Skip to main content
SpringerLink
Log in

The Origin and Early Evolution of Adaptive Immune Systems

  • Chapter
  • First Online:
Advances in Comparative Immunology

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751

    Article  CAS  PubMed  Google Scholar 

  • Alder MN, Rogozin IB, Iyer LM, Glazko GV et al (2005) Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970–1973

    Article  CAS  PubMed  Google Scholar 

  • Alder MN, Herrin BR, Sadlonova A, Stockard CR et al (2008) Antibody responses of variable lymphocyte receptors in the lamprey. Nat Immunol 9:319–327

    Article  CAS  PubMed  Google Scholar 

  • 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 55:570–581

    Article  CAS  PubMed  Google Scholar 

  • Bajoghli B, Guo P, Aghaallaei N, Hirano M et al (2011) A thymus candidate in lampreys. Nature 470:90–94

    Article  CAS  PubMed  Google Scholar 

  • 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 37:561–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baulcombe DC (1996) Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8:1833–1844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell JJ, Bhandoola A (2008) The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452:764–767

    Article  CAS  PubMed  Google Scholar 

  • Bergstrom CT, Antia R (2006) How do adaptive immune systems control pathogens while avoiding autoimmunity? Trends Ecol Evol 21:22–28

    Article  PubMed  Google Scholar 

  • Beutler B (2004) Innate immunity: an overview. Mol Immunol 40:845–859

    Article  CAS  PubMed  Google Scholar 

  • Bilej M, Rossmann P, Sinkora M, Hanusova R et al (1998) Cellular expression of the cytolytic factor in earthworms Eisenia foetida. Immunol Lett 60:23–29

    Article  CAS  PubMed  Google Scholar 

  • 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 329:512–518

    Article  CAS  PubMed  Google Scholar 

  • Boehm T, Hirano M, Holland SJ, Das S et al (2018) Evolution of alternative adaptive immune systems in vertebrates. Annu Rev Immunol 36:19–42

    Article  CAS  PubMed  Google Scholar 

  • Bosch TC, David CN (1984) Growth regulation in Hydra: relationship between epithelial cell cycle length and growth rate. Dev Biol 104:161–171

    Article  CAS  PubMed  Google Scholar 

  • 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–E3613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan SG, Gay NJ (1996) Structural and functional diversity in the leucine-rich repeat family of proteins. Prog Biophys Mol Biol 65:1–44

    Article  CAS  PubMed  Google Scholar 

  • 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 19:1449–1455

    Article  CAS  PubMed  Google Scholar 

  • Burnet FM (1968) Evolution of the immune process in vertebrates. Nature 218:426–430

    Article  CAS  PubMed  Google Scholar 

  • Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3:1200–1207

    Article  CAS  PubMed  Google Scholar 

  • 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 29:228–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaudhuri J, Basu U, Zarrin A, Yan C et al (2007) Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol 94:157–214

    Article  CAS  PubMed  Google Scholar 

  • Cheng TC, Streisfeld SD (1963) Innate phagocytosis in the trematodes Megalodiscus temperatus and Haematoloechus sp. J Morphol 113:375–380

    Article  CAS  PubMed  Google Scholar 

  • Cohen IR (2007) Biomarkers, self-antigens and the immunological homunculus. J Autoimmun 29:246–249

    Article  CAS  PubMed  Google Scholar 

  • 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 1–10

    Google Scholar 

  • Cooper EL (1976) Immunity mechanisms. In: Lofts B (ed) Physiology of the Amphibia. Academic Press, New York, pp 163–272

    Chapter  Google Scholar 

  • Cooper EL (2006) Comparative immunology. Integr Zool 1:32–43

    Article  PubMed  Google Scholar 

  • Cooper EL (2010) Evolution of immune systems from self/not self to danger to artificial immune systems (AIS). Phys Life Rev 7:55–78

    Article  PubMed  Google Scholar 

  • Cooper EL, Overstreet N (2014) Diversity, evolution, and therapeutic applications of small RNAs in prokaryotic and eukaryotic immune systems. Phys Life Rev 11:113–134

    Article  PubMed  Google Scholar 

  • Cooper MD, Peterson RD, Good RA (1965) Delineation of the thymic and bursal lymphoid systems in the chicken. Nature 205:143–146

    Article  CAS  PubMed  Google Scholar 

  • Cooper EL, Cossarizza A, Kauschke E, Franceschi C (1999) Cell adhesion and the immune system: a case study using earthworms. Microsc Res Tech 44:237–253

