Co-evolution of the MHC class I and KIR gene families in rhesus macaques: Ancestry and plasticity

Immunological Reviews

Volumn 267, Issue 1, 2015, Pages 228-245

  de Groot, Natasja G ^a   Blokhuis, Jeroen H ^a,c   Otting, Nel ^a   Doxiadis, Gaby G M ^a   Bontrop, Ronald E ^a,b  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Co evolution; KIR; MHC; Rhesus macaque

Indexed keywords

HLA G ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR; HLA ANTIGEN CLASS 1;

ANIMAL GENETICS; ARTICLE; BIODIVERSITY; C GENE; CERCOPITHECIDAE; COEVOLUTION; GENE; GENE DELETION; GENE DOSAGE; GENE EXPRESSION; GENE FUNCTION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; IMMUNE SYSTEM; IMMUNITY; MIC GENE; MULTIGENE FAMILY; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PATHOGENESIS; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; REPRODUCTIVE SUCCESS; RHESUS MONKEY; ANIMAL; COPY NUMBER VARIATION; GENETIC VARIATION; GENETICS; IMMUNOLOGY; MOLECULAR EVOLUTION;

ANIMALS; DNA COPY NUMBER VARIATIONS; EVOLUTION, MOLECULAR; GENETIC VARIATION; HAPLOTYPES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MACACA MULATTA; MULTIGENE FAMILY; RECEPTORS, KIR;

EID: 84939545871     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12313     Document Type: Article

References (136)

1. Parham P, Ohta T. Population biology of antigen presentation by MHC class I molecules. Science 1996;272:67-74.
2. de Groot NG, Bontrop RE. The HIV-1 pandemic: does the selective sweep in chimpanzees mirror humankind's future? Retrovirology 2013;10:53.
3. Tosi AJ, Morales JC, Melnick DJ. Y-chromosome and mitochondrial markers in Macaca fascicularis indicate introgression with Indochinese M. mulatta and a biogeogrphic barrier in the Isthmus of Kra. Int J Primatol 2002;23:161-178.
4. Glazko GV, Nei M. Estimation of divergence times for major lineages of primate species. Mol Biol Evol 2003;20:424-434.
5. Perelman P, et al. A molecular phylogeny of living primates. PLoS Genet 2011;7:e1001342.
6. Bontrop RE. Non-human primates: essential partners in biomedical research. Immunol Rev 2001;183:5-9.
7. Cook DJ, Teves L, Tymianski M. Treatment of stroke with a PSD-95 inhibitor in the gyrencephalic primate brain. Nature 2012;483:213-217.
8. Kawai T, et al. Mixed allogeneic chimerism and renal allograft tolerance in cynomolgus monkeys. Transplantation 1995;59:256-262.
9. Klein F, et al. Enhanced HIV-1 immunotherapy by commonly arising antibodies that target virus escape variants. J Exp Med 2014;211:2361-2372.
10. McNamara CW, et al. Targeting Plasmodium PI(4)K to eliminate malaria. Nature 2013;504:248-253.
11. + T cells control AIDS virus replication. Nature 2012;491:129-133.
12. Poliani PL, et al. Delivery to the central nervous system of a nonreplicative herpes simplex type 1 vector engineered with the interleukin 4 gene protects rhesus monkeys from hyperacute autoimmune encephalomyelitis. Hum Gene Ther 2001;12:905-920.
13. Qiu X, et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 2014;514:47-53.
14. Whitehouse J, Micheletta J, Powell LE, Bordier C, Waller BM. The impact of cognitive testing on the welfare of group housed primates. PLoS ONE 2013;8:e78308.
15. Rhesus Macaque Genome S, et al. Evolutionary and biomedical insights from the rhesus macaque genome. Science 2007;316:222-234.
16. Hernandez RD, et al. Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques. Science 2007;316:240-243.
17. Marsh SG, et al. Nomenclature for factors of the HLA system, 2010. Tissue Antigens 2010;75:291-455.
18. Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE. Genetic divergence of the rhesus macaque major histocompa-tibility complex. Genome Res 2004;14:1501-1515.
