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Chinese origin rhesus macaque major histocompatibility complex class I molecules promiscuously present epitopes from SIV associated with molecules of Indian origin; implications for immunodominance and viral escape

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Abstract

The presentation of identical peptides by different major histocompatibility complex class I (MHC-I) molecules, termed promiscuity, is a controversial feature of T cell-mediated immunity to pathogens. The astounding diversity of MHC-I molecules in human populations, presumably to enable binding of equally diverse peptides, implies promiscuity would be a rare phenomenon. However, if it occurs, it would have important implications for immunity. We screened 77 animals for responses to peptides known to bind MHC-I molecules that were not expressed by these animals. Some cases of supposed promiscuity were determined to be the result of either non-identical optimal peptides or were simply not mapped to the correct MHC-I molecule in previous studies. Cases of promiscuity, however, were associated with alterations of immunodominance hierarchies, either in terms of the repertoire of peptides presented by the different MHC-I molecules or in the magnitude of the responses directed against the epitopes themselves. Specifically, we found that the Mamu-B*017:01-restricted peptides Vif HW8 and cRW9 were also presented by Mamu-A2*05:26 and targeted by an animal expressing that allele. We also found that the normally subdominant Mamu-A1*001:01 presented peptide Gag QI9 was also presented by Mamu-B*056:01. Both A2*05:26 and B*056:01 are molecules typically or exclusively expressed by animals of Chinese origin. These data clearly demonstrate that MHC-I epitope promiscuity, though rare, might have important implications for immunodominance and for the transmission of escape mutations, depending on the relative frequencies of the given alleles in a population.

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References

  • 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 immunodominant CTL epitope from simian immunodeficiency virus. J Immunol 160:6062–6071

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Axelsson-Robertson R, Weichold F, Sizemore D, Wulf M, Skeiky YA, Sadoff J, Maeurer MJ (2010) Extensive major histocompatibility complex class I binding promiscuity for Mycobacterium tuberculosis TB10.4 peptides and immune dominance of human leucocyte antigen (HLA)-B*0702 and HLA-B*0801 alleles in TB10.4 CD8 T-cell responses. Immunology 129:496–505

    Article  PubMed  CAS  Google Scholar 

  • Barouch DH, Kunstman J, Kuroda MJ, Schmitz JE, Santra S, Peyerl FW, Krivulka GR, Beaudry K, Lifton MA, Gorgone DA, Montefiori DC, Lewis MG, Wolinsky SM, Letvin NL (2002) Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335–339

    Article  PubMed  CAS  Google Scholar 

  • Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB (1994) Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 68:6103–6110

    PubMed  CAS  Google Scholar 

  • Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, Meyers H, Nelson JA, Gairin JE, Hahn BH, Oldstone MB, Shaw GM (1997) Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 3:205–211

    Article  PubMed  CAS  Google Scholar 

  • Burdo TH, Marcondes MC, Lanigan CM, Penedo MC, Fox HS (2005) Susceptibility of Chinese rhesus monkeys to SIV infection. AIDS 19:1704–1706

    Article  PubMed  Google Scholar 

  • Carrington M, O'Brien SJ (2003) The influence of HLA genotype on AIDS. Annu Rev Med 54:535–551

    Article  PubMed  CAS  Google Scholar 

  • Casimiro DR, Wang F, Schleif WA, Liang X, Zhang ZQ, Tobery TW, Davies ME, McDermott AB, O'Connor DH, Fridman A, Bagchi A, Tussey LG, Bett AJ, Finnefrock AC, Fu TM, Tang A, Wilson KA, Chen M, Perry HC, Heidecker GJ, Freed DC, Carella A, Punt KS, Sykes KJ, Huang L, Ausensi VI, Bachinsky M, Sadasivan-Nair U, Watkins DI, Emini EA, Shiver JW (2005) Attenuation of simian immunodeficiency virus SIVmac239 infection by prophylactic immunization with DNA and recombinant adenoviral vaccine vectors expressing Gag. J Virol 79:15547–15555

    Article  PubMed  CAS  Google Scholar 

  • DeMars R, Rudersdorf R, Chang C, Petersen J, Strandtmann J, Korn N, Sidwell B, Orr HT (1985) Mutations that impair a posttranscriptional step in expression of HLA-A and -B antigens. Proc Natl Acad Sci USA 82:8183–8187

    Article  PubMed  CAS  Google Scholar 

  • Doxiadis GG, de Groot N, Otting N, Blokhuis JH, Bontrop RE (2011) Genomic plasticity of the MHC class I A region in rhesus macaques: extensive haplotype diversity at the population level as revealed by microsatellites. Immunogenetics 63:73–83