    Article  CAS  PubMed  Google Scholar 

  • Cooper EL, Kauschke E, Cossarizza A (2002) Digging for innate immunity since Darwin and Metchnikoff. BioEssays 24:319–333

    Article  CAS  PubMed  Google Scholar 

  • Deveau H, Garneau JE, Moineau S (2010) CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64:475–493

    Article  CAS  PubMed  Google Scholar 

  • 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 86:43–112

    Article  CAS  PubMed  Google Scholar 

  • Fange R, Pulsford A (1983) Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L. Cell Tissue Res 230:337–351

    Article  CAS  PubMed  Google Scholar 

  • Finstad J, Good RA (1964) The evolution of the immune response. 3. Immunologic responses in the lamprey. J Exp Med 120:1151–1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fire A, Xu S, Montgomery MK, Kostas SA et al (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  CAS  PubMed  Google Scholar 

  • Flajnik MF (2002) Comparative analyses of immunoglobulin genes: surprises and portents. Nat Rev Immunol 2:688–698

    Article  CAS  PubMed  Google Scholar 

  • Flajnik MF, Kasahara M (2010) Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 11:47–59

    Article  CAS  PubMed  Google Scholar 

  • 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 3:441–451

    Article  CAS  PubMed  Google Scholar 

  • 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 3:609–620

    Article  CAS  PubMed  Google Scholar 

  • Goodnow CC, Sprent J, Fazekas de St Groth B, Vinuesa CG (2005) Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 435:590–597

    Article  CAS  PubMed  Google Scholar 

  • Gowans JL, Knight EJ (1964) The route of re-circulation of lymphocytes in the rat. Proc Biol Sci 159:257–282

    CAS  Google Scholar 

  • Greaves MF, Roitt IM, Rose ME (1968) Effect of bursectomy and thymectomy on the responses of chicken peripheral blood lymphocytes to phytohaemagglutinin. Nature 220:293–295

    Article  CAS  PubMed  Google Scholar 

  • Guo P, Hirano M, Herrin BR, Li J et al (2009) Dual nature of the adaptive immune system in lampreys. Nature 459:796–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedrick SM, Cohen DI, Nielsen EA, Davis MM (1984) Isolation of cDNA clones encoding T cell-specific membrane-associated proteins. Nature 308:149–153

    Article  CAS  PubMed  Google Scholar 

  • 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 105:2040–2045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 121–132

    Google Scholar 

  • Hiom K, Gellert M (1997) A stable RAG1-RAG2-DNA complex that is active in V(D)J cleavage. Cell 88:65–72

    Article  CAS  PubMed  Google Scholar 

  • Hirano M (2015) Evolution of vertebrate adaptive immunity: immune cells and tissues, and AID/APOBEC cytidine deaminases. BioEssays 37:877–887

    Article  CAS  PubMed  Google Scholar 

  • Hirano M, Das S, Guo P, Cooper MD (2011) The evolution of adaptive immunity in vertebrates. Adv Immunol 109:125–157

    Article  CAS  PubMed  Google Scholar 

  • Hirano M, Guo P, McCurley N, Schorpp M et al (2013) Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501:435–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284:1313–1318

    Article  CAS  PubMed  Google Scholar 

  • 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:e206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jameson SC, Hogquist KA, Bevan MJ (1995) Positive selection of thymocytes. Annu Rev Immunol 13:93–126

    Article  CAS  PubMed  Google Scholar 

  • Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54:1–13

    Article  CAS  PubMed  Google Scholar 

  • Jinek M, Chylinski K, Fonfara I, Hauer M et al (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung D, Alt FW (2004) Unraveling V(D)J recombination; insights into gene regulation. Cell 16(2):299–311

    Article  CAS  PubMed  Google Scholar 

  • 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 107:14304–14308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kau AL, Ahern PP, Griffin NW, Goodman AL et al (2011) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kendall MD (1980) Avian thymus glands: a review. Dev Comp Immunol 4:191–209

    Article  CAS  PubMed  Google Scholar 

  • 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 8:323–338

    Article  CAS  PubMed  Google Scholar 

  • Korn ED, Weisman RA (1967) Phagocytosis of latex beads by Acanthamoeba. II. Electron microscopic study of the initial events. J Cell Biol 34:219–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Barreda DR, Zhang YA, Boshra H et al (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 7:1116–1124

