1932

Abstract

The major histocompatibility complex (MHC) is a large genetic region with many genes, including the highly polymorphic classical class I and II genes that play crucial roles in adaptive as well as innate immune responses. The organization of the MHC varies enormously among jawed vertebrates, but class I and II genes have not been found in other animals. How did the MHC arise, and are there underlying principles that can help us to understand the evolution of the MHC? This review considers what it means to be an MHC and the potential importance of genome-wide duplication, gene linkage, and gene coevolution for the emergence and evolution of an adaptive immune system. Then it considers what the original antigen-specific receptor and MHC molecule might have looked like, how peptide binding might have evolved, and finally the importance of adaptive immunity in general.

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2018-04-26
2024-10-13
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Literature Cited

  1. Klein J. 1.  1986. The Natural History of the Major Histocompatibility Complex New York: Wiley [Google Scholar]
  2. Beck S, Trowsdale J. 2.  2000. The human major histocompatibility complex: lessons from the DNA sequence. Annu. Rev. Genom. Hum. Genet. 1:117–37 [Google Scholar]
  3. Trowsdale J, Knight JC. 3.  2013. Major histocompatibility complex genomics and human disease. Annu. Rev. Genom. Hum. Genet. 14:301–23 [Google Scholar]
  4. Blum JS, Wearsch PA, Cresswell P. 4.  2013. Pathways of antigen processing. Annu. Rev. Immunol. 31:443–73 [Google Scholar]
  5. Bernatchez L, Landry C. 5.  2003. MHC studies in nonmodel vertebrates: What have we learned about natural selection in 15 years?. J. Evol. Biol. 16:363–77 [Google Scholar]
  6. Spurgin LG, Richardson DS. 6.  2010. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc. Biol. Sci. 277:979–88 [Google Scholar]
  7. Kamiya T, O'Dwyer K, Westerdahl H, Senior A, Nakagawa S. 7.  2014. A quantitative review of MHC-based mating preference: the role of diversity and dissimilarity. Mol. Ecol. 23:5151–63 [Google Scholar]
  8. Parham P, Moffett A. 8.  2013. Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat. Rev. Immunol. 13:133–44 [Google Scholar]
  9. Petersdorf EW, Shuler KB, Longton GM, Spies T, Hansen JA. 9.  1999. Population study of allelic diversity in the human MHC class I-related MIC-A gene. Immunogenetics 49:605–12 [Google Scholar]
  10. Adams EJ, Luoma AM. 10.  2013. The adaptable major histocompatibility complex (MHC) fold: structure and function of nonclassical and MHC class I-like molecules. Annu. Rev. Immunol. 31:529–61 [Google Scholar]
  11. Dijkstra JM, Yamaguchi T, Grimholt U. 11.  2018. Conservation of sequence motifs suggests that the nonclassical MHC class I lineages CD1/PRoCR and UT were established before the emergence of tetrapod species. Immunogenetics. In press. http://doi.org/10.1007/s00251-017-1050-2 [Crossref] [Google Scholar]
  12. Horton R, Wilming L, Rand V, Lovering RC, Bruford EA. 12.  et al. 2004. Gene map of the extended human MHC. Nat. Rev. Genet. 5:889–99 [Google Scholar]
  13. Amadou C. 13.  1999. Evolution of the Mhc class I region: the framework hypothesis. Immunogenetics 49:362–67 [Google Scholar]
  14. Kelley J, Walter L, Trowsdale J. 14.  2005. Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–95 [Google Scholar]
  15. Kumánovics A, Takada T, Lindahl KF. 15.  2003. Genomic organization of the mammalian MHC. Annu. Rev. Immunol. 21:629–57 [Google Scholar]
  16. Hurt P, Walter L, Sudbrak R, Klages S, Müller I. 16.  et al. 2004. The genomic sequence and comparative analysis of the rat major histocompatibility complex. Genome Res 14:631–39 [Google Scholar]
  17. Ellis SA, Hammond JA. 17.  2014. The functional significance of cattle major histocompatibility complex class I genetic diversity. Annu. Rev. Anim. Biosci. 2:285–306 [Google Scholar]
  18. Lunney JK, Ho CS, Wysocki M, Smith DM. 18.  2009. Molecular genetics of the swine major histocompatibility complex, the SLA complex. Dev. Comp. Immunol. 33:362–74 [Google Scholar]
  19. Dukkipati VS, Blair HT, Garrick DJ, Murray A. 19.  2006. Ovar-Mhc’—ovine major histocompatibility complex: structure and gene polymorphisms. Genet. Mol. Res. 5:581–608 [Google Scholar]