19. Otting N, et al. Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci USA 2005;102:1626-1631.
20. Shiina T, et al. Rapid evolution of major histocompatibility complex class I genes in primates generates new disease alleles in humans via hitchhiking diversity. Genetics 2006;173:1555-1570.
21. Watkins DI. The evolution of major histocompatibility class I genes in primates. Crit Rev Immunol 1995;15:1-29.
22. Doxiadis GG, de Groot N, Otting N, Blokhuis JH, Bontrop RE. Genomic plasticity of the MHC class I A region in rhesus macaques: extensive haplotype diversity at the population level as revealed by microsatellites. Immunogenetics 2011;63:73-83.
23. Otting N, de Vos-Rouweler AJ, Heijmans CM, de Groot NG, Doxiadis GG, Bontrop RE. MHC class I A region diversity and polymorphism in macaque species. Immunogenetics 2007;59:367-375.
24. de Groot NG, et al. Nomenclature report on the major histocompatibility complex genes and alleles of Great Ape, Old and New World monkey species. Immunogenetics 2012;64:615-631.
25. Urvater JA, Steffen SR, Rehrauer W, Watkins DI. An unusual insertion in intron 2 of apparently functional MHC class I alleles in rhesus macaques. Tissue Antigens 2000;55:153-156.
26. de Groot N, Doxiadis GG, Otting N, de Vos-Rouweler AJ, Bontrop RE. Differential recombination dynamics within the MHC of macaque species. Immunogenetics 2014;66:535-544.
27. Otting N, Doxiadis GG, Bontrop RE. Definition of Mafa-A and -B haplotypes in pedigreed cynomolgus macaques (Macaca fascicularis). Immunogenetics 2009;61:745-753.
28. Doxiadis GG, et al. Haplotype diversity generated by ancient recombination-like events in the MHC of Indian rhesus macaques. Immunogenetics 2013;65:569-584.
29. Piontkivska H, Nei M. Birth-and-death evolution in primate MHC class I genes: divergence time estimates. Mol Biol Evol 2003;20:601-609.
30. Chen ZW, McAdam SN, Hughes AL, Dogon AL, Letvin NL, Watkins DI. Molecular cloning of orangutan and gibbon MHC class I cDNA. The HLA-A and -B loci diverged over 30 million years ago. J Immunol 1992;148:2547-2554.
31. Adams EJ, Thomson G, Parham P. Evidence for an HLA-C-like locus in the orangutan Pongo pygmaeus. Immunogenetics 1999;49:865-871.
32. Boyson JE, et al. The MHC class I genes of the rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates. J Immunol 1996;156:4656-4665.
33. de Groot N, et al. Genetic makeup of the DR region in rhesus macaques: gene content, transcripts, and pseudogenes. J Immunol 2004;172:6152-6157.
34. Abi-Rached L, et al. A small, variable, and irregular killer cell Ig-like receptor locus accompanies the absence of MHC-C and MHC-G in gibbons. J Immunol 2010;184:1379-1391.
35. Apps R, et al. Influence of HLA-C expression level on HIV control. Science 2013;340:87-91.
36. + T cell responses. J Virol 2011;85:3250-3261.
37. Greene JM, et al. Differential MHC class I expression in distinct leukocyte subsets. BMC Immunol 2011;12:39.
38. Sidney J, Peters B, Frahm N, Brander C, Sette A. HLA class I supertypes: a revised and updated classification. BMC Immunol 2008;9:1.
39. de Groot NG, et al. Unique peptide-binding motif for Mamu-B*037:01: an MHC class I allele common to Indian and Chinese rhesus macaques. Immunogenetics 2013;65:897-900.
40. de Groot NG, et al. AIDS-protective HLA-B*27/B*57 and chimpanzee MHC class I molecules target analogous conserved areas of HIV-1/SIVcpz. Proc Natl Acad Sci USA 2010;107:15175-15180.
41. Rosner C, Kruse PH, Lubke T, Walter L. Rhesus macaque MHC class I molecules show differential subcellular localizations. Immunogenetics 2010;62:149-158.
