Origin and evolution of adaptive immunity

Annual Review of Animal Biosciences

Volumn 2, Issue , 2014, Pages 259-283

  Boehm, Thomas ^a   Swann, Jeremy B ^a  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

antigen receptor; lymphocyte; lymphoid organ; somatic diversification

Indexed keywords

ADAPTIVE IMMUNITY; ANIMAL; EVOLUTION; GENETICS; IMMUNOLOGY; LYMPHOID TISSUE; VERTEBRATE;

ADAPTIVE IMMUNITY; ANIMALS; BIOLOGICAL EVOLUTION; LYMPHOID TISSUE; VERTEBRATES;

EID: 84906272537     PISSN: 21658102     EISSN: 21658110     Source Type: Journal    
DOI: 10.1146/annurev-animal-022513-114201     Document Type: Article

References (160)

1. Pancer Z, Amemiya CT, Ehrhardt GRA, Ceitlin J, Gartland GL, Cooper MD. 2004. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174-80
2. Guo P, Hirano M, Herrin BR, Li J, Yu C, et al. 2009. Dual nature of the adaptive immune system in lampreys. Nature 459:796-801
3. Flajnik MF, Du Pasquier L. 2004. Evolution of innate and adaptive immunity: Can we draw a line? Trends Immunol. 25:640-44
4. Pancer Z, Cooper MD. 2006. The evolution of adaptive immunity. Annu. Rev. Immunol. 24:497-518
5. Cooper MD, Alder MN. 2006. The evolution of adaptive immune systems. Cell 124:815-22
6. Du Pasquier L. 2005. Meeting the demand for innate and adaptive immunities during evolution. Scand. J. Immunol. 62(Suppl. 1):39-48
7. Litman GW, Rast JP, Fugmann SD. 2010. The origins of vertebrate adaptive immunity. Nat. Rev. Immunol. 10:543-53
8. Flajnik MF, Kasahara M. 2010. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11:47-59
9. Herrin BR, Cooper MD. 2010. Alternative adaptive immunity in jawless vertebrates. J. Immunol. 185:1367-74
10. CooperMD, Herrin BR. 2010. How did our complex immune system evolve? Nat. Rev. Immunol. 10:2-3
11. Boehm T. 2011. Design principles of adaptive immune systems. Nat. Rev. Immunol. 11:307-17
12. Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD. 2012. VLR-based adaptive immunity. Annu. Rev. Immunol. 30:203-20
13. Boehm T, Iwanami N, Hess I. 2012. Evolution of the immune system in the lower vertebrates. Annu. Rev. Genomics Hum. Genet. 13:127-49
14. Boehm T. 2012. Evolution of vertebrate immunity. Curr. Biol. 22:R722-32
15. Shintani S, Terzic J, Sato A, Saraga-Babic M, O'hUigin C, et al. 2000. Do lampreys have lymphocytes? The Spi evidence. Proc. Natl. Acad. Sci. USA 97:7417-22
16. Mayer WE, Uinuk-ool T, Tichy H, Gartland LA, Klein J, Cooper MD. 2002. Isolation and characterization of lymphocyte-like cells from a lamprey. Proc. Natl. Acad. Sci. USA 99:14350-55
17. Uinuk-ool T, Mayer WE, Sato A, Dongak R, Cooper MD, Klein J. 2002. Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. Proc. Natl. Acad. Sci. USA 99:14356-61
18. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, et al. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946-57
19. Heimberg AM, Cowper-Sal-lari R, Sémon M, Donoghue PCJ, Peterson KJ. 2010. microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc. Natl. Acad. Sci. USA 107:19379-83
20. Janvier P. 2010. microRNAs revive old views about jawless vertebrate divergence and evolution. Proc. Natl. Acad. Sci. USA 107:19137-38
21. King BL, Gillis JA, Carlisle HR, Dahn RD. 2011.Anatural deletion of the HoxC cluster in elasmobranch fishes. Science 334:1517
22. Boehm T, Hess I, Swann JB. 2012. Evolution of lymphoid tissues. Trends Immunol. 33:315-21