  20. Belov K, Deakin JE, Papenfuss AT, Baker ML, Melman SD. 20.  et al. 2006. Reconstructing an ancestral mammalian immune supercomplex from a marsupial major histocompatibility complex. PLOS Biol 4:e46 [Google Scholar]
  21. Cheng Y, Stuart A, Morris K, Taylor R, Siddle H. 21.  et al. 2012. Antigen-presenting genes and genomic copy number variations in the Tasmanian devil MHC. BMC Genom 13:87 [Google Scholar]
  22. Deakin JE, Siddle HV, Cross JG, Belov K, Graves JA. 22.  2007. Class I genes have split from the MHC in the tammar wallaby. Cytogenet. Genome Res 116:205–11 [Google Scholar]
  23. Siddle HV, Deakin JE, Coggill P, Hart E, Cheng Y. 23.  et al. 2009. MHC-linked and un-linked class I genes in the wallaby. BMC Genom 10:310 [Google Scholar]
  24. Siddle HV, Deakin JE, Coggill P, Whilming LG, Harrow J. 24.  et al. 2011. The tammar wallaby major histocompatibility complex shows evidence of past genomic instability. BMC Genom 12:421 [Google Scholar]
  25. Balasubramaniam S, Bray RD, Mulder RA, Sunnucks P, Pavlova A, Melville J. 25.  2016. New data from basal Australian songbird lineages show that complex structure of MHC class II β genes has early evolutionary origins within passerines. BMC Evol. Biol. 16:112 [Google Scholar]
  26. Balakrishnan CN, Ekblom R, Völker M, Westerdahl H, Godinez R. 26.  et al. 2010. Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol 8:29 [Google Scholar]
  27. Ekblom R, Stapley J, Ball AD, Birkhead T, Burke T, Slate J. 27.  2011. Genetic mapping of the major histocompatibility complex in the zebra finch (Taeniopygia guttata). Immunogenetics 63:523–30 [Google Scholar]
  28. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW. 28.  et al. 2010. The genome of a songbird. Nature 464:757–62 [Google Scholar]
  29. Ellegren H, Smeds L, Burri R, Olason PI, Backström N. 29.  et al. 2012. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491:756–60 [Google Scholar]
  30. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P. 30.  et al. 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320–31 [Google Scholar]
  31. Zhang G, Li C, Li Q, Li B, Larkin DM. 31.  et al. 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311–20 [Google Scholar]
  32. Chen LC, Lan H, Sun L, Deng YL, Tang KY, Wan QH. 32.  2015. Genomic organization of the crested ibis MHC provides new insight into ancestral avian MHC structure. Sci. Rep. 5:7963 [Google Scholar]
  33. Rogers SL, Kaufman J. 33.  2016. Location, location, location: the evolutionary history of CD1 genes and the NKR-P1/ligand systems. Immunogenetics 68:499–513 [Google Scholar]
  34. Kaufman J, Milne S, Göbel TW, Walker BA, Jacob JP. 34.  et al. 1999. The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–25 [Google Scholar]
  35. Shiina T, Briles WE, Goto RM, Hosomichi K, Yanagiya K. 35.  et al. 2007. Extended gene map reveals tripartite motif, C-type lectin, and Ig superfamily type genes within a subregion of the chicken MHC-B affecting infectious disease. J. Immunol. 178:7162–72 [Google Scholar]
  36. Salomonsen J, Chattaway JA, Chan AC, Parker A, Huguet S. 36.  et al. 2014. Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns. PLOS Genet 10:e1004417 [Google Scholar]
  37. Salomonsen J, Sørensen MR, Marston DA, Rogers SL, Collen T. 37.  et al. 2005. Two CD1 genes map to the chicken MHC, indicating that CD1 genes are ancient and likely to have been present in the primordial MHC. PNAS 102:8668–73 [Google Scholar]
  38. Miller MM, Goto RM, Taylor RL Jr., Zoorob R, Auffray C. 38.  et al. 1996. Assignment of Rfp-Y to the chicken major histocompatibility complex/NOR microchromosome and evidence for high-frequency recombination associated with the nucleolar organizer region. PNAS 93:3958–62 [Google Scholar]
  39. Kaufman J. 39.  2013. The Avian MHC. Avian Immunology KA Schat, P Kaiser, B Kaspers 149–67 London/New York: Elsevier, 2nd ed.. [Google Scholar]
  40. Miller MM, Taylor RL Jr. 40.  2016. Brief review of the chicken Major Histocompatibility Complex: the genes, their distribution on chromosome 16, and their contributions to disease resistance. Poult. Sci. 95:375–92 [Google Scholar]
  41. Shiina T, Shimizu S, Hosomichi K, Kohara S, Watanabe S. 41.  et al. 2004. Comparative genomic analysis of two avian (quail and chicken) MHC regions. J. Immunol. 172:6751–63 [Google Scholar]
  42. Green RE, Braun EL, Armstrong J, Earl D, Nguyen N. 42.  et al. 2014. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346:1254449 [Google Scholar]
