A shared MHC supertype motif emerges by convergent evolution in macaques and mice, but is totally absent in human MHC molecules

Immunogenetics

Volumn 64, Issue 6, 2012, Pages 421-434

  Sette, Alessandro ^a   Sidney, John ^a   Southwood, Scott ^a   Moore, Carrie ^a   Berry, Jessica ^b   Dow, Courtney ^b   Bradley, Kate ^a   Hoof, Ilka ^c   Lewis, Mark G ^d   Hildebrand, William H ^e   McMurtrey, Curtis P ^e   Wilson, Nancy A ^f   Watkins, David I ^f   Mothé, Bianca R ^a,b  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

^c UTRECHT UNIVERSITY   (Netherlands)

^d BIOQUAL INC   (United States)

^e UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

HLA supertype; MHC; Peptide binding motif; Rhesus macaque

Indexed keywords

GLYCINE; H2 ANTIGEN; HISTOCOMPATIBILITY ANTIGEN; HISTOCOMPATIBILITY ANTIGEN H 2D(B); HISTOCOMPATIBILITY ANTIGEN H-2D(B); HLA ANTIGEN CLASS 1; MAMU B 01 ANTIGEN, MACACA MULATTA; MAMU-B 01 ANTIGEN, MACACA MULATTA;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ANTIGENIC VARIATION; ARTICLE; CELLULAR IMMUNITY; CONVERGENT EVOLUTION; HUMAN; MACACA MULATTA; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; ANIMAL; CELL LINE; CHEMISTRY; IMMUNOLOGY; METABOLISM; MOLECULAR EVOLUTION; PROTEIN MOTIF; SEQUENCE ALIGNMENT;

ANIMALIA; MACACA; MACACA MULATTA; MURINAE; MUS; PRIMATES; SIMIAN IMMUNODEFICIENCY VIRUS;

AMINO ACID MOTIFS; ANIMALS; CELL LINE; EVOLUTION, MOLECULAR; H-2 ANTIGENS; HISTOCOMPATIBILITY ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MACACA MULATTA; MICE; SEQUENCE ALIGNMENT;

EID: 84864002335     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-011-0598-5     Document Type: Article

References (50)