23. Finstad J, Papermaster BW, Good RA. 1964. Evolution of the immune response. II. Morphologic studies on the origin of the thymus and organized lymphoid tissue. Lab. Investig. 13:490-512
24. Hansen JD, Zapata AG. 1998. Lymphocyte development in fish and amphibians. Immunol. Rev. 166:199-220
25. Matsunaga T, Rahman A. 2001. In search of the origin of the thymus: The thymus and GALT may be evolutionarily related. Scand. J. Immunol. 53:1-6
26. Hartenstein V. 2006. Blood cells and blood cell development in the animal kingdom. Annu. Rev. Cell Dev. Biol. 22:677-712
27. Tokoyoda K, Egawa T, Sugiyama T, Choi B-I, Nagasawa T. 2004. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20:707-18
28. Nagasawa T. 2006. Microenvironmental niches in the bone marrow required for B-cell development. Nat. Rev. Immunol. 6:107-16
29. Di Santo JP, Rodewald H-R. 1998. In vivo roles of receptor tyrosine kinases and cytokine receptors in early thymocyte development. Curr. Opin. Immunol. 10:196-207
30. Jensen CT, Kharazi S, Böiers C, Cheng M, Lübking A, et al. 2008. FLT3 ligand and not TSLP is the key regulator of IL-7-independent B-1 and B-2 B lymphopoiesis. Blood 112:2297-304
31. Bajoghli B, Guo P, Aghaallaei N, Hirano M, Strohmeier C, et al. 2011. A thymus candidate in lampreys. Nature 470:90-94
32. Nehls M, Kyewski B,Messerle M, Waldschütz R, Schüddekopf K, et al. 1996. Two genetically separable steps in the differentiation of thymic epithelium. Science 272:886-89
33. Corbeaux T, Hess I, Swann JB, Kanzler B, Haas-Assenbaum A, Boehm T. 2010. Thymopoiesis in mice depends on a Foxn1-positive thymic epithelial cell lineage. Proc. Natl. Acad. Sci. USA 107:16613-18
34. Bajoghli B, Aghaallaei N, Hess I, Rode I, Netuschil N, et al. 2009. Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell 138:186-97
35. Calderón L, Boehm T. 2011. Three chemokine receptors cooperatively regulate homing of hematopoietic progenitors to the embryonic mouse thymus. Proc. Natl. Acad. Sci. USA 108:7517-22
36. Hess I, Boehm T. 2012. Intravital imaging of thymopoiesis reveals dynamic lympho-epithelial interactions. Immunity 36:298-309
37. Lloyd-Evans P. 1993. Development of the lymphomyeloid system in the dogfish, Scyliorhinus canicula. Dev. Comp. Immunol. 17:501-14
38. Zapata A, Diez B, Cejalvo T, Gutiérrez-de Frías C, Cortés A. 2006. Ontogeny of the immune system of fish. Fish Shellfish Immunol. 20:126-36
39. Kendall MD. 1980. Avian thymus glands: a review. Dev. Comp. Immunol. 4:191-209
40. Miller JF. 1961. Immunological function of the thymus. Lancet 2:748-49
41. TerszowskiG,Müller SM, Bleul CC, Blum C, Schirmbeck R, et al. 2006. Evidence for a functional second thymus in mice. Science 312:284-87
42. Dooley J, EricksonM, GillardGO, Farr AG. 2006. Cervical thymus in themouse. J. Immunol. 176:6484-90
43. Rossi SW, JenkinsonWE,Anderson G, Jenkinson EJ. 2006. Clonal analysis reveals a common progenitor for thymic cortical and medullary epithelium. Nature 441:988-91
44. Bleul CC, Corbeaux T, Reuter A, Fisch P, Mönting JS, Boehm T. 2006. Formation of a functional thymus initiated by a postnatal epithelial progenitor cell. Nature 441:992-96
45. Petrie HT, Zúñiga-Pflücker JC. 2007. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu. Rev. Immunol. 25:649-79
46. Rodewald H-R. 2008. Thymus organogenesis. Annu. Rev. Immunol. 26:355-88