  43. Jaratlerdsiri W, Deakin J, Godinez RM, Shan X, Peterson DG. 43.  et al. 2014. Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC. PLOS ONE 9:e114631 [Google Scholar]
  44. Miller HC, O'Meally D, Ezaz T, Amemiya C, Marshall-Graves JA, Edwards S. 44.  2015. Major histocompatibility complex genes map to two chromosomes in an evolutionarily ancient reptile, the Tuatara Sphenodon punctatus. . G3 5:1439–51 [Google Scholar]
  45. Ohta Y, Goetz W, Hossain MZ, Nonaka M, Flajnik MF. 45.  2006. Ancestral organization of the MHC revealed in the amphibian Xenopus. . J. Immunol. 176:63674–85 [Google Scholar]
  46. Flajnik MF, Kasahara M, Shum BP, Salter-Cid L, Taylor E, Du Pasquier L. 46.  1993. A novel type of class I gene organization in vertebrates: A large family of non-MHC-linked class I genes is expressed at the RNA level in the amphibian Xenopus. . EMBO J 12:4385–96 [Google Scholar]
  47. Courtet M, Flajnik M, Du Pasquier L. 47.  2001. Major histocompatibility complex and immunoglobulin loci visualized by in situ hybridization on Xenopus chromosomes. Dev. Comp. Immunol. 25:149–57 [Google Scholar]
  48. Edholm ES, Banach M, Robert J. 48.  2016. Evolution of innate-like T cells and their selection by MHC class I-like molecules. Immunogenetics 68:525–36 [Google Scholar]
  49. Sammut B, Du Pasquier L, Ducoroy P, Laurens V, Marcuz A, Tournefier A. 49.  1999. Axolotl MHC architecture and polymorphism. Eur. J. Immunol. 29:2897–907 [Google Scholar]
  50. Laurens V, Chapusot C, del Rosario Ordonez M, Bentrari F, Padros MR, Tournefier A. 50.  2001. Axolotl MHC class II β chain: predominance of one allele and alternative splicing of the β1 domain. Eur. J. Immunol. 31:506–15 [Google Scholar]
  51. Takami K, Zaleska-Rutczynska Z, Figueroa F, Klein J. 51.  1997. Linkage of LMP, TAP, and RING3 with Mhc class I rather than class II genes in the zebrafish. J. Immunol. 159:6052–60 [Google Scholar]
  52. Sato A, Figueroa F, Murray BW, Málaga-Trillo E, Zaleska-Rutczynska Z. 52.  et al. 2000. Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51:108–16 [Google Scholar]
  53. Grimholt U, Tsukamoto K, Azuma T, Leong J, Koop BF, Dijkstra JM. 53.  2015. A comprehensive analysis of teleost MHC class I sequences. BMC Evol. Biol. 15:32 [Google Scholar]
  54. Sambrook JG, Figueroa F, Beck S. 54.  2005. A genome-wide survey of Major Histocompatibility Complex (MHC) genes and their paralogues in zebrafish. BMC Genom 6:152 [Google Scholar]
  55. Dijkstra JM, Grimholt U, Leong J, Koop BF, Hashimoto K. 55.  2013. Comprehensive analysis of MHC class II genes in teleost fish genomes reveals dispensability of the peptide-loading DM system in a large part of vertebrates. BMC Evol. Biol. 13:260 [Google Scholar]
  56. Deakin JE, Papenfuss AT, Belov K, Cross JG, Coggill P. 56.  et al. 2006. Evolution and comparative analysis of the MHC class III inflammatory region. BMC Genom 7:281 [Google Scholar]
  57. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrøm M. 57.  et al. 2011. The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207–10 [Google Scholar]
  58. Ohta Y, Okamura K, McKinney EC, Bartl S, Hashimoto K, Flajnik MF. 58.  2000. Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. PNAS 97:4712–17 [Google Scholar]
  59. Ohta Y, McKinney EC, Criscitiello MF, Flajnik MF. 59.  2002. Proteasome, transporter associated with antigen processing, and class I genes in the nurse shark Ginglymostoma cirratum: evidence for a stable class I region and MHC haplotype lineages. J. Immunol. 168:771–81 [Google Scholar]
  60. Terado T, Okamura K, Ohta Y, Shin DH, Smith SL. 60.  et al. 2003. Molecular cloning of C4 gene and identification of the class III complement region in the shark MHC. J. Immunol. 171:2461–66 [Google Scholar]
  61. Ohta Y, Shiina T, Lohr RL, Hosomichi K, Pollin TI. 61.  et al. 2011. Primordial linkage of β2-microglobulin to the MHC. J. Immunol. 186:3563–71 [Google Scholar]
  62. Younger RM, Amadou C, Bethel G, Ehlers A, Lindahl KF. 62.  et al. 2001. Characterization of clustered MHC-linked olfactory receptor genes in human and mouse. Genome Res 11:519–30 [Google Scholar]
  63. Kaufman J. 63.  1999. Co-evolving genes in MHC haplotypes: the “rule” for nonmammalian vertebrates?. Immunogenetics 50:228–36 [Google Scholar]
  64. Kaufman J. 64.  2015. Co-evolution with chicken class I genes. Immunol. Rev. 267:56–71 [Google Scholar]