42. Miura M, et al. Characterization of simian T-cell leukemia virus type 1 in naturally infected Japanese macaques as a model of HTLV-1 infection. Retrovirology 2013;10:118.
43. Montiel NA. An updated review of simian betaretrovirus (SRV) in macaque hosts. J Med Primatol 2010;39:303-314.
44. O'Callaghan CA, et al. Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol Cell 1998;1:531-541.
45. Braud VM, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A. B and C. Nature 1998;391:795-799.
46. Boyson JE, et al. The MHC E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 1995;41:59-68.
47. Lafont BA, Buckler-White A, Plishka R, Buckler C, Martin MA. Pig-tailed macaques (Macaca nemestrina) possess six MHC-E families that are conserved among macaque species: implication for their binding to natural killer receptor variants. Immunogenetics 2004;56:142-154.
48. LaBonte ML, Hershberger KL, Korber B, Letvin NL. The KIR and CD94/NKG2 families of molecules in the rhesus monkey. Immunol Rev 2001;183:25-40.
49. Lee N, Ishitani A, Geraghty DE. HLA-F is a surface marker on activated lymphocytes. Eur J Immunol 2010;40:2308-2318.
50. Goodridge JP, Burian A, Lee N, Geraghty DE. HLA-F complex without peptide binds to MHC class I protein in the open conformer form. J Immunol 2010;184:6199-6208.
51. Otting N, Bontrop RE. Characterization of the rhesus macaque (Macaca mulatta) equivalent of HLA-F. Immunogenetics 1993;38:141-145.
52. Djurisic S, Hviid TV. HLA class Ib molecules and immune cells in pregnancy and preeclampsia. Front Immunol 2014;5:652.
53. Boyson JE, Iwanaga KK, Golos TG, Watkins DI. Identification of the rhesus monkey HLA-G ortholog. Mamu-G is a pseudogene. J Immunol 1996;157:5428-5437.
54. Bondarenko GI, et al. Characterization of cynomolgus and vervet monkey placental MHC class I expression: diversity of the nonhuman primate AG locus. Immunogenetics 2009;61:431-442.
55. Boyson JE, Iwanaga KK, Golos TG, Watkins DI. Identification of a novel MHC class I gene, Mamu-AG, expressed in the placenta of a primate with an inactivated G locus. J Immunol 1997;159:3311-3321.
56. van der Wiel MK, Otting N, de Groot NG, Doxiadis GG, Bontrop RE. The repertoire of MHC class I genes in the common marmoset: evidence for functional plasticity. Immunogenetics 2013;65:841-849.
57. Urvater JA, et al. Mamu-I: a novel primate MHC class I B-related locus with unusually low variability. J Immunol 2000;164:1386-1398.
58. Seo JW, Walter L, Gunther E. Genomic analysis of MIC genes in rhesus macaques. Tissue Antigens 2001;58:159-165.
59. Averdam A, et al. Genotyping and segregation analyses indicate the presence of only two functional MIC genes in rhesus macaques. Immunogenetics 2007;59:247-251.
60. Doxiadis GG, Heijmans CM, Otting N, Bontrop RE. MIC gene polymorphism and haplotype diversity in rhesus macaques. Tissue Antigens 2007;69:212-219.
61. Meyer A, et al. High diversity of MIC genes in non-human primates. Immunogenetics 2014;66:581-587.
62. Luoma AM, et al. Crystal structure of Vdelta1 T cell receptor in complex with CD1d-sulfatide shows MHC-like recognition of a self-lipid by human gammadelta T cells. Immunity 2013;39:1032-1042.
63. Xu B, et al. Crystal structure of a gammadelta T-cell receptor specific for the human MHC class I homolog MICA. Proc Natl Acad Sci USA 2011;108:2414-2419.
64. Bontrop RE, Otting N, Slierendregt BL, Lanchbury JS. Evolution of major histocompatibility complex polymorphisms and T-cell receptor diversity in primates. Immunol Rev 1995;143:33-62.
