Sci 61:937–941Google Scholar
  115. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL et al (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309:1874–1878PubMedGoogle Scholar
  116. Wilson GG, Murray NE (1991) Restriction and modification systems. Annu Rev Genet 25:585–627PubMedGoogle Scholar
  117. Woodhams DC, Bell SC, Bigler L, Caprioli RM et al (2016) Life history linked to immune investment in developing amphibians. Conserv Physiol 4:cow025PubMedPubMedCentralGoogle Scholar
  118. Yanagi Y, Yoshikai Y, Leggett K, Clark SP et al (1984) A human T cell-specific cDNA clone encodes a protein having extensive homology to immunoglobulin chains. Nature 308:145–149PubMedGoogle Scholar
  119. Yoder JA (2009) Form, function and phylogenetics of NITRs in bony fish. Dev Comp Immunol 33:135–144PubMedGoogle Scholar
  120. Zapata A, Diez B, Cejalvo T, Gutierrez-de Frias C et al (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20:126–136PubMedGoogle Scholar
  121. Zhang SM, Adema CM, Kepler TB, Loker ES (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305:251–254PubMedGoogle Scholar
  122. Zhu C, Lee V, Finn A, Senger K et al (2012) Origin of immunoglobulin isotype switching. Curr Biol 22:872–880PubMedPubMedCentralGoogle Scholar
  123. Zinkernagel RM, Doherty PC (1974) Immunological surveillance against altered self components by sensitised T lymphocytes in lymphocytic choriomeningitis. Nature 251:547–548PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Emory Vaccine Center and Department of Pathology and Laboratory Medicine, Emory UniversityAtlantaUSA

Personalised recommendations

Cite chapter

Buy options