  65. Katsanis N, Fitzgibbon J, Fisher EM. 65.  1996. Paralogy mapping: identification of a region in the human MHC triplicated onto human chromosomes 1 and 9 allows the prediction and isolation of novel PBX and NOTCH loci. Genomics 35:101–8 [Google Scholar]
  66. Kasahara M, Hayashi M, Tanaka K, Inoko H, Sugaya K. 66.  et al. 1996. Chromosomal localization of the proteasome Z subunit gene reveals an ancient chromosomal duplication involving the major histocompatibility complex. PNAS 93:9096–101 [Google Scholar]
  67. Kasahara M, Nakaya J, Satta Y, Takahata N. 67.  1997. Chromosomal duplication and the emergence of the adaptive immune system. Trends Genet 13:90–92 [Google Scholar]
  68. Ohno S. 68.  1970. Evolution by Gene Duplication New York: Springer-Verlag [Google Scholar]
  69. Schluter SF, Bernstein RM, Bernstein H, Marchalonis JJ. 69.  1999. ‘Big Bang’ emergence of the combinatorial immune system. Dev. Comp. Immunol. 23:107–11 [Google Scholar]
  70. Flajnik MF. 70.  2014. Re-evaluation of the immunological Big Bang. Curr. Biol. 24:R1060–65 [Google Scholar]
  71. Abi-Rached L, Gilles A, Shiina T, Pontarotti P, Inoko H. 71.  2002. Evidence of en bloc duplication in vertebrate genomes. Nat. Genet. 31:100–5 [Google Scholar]
  72. Suurväli J, Jouneau L, Thépot D, Grusea S, Pontarotti P. 72.  et al. 2014. The proto-MHC of placozoans, a region specialized in cellular stress and ubiquitination/proteasome pathways. J. Immunol. 193:2891–901 [Google Scholar]
  73. Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N. 73.  et al. 2013. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat. Genet. 45:415–21 [Google Scholar]
  74. Lien S, Koop BF, Sandve SR, Miller JR, Kent MP. 74.  et al. 2016. The Atlantic salmon genome provides insights into rediploidization. Nature 533:200–5 [Google Scholar]
  75. Du Pasquier L, Miggiano VC, Kobel H-R, Fischberg M. 75.  1977. The genetic control of histocompatibility reactions in natural and laboratory-made polyploid individuals of the clawed toad. Xenopus. Immunogenetics 5:129–41 [Google Scholar]
  76. Du Pasquier L, Wilson M, Sammut B. 76.  2009. The fate of duplicated immunity genes in the dodecaploid Xenopus ruwenzoriensis. . Front. Biosci. 14:177–91 [Google Scholar]
  77. Donoghue PC, Purnell MA. 77.  2005. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20:312–19 [Google Scholar]
  78. Kandil E, Egashira M, Miyoshi O, Niikawa N, Ishibashi T, Kasahara M. 78.  1996. The human gene encoding the heavy chain of the major histocompatibility complex class I-like Fc receptor (FCGRT) maps to 19q13.3. Cytogenet. Cell Genet. 73:97–98 [Google Scholar]
  79. Kasahara M, Kandil E, Salter-Cid L, Flajnik MF. 79.  1996. Origin and evolution of the class I gene family: Why are some of the mammalian class I genes encoded outside the major histocompatibility complex?. Res. Immunol. 147:278–84 [Google Scholar]
  80. Tsukamoto K, Deakin JE, Graves JA, Hashimoto K. 80.  2013. Exceptionally high conservation of the MHC class I-related gene, MR1, among mammals. Immunogenetics 65:115–24 [Google Scholar]
  81. Yang Z, Wang C, Wang T, Bai J, Zhao Y. 81.  et al. 2015. Analysis of the reptile CD1 genes: evolutionary implications. Immunogenetics 67:337–46 [Google Scholar]
  82. Hughes AL. 82.  1991. Evolutionary origin and diversification of the mammalian CD1 antigen genes. Mol. Biol. Evol. 8:185–201 [Google Scholar]
  83. Dascher CC. 83.  2007. Evolutionary biology of CD1. Curr. Top. Microbiol. Immunol. 314:3–26 [Google Scholar]
  84. Germain RN, Bentley DM, Quill H. 84.  1985. Influence of allelic polymorphism on the assembly and surface expression of class II MHC (Ia) molecules. Cell 43:233–42 [Google Scholar]
  85. Deverson EV, Leong L, Seelig A, Coadwell WJ, Tredgett EM. 85.  et al. 1998. Functional analysis by site-directed mutagenesis of the complex polymorphism in rat transporter associated with antigen processing. J. Immunol. 160:2767–79 [Google Scholar]
  86. Joly E, Le Rolle AF, González AL, Mehling B, Stevens J. 86.  et al. 1998. Co-evolution of rat TAP transporters and MHC class I RT1-A molecules. Curr. Biol. 8:169–72 [Google Scholar]
  87. Moffett A, Colucci F. 87.  2015. Co-evolution of NK receptors and HLA ligands in humans is driven by reproduction.. Immunol. Rev 267:283–97 [Google Scholar]
  88. Kaufman J. 88.  2015. What chickens would tell you about the evolution of antigen processing and presentation. Curr. Opin. Immunol. 34:35–42 [Google Scholar]
