1932

Abstract

Adaptive immunity in jawless fishes is based on antigen recognition by three types of variable lymphocyte receptors (VLRs) composed of variable leucine-rich repeats, which are differentially expressed by two T-like lymphocyte lineages and one B-like lymphocyte lineage. The T-like cells express either VLRAs or VLRCs of yet undefined antigen specificity, whereas the VLRB antibodies secreted by B-like cells bind proteinaceous and carbohydrate antigens. The incomplete VLR germline genes are assembled into functional units by a gene conversion–like mechanism that employs flanking variable leucine-rich repeat sequences as templates in association with lineage-specific expression of cytidine deaminases. B-like cells develop in the hematopoietic typhlosole and kidneys, whereas T-like cells develop in the thymoid, a thymus-equivalent region at the gill fold tips. Thus, the dichotomy between T-like and B-like cells and the presence of dedicated lymphopoietic tissues emerge as ancestral vertebrate features, whereas the somatic diversification of structurally distinct antigen receptor genes evolved independently in jawless and jawed vertebrates.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-immunol-042617-053028
2018-04-26
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/immunol/36/1/annurev-immunol-042617-053028.html?itemId=/content/journals/10.1146/annurev-immunol-042617-053028&mimeType=html&fmt=ahah

Literature Cited

  1. Janvier P. 1.  2015. Facts and fancies about early fossil chordates and vertebrates. Nature 520:483–89 [Google Scholar]
  2. Finstad J, Good RA. 2.  1964. The evolution of the immune response: III. Immunologic responses in the lamprey. J. Exp. Med. 120:1151–68 [Google Scholar]
  3. Fujii T, Nakagawa H, Murakawa S. 3.  1979. Immunity in lamprey: I. Production of haemolytic and haemagglutinating antibody to sheep red blood cells in Japanese lampreys. Dev. Comp. Immunol. 3:441–51 [Google Scholar]
  4. Litman GW, Finstad FJ, Howell J, Pollara BW, Good RA. 4.  1970. The evolution of the immune response: VIII. Structural studies of the lamprey immunoglobulin. J. Immunol. 105:1278–85 [Google Scholar]
  5. Pollara B, Litman GW, Finstad J, Howell J, Good RA. 5.  1970. The evolution of the immune response: VII. Antibody to human “O” cells and properties of the immunoglobulin in lamprey. J. Immunol. 105:738–45 [Google Scholar]
  6. Hagen M, Filosa MF, Youson JH. 6.  1985. The immune response in adult sea lamprey (Petromyzon marinus L.): the effect of temperature. Comp. Biochem. Physiol. 82:207–10 [Google Scholar]
  7. Linthicum DS, Hildemann WH. 7.  1970. Immunologic responses of Pacific hagfish: III. Serum antibodies to cellular antigens. J. Immunol. 105:912–18 [Google Scholar]
  8. Fujii T, Hayakawa I. 8.  1983. A histological and electron-microscopic study of the cell types involved in rejection of skin allografts in ammocoetes. Cell Tissue Res 231:301–12 [Google Scholar]
  9. Hildemann WH, Thoenes GH. 9.  1969. Immunological responses of Pacific hagfish: I. Skin transplantation immunity. Transplantation 7:506–21 [Google Scholar]
  10. Mayer WE, Uinuk-ool T, Tichy H, Gartland LA, Klein J, Cooper MD. 10.  2002. Isolation and characterization of lymphocyte-like cells from a lamprey. PNAS 99:14350–55 [Google Scholar]