1. Achour A, Persson K, Harris RA, Sundback J, Sentman CL, Lindqvist Y, Schneider G, Karre K (1998) The crystal structure of H-2Dd MHC class I complexed with the HIV-1-derived peptide P18-I10 at 2.4 A resolution: implications for T cell and NK cell recognition. Immunity 9:199-208 (Pubitemid 28400033)
2. Allen TM, Mothe BR, Sidney J, Jing P, Dzuris JL, Liebl ME, Vogel TU, O'Connor DH, Wang X, Wussow MC, Thomson JA, Altman JD, Watkins DI, Sette A (2001) CD8(+) lymphocytes from simian immunodeficiency virus-infected rhesus macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule mamu-a*01: implications for vaccine design and testing. J Virol 75:738-749 (Pubitemid 32037277)
3. Allen TM, Sidney J, del Guercio MF, Glickman RL, Lensmeyer GL, Wiebe DA, DeMars R, Pauza CD, Johnson RP, Sette A, Watkins DI (1998) Characterization of the peptide binding motif of a rhesus MHC class I molecule (Mamu-A*01) that binds an immu-nodominant CTL epitope from simian immunodeficiency virus. J Immunol 160:6062-6071 (Pubitemid 28298070)
4. Corr M, Boyd LF, Padlan EA, Margulies DH (1993) H-2Dd exploits a four residue peptide binding motif. J Exp Med 178:1877-1892
5. de Groot NG, Heijmans CM, de Groot N, Otting N, de Vos-Rouweller AJ, Remarque EJ, Bonhomme M, Doxiadis GG, Crouau-Roy B, Bontrop RE (2008) Pinpointing a selective sweep to the chimpanzee MHC class I region by comparative genomics. Mol Ecol 17:2074-2088 (Pubitemid 351521510)
6. de Groot NG, Otting N, Doxiadis GG, Balla-Jhagjhoorsingh SS, Heeney JL, van Rood JJ, Gagneux P, Bontrop RE (2002) Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc Natl Acad Sci USA 99:11748-11753 (Pubitemid 34994470)
7. Dzuris JL, Sidney J, Appella E, Chesnut RW, Watkins DI, Sette A (2000) Conserved MHC class I peptide binding motif between humans and rhesus macaques. J Immunol 164:283-291 (Pubitemid 30013001)
8. Dzuris JL, Sidney J, Horton H, Correa R, Carter D, Chesnut RW, Watkins DI, Sette A (2001) Molecular determinants of peptide binding to two common rhesus macaque major histocompatibility complex class II molecules. J Virol 75:10958-10968 (Pubitemid 33031563)
9. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG (1991) Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351:290-296 (Pubitemid 21896578)
10. Gardner MB, Luciw PA (2008) Macaque models of human infectious disease. ILAR J 49:220-255
11. Giraldo-Vela JP, Rudersdorf R, Chung C, Qi Y, Wallace LT, Bimber B, Borchardt GJ, Fisk DL, Glidden CE, Loffredo JT, Piaskowski SM, Furlott JR, Morales-Martinez JP, Wilson NA, Rehrauer WM, Lifson JD, Carrington M, Watkins DI (2008) The major histocompatibility complex class II alleles Mamu-DRB1*1003 and-DRB1*0306 are enriched in a cohort of simian immunodeficiency virus-infected rhesus macaque elite controllers. J Virol 82:859-870
12. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704 (Pubitemid 37365050)
13. Gulukota K, Sidney J, Sette A, DeLisi C (1997) Two complementary methods for predicting peptides binding major histocompatibility complex molecules. J Mol Biol 267:1258-1267 (Pubitemid 27192636)
14. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160-174 (Pubitemid 16227864)
15. Hawkins OE, Vangundy RS, Eckerd AM, Bardet W, Buchli R, Weidanz JA, Hildebrand WH (2008) Identification of breast cancer pep-tide epitopes presented by HLA-A*0201. J Proteome Res 7:1445-1457
16. Hickman HD, Batson CL, Prilliman KR, Crawford DL, Jackson KL, Hildebrand WH (2000) C-terminal epitope tagging facilitates comparative ligand mapping from MHC class I positive cells. Hum Immunol 61:1339-1346 (Pubitemid 32102423)
17. Hickman-Miller HD, Bardet W, Gilb A, Luis AD, Jackson KW, Watkins DI, Hildebrand WH (2005) Rhesus macaque MHC class I molecules present HLA-B-like peptides. J Immunol 175:367-375 (Pubitemid 40884340)
18. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254-267 (Pubitemid 43100040)
19. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460
20. Karl JA, Wiseman RW, Campbell KJ, Blasky AJ, Hughes AL, Ferguson B, Read DS, O'Connor DH (2008) Identification of MHC class I sequences in Chinese-origin rhesus macaques. Immunogenetics 60:37-46
21. Kestler H, Kodama T, Ringler D, Marthas M, Pedersen N, Lackner A, Regier D, Sehgal P, Daniel M, King N et al (1990) Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 248:1109-1112
22. Kubo RT, Sette A, Grey HM, Appella E, Sakaguchi K, Zhu NZ, Arnott D, Sherman N, Shabanowitz J, Michel H et al (1994) Definition of specific peptide motifs for four major HLA-A alleles. J Immunol 152:3913-3924 (Pubitemid 24111063)
23. Li H, Natarajan K, Malchiodi EL, Margulies DH, Mariuzza RA (1998) Three-dimensional structure of H-2Dd complexed with an immu-nodominant peptide from human immunodeficiency virus envelope glycoprotein 120. J Mol Biol 283:179-191 (Pubitemid 28466648)
24. Loffredo JT, Bean AT, Beal DR, Leon EJ, May GE, Piaskowski SM, Furlott JR, Reed J, Musani SK, Rakasz EG, Friedrich TC, Wilson NA, Allison DB, Watkins DI (2008) Patterns of CD8+ immuno-dominance may influence the ability of Mamu-B*08-positive macaques to naturally control simian immunodeficiency virus SIVmac239 replication. J Virol 82:1723-1738 (Pubitemid 351206923)
25. Loffredo JT, Maxwell J, Qi Y, Glidden CE, Borchardt GJ, Soma T, Bean AT, Beal DR, Wilson NA, Rehrauer WM, Lifson JD, Carrington M, Watkins DI (2007) Mamu-B*08-positive macaques control simian immunodeficiency virus replication. J Virol 81:8827-8832 (Pubitemid 47242856)
26. Loffredo JT, Sidney J, Bean AT, Beal DR, Bardet W, Wahl A, Hawkins OE, Piaskowski S, Wilson NA, Hildebrand WH, Watkins DI, Sette A (2009) 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 182:7763-7775
27. Loffredo JT, Sidney J, Piaskowski S, Szymanski A, Furlott J, Rudersdorf R, Reed J, Peters B, Hickman-Miller HD, Bardet W, Rehrauer WM, O'Connor DH, Wilson NA, Hildebrand WH, Sette A, Watkins DI (2005) The high frequency indian rhesus macaque MHC class I molecule, mamu-b*01, does not appear to be involved in cd8+ T lymphocyte responses to sivmac239. J Immunol 175:5986-5997 (Pubitemid 41508084)
28. Loffredo JT, Sidney J, Wojewoda C, Dodds E, Reynolds MR, Napoe G, Mothe BR, O'Connor DH, Wilson NA, Watkins DI, Sette A (2004) Identification of seventeen new simian immunodeficiency virus-derived CD8+ T cell epitopes restricted by the high frequency molecule, Mamu-A*02, and potential escape from CTL recognition. J Immunol 173:5064-5076 (Pubitemid 39387789)
29. Madden DR (1995) The three-dimensional structure of peptide-MHC complexes. Annu Rev Immunol 13:587-622
30. Miller CJ, Alexander NJ, Sutjipto S, Lackner AA, Gettie A, Hendrickx AG, Lowenstine LJ, Jennings M, Marx PA (1989) Genital muco-sal transmission of simian immunodeficiency virus: animal model for heterosexual transmission of human immunodeficiency virus. J Virol 63:4277-4284 (Pubitemid 19229423)
31. Mothe BR, Sidney J, Dzuris JL, Liebl ME, Fuenger S, Watkins DI, Sette A (2002) Characterization of the peptide-binding specificity of mamu-b*17 and identification of mamu-b*17-restricted epit-opes derived from simian immunodeficiency virus proteins. J Immunol 169:210-219 (Pubitemid 34686138)
32. Parham P (2005) MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5:201-214 (Pubitemid 40364822)
33. Pinilla C, Martin R, Gran B, Appel JR, Boggiano C, Wilson DB, Houghten RA (1999) Exploring immunological specificity using synthetic pep-tide combinatorial libraries. Curr Opin Immunol 11:193-202 (Pubitemid 29154906)
34. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253-1256 (Pubitemid 351882013)