  89. Wallny HJ, Avila D, Hunt LG, Powell TJ, Riegert P. 89.  et al. 2006. Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. PNAS 103:1434–39 [Google Scholar]
  90. Koch M, Camp S, Collen T, Avila D, Salomonsen J. 90.  et al. 2007. Structures of an MHC class I molecule from B21 chickens illustrate promiscuous peptide binding. Immunity 27:885–99 [Google Scholar]
  91. Chappell P, Meziane ELK, Harrison M, Magiera Ł, Hermann C. 91.  et al. 2015. Expression levels of MHC class I molecules are inversely correlated with promiscuity of peptide binding. eLife 4:e05345 [Google Scholar]
  92. Walker BA, Hunt LG, Sowa AK, Skjødt K, Göbel TW. 92.  et al. 2011. The dominantly expressed class I molecule of the chicken MHC is explained by coevolution with the polymorphic peptide transporter (TAP) genes. PNAS 108:8396–401 [Google Scholar]
  93. Tregaskes CA, Harrison M, Sowa AK, van Hateren A, Hunt LG. 93.  et al. 2016. Surface expression, peptide repertoire, and thermostability of chicken class I molecules correlate with peptide transporter specificity. PNAS 113:692–97 [Google Scholar]
  94. van Hateren A, Carter R, Bailey A, Kontouli N, Williams AP. 94.  et al. 2013. A mechanistic basis for the co-evolution of chicken tapasin and major histocompatibility complex class I (MHC I) proteins. J. Biol. Chem. 288:32797–808 [Google Scholar]
  95. McLaren PJ, Coulonges C, Bartha I, Lenz TL, Deutsch AJ. 95.  et al. 2015. Polymorphisms of large effect explain the majority of the host genetic contribution to variation of HIV-1 virus load. PNAS 112:14658–63 [Google Scholar]
  96. Mesa CM, Thulien KJ, Moon DA, Veniamin SM, Magor KE. 96.  2004. The dominant MHC class I gene is adjacent to the polymorphic TAP2 gene in the duck. Anas platyrhynchos. Immunogenetics 56:192–203 [Google Scholar]
  97. Tsuji H, Taniguchi Y, Ishizuka S, Matsuda H, Yamada T. 97.  et al. 2017. Structure and polymorphisms of the major histocompatibility complex in the Oriental stork. Ciconia boyciana. Sci. Rep. 7:42864 [Google Scholar]
  98. Ohta Y, Powis SJ, Lohr RL, Nonaka M, Du Pasquier L, Flajnik MF. 98.  2003. Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co-evolution among MHC class I region genes. Eur. J. Immunol. 33:3017–27 [Google Scholar]
  99. Tsukamoto K, Miura F, Fujito NT, Yoshizaki G, Nonaka M. 99.  2012. Long-lived dichotomous lineages of the proteasome subunit beta type 8 (PSMB8) gene surviving more than 500 million years as alleles or paralogs. Mol. Biol. Evol. 29:3071–79 [Google Scholar]
  100. McConnell SC, Hernandez KM, Wcisel DJ, Kettleborough RN, Stemple DL. 100.  et al. 2016. Alternative haplotypes of antigen processing genes in zebrafish diverged early in vertebrate evolution. PNAS 113:E5014–23 [Google Scholar]
  101. Shiina T, Hosomichi K, Hanzawa K. 101.  2006. Comparative genomics of the poultry major histocompatibility complex. Anim. Sci. J. 77:151–62 [Google Scholar]
  102. Drews A, Strandh M, Råberg L, Westerdahl H. 102.  2017. Expression and phylogenetic analyses reveal paralogous lineages of putatively classical and non-classical MHC-I genes in three sparrow species (Passer). BMC Evol. Biol. 17:152 [Google Scholar]
  103. Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S. 103.  et al. 2003. MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar): facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55:210–19 [Google Scholar]
  104. Moon DA, Veniamin SM, Parks-Dely JA, Magor KE. 104.  2005. The MHC of the duck (Anas platyrhynchos) contains five differentially expressed class I genes. J. Immunol. 175:6702–12 [Google Scholar]
  105. Okamura K, Ototake M, Nakanishi T, Kurosawa Y, Hashimoto K. 105.  1997. The most primitive vertebrates with jaws possess highly polymorphic MHC class I genes comparable to those of humans. Immunity 7:777–90 [Google Scholar]
  106. Bonneaud C, Pérez-Tris J, Federici P, Chastel O, Sorci G. 106.  2006. Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60:383–89 [Google Scholar]
  107. Savage AE, Zamudio KR. 107.  2011. MHC genotypes associate with resistance to a frog-killing fungus. PNAS 108:16705–10 [Google Scholar]
  108. Kaufman J. 108.  2011. The evolutionary origins of the adaptive immune system of jawed vertebrates. The Immune Response to Infection SHE Kaufmann, BT Rouse, DL Sachs 41–55 Washington, DC: Am. Soc. Microbiol. [Google Scholar]