47. Anderson G, Lane PJL, Jenkinson EJ. 2007. Generating intrathymic microenvironments to establish T-cell tolerance. Nat. Rev. Immunol. 7:954-63
48. Hozumi K, Mailhos C, Negishi I, Hirano K, Yahata T, et al. 2008. Delta-like 4 is indispensable in thymic environment specific for T cell development. J. Exp. Med. 205:2507-13
49. Koch U, Fiorini E, Benedito R, Besseyrias V, Schuster-Gossler K, et al. 2008. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205:2515-23
50. Brendolan A, Rosado MM, Carsetti R, Selleri L, Dear TN. 2007. Development and function of the mammalian spleen. Bioessays 29:166-77
51. Finstad J, Good RA. 1964. The evolution of the immune response. III. Immunologic responses in the lamprey. J. Exp. Med. 120:1151-68
52. Borysenko M, Cooper EL. 1972. Lymphoid tissue in the snapping turtle, Chelydra serpentina. J. Morphol. 138:487-97
53. Sugimura M, Hashimoto Y, Nakanishi YH. 1977. Thymus-and bursa-dependent areas in duck lymph nodes. Jpn. J. Vet. Res. 25:7-16
54. Mueller SN, Germain RN. 2009. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat. Rev. Immunol. 9:618-29
55. Junt T, Scandella E, Ludewig B. 2008. Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat. Rev. Immunol. 8:764-75
56. van de Pavert SA, Mebius RE. 2010. New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 10:664-74
57. Biggs PM. 1957. The association of lymphoid tissue with the lymph vessels in the domestic chicken (Gallus domesticus). Acta Anat. 29:36-47
58. Ruddle NH, Akirav EM. 2009. Secondary lymphoid organs: responding to genetic and environmental cues in ontogeny and the immune response. J. Immunol. 183:2205-12
59. Lane PJL, McConnell FM,Withers D, Gaspal F, Saini M, Anderson G. 2010. Lymphoid tissue inducer cells and the evolution of CD4 dependent high-affinity antibody responses. Prog. Mol. Biol. Transl. Sci. 92:159-74
60. Castagnaro L, Lenti E, Maruzzelli S, Spinardi L, Migliori E, et al. 2013. Nkx2-5\+Islet1\+ mesenchymal precursors generate distinct spleen stromal cell subsets and participate in restoring stromal network integrity. Immunity 38:782-91
61. Bénézech C, Mader E, Desanti G, Khan M, Nakamura K, et al. 2012. Lymphotoxin-b receptor signaling through NF-kB2-RelB pathway reprograms adipocyte precursors as lymph node stromal cells. Immunity 37:721-34
62. Han Y, Huang G, Zhang Q, Yuan S, Liu J, et al. 2010. The primitive immune system of amphioxus provides insights into the ancestral structure of the vertebrate immune system. Dev. Comp. Immunol. 34:791-96
63. Cooper MD, Peterson RD, Good RA. 1965. Delineation of the thymic and bursal lymphoid systems in the chicken. Nature 205:143-46
64. Dias S, Xu W, McGregor S, Kee B. 2008. Transcriptional regulation of lymphocyte development. Curr. Opin. Genet. Dev. 18:441-48
65. Ramírez J, Lukin K, Hagman J. 2010. From hematopoietic progenitors to B cells: mechanisms of lineage restriction and commitment. Curr. Opin. Immunol. 22:177-84
66. Rothenberg EV, Zhang J, Li L. 2010. Multilayered specification of the T-cell lineage fate. Immunol. Rev. 238:150-68
67. Sakano H, Hüppi K, Heinrich G, Tonegawa S. 1979. Sequences at the somatic recombination sites of immunoglobulin light-chain genes. Nature 280:288-94
68. Davis MM, Bjorkman PJ. 1988. T-cell antigen receptor genes and T-cell recognition. Nature 334:395-402
69. Kasamatsu J, Sutoh Y, Fugo K, Otsuka N, Iwabuchi K, Kasahara M. 2010. Identification of a third variable lymphocyte receptor in the lamprey. Proc. Natl. Acad. Sci. USA 107:14304-8