  11. Uinuk-ool T, Mayer WE, Sato A, Dongak R, Cooper MD, Klein J. 11.  2002. Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. PNAS 99:14356–61 [Google Scholar]
  12. McCurley N, Hirano M, Das S, Cooper MD. 12.  2012. Immune related genes underpin the evolution of adaptive immunity in jawless vertebrates. Curr. Genom. 13:86–94 [Google Scholar]
  13. Pancer Z, Amemiya CT, Ehrhardt GRA, Ceitlin J, Gartland GL, Cooper MD. 13.  2004. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174–80 [Google Scholar]
  14. Guo P, Hirano M, Herrin BR, Li J, Yu C. 14.  et al. 2009. Dual nature of the adaptive immune system in lampreys. Nature 459:796–801 [Google Scholar]
  15. Rogozin IB, Iyer LM, Liang L, Glazko GV, Liston VG. 15.  et al. 2007. Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat. Immunol. 8:647–56 [Google Scholar]
  16. Li J, Das S, Herrin BR, Hirano M, Cooper MD. 16.  2013. Definition of a third VLR gene in hagfish. PNAS 110:15013–18 [Google Scholar]
  17. Pancer Z, Saha NR, Kasamatsu J, Suzuki T, Amemiya CT. 17.  et al. 2005. Variable lymphocyte receptors in hagfish. PNAS 102:9224–29 [Google Scholar]
  18. Kasamatsu J, Sutoh Y, Fugo K, Otsuka N, Iwabuchi K, Kasahara M. 18.  2010. Identification of a third variable lymphocyte receptor in the lamprey. PNAS 107:14304–8 [Google Scholar]
  19. Alder MN, Rogozin IB, Iyer LM, Glazko GV, Cooper MD, Pancer Z. 19.  2005. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970–73 [Google Scholar]
  20. Nagawa F, Kishishita N, Shimizu K, Hirose S, Miyoshi M. 20.  et al. 2007. Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nat. Immunol. 8:206–13 [Google Scholar]
  21. Han BW, Herrin BR, Cooper MD, Wilson IA. 21.  2008. Antigen recognition by variable lymphocyte receptors. Science 321:1834–37 [Google Scholar]
  22. Velikovsky CA, Deng L, Tasumi S, Iyer LM, Kerzic MC. 22.  et al. 2009. Structure of a lamprey variable lymphocyte receptor in complex with a protein antigen. Nat. Struct. Mol. Biol. 16:725–30 [Google Scholar]
  23. Kishishita N, Matsuno T, Takahashi Y, Takaba H, Nishizumi H, Nagawa F. 23.  2010. Regulation of antigen-receptor gene assembly in hagfish. EMBO Rep 11:126–32 [Google Scholar]
  24. Herrin BR, Alder MN, Roux KH, Sina C, Ehrhardt GR. 24.  et al. 2008. Structure and specificity of lamprey monoclonal antibodies. PNAS 105:2040–45 [Google Scholar]
  25. Tasumi S, Velikovsky CA, Xu G, Gai SA, Wittrup KD. 25.  et al. 2009. High-affinity lamprey VLRA and VLRB monoclonal antibodies. PNAS 106:12891–96 [Google Scholar]
  26. Deng L, Velikovsky CA, Xu G, Iyer LM, Tasumi S. 26.  et al. 2010. A structural basis for antigen recognition by the T cell-like lymphocytes of sea lamprey. PNAS 107:13408–13 [Google Scholar]
  27. Kim HM, Oh SC, Lim KJ, Kasamatsu J, Heo JY. 27.  et al. 2007. Structural diversity of the hagfish variable lymphocyte receptors. J. Biol. Chem. 282:6726–32 [Google Scholar]
  28. Das S, Hirano M, Aghaallaei N, Bajoghli B, Boehm T, Cooper MD. 28.  2013. Organization of lamprey variable lymphocyte receptor C locus and repertoire development. PNAS 110:6043–48 [Google Scholar]
  29. Kirchdoerfer RN, Herrin BR, Han BW, Turnbough CL Jr., Cooper MD, Wilson IA. 29.  2012. Variable lymphocyte receptor recognition of the immunodominant glycoprotein of Bacillus anthracis spores. Structure 20:479–86 [Google Scholar]