  109. Rogers SL, Göbel TW, Viertlboeck BC, Milne S, Beck S, Kaufman J. 109.  2005. Characterization of the chicken C-type lectin-like receptors B-NK and B-lec suggests that the NK complex and the MHC share a common ancestral region. J. Immunol. 174:3475–83 [Google Scholar]
  110. Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM. 110.  et al. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–79 [Google Scholar]
  111. Kasahara M, Watanabe Y, Sumasu M, Nagata T. 111.  2002. A family of MHC class I-like genes located in the vicinity of the mouse leukocyte receptor complex. PNAS 99:13687–92 [Google Scholar]
  112. Du Pasquier L, Zucchetti I, De Santis R. 112.  2004. Immunoglobulin superfamily receptors in protochordates: before RAG time. Immunol. Rev. 198:233–48 [Google Scholar]
  113. Flajnik MF, Kasahara M. 113.  2010. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11:47–59 [Google Scholar]
  114. Flajnik MF, Tlapakova T, Criscitiello MF, Krylov V, Ohta Y. 114.  2012. Evolution of the B7 family: co-evolution of B7H6 and NKp30, identification of a new B7 family member, B7H7, and of B7’s historical relationship with the MHC. Immunogenetics 64:571–90 [Google Scholar]
  115. Boyle LH, Hermann C, Boname JM, Porter KM, Patel PA. 115.  et al. 2013. Tapasin-related protein TAPBPR is an additional component of the MHC class I presentation pathway. PNAS 110:3465–70 [Google Scholar]
  116. Olinski RP, Lundin LG, Hallböök F. 116.  2006. Conserved synteny between the Ciona genome and human paralogons identifies large duplication events in the molecular evolution of the insulin-relaxin gene family. Mol. Biol. Evol. 23:10–22 [Google Scholar]
  117. Isobe M, Russo G, Haluska FG, Croce CM. 117.  1988. Cloning of the gene encoding the δ subunit of the human T-cell receptor reveals its physical organization within the α-subunit locus and its involvement in chromosome translocations in T-cell malignancy. PNAS 85:3933–37 [Google Scholar]
  118. Krangel MS, Carabana J, Abbarategui I, Schlimgen R, Hawwari A. 118.  2004. Enforcing order within a complex locus: current perspectives on the control of V(D)J recombination at the murine T-cell receptor α/δ locus. Immunol. Rev. 200:224–32 [Google Scholar]
  119. Rossjohn J, Gras S, Miles JJ, Turner SJ, Godfrey DI, McCluskey J. 119.  2015. T cell antigen receptor recognition of antigen-presenting molecules. Annu. Rev. Immunol. 33:169–200 [Google Scholar]
  120. Fugmann SD, Lee AI, Shockett PE, Villey IJ, Schatz DG. 120.  2000. The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Annu. Rev. Immunol. 18:495–527 [Google Scholar]
  121. Koonin EV, Krupovic M. 121.  2015. Evolution of adaptive immunity from transposable elements combined with innate immune systems. Nat. Rev. Genet. 16:184–92 [Google Scholar]
  122. Fugmann SD, Messier C, Novack LA, Cameron RA, Rast JP. 122.  2006. An ancient evolutionary origin of the Rag1/2 gene locus. PNAS 103:3728–33 [Google Scholar]
  123. Huang S, Tao X, Yuan S, Zhang Y, Li P. 123.  et al. 2016. Discovery of an active RAG transposon illuminates the origins of V(D)J recombination. Cell 166:102–14 [Google Scholar]
  124. Davis MM, Bjorkman PJ. 124.  1988. T-cell antigen receptor genes and T-cell recognition. Nature 334:395–402 [Google Scholar]
  125. Litman GW, Rast JP, Fugmann SD. 125.  2010. The origins of vertebrate adaptive immunity. Nat. Rev. Immunol. 10:543–53 [Google Scholar]
  126. Abeler-Dörner L, Swamy M, Williams G, Hayday AC, Bas A. 126.  2012. Butyrophilins: an emerging family of immune regulators. Trends Immunol 33:34–41 [Google Scholar]
  127. Di Marco Barros R, Roberts NA, Dart RJ, Vantourout P, Jandke A. 127.  et al. 2016. Epithelia use butyrophilin-like molecules to shape organ-specific γδ T cell compartments. Cell 167:203–218 [Google Scholar]
  128. Afrache H, Gouret P, Ainouche S, Pontarotti P, Olive D. 128.  2012. The butyrophilin (BTN) gene family: from milk fat to the regulation of the immune response. Immunogenetics 64:781–94 [Google Scholar]
  129. Rhodes DA, Reith W, Trowsdale J. 129.  2016. Regulation of immunity by butyrophilins. Annu. Rev. Immunol. 34:151–72 [Google Scholar]
  130. Du Pasquier L. 130.  2000. The phylogenetic origin of antigen-specific receptors. Curr. Top. Microbiol. Immunol. 248:160–85 [Google Scholar]
  131. Lanier LL. 131.  2005. NK cell recognition. Annu. Rev. Immunol. 23:225–74 [Google Scholar]
  132. Holcik M, Sonenberg N. 132.  2005. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6:318–27 [Google Scholar]