65. Olivieri DN, Gambon-Deza F. V genes in primates from whole genome sequencing data. Immunogenetics 2015;67:211-228.
66. Hansen TH, Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nat Rev Immunol 2009;9:503-513.
67. Vossen MT, Westerhout EM, Soderberg-Naucler C, Wiertz EJ. Viral immune evasion: a masterpiece of evolution. Immunogenetics 2002;54:527-542.
68. Ljunggren HG, Karre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today 1990;11:237-244.
69. Colonna M, Samaridis J. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 1995;268:405-408.
70. Vilches C, Parham P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 2002;20:217-251.
71. Hoglund P, Brodin P. Current perspectives of natural killer cell education by MHC class I molecules. Nat Rev Immunol 2010;10:724-734.
72. Raulet DH, Vance RE. Self-tolerance of natural killer cells. Nat Rev Immunol 2006;6:520-531.
73. Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225-274.
74. Trowsdale J. Genetic and functional relationships between MHC and NK receptor genes. Immunity 2001;15:363-374.
75. Guethlein LA, Flodin LR, Adams EJ, Parham P. NK cell receptors of the orangutan (Pongo pygmaeus): a pivotal species for tracking the coevolution of killer cell Ig-like receptors with MHC-C. J Immunol 2002;169:220-229.
76. Khakoo SI, et al. Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 2000;12:687-698.
77. Blokhuis JH, Doxiadis GG, Bontrop RE. A splice site mutation converts an inhibitory killer cell Ig-like receptor into an activating one. Mol Immunol 2009;46:640-648.
78. Kruse PH, Rosner C, Walter L. Characterization of rhesus macaque KIR genotypes and haplotypes. Immunogenetics 2010;62:281-293.
79. Cadavid LF, Lun CM. Lineage-specific diversification of killer cell Ig-like receptors in the owl monkey, a New World primate. Immunogenetics 2009;61:27-41.
80. Cadavid LF, Palacios C, Lugo JS. Bimodal evolution of the killer cell Ig-like receptor (KIR) family in New World primates. Immunogenetics 2013;65:725-736.
81. Sambrook JG, et al. Identification of the ancestral killer immunoglobulin-like receptor gene in primates. BMC Genom 2006;7:209.
82. Rajagopalan S, Long EO. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 1999;189:1093-1100.
83. Vilches C, Rajalingam R, Uhrberg M, Gardiner CM, Young NT, Parham P. KIR2DL5, a novel killer-cell receptor with a D0-D2 configuration of Ig-like domains. J Immunol 2000;164:5797-5804.
84. Blokhuis JH, van der Wiel MK, Doxiadis GG, Bontrop RE. Evidence for balancing selection acting on KIR2DL4 genotypes in rhesus macaques of Indian origin. Immunogenetics 2009;61:503-512.
85. Bimber BN, Moreland AJ, Wiseman RW, Hughes AL, O'Connor DH. Complete characterization of killer Ig-like receptor (KIR) haplotypes in Mauritian cynomolgus macaques: novel insights into nonhuman primate KIR gene content and organization. J Immunol 2008;181:6301-6308.
86. Pyo CW, et al. Different patterns of evolution in the centromeric and telomeric regions of group A and B haplotypes of the human killer cell Ig-like receptor locus. PLoS ONE 2010;5:e15115.
87. O'Connor GM, et al. Peptide-dependent recognition of HLA-B*57:01 by KIR3DS1. J Virol 2015;89:5213-5221.
88. Blokhuis JH, van der Wiel MK, Doxiadis GG, Bontrop RE. The mosaic of KIR haplotypes in rhesus macaques. Immunogenetics 2010;62:295-306.
89. Colantonio AD, et al. KIR polymorphisms modulate peptide-dependent binding to an MHC class I ligand with a Bw6 motif. PLoS Pathog 2011;7:e1001316.
90. Rosner C, Kruse PH, Hermes M, Otto N, Walter L. Rhesus macaque inhibitory and activating KIR3D interact with Mamu-A-encoded ligands. J Immunol 2011;186:2156-2163.