  30. Hirano M, Guo P, McCurley N, Schorpp M, Das S. 30.  et al. 2013. Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501:435–38 [Google Scholar]
  31. Luo M, Velikovsky CA, Yang X, Siddiqui MA, Hong X. 31.  et al. 2013. Recognition of the Thomsen-Friedenreich pancarcinoma carbohydrate antigen by a lamprey variable lymphocyte receptor. J. Biol. Chem. 288:23597–606 [Google Scholar]
  32. Holland SJ, Gao M, Hirano M, Iyer LM, Luo M. 32.  et al. 2014. Selection of the lamprey VLRC antigen receptor repertoire. PNAS 111:14834–39 [Google Scholar]
  33. Das S, Li J, Holland SJ, Iyer LM, Hirano M. 33.  et al. 2014. Genomic donor cassette sharing during VLRA and VLRC assembly in jawless vertebrates. PNAS 111:14828–33 [Google Scholar]
  34. Sutoh Y, Kasahara M. 34.  2014. Copy number and sequence variation of leucine-rich repeat modules suggests distinct functional constraints operating on variable lymphocyte receptors expressed by agnathan T cell-like and B cell-like lymphocytes. Immunogenetics 66:403–9 [Google Scholar]
  35. Im SP, Lee JS, Kim SW, Yu JE, Kim YR. 35.  et al. 2016. Investigation of variable lymphocyte receptors in the alternative adaptive immune response of hagfish. Dev. Comp. Immunol. 55:203–10 [Google Scholar]
  36. Alder MN, Herrin BR, Sadlonova A, Stockard CR, Grizzle WE. 36.  et al. 2008. Antibody responses of variable lymphocyte receptors in the lamprey. Nat. Immunol. 9:319–27 [Google Scholar]
  37. Altman MO, Bennink JR, Yewdell JW, Herrin BR. 37.  2015. Lamprey VLRB response to influenza virus supports universal rules of immunogenicity and antigenicity. eLife 4:e07467 [Google Scholar]
  38. Kanda R, Sutoh Y, Kasamatsu J, Maenaka K, Kasahara M, Ose T. 38.  2014. Crystal structure of the lamprey variable lymphocyte receptor C reveals an unusual feature in its N-terminal capping module. PLOS ONE 9:e85875 [Google Scholar]
  39. Lee SC, Park K, Han J, Lee JJ, Kim HJ. 39.  et al. 2012. Design of a binding scaffold based on variable lymphocyte receptors of jawless vertebrates by module engineering. PNAS 109:3299–304 [Google Scholar]
  40. Stanfield RL, Dooley H, Flajnik MF, Wilson IA. 40.  2004. Crystal structure of a shark single-domain antibody V region in complex with lysozyme. Science 305:1770–73 [Google Scholar]
  41. Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD. 41.  2012. VLR-based adaptive immunity. Annu. Rev. Immunol. 30:203–20 [Google Scholar]
  42. Das S, Li J, Hirano M, Sutoh Y, Herrin BR, Cooper MD. 42.  2015. Evolution of two prototypic T cell lineages. Cell. Immunol. 296:87–94 [Google Scholar]
  43. Kasahara M. 43.  2015. Variable lymphocyte receptors: a current overview. Pathogen-Host Interactions: Antigenic Variation v. Somatic Adaptations E Hsu, L Du Pasquier 175–92 Results Probl. Cell Differ 57 Basel, Switz: Springer Int https://doi.org/10.1007/978-3-319-20819-0_8 [Crossref] [Google Scholar]
  44. Kishishita N, Nagawa F. 44.  2014. Evolution of adaptive immunity: implications of a third lymphocyte lineage in lampreys. BioEssays 36:244–50 [Google Scholar]
  45. Kasamatsu J, Suzuki T, Ishijima J, Matsuda Y, Kasahara M. 45.  2007. Two variable lymphocyte receptor genes of the inshore hagfish are located far apart on the same chromosome. Immunogenetics 59:329–31 [Google Scholar]
  46. Krangel MS, McMurry MT, Hernandez-Munain C, Zhong X-P, Carabana J. 46.  2000. Accessibility control of T cell receptor gene rearrangement in developing thymocytes: the TCR α/δ locus. Immunol. Res. 22:127–35 [Google Scholar]