  133. Starck SR, Jiang V, Pavon-Eternod M, Prasad S, McCarthy B. 133.  et al. 2012. Leucine-tRNA initiates at CUG start codons for protein synthesis and presentation by MHC class I. Science 336:1719–23 [Google Scholar]
  134. Jensen PE, Sullivan BA, Reed-Loisel LM, Weber DA. 134.  2004. Qa-1, a nonclassical class I histocompatibility molecule with roles in innate and adaptive immunity. Immunol. Res. 29:81–92 [Google Scholar]
  135. Fischer-Lindahl K, Hermel E, Loveland BE, Wang CR. 135.  1991. Maternally transmitted antigen of mice: a model transplantation antigen. Annu. Rev. Immunol. 9:351–72 [Google Scholar]
  136. Yaneva R, Schneeweiss C, Zacharias M, Springer S. 136.  2010. Peptide binding to MHC class I and II proteins: new avenues from new methods. Mol. Immunol. 47:649–57 [Google Scholar]
  137. Flajnik MF, Canel C, Kramer J, Kasahara M. 137.  1991. Which came first, MHC class I or class II?. Immunogenetics 33:295–300 [Google Scholar]
  138. Rock KL, Reits E, Neefjes J. 138.  2016. Present yourself! By MHC class I and MHC class II molecules. Trends Immunol 37:724–737 [Google Scholar]
  139. Zhang P, Leu JI, Murphy ME, George DL, Marmorstein R. 139.  2014. Crystal structure of the stress-inducible human heat shock protein 70 substrate-binding domain in complex with peptide substrate. PLOS ONE 9:e103518 [Google Scholar]
  140. Kaufman JF, Auffray C, Korman AJ, Shackelford DA, Strominger J. 140.  1984. The class II molecules of the human and murine major histocompatibility complex. Cell 36:1–13 [Google Scholar]
  141. Kaufman J. 141.  1988. Vertebrates and the evolution of the major histocompatibility complex class I and class II molecules. Verh. Dtsch. Zool. Ges. 81:131–44 [Google Scholar]
  142. Benoist C, Mathis D. 142.  1990. Regulation of major histocompatibility complex class-II genes: X, Y and other letters of the alphabet. Annu. Rev. Immunol. 8:681–715 [Google Scholar]
  143. Boehm U, Klamp T, Groot M, Howard JC. 143.  1997. Cellular responses to interferon-γ. Annu. Rev. Immunol. 15:749–95 [Google Scholar]
  144. Zollmann T, Bock C, Graab P, Abele R. 144.  2015. Team work at its best—TAPL and its two domains. Biol. Chem 396:967–74 [Google Scholar]
  145. Motozono C, Pearson JA, De Leenheer E, Rizkallah PJ, Beck K. 145.  et al. 2015. Distortion of the major histocompatibility complex class I binding groove to accommodate an insulin-derived 10-mer peptide. J. Biol. Chem. 290:18924–33 [Google Scholar]
  146. McMurtrey C, Trolle T, Sansom T, Remesh SG, Kaever T. 146.  et al. 2016. Toxoplasma gondii peptide ligands open the gate of the HLA class I binding groove. eLife 5:e12556 [Google Scholar]
  147. Remesh SG, Andreatta M, Ying G, Kaever T, Nielsen M. 147.  et al. 2017. Unconventional peptide presentation by major histocompatibility complex (MHC) class I allele HLA-A*02:01: BREAKING CONFINEMENT. J. Biol. Chem. 292:5262–70 [Google Scholar]
  148. Li X, Lamothe PA, Walker BD, Wang JH. 148.  2017. Crystal structure of HLA-B*5801 with a TW10 HIV Gag epitope reveals a novel mode of peptide presentation. Cell. Mol. Immunol. 14:1–4 [Google Scholar]
  149. Kaufman JF, Strominger JL. 149.  1979. Both chains of HLA-DR bind to the membrane with a penultimate hydrophobic region and the heavy chain is phosphorylated at its hydrophilic carboxy terminus. PNAS 76:6304–8 [Google Scholar]
  150. Dixon AM, Drake L, Hughes KT, Sargent E, Hunt D. 150.  et al. 2014. Differential transmembrane domain GXXXG motif pairing impacts major histocompatibility complex (MHC) class II structure. J. Biol. Chem. 289:11695–703 [Google Scholar]
  151. Pancer Z, Mayer WE, Klein J, Cooper MD. 151.  2004. Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. PNAS 101:13273–78 [Google Scholar]
  152. Krasnec KV, Papenfuss AT, Miller RD. 152.  2016. The UT family of MHC class I loci unique to non-eutherian mammals has limited polymorphism and tissue specific patterns of expression in the opossum. BMC Immunol 17:43 [Google Scholar]
  153. Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J, Gartland GL, Cooper MD. 153.  2004. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174–80 [Google Scholar]
  154. Alder MN, Rogozin IB, Iyer LM, Glazko GV, Cooper MD, Pancer Z. 154.  2005. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310:1970–73 [Google Scholar]