70. BusslingerM. 2004. Transcriptional control of early B cell development. Annu. Rev. Immunol. 22:55-79
71. Bertrand JY, Traver D. 2009. Hematopoietic cell development in the zebrafish embryo. Curr. Opin. Hematol. 16:243-48
72. Jing L, Zon LI. 2011. Zebrafish as a model for normal and malignant hematopoiesis. Dis. Model. Mech. 4:433-38
73. Ellett F, Lieschke GJ. 2010. Zebrafish as a model for vertebrate hematopoiesis. Curr. Opin. Pharmacol. 10:563-70
74. Anderson MK, Pant R, Miracle AL, Sun X, Luer CA, et al. 2004. Evolutionary origins of lymphocytes: ensembles of T cell and B cell transcriptional regulators in a cartilaginous fish. J. Immunol. 172:5851-60
75. Zlotoff DA, Bhandoola A. 2011. Hematopoietic progenitor migration to the adult thymus. Ann. N.Y. Acad. Sci. 1217:122-38
76. Janas ML, Turner M. 2010. Stromal cell-derived factor 1a and CXCR4: newly defined requirements for efficient thymic b-selection. Trends Immunol. 31:370-76
77. Calderón L, Boehm T. 2012. Synergistic, context-dependent and hierarchical functions of epithelial components in thymic microenvironments. Cell 149:159-72
78. Kisielow P, von Boehmer H. 1991. Kinetics of negative and positive selection in the thymus. Adv. Exp. Med. Biol. 292:31-42
79. Kreslavsky T, von Boehmer H. 2010. gdTCR ligands and lineage commitment. Semin. Immunol. 22:214-21
80. Maki K, Sunaga S, Komagata Y, Kodaira Y, Mabuchi A, et al. 1996. Interleukin 7 receptor-deficient mice lack gd T cells. Proc. Natl. Acad. Sci. USA 93:7172-77
81. He YW,Malek TR. 1996. Interleukin-7 receptor a is essential for the development of gd \+ T cells, but not natural killer cells. J. Exp. Med. 184:289-93
82. Miller JP, Izon D, DeMuth W, Gerstein R, Bhandoola A, Allman D. 2002. The earliest step in B lineage differentiation from common lymphoid progenitors is critically dependent upon interleukin 7. J. Exp. Med. 196:705-11
83. Schatz DG. 2004. V(D)J recombination. Immunol. Rev. 200:5-11
84. Rogozin IB, Iyer LM, Liang L, Glazko GV, Liston VG, 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
85. Nagawa F, Kishishita N, Shimizu K, Hirose S, Miyoshi M, et al. 2007. Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nat. Immunol. 8:206-13
86. Han BW, Herrin BR, Cooper MD, Wilson IA. 2008. Antigen recognition by variable lymphocyte receptors. Science 321:1834-37
87. Velikovsky CA, Deng L, Tasumi S, Iyer LM, Kerzic MC, et al. 2009. Structure of a lamprey variable lymphocyte receptor in complex with a protein antigen. Nat. Struct. Mol. Biol. 16:725-30
88. Herrin BR, Alder MN, Roux KH, Sina C, Ehrhardt GR, et al. 2008. Structure and specificity of lamprey monoclonal antibodies. Proc. Natl. Acad. Sci. USA 105:2040-45
89. Tasumi S, Velikovsky CA, Xu G, Gai SA, Wittrup KD, et al. 2009. High-affinity lamprey VLRA and VLRB monoclonal antibodies. Proc. Natl. Acad. Sci. USA 106:12891-96
90. Deng L, Velikovsky CA, Xu G, Iyer LM, Tasumi S, et al. 2010. A structural basis for antigen recognition by the T cell-like lymphocytes of sea lamprey. Proc. Natl. Acad. Sci. USA 107:13408-13
91. Kirchdoerfer RN, Herrin BR, Han BW, Turnbough CL Jr, Cooper MD, Wilson IA. 2012. Variable lymphocyte receptor recognition of the immunodominant glycoprotein of Bacillus anthracis spores. Structure 20:479-86
92. Alder MN, Rogozin IB, Iyer LM, Glazko GV, Cooper MD, Pancer Z. 2005. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970-73