  47. Vettermann C, Schlissel MS. 47.  2010. Allelic exclusion of immunoglobulin genes: models and mechanisms. Immunol. Rev. 237:22–42 [Google Scholar]
  48. Parsons MJ, Chan JTH, Sun H, Ehrhardt GRA. 48.  2014. Variable lymphocyte receptor-based adaptive immunity in the agnathan sea lamprey. Comparative Immunoglobulin Genetics AK Kaushik, Y Pasman 1–16 Oakville, Can.: Apple Acad. [Google Scholar]
  49. Vantourout P, Hayday A. 49.  2013. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat. Rev. Immunol. 13:88–100 [Google Scholar]
  50. Van Rhijn I, Godfrey DI, Rossjohn J, Moody DB. 50.  2015. Lipid and small-molecule display by CD1 and MR1. Nat. Rev. Immunol. 15:643–54 [Google Scholar]
  51. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. 51.  2003. Predominant autoantibody production by early human B cell precursors. Science 301:1374–77 [Google Scholar]
  52. Xing Y, Hogquist KA. 52.  2012. T-cell tolerance: central and peripheral. Cold Spring Harb. Perspect. Biol. 4:a006957 [Google Scholar]
  53. Bajoghli B, Guo P, Aghaallaei N, Hirano M, Strohmeier C. 53.  et al. 2011. A thymus candidate in lampreys. Nature 470:90–94 [Google Scholar]
  54. Di Noia JM, Neuberger MS. 54.  2007. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76:1–22 [Google Scholar]
  55. Chen H, Kshirsagar S, Jensen I, Lau K, Covarrubias R. 55.  et al. 2009. Characterization of arrangement and expression of the T cell receptor γ locus in the sandbar shark. PNAS 106:8591–96 [Google Scholar]
  56. Qi Q, Liu Y, Cheng Y, Glanville J, Zhang D. 56.  et al. 2014. Diversity and clonal selection in the human T-cell repertoire. PNAS 111:13139–44 [Google Scholar]
  57. Čičin-Šain L, Messaoudi I, Park B, Currier N, Planer S. 57.  et al. 2007. Dramatic increase in naive T cell turnover is linked to loss of naive T cells from old primates. PNAS 104:19960–65 [Google Scholar]
  58. Thompson CB, Neiman PE. 58.  1987. Somatic diversification of the chicken immunoglobulin light chain gene is limited to the rearranged variable gene segment. Cell 48:369–78 [Google Scholar]
  59. Reynaud C-A, Anquez V, Grimal H, Weill J-C. 59.  1987. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell 48:379–88 [Google Scholar]
  60. Becker RS, Knight KL. 60.  1990. Somatic diversification of immunoglobulin heavy chain VDJ genes: evidence for somatic gene conversion in rabbits. Cell 63:987–97 [Google Scholar]
  61. Parng C-L, Hansal S, Goldsby RA, Osborne BA. 61.  1996. Gene conversion contributes to Ig light chain diversity in cattle. J. Immunol. 157:5478–86 [Google Scholar]
  62. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. 62.  2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553–63 [Google Scholar]
  63. Revy P, Muto T, Levy Y, Geissmann F, Plebani A. 63.  et al. 2000. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell 102:565–75 [Google Scholar]
  64. Conticello SG, Langlois M-A, Yang Z, Neuberger MS. 64.  2007. DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv. Immunol. 94:37–73 [Google Scholar]
  65. Hirano M. 65.  2015. Evolution of vertebrate adaptive immunity: immune cells and tissues, and AID/APOBEC cytidine deaminases. BioEssays 37:877–87 [Google Scholar]
  66. Schatz DG, Oettinger MA, Schlissel MS. 66.  1992. V(D)J recombination: molecular biology and regulation. Annu. Rev. Immunol. 10:359–83 [Google Scholar]