91. Schafer JL, et al. KIR3DL01 recognition of Bw4 ligands in the rhesus macaque: maintenance of Bw4 specificity since the divergence of apes and Old World monkeys. J Immunol 2014;192:1907-1917.
92. Jiang W, et al. Copy number variation leads to considerable diversity for B but not A haplotypes of the human KIR genes encoding NK cell receptors. Genome Res 2012;22:1845-1854.
93. Blokhuis JH, van der Wiel MK, Doxiadis GG, Bontrop RE. The extreme plasticity of killer cell Ig-like receptor (KIR) haplotypes differentiates rhesus macaques from humans. Eur J Immunol 2011;41:2719-2728.
94. Sambrook JG, et al. Single haplotype analysis demonstrates rapid evolution of the killer immunoglobulin-like receptor (KIR) loci in primates. Genome Res 2005;15:25-35.
95. Uhrberg M, Parham P, Wernet P. Definition of gene content for nine common group B haplotypes of the Caucasoid population: KIR haplotypes contain between seven and eleven KIR genes. Immunogenetics 2002;54:221-229.
96. Uhrberg M, et al. Human diversity in killer cell inhibitory receptor genes. Immunity 1997;7:753-763.
97. Wilson MJ, et al. Plasticity in the organization and sequences of human KIR/ILT gene families. Proc Natl Acad Sci USA 2000;97:4778-4783.
98. Khakoo SI, et al. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 2004;305:872-874.
99. Martin MP, et al. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 2002;31:429-434.
100. Martin MP, et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 2007;39:733-740.
101. Pelak K, et al. Copy number variation of KIR genes influences HIV-1 control. PLoS Biol 2011;9:e1001208.
102. Bakker NP, et al. Resistance to collagen-induced arthritis in a nonhuman primate species maps to the major histocompatibility complex class I region. J Exp Med 1992;175:933-937.
103. Bontrop RE, Watkins DI. MHC polymorphism: AIDS susceptibility in non-human primates. Trends Immunol 2005;26:227-233.
104. Evans DT, et al. Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nat Med 1999;5:1270-1276.
105. Albrecht C, Malzahn D, Brameier M, Hermes M, Ansari AA, Walter L. Progression to AIDS in SIV-infected rhesus macaques is associated with distinct KIR and MHC class I polymorphisms and NK cell dysfunction. Front Immunol 2014;5:600.
106. Chaichompoo P, et al. Multiple KIR gene polymorphisms are associated with plasma viral loads in SIV-infected rhesus macaques. Cell Immunol 2010;263:176-187.
107. Hellmann I, Lim SY, Gelman RS, Letvin NL. Association of activating KIR copy number variation of NK cells with containment of SIV replication in rhesus monkeys. PLoS Pathog 2011;7:e1002436.
108. Hellmann I, Schmitz JE, Letvin NL. Activating KIR copy number variation is associated with granzyme B release by NK cells during primary simian immunodeficiency virus infection in rhesus monkeys. J Virol 2012;86:13103-13107.
109. Maloveste SM, et al. Degenerate recognition of MHC class I molecules with Bw4 and Bw6 motifs by a killer cell Ig-like receptor 3DL expressed by macaque NK cells. J Immunol 2012;189:4338-4348.
110. Alter G, et al. HIV-1 adaptation to NK-cell-mediated immune pressure. Nature 2011;476:96-100.
111. Hiby SE, et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med 2004;200:957-965.
112. Nakimuli A, et al. A KIR B centromeric region present in Africans but not Europeans protects pregnant women from pre-eclampsia. Proc Natl Acad Sci USA 2015;112:845-850.
113. Norman PJ, et al. Co-evolution of human leukocyte antigen (HLA) class I ligands with killer-cell immunoglobulin-like receptors (KIR) in a genetically diverse population of sub-Saharan Africans. PLoS Genet 2013;9:e1003938.
114. Parham P, Moffett A. Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat Rev Immunol 2013;13:133-144.
115. Fadda L, et al. Peptide antagonism as a mechanism for NK cell activation. Proc Natl Acad Sci USA 2010;107:10160-10165.