93. Das S, Hirano M, Aghaallaei N, Bajoghli B, Boehm T, Cooper MD. 2013. Organization of lamprey variable lymphocyte receptor C locus and repertoire development. Proc. Natl. Acad. Sci. USA 110:6043-48
94. Alder MN, Herrin BR, Sadlonova A, Stockard CR, Grizzle WE, et al. 2008. Antibody responses of variable lymphocyte receptors in the lamprey. Nat. Immunol. 9:319-27
95. Koshland ME. 1985. The coming of age of the immunoglobulin J chain. Annu. Rev. Immunol. 3:425-53
96. Ghosh J, Lun CM,Majeske AJ, Sacchi S, Schrankel CS, Smith LC. 2011. Invertebrate immune diversity. Dev. Comp. Immunol. 35:959-74
97. Yu C, Dong M, Wu X, Li S, Huang S, et al. 2005. Genes "waiting" for recruitment by the adaptive immune system: the insights from amphioxus. J. Immunol. 174:3493-500
98. DuPasquier L, Zucchetti I, De Santis R. 2004. Immunoglobulin superfamily receptors in protochordates: before RAG time. Immunol. Rev. 198:233-48
99. Hamilton CE, Papavasiliou FN, Rosenberg BR. 2010. Diverse functions for DNA and RNA editing in the immune system. RNA Biol. 7:220-28
100. Kapitonov VV, Jurka J. 2005. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 3:e181
101. Schatz DG, Oettinger MA, Schlissel MS. 1992. V(D)J recombination: molecular biology and regulation. Annu. Rev. Immunol. 10:359-83
102. Fugmann SD, Messier C, Novack LA, Cameron RA, Rast JP. 2006. An ancient evolutionary origin of the Rag1/2 gene locus. Proc. Natl. Acad. Sci. USA 103:3728-33
103. Hirano M, Guo P, McCurley N, Schorpp M, Das S, et al. 2013. Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501:435-38
104. Arstila TP, Casrouge A, Baron V, Even J, Kanellopoulos J, Kourilsky P. 1999. A direct estimate of the human ab T cell receptor diversity. Science 286:958-61
105. Weinstein JA, Jiang N, White RA III, Fisher DS, Quake SR. 2009. High-throughput sequencing of the zebrafish antibody repertoire. Science 324:807-10
106. Casrouge A, Beaudoing E, Dalle S, Pannetier C, Kanellopoulos J, Kourilsky P. 2000. Size estimate of the ab TCR repertoire of naive mouse splenocytes. J. Immunol. 164:5782-87
107. DeKosky BJ, Ippolito GC, Deschner RP, Lavinder JJ, Wine Y, et al. 2013. High-throughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat. Biotechnol. 31:166-69
108. Klein L, Hinterberger M, Wirnsberger G, Kyewski B. 2009. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat. Rev. Immunol. 9:833-44
109. Pobezinsky LA, Angelov GS, Tai X, Jeurling S, Van Laethem F, et al. 2012. Clonal deletion and the fate of autoreactive thymocytes that survive negative selection. Nat. Immunol. 13:569-78
110. Wardemann H, Yurasov S, Schaefer A, Young JW, Meffre E, Nussenzweig MC. 2003. Predominant autoantibody production by early human B cell precursors. Science 301:1374-77
111. van Meerwijk JPM, Marguerat S, Lees RK, Germain RN, Fowlkes BJ, MacDonald HR. 1997. Quantitative impact of thymic clonal deletion on the T cell repertoire. J. Exp. Med. 185:377-83
112. Takada K, Jameson SC. 2009. Naive T cell homeostasis: from awareness of space to a sense of place. Nat. Rev. Immunol. 9:823-32
113. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. 2011. Human nutrition, the gut microbiome and the immune system. Nature 474:327-36
114. Rath CM, Dorrestein PC. 2012. The bacterial chemical repertoire mediates metabolic exchange within gut microbiomes. Curr. Opin. Microbiol. 15:147-54