  67. Ardavin CF, Gomariz RP, Barrutia MG, Fonfria J, Zapata A. 67.  1984. The lympho-hemopoietic organs of the anadromous sea lamprey, Petromyzon marinus: a comparative study throughout its life span. Acta Zool 65:1–15 [Google Scholar]
  68. Lada AG, Dhar A, Boissy RJ, Hirano M, Rubel AA. 68.  et al. 2012. AID/APOBEC cytosine deaminase induces genome-wide kataegis. Biol. Direct 7:47 [Google Scholar]
  69. Square T, Romášek M, Jandzik D, Cattell MV, Klymkowsky M, Medeiros DM. 69.  2015. CRISPR/Cas9-mediated mutagenesis in the sea lamprey Petromyzon marinus: a powerful tool for understanding ancestral gene functions in vertebrates. Development 142:4180–87 [Google Scholar]
  70. Lada AG, Krick CF, Kozmin SG, Mayorov VI, Karpova TS. 70.  et al. 2011. Mutator effects and mutation signatures of editing deaminases produced in bacteria and yeast. Biochemistry 76:131–46 [Google Scholar]
  71. Lada AG, Stepchenkova EI, Waisertreiger IS, Noskov VN, Dhar A. 71.  et al. 2013. Genome-wide mutation avalanches induced in diploid yeast cells by a base analog or an APOBEC deaminase. PLOS Genet 9:e1003736 [Google Scholar]
  72. Helleday T, Eshtad S, Nik-Zainal S. 72.  2014. Mechanisms underlying mutational signatures in human cancers. Nat. Rev. Genet. 15:585–98 [Google Scholar]
  73. Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M. 73.  et al. 2016. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353:aaf8729 [Google Scholar]
  74. Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T. 74.  et al. 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol. 35:441–43 [Google Scholar]
  75. Choe J, Kelker MS, Wilson IA. 75.  2005. Crystal structure of human Toll-like receptor 3 (TLR3) ectodomain. Science 309:581–85 [Google Scholar]
  76. Bell JK, Botos I, Hall PR, Askins J, Shiloach J. 76.  et al. 2005. The molecular structure of the Toll-like receptor 3 ligand-binding domain. PNAS 102:10976–80 [Google Scholar]
  77. Hong X, Ma MZ, Gildersleeve JC, Chowdhury S, Barchi JJ Jr.. 77.  et al. 2013. Sugar-binding proteins from fish: selection of high affinity “lambodies” that recognize biomedically relevant glycans. ACS Chem. Biol. 8:152–60 [Google Scholar]
  78. Imberty A, Mitchell EP, Wimmerová M. 78.  2005. Structural basis of high-affinity glycan recognition by bacterial and fungal lectins. Curr. Opin. Struct. Biol. 15:525–34 [Google Scholar]
  79. Bundle DR, Eichler E, Gidney MAJ, Meldal M, Ragauskas A. 79.  et al. 1994. Molecular recognition of a Salmonella trisaccharide epitope by monoclonal antibody Se155-4. Biochemistry 33:5172–82 [Google Scholar]
  80. De Genst E, Silence K, Decanniere K, Conrath K, Loris R. 80.  et al. 2006. Molecular basis for the preferential cleft recognition by dromedary heavy-chain antibodies. PNAS 103:4586–91 [Google Scholar]
  81. Wu F, Chen L, Ren Y, Yang X, Yu T. 81.  et al. 2016. An inhibitory receptor of VLRB in the agnathan lamprey. Sci. Rep. 6:33760 [Google Scholar]
  82. Ravetch JV, Lanier LL. 82.  2000. Immune inhibitory receptors. Science 290:84–89 [Google Scholar]
  83. Chien Y-H, Konigshofer Y. 83.  2007. Antigen recognition by γδ T cells. Immunol. Rev. 215:46–58 [Google Scholar]
  84. Nakahara H, Herrin BR, Alder MN, Catera R, Yan XJ. 84.  et al. 2013. Chronic lymphocytic leukemia monitoring with a lamprey idiotope-specific antibody. Cancer Immunol. Res. 1:223–28 [Google Scholar]