    Article  CAS  PubMed  Google Scholar 

  • 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 110:15013–15018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 290:741–750

    Article  CAS  PubMed  Google Scholar 

  • Linthicum DS, Hildemann WH (1970) Immunologic responses of Pacific hagfish. 3. Serum antibodies to cellular antigens. J Immunol 105:912–918

    CAS  PubMed  Google Scholar 

  • Litman GW, Cannon JP, Rast JP (2005) New insights into alternative mechanisms of immune receptor diversification. Adv Immunol 87:209–236

    Article  CAS  PubMed  Google Scholar 

  • Litman GW, Rast JP, Fugmann SD (2010) The origins of vertebrate adaptive immunity. Nat Rev Immunol 10:543–553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd-Evans P (1993) Development of the lymphomyeloid system in the dogfish, Scyliorhinus canicula. Dev Comp Immunol 17:501–514

    Article  CAS  PubMed  Google Scholar 

  • Lu R, Maduro M, Li F, Li HW et al (2005) Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436:1040–1043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 99:14350–14355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKitrick TR, De Tomaso AW (2010) Molecular mechanisms of allorecognition in a basal chordate. Semin Immunol 22:34–38

    Article  CAS  PubMed  Google Scholar 

  • Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449:819–826

    Article  CAS  PubMed  Google Scholar 

  • Metchnikoff E (ed) (1893) Lectures on the comparative pathology of inflammation delivered at Pasteur Institute in 1891. Kegan Paul, London

    Google Scholar 

  • Miller JF (1961) Immunological function of the thymus. Lancet 2:748–749

    Article  CAS  PubMed  Google Scholar 

  • Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447

    Article  CAS  PubMed  Google Scholar 

  • Moore MA, Owen JJ (1965) Chromosome marker studies on the development of the haemopoietic system in the chick embryo. Nature 208:956. passim

    Article  PubMed  Google Scholar 

  • Morita M (1991) Phagocytic response of planarian reticular cells to heat-killed bacteria. Hydrobiologia 227:193–199

    Article  Google Scholar 

  • 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 106:18309–18314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 54:286–291

    Article  CAS  PubMed  Google Scholar 

  • 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 8:206–213

    Article  CAS  PubMed  Google Scholar 

  • 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 29:375–382

    Article  CAS  PubMed  Google Scholar 

  • 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):1517–1523

    Article  CAS  PubMed  Google Scholar 

  • Owen JJ, Moore MA, Harrison GA (1965) Chromosome marker studies in the graft-versus-host reaction in the chick embryo. Nature 207:313–315

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Cooper MD (2006) The evolution of adaptive immunity. Annu Rev Immunology 24:497–518

    Article  CAS  Google Scholar 

  • Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J et al (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174–180

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Saha NR, Kasamatsu J, Suzuki T et al (2005) Variable lymphocyte receptors in hagfish. Proc Natl Acad Sci U S A 102:9224–9229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul WE (2008) Fundamental Immunology, 6th edn. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  • Paust S, von Andrian UH (2011) Natural killer cell memory. Nat Immunol 12:500–508

    Article  CAS  PubMed  Google Scholar 

  • Putnam NH, Butts T, Ferrier DE, Furlong RF et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071

    Article  CAS  PubMed  Google Scholar 

  • 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 6:1–11

    Article  CAS  PubMed  Google Scholar 

  • Rast JP, Smith LC, Loza-Coll M, Hibino T et al (2006) Genomic insights into the immune system of the sea urchin. Science 314:952–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rimer J, Cohen IR, Friedman N (2014) Do all creatures possess an acquired immune system of some sort? BioEssays 36:273–281

    Article  CAS  PubMed  Google Scholar 

  • Rogers SL, Viertlboeck BC, Gobel TW, Kaufman J (2008) Avian NK activities, cells and receptors. Semin Immunol 20:353–360

    Article  CAS  PubMed  Google Scholar 

  • 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 8:647–656

    Article  CAS  PubMed  Google Scholar 

  • Schatz DG, Oettinger MA, Baltimore D (1989) The V(D)J recombination activating gene, RAG-1. Cell 59:1035–1048

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel P (2008) Parasite immune evasion: a momentous molecular war. Trends Ecol Evol 23:318–326

    Article  PubMed  Google Scholar 

  • Sherif M, el Ridi R (1992) Natural cytotoxic cell activity in the snake Psammophis sibilans. Immunobiology 184:348–358