115. Lee YK, Mazmanian SK. 2010. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330:1768-73
116. Jarchum I, Pamer EG. 2011. Regulation of innate and adaptive immunity by the commensal microbiota. Curr. Opin. Immunol. 23:353-60
117. Kawamoto S, Tran TH, Maruya M, Suzuki K, Doi Y, et al. 2012. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science 336:485-89
118. Hapfelmeier S, LawsonMAE,Slack E, Kirundi JK, StoelM,et al. 2010. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 328:1705-9
119. Mantis NJ, Rol N, Corthésy B. 2011. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 4:603-11
120. Chow J, Tang H, Mazmanian SK. 2011. Pathobionts of the gastrointestinal microbiota and inflammatory disease. Curr. Opin. Immunol. 23:473-80
121. Fagarasan S, Muramatsu M, Suzuki K, Nagaoka H, Hiai H, Honjo T. 2002. Critical roles of activationinduced cytidine deaminase in the homeostasis of gut flora. Science 298:1424-27
122. Johansen F-E, Pekna M, Norderhaug IN, Haneberg B, Hietala MA, et al. 1999. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component-deficient mice. J. Exp. Med. 190:915-22
123. Sait LC,GalicM, Price JD, Simpfendorfer KR,DiavatopoulosDA, et al. 2007. Secretory antibodies reduce systemic antibody responses against the gastrointestinal commensal flora. Int. Immunol. 19:257-65
124. WeiM, Shinkura R, Doi Y, Maruya M, Fagarasan S, Honjo T. 2011. Mice carrying a knock-in mutation of Aicda resulting in a defect in somatic hypermutation have impaired gut homeostasis and compromised mucosal defense. Nat. Immunol. 12:264-70
125. Sutherland DB, Fagarasan S. 2012. IgA synthesis: a form of functional immune adaptation extending beyond gut. Curr. Opin. Immunol. 24:261-68
126. Dishaw LJ, Ota T, MuellerMG,Cannon JP, Haire RN, et al. 2010. The basis for haplotype complexity in VCBPs, an immune-type receptor in amphioxus. Immunogenetics 62:623-31
127. Dishaw LJ, Giacomelli S, Melillo D, Zucchetti I, Haire RN, et al. 2011. A role for variable regioncontaining chitin-binding proteins (VCBPs) in host gut-bacteria interactions. Proc. Natl. Acad. Sci. USA 108:16747-52
128. Weaver CT, Hatton RD. 2009. Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective. Nat. Rev. Immunol. 9:883-89
129. Du Pasquier L. 1973. Ontogeny of the immune response in cold-blooded vertebrates. Curr. Top. Microbiol. Immunol. 61:37-88
130. Le Douarin NM, Jotereau FV. 1975. Tracing of cells of the avian thymus through embryonic life in interspecific chimeras. J. Exp. Med. 142:17-40
131. Reynaud CA, Bertocci B, Dahan A, Weill JC. 1994. Formation of the chicken B-cell repertoire: ontogenesis, regulation of Ig gene rearrangement, and diversification by gene conversion. Adv. Immunol. 57:353-78
132. Kaufman J, Milne S, Göbel TWF, Walker BA, Jacob JP, et al. 1999. The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923-25
133. Chen K, Xu W, Wilson M, He B, Miller NW, et al. 2009. Immunoglobulin D enhances immune surveillance by activating antimicrobial, proinflammatory and B cell-stimulating programs in basophils. Nat. Immunol. 10:889-98
134. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrøm M, et al. 2011. The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207-10
135. Bluestone JA, Mackay CR,O'Shea JJ, Stockinger B. 2009. The functional plasticity of T cell subsets. Nat. Rev. Immunol. 9:811-16