  85. Wezner-Ptasinska M, Otlewski J. 85.  2015. Selection of specific interactors from phage display library based on sea lamprey variable lymphocyte receptor sequences. Biochim. Biophys. Acta 1854:1833–41 [Google Scholar]
  86. Yu C, Ali S, St-Germain J, Liu Y, Yu X. 86.  et al. 2012. Purification and identification of cell surface antigens using lamprey monoclonal antibodies. J. Immunol. Methods 386:43–49 [Google Scholar]
  87. Yu C, Liu Y, Chan JTH, Tong J, Li Z. 87.  et al. 2016. Identification of human plasma cells with a lamprey monoclonal antibody. JCI Insight 1:e84738 [Google Scholar]
  88. Maus MV, June CH. 88.  2016. Making better chimeric antigen receptors for adoptive T-cell therapy. Clin. Cancer Res. 22:1875–84 [Google Scholar]
  89. Moot R, Raikar SS, Fleischer L, Querrey M, Tylawsky DE. 89.  et al. 2016. Genetic engineering of chimeric antigen receptors using lamprey derived variable lymphocyte receptors. Mol. Ther. Oncolytics 3:16026 [Google Scholar]
  90. Velásquez AC, Nomura K, Cooper MD, Herrin BR, He SY. 90.  2017. Leucine-rich-repeat-containing variable lymphocyte receptors as modules to target plant-expressed proteins. Plant Methods 13:29 [Google Scholar]
  91. Ramirez K, Witherden DA, Havran WL. 91.  2015. All hands on DE(T)C: Epithelial-resident γδ T cells respond to tissue injury. Cell. Immunol. 296:57–61 [Google Scholar]
  92. Boehm T. 92.  2011. Design principles of adaptive immune systems. Nat. Rev. Immunol. 11:307–17 [Google Scholar]
  93. Boehm T, Hess I, Swann JB. 93.  2012. Evolution of lymphoid tissues. Trends Immunol 33:315–21 [Google Scholar]
  94. Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N. 94.  et al. 2013. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat. Genet. 45:415–21, 421e1–2 [Google Scholar]
  95. Mehta TK, Ravi V, Yamasaki S, Lee AP, Lian MM. 95.  et al. 2013. Evidence for at least six Hox clusters in the Japanese lamprey (Lethenteron japonicum). PNAS 110:16044–49 [Google Scholar]
  96. Smith LC, Clow LA, Terwilliger DP. 96.  2001. The ancestral complement system in sea urchins. Immunol. Rev. 180:16–34 [Google Scholar]
  97. Matsushita M, Matsushita A, Endo Y, Nakata M, Kojima N. 97.  et al. 2004. Origin of the classical complement pathway: lamprey orthologue of mammalian C1q acts as a lectin. PNAS 101:10127–31 [Google Scholar]
  98. Wu F, Chen L, Liu X, Wang H, Su P. 98.  et al. 2013. Lamprey variable lymphocyte receptors mediate complement-dependent cytotoxicity. J. Immunol. 190:922–30 [Google Scholar]
  99. Kuroda N, Uinuk-ool TS, Sato A, Samonte IE, Figueroa F. 99.  et al. 2003. Identification of chemokines and a chemokine receptor in cichlid fish, shark, and lamprey. Immunogenetics 54:884–95 [Google Scholar]
  100. Bajoghli B, Aghaallaei N, Hess I, Rode I, Netuschil N. 100.  et al. 2009. Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell 138:186–97 [Google Scholar]
  101. Han Q, Das S, Hirano M, Holland SJ, McCurley N. 101.  et al. 2015. Characterization of lamprey IL-17 family members and their receptors. J. Immunol. 195:5440–51 [Google Scholar]
  102. Raison RL, Gilbertson P, Wotherspoon J. 102.  1987. Cellular requirements for mixed leucocyte reactivity in the cyclostome, Eptatretus stoutii. . Immunol. Cell Biol. 65:Part 2183–88 [Google Scholar]