  155. Weill JC, Reynaud CA. 155.  1987. The chicken B cell compartment. Science 238:1094–98 [Google Scholar]
  156. Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD. 156.  2012. VLR-based adaptive immunity. Annu. Rev. Immunol. 30:203–20 [Google Scholar]
  157. Hirano M, Guo P, McCurley N, Schorpp M, Das S. 157.  et al. 2013. Evolutionary implications of a third lymphocyte lineage in lampreys. Nature 501:435–38 [Google Scholar]
  158. Li J, Das S, Herrin BR, Hirano M, Cooper MD. 158.  2013. Definition of a third VLR gene in hagfish. PNAS 110:15013–18 [Google Scholar]
  159. Bajoghli B, Guo P, Aghaallaei N, Hirano M, Strohmeier C. 159.  et al. 2011. A thymus candidate in lampreys. Nature 470:90–94 [Google Scholar]
  160. Holland SJ, Gao M, Hirano M, Iyer LM, Luo M. 160.  et al. 2014. Selection of the lamprey VLRC antigen receptor repertoire. PNAS 111:14834–39 [Google Scholar]
  161. Takaba H, Imai T, Miki S, Morishita Y, Miyashita A. 161.  et al. 2013. A major allogenic leukocyte antigen in the agnathan hagfish. Sci. Rep. 3:1716 [Google Scholar]
  162. Yoder JA, Litman GW. 162.  2011. The phylogenetic origins of natural killer receptors and recognition: relationships, possibilities, and realities. Immunogenetics 63:123–41 [Google Scholar]
  163. Hammond JA, Guethlein LA, Abi-Rached L, Moesta AK, Parham P. 163.  2009. Evolution and survival of marine carnivores did not require a diversity of killer cell Ig-like receptors or Ly49 NK cell receptors. J. Immunol. 182:3618–27 [Google Scholar]
  164. van den Berg TK, Yoder JA, Litman GW. 164.  2004. On the origins of adaptive immunity: Innate immune receptors join the tale. Trends Immunol 25:11–16 [Google Scholar]
  165. Cao DD, Liao X, Cheng W, Jiang YL, Wang WJ. 165.  et al. 2016. Structure of a variable lymphocyte receptor-like protein from the amphioxus Branchiostoma floridae. . Sci. Rep. 6:19951 [Google Scholar]
  166. Cerenius L, Söderhäll K. 166.  2013. Variable immune molecules in invertebrates. J. Exp. Biol. 216:4313–19 [Google Scholar]
  167. Zhang SM, Adema CM, Kepler TB, Loker ES. 167.  2004. Diversification of Ig superfamily genes in an invertebrate. Science 305:251–54 [Google Scholar]
  168. Watson FL, Püttmann-Holgado R, Thomas F, Lamar DL, Hughes M. 168.  et al. 2005. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309:1874–78 [Google Scholar]
  169. Armitage SA, Peuss R, Kurtz J. 169.  2015. Dscam and pancrustacean immune memory—a review of the evidence. Dev. Comp. Immunol. 48:315–23 [Google Scholar]
  170. Buckley KM, Rast JP. 170.  2015. Diversity of animal immune receptors and the origins of recognition complexity in the deuterostomes. Dev. Comp. Immunol. 49:179–89 [Google Scholar]
  171. Flajnik MF, Du Pasquier L. 171.  2004. Evolution of innate and adaptive immunity: Can we draw a line?. Trends Immunol 25:640–44 [Google Scholar]
  172. Howe K, Schiffer PH, Zielinski J, Wiehe T, Laird GK. 172.  et al. 2016. Structure and evolutionary history of a large family of NLR proteins in the zebrafish. Open Biol 6:160009 [Google Scholar]
  173. Koonin EV, Makarova KS, Wolf YI. 173.  2017. Evolutionary genomics of defense systems in archaea and bacteria. Annu. Rev. Microbiol. 71:233–61 [Google Scholar]
  174. Marques JT, Carthew RW. 174.  2007. A call to arms: coevolution of animal viruses and host innate immune responses. Trends Genet 23:359–64 [Google Scholar]
  175. Obbard DJ, Gordon KH, Buck AH, Jiggins FM. 175.  2009. The evolution of RNAi as a defence against viruses and transposable elements. Philos. Trans. R. Soc. Lond. B 364:99–115 [Google Scholar]
  176. Gilman RT, Nuismer SL, Jhwueng DC. 176.  2012. Coevolution in multidimensional trait space favours escape from parasites and pathogens. Nature 483:328–30 [Google Scholar]
  177. Hedrick SM. 177.  2004. The acquired immune system: a vantage from beneath. Immunity 21:607–15 [Google Scholar]
  178. Kaufman J, Völk H, Wallny HJ. 178.  1995. A “minimal essential Mhc” and an “unrecognized Mhc”: two extremes in selection for polymorphism. Immunol. Rev. 143:63–88 [Google Scholar]
  179. Kaufman J, Jacob J, Shaw I, Walker B, Milne S. 179.  et al. 1999. Gene organisation determines evolution of function in the chicken MHC. Immunol. Rev. 167:101–17 [Google Scholar]
  180. Kaufman J, Skjoedt K, Salomonsen J. 180.  1990. The MHC molecules of nonmammalian vertebrates. Immunol. Rev. 113:83–117 [Google Scholar]
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