136. Hsu E. 1998. Mutation, selection, and memory in B lymphocytes of exothermic vertebrates. Immunol. Rev. 162:25-36
137. Rumfelt LL, McKinney EC, Taylor E, Flajnik MF. 2002. The development of primary and secondary lymphoid tissues in the nurse shark Ginglymostoma cirratum: B-cell zones precede dendritic cell immigration and T-cell zone formation during ontogeny of the spleen. Scand. J. Immunol. 56:130-48
138. Hsieh C-S, Lee H-M, Lio C-WJ. 2012. Selection of regulatory T cells in the thymus. Nat. Rev. Immunol. 12:157-67
139. Sakaguchi S, Vignali DA, Rudensky AY, Niec RE, Waldmann H. 2013. The plasticity and stability of regulatory T cells. Nat. Rev. Immunol. 13:461-67
140. Andersen KG, Nissen JK, Betz AG. 2012. Comparative genomics reveals key gain-of-function events in Foxp3 during regulatory T cell evolution. Front. Immunol. 3:113
141. CowanJE, Parnell SM, Nakamura K, CaamanoJH, Lane PJL, et al. 2013. The thymic medulla is required for Foxp3\+ regulatory but not conventional CD4\+ thymocyte development. J. Exp. Med. 210:675-81
142. Wu B, Jin M, Zhang Y, Wei T, Bai Z. 2011. Evolution of the IL17 receptor family in chordates: a new subfamily IL17REL. Immunogenetics 63:835-45
143. Saraiva M, O'Garra A. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10:170-81
144. Cui C, Benard EL, Kanwal Z, Stockhammer OW, van der Vaart M, et al. 2011. Infectious disease modeling and innate immune function in zebrafish embryos. Methods Cell Biol. 105:273-308
145. Roca FJ, Ramakrishnan L. 2013. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 153:521-34
146. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D. 2010. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464:108-11
147. Hess I, Iwanami N, Schorpp M, Boehm T. 2013. Zebrafish model for allogeneic hematopoietic cell transplantation not requiring preconditioning. Proc. Natl. Acad. Sci. USA 110:4327-32
148. Sun JC, Lanier LL. 2011. NK cell development, homeostasis and function: parallels with CD8\+ T cells. Nat. Rev. Immunol. 11:645-57
149. Raulet DH, Vance RE, McMahon CW. 2001. Regulation of the natural killer cell receptor repertoire. Annu. Rev. Immunol. 19:291-330
150. Cooper MA, Yokoyama WM. 2010. Memory-like responses of natural killer cells. Immunol. Rev. 235:297-305
151. Kurtz J. 2005. Specific memory within innate immune systems. Trends Immunol. 26:186-92
152. Netea MG, Quintin J, van der Meer JWM. 2011. Trained immunity: a memory for innate host defense. Cell Host Microbe 9:355-61
153. Toft C, Andersson SG. 2010. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat. Rev. Genet. 11:465-75
154. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat. Rev. Genet. 11:181-90
155. Westra ER, Swarts DC, Staals RH, Jore MM, Brouns SJ, van der Oost J. 2012. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311-39
156. Sorek R, Lawrence CM, Wiedenheft B. 2013. CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem. 82:237-66
157. Fineran PC, Charpentier E. 2012. Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information. Virology 434:202-9
158. Sampson TR, Saroj SD, Llewellyn AC, Tzeng YL, Weiss DS. 2013. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497:254-57
159. Kumar S, Hedges SB. 1998. A molecular timescale for vertebrate evolution. Nature 392:917-20
160. Hirano M, Guo P, McCurley N, Schorpp M, Das S, et al. 2013. Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501:435-38