  103. Yamaguchi T, Takamune K, Kondo M, Takahashi Y, Kato-Unoki Y. 103.  et al. 2014. Hagfish C1q: its unique binding property. Dev. Comp. Immunol. 43:47–53 [Google Scholar]
  104. Takaba H, Imai T, Miki S, Morishita Y, Miyashita A. 104.  et al. 2013. A major allogenic leukocyte antigen in the agnathan hagfish. Sci. Rep. 3:1716 [Google Scholar]
  105. Haruta C, Suzuki T, Kasahara M. 105.  2006. Variable domains in hagfish: NICIR is a polymorphic multigene family expressed preferentially in leukocytes and is related to lamprey TCR-like. . Immunogenetics 58:216–25 [Google Scholar]
  106. Suzuki T, Shin IT, Kohara Y, Kasahara M. 106.  2004. Transcriptome analysis of hagfish leukocytes: a framework for understanding the immune system of jawless fishes. Dev. Comp. Immunol. 28:993–1003 [Google Scholar]
  107. Cao D-D, Liao X, Cheng W, Jiang Y-L, Wang W-J. 107.  et al. 2016. Structure of a variable lymphocyte receptor-like protein from the amphioxus Branchiostoma floridae. . Sci. Rep. 6:19951 [Google Scholar]
  108. Cooper MD, Alder MN. 108.  2006. The evolution of adaptive immune systems. Cell 124:815–22 [Google Scholar]
  109. Litman GW, Rast JP, Fugmann SD. 109.  2010. The origins of vertebrate adaptive immunity. Nat. Rev. Immunol. 10:543–53 [Google Scholar]
  110. Flajnik MF, Kasahara M. 110.  2010. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11:47–59 [Google Scholar]
  111. Zhang Y, Xu K, Deng A, Fu X, Xu A, Liu X. 111.  2014. An amphioxus RAG1-like DNA fragment encodes a functional central domain of vertebrate core RAG1. PNAS 111:397–402 [Google Scholar]
  112. Huang S, Tao X, Yuan S, Zhang Y, Li P. 112.  et al. 2016. Discovery of an active RAG transposon illuminates the origins of V(D)J recombination. Cell 166:102–14 [Google Scholar]
  113. Fujii T. 113.  1982. Electron microscopy of the leucocytes of the typhlosole in ammocoetes, with special attention to the antibody-producing cells. J. Morphol. 173:87–100 [Google Scholar]
  114. Linthicum DS. 114.  1975. Ultrastructure of hagfish blood leucocytes. Adv. Exp. Med. Biol. 64:241–50 [Google Scholar]
  115. Lim AI, Verrier T, Vosshenrich CAJ, Di Santo JP. 115.  2017. Developmental options and functional plasticity of innate lymphoid cells. Curr. Opin. Immunol. 44:61–68 [Google Scholar]
  116. Vivier E, van de Pavert SA, Cooper MD, Belz GT. 116.  2016. The evolution of innate lymphoid cells. Nat. Immunol. 17:790–94 [Google Scholar]
  117. Fukuda M. 117.  2006. Rab27 and its effectors in secretory granule exocytosis: a novel docking machinery composed of a Rab27·effector complex. Biochem. Soc. Trans. 34:691–95 [Google Scholar]
  118. Macaulay IC, Ponting CP, Voet T. 118.  2017. Single-cell multiomics: multiple measurements from single cells. Trends Genet 33:155–68 [Google Scholar]
  119. Herrin BR, Hirano M, Li J, Das S, Sutoh Y, Cooper MD. 119.  2015. B cells and antibodies in jawless vertebrates. Molecular Biology of B Cells T Honjo, M Reth, A Radbruch, F Alt 121–32 Cambridge, MA: Academic, 2nd ed.. [Google Scholar]
  120. Hirano M, Das S, Guo P, Cooper MD. 120.  2011. The evolution of adaptive immunity in vertebrates. Adv. Immunol. 109:125–57 [Google Scholar]
/content/journals/10.1146/annurev-immunol-042617-053028
Loading
/content/journals/10.1146/annurev-immunol-042617-053028
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error