116. Vivian JP, et al. Killer cell immunoglobulin-like receptor 3DL1-mediated recognition of human leukocyte antigen B. Nature 2011;479:401-405.
117. Beziat V, et al. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 2013;121:2678-2688.
118. Wilkinson GW, et al. Modulation of natural killer cells by human cytomegalovirus. J Clin Virol 2008;41:206-212.
119. De Re V, et al. Genetic diversity of the KIR/HLA system and outcome of patients with metastatic colorectal cancer treated with chemotherapy. PLoS ONE 2014;9:e84940.
120. Dutta A, Saikia N, Phookan J, Baruah MN, Baruah S. Association of killer cell immunoglobulin-like receptor gene 2DL1 and its HLA-C2 ligand with family history of cancer in oral squamous cell carcinoma. Immunogenetics 2014;66:439-448.
121. Verneris MR, Miller JS. KIR B or not to be?...that is the question for ALL. Blood 2014;124:2623-2624.
122. Allen TM, et al. Characterization of the peptide binding motif of a rhesus MHC class I molecule (Mamu-A*01) that binds an immunodominant CTL epitope from simian immunodeficiency virus. J Immunol 1998;160:6062-6071.
123. Dzuris JL, Sidney J, Appella E, Chesnut RW, Watkins DI, Sette A. Conserved MHC class I peptide binding motif between humans and rhesus macaques. J Immunol 2000;164:283-291.
124. Hickman-Miller HD, et al. Rhesus macaque MHC class I molecules present HLA-B-like peptides. J Immunol 2005;175:367-375.
125. + T cell epitopes restricted by the high frequency molecule, Mamu-A*02, and potential escape from CTL recognition. J Immunol 2004;173:5064-5076.
126. + T lymphocyte responses to SIVmac239. J Immunol 2005;175:5986-5997.
127. Loffredo JT, et al. Two MHC class I molecules associated with elite control of immunodeficiency virus replication, Mamu-B*08 and HLA-B*2705, bind peptides with sequence similarity. J Immunol 2009;182:7763-7775.
128. Liu J, et al. Diverse peptide presentation of rhesus macaque major histocompatibility complex class I Mamu-A 02 revealed by two peptide complex structures and insights into immune escape of simian immunodeficiency virus. J Virol 2011;85:7372-7383.
129. Mothe BR, et al. Characterization of the peptide-binding specificity of Mamu-B*17 and identification of Mamu-B*17-restricted epitopes derived from simian immunodeficiency virus proteins. J Immunol 2002;169:210-219.
130. Mothe BR, et al. Peptide-binding motifs associated with MHC molecules common in Chinese rhesus macaques are analogous to those of human HLA supertypes and include HLA-B27-like alleles. Immunogenetics 2013;65:371-386.
131. Reed JS, et al. The role of MHC class I allele Mamu-A*07 during SIV(mac)239 infection. Immunogenetics 2011;63:789-807.
132. Sette A, et al. Characterization of the peptide-binding specificity of Mamu-A*11 results in the identification of SIV-derived epitopes and interspecies cross-reactivity. Immunogenetics 2005;57:53-68.
133. Sette A, et al. A shared MHC supertype motif emerges by convergent evolution in macaques and mice, but is totally absent in human MHC molecules. Immunogenetics 2012;64:421-434.
134. Solomon C, et al. The most common Chinese rhesus macaque MHC class I molecule shares peptide binding repertoire with the HLA-B7 supertype. Immunogenetics 2010;62:451-464.
135. Southwood S, et al. Functional analysis of frequently expressed Chinese rhesus macaque MHC class I molecules Mamu-A1*02601 and Mamu-B*08301 reveals HLA-A2 and HLA-A3 supertypic specificities. Immunogenetics 2011;63:275-290.
136. Wu Y, et al. Structural basis of diverse peptide accommodation by the rhesus macaque MHC class I molecule Mamu-B*17: insights into immune protection from simian immunodeficiency virus. J Immunol 2011;187:6382-6392.