    Article  CAS  PubMed  Google Scholar 

  • 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):562

    Article  CAS  PubMed  Google Scholar 

  • Storni T, Bachmann MF (2003) On the role of APC-activation for in vitro versus in vivo T cell priming. Cell Immunol 225:1–11

    Article  CAS  PubMed  Google Scholar 

  • Sun JC, Lanier LL (2009) Natural killer cells remember: an evolutionary bridge between innate and adaptive immunity? Eur J Immunol 39:2059–2064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi K, Naito M, Takeya M (1996) Development and heterogeneity of macrophages and their related cells through their differentiation pathways. Pathol Int 46:473–485

    Article  CAS  PubMed  Google Scholar 

  • Terebey N (1972) A light microscopic study of the mononuclear cells infiltrating skin homografts in the garter snake, Thamnophis sirtalis (Reptilia: Colubridae). J Morphol 137:149–159

    Article  CAS  PubMed  Google Scholar 

  • Terszowski G, Muller SM, Bleul CC, Blum C et al (2006) Evidence for a functional second thymus in mice. Science 312:284–287

    Article  CAS  PubMed  Google Scholar 

  • Tizard I (2001) Comparative Immunology. In: Kreier J (ed) Infection, resistance, and immunity, 2nd edn. CRC Press, London, pp 247–264

    Google Scholar 

  • Tomonaga S, Yamaguchi K, Ihara K, Awaya K (1986) Mononuclear phagocytic cells (Kupffer cells) in hagfish liver sinusoids. Zool Sci 3:613–620

    Google Scholar 

  • Tonegawa S (1983) Somatic generation of antibody diversity. Nature 302:575–581

    Article  CAS  PubMed  Google Scholar 

  • 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 99:14356–14361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unanue ER (1980) Cooperation between mononuclear phagocytes and lymphocytes in immunity. N Engl J Med 303:977–985

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2001) RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459

    Article  CAS  PubMed  Google Scholar 

  • von Boehmer H (2004) Selection of the T-cell repertoire: receptor-controlled checkpoints in T-cell development. Adv Immunol 84:201–238

    Article  Google Scholar 

  • Wada H, Masuda K, Satoh R, Kakugawa K et al (2008) Adult T-cell progenitors retain myeloid potential. Nature 452:768–772

    Article  CAS  PubMed  Google Scholar 

  • 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 241:545–550

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Kamijo A, Narita H, Kitayama K et al (1995) Resident peritoneal cells in red sea bream Pargrus major. Fish Sci 61:937–941

    Article  CAS  Google Scholar 

  • 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 309:1874–1878

    Article  CAS  PubMed  Google Scholar 

  • Wilson GG, Murray NE (1991) Restriction and modification systems. Annu Rev Genet 25:585–627

    Article  CAS  PubMed  Google Scholar 

  • Woodhams DC, Bell SC, Bigler L, Caprioli RM et al (2016) Life history linked to immune investment in developing amphibians. Conserv Physiol 4:cow025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 308:145–149

    Article  CAS  PubMed  Google Scholar 

  • Yoder JA (2009) Form, function and phylogenetics of NITRs in bony fish. Dev Comp Immunol 33:135–144

    Article  CAS  PubMed  Google Scholar 

  • Zapata A, Diez B, Cejalvo T, Gutierrez-de Frias C et al (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20:126–136

    Article  CAS  PubMed  Google Scholar 

  • Zhang SM, Adema CM, Kepler TB, Loker ES (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305:251–254

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Lee V, Finn A, Senger K et al (2012) Origin of immunoglobulin isotype switching. Curr Biol 22:872–880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zinkernagel RM, Doherty PC (1974) Immunological surveillance against altered self components by sensitised T lymphocytes in lymphocytic choriomeningitis. Nature 251:547–548

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Emory Vaccine Center and Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, USA

    Masayuki Hirano

Authors
  1. Masayuki Hirano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masayuki Hirano .

Editor information

Editors and Affiliations

  1. Laboratory of Comparative Immunology, Department of Neurobiology, David Geffen School of Medicine, UCLA, Los Angeles, CA, USA

    Edwin L. Cooper

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hirano, M. (2018). The Origin and Early Evolution of Adaptive Immune Systems. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_17

Download citation

Publish with us

Policies and ethics

Search

Navigation