35. Reed JS, Sidney J, Piaskowski SM, Glidden CE, Leon EJ, Burwitz BJ, Kolar HL, Eernisse CM, Furlott JR, Maness NJ, Walsh AD, Rudersdorf RA, Bardet W, McMurtrey CP, O'Connor DH, Hilde-brand WH, Sette A, Watkins DI, Wilson NA (2011) The role of MHC class I allele mamu-a*07 during SIV(mac)239 infection. Immunogenetics 63:789-807
36. Robinson J, Mistry K, McWilliam H, Lopez R, Marsh SG (2010) IPD-the Immuno Polymorphism Database. Nucleic Acids Res 38:D863-D869
37. Saper MA, Bjorkman PJ, Wiley DC (1991) Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J Mol Biol 219:277-319
38. Schneidewind A, Brockman MA, Sidney J, Wang YE, Chen H, Suscovich TJ, Li B, Adam RI, Allgaier RL, Mothe BR, Kuntzen T, Oniangue-Ndza C, Trocha A, Yu XG, Brander C, Sette A, Walker BD, Allen TM (2008) Structural and functional constraints limit options for cytotoxic T-lymphocyte escape in the immunodominant HLA-B27-restricted epitope in human immunodeficiency virus type 1 capsid. J Virol 82:5594-5605 (Pubitemid 351705266)
39. Sette A, Sidney J (1998) HLA supertypes and supermotifs: a functional perspective on HLA polymorphism. Curr Opin Immunol 10:478-482 (Pubitemid 28393833)
40. Sette A, Sidney J (1999) Nine major HLA class I supertypes account for the vast preponderance of HLA-A and-B polymorphism. Immunogenetics 50:201-212 (Pubitemid 30099525)
41. Sette A, Sidney J, Bui HH, Del Guercio MF, Alexander J, Loffredo J, Watkins DI, Mothe BR (2005) Characterization of the peptide-binding specificity of mamu-a*11 results in the identification of siv-derived epitopes and interspecies cross-reactivity. Immunogenetics 57(1-2):53-68 (Pubitemid 40598019)
42. Sette A, Sidney J, del Guercio MF, Southwood S, Ruppert J, Dahlberg C, Grey HM, Kubo RT (1994) Peptide binding to the most frequent HLA-A class I alleles measured by quantitative molecular binding assays. Mol Immunol 31:813-822 (Pubitemid 24254672)
43. Sette A, Sidney J, Livingston B, Dzuris J, Crimi C, Walker CM, Southwood S, Collins EJ, Hughes A (2003) Class I molecules with similar peptide binding specificities are the result of both common ancestry and convergent evolution. Immunogenetics 54:830-841 (Pubitemid 36470076)
44. Sidney J, Assarsson E, Moore C, Ngo S, Pinilla C, Sette A, Peters B (2008) Quantitative peptide binding motifs for 19 human and mouse MHC class I molecules derived using positional scanning combinatorial peptide libraries. Immunome Res 4:2
45. Sidney J, Southwood S, Mann DL, Fernandez-Vina MA, Newman MJ, Sette A (2001) Majority of peptides binding HLA-A*0201 with high affinity crossreact with other A2-supertype molecules. Hum Immunol 62:1200-1216 (Pubitemid 33032272)
46. Sidney J, Southwood S, Sette A (2005) Classification of A1-and A24-supertype molecules by analysis of their MHC-peptide binding repertoires. Immunogenetics 57:393-408 (Pubitemid 41396764)
47. Smith SM, Holland B, Russo C, Dailey PJ, Marx PA, Connor RI (1999) Retrospective analysis of viral load and SIV antibody responses in rhesus macaques infected with pathogenic SIV: predictive value for disease progression. AIDS Res Hum Retro-viruses 15:1691-1701
48. Solomon C, Southwood S, Hoof I, Rudersdorf R, Peters B, Sidney J, Pinilla C, Marcondes MC, Ling B, Marx P, Sette A, Mothe BR (2010) The most common chinese rhesus macaque MHC class I molecule shares peptide binding repertoire with the hla-b7 supertype. Immunogenetics 62:451-464
49. Southwood S, Solomon C, Hoof I, Rudersdorf R, Sidney J, Peters B, Wahl A, Hawkins O, Hildebrand W, Mothe BR, Sette A (2011) 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 63:275-290
50. Wiseman RW, Karl JA, Bimber BN, O'Leary CE, Lank SM, Tuscher JJ, Detmer AM, Bouffard P, Levenkova N, Turcotte CL, Szekeres E Jr, Wright C, Harkins T, O'Connor DH (2009) Major histocom-patibility complex genotyping with massively parallel pyrose-quencing. Nat Med 15:1322-1326