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Frahm N, Yusim K, Suscovich TJ, Adams S, Sidney J, Hraber P, Hewitt HS, Linde CH, Kavanagh DG, Woodberry T, Henry LM, Faircloth K, Listgarten J, Kadie C, Jojic N, Sango K, Brown NV, Pae E, Zaman MT, Bihl F, Khatri A, John M, Mallal S, Marincola FM, Walker BD, Sette A, Heckerman D, Korber BT, Brander C (2007) Extensive HLA class I allele promiscuity among viral CTL epitopes. Eur J Immunol 37:2419–2433

    Article  PubMed  CAS  Google Scholar 

  • Friedrich TC, Dodds EJ, Yant LJ, Vojnov L, Rudersdorf R, Cullen C, Evans DT, Desrosiers RC, Mothe BR, Sidney J, Sette A, Kunstman K, Wolinsky S, Piatak M, Lifson J, Hughes AL, Wilson N, O'Connor DH, Watkins DI (2004a) Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat Med 10:275–281

    Article  PubMed  CAS  Google Scholar 

  • Friedrich TC, Frye CA, Yant LJ, O'Connor DH, Kriewaldt NA, Benson M, Vojnov L, Dodds EJ, Cullen C, Rudersdorf R, Hughes AL, Wilson N, Watkins DI (2004b) Extraepitopic compensatory substitutions partially restore fitness to simian immunodeficiency virus variants that escape from an immunodominant cytotoxic-T-lymphocyte response. J Virol 78:2581–2585

    Article  PubMed  CAS  Google Scholar 

  • Friedrich TC, Valentine LE, Yant LJ, Rakasz EG, Piaskowski SM, Furlott JR, Weisgrau KL, Burwitz B, May GE, Leon EJ, Soma T, Napoe G, Capuano S, Friedrich TC, Valentine LE, Yant LJ, Rakasz EG, Piaskowski SM, Furlott JR, Weisgrau KL, Burwitz B, May GE, Leon EJ, Soma T, Napoe G, Capuano SVr, Wilson NA, Watkins DI (2007) Subdominant CD8+ T-cell responses are involved in durable control of AIDS virus replication. J Virol 81:3465–3476

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170

    Article  PubMed  CAS  Google Scholar 

  • Hughes AL, Ota T, Nei M (1990) Positive Darwinian selection promotes charge profile diversity in the antigen-binding cleft of class I major-histocompatibility-complex molecules. Mol Biol Evol 7:515–524

    PubMed  CAS  Google Scholar 

  • Joag SV, Stephens EB, Adams RJ, Foresman L, Narayan O (1994) Pathogenesis of SIVmac infection in Chinese and Indian rhesus macaques: effects of splenectomy on virus burden. Virology 200:436–446

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Leslie A, Price DA, Mkhize P, Bishop K, Rathod A, Day C, Crawford H, Honeyborne I, Asher TE, Luzzi G, Edwards A, Rousseau CM, Mullins JI, Tudor-Williams G, Novelli V, Brander C, Douek DC, Kiepiela P, Walker BD, Goulder PJ (2006) Differential selection pressure exerted on HIV by CTL targeting identical epitopes but restricted by distinct HLA alleles from the same HLA supertype. J Immunol 177:4699–4708

    PubMed  CAS  Google Scholar 

  • Ling B, Veazey RS, Penedo C, Xu K, Lifson JD, Marx PA (2002) Longitudinal follow up of SIVmac pathogenesis in rhesus macaques of Chinese origin: emergence of B cell lymphoma. J Med Primatol 31:154–163

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Loffredo JT, Friedrich TC, Leon EJ, Stephany JJ, Rodrigues DS, Spencer SP, Bean AT, Beal DR, Burwitz BJ, Rudersdorf RA, Wallace LT, Piaskowski SM, May GE, Sidney J, Gostick E, Wilson NA, Price DA, Kallas EG, Piontkivska H, Hughes AL, Sette A, Watkins DI (2007a) CD8+ T cells from SIV elite controller macaques recognize Mamu-B*08-bound epitopes and select for widespread viral variation. PLoS ONE 2:e1152

    Article  PubMed  Google Scholar 

  • 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 (2007b) Mamu-B*08-positive macaques control simian immunodeficiency virus replication. J Virol 81:8827–8832

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Madden DR, Gorga JC, Strominger JL, Wiley DC (1992) The three-dimensional structure of HLA-B27 at 2.1 A resolution suggests a general mechanism for tight peptide binding to MHC. Cell 70:1035–1048

    Article  PubMed  CAS  Google Scholar 

  • Maness NJ, Valentine LE, May GE, Reed J, Piaskowski SM, Soma T, Furlott J, Rakasz EG, Friedrich TC, Price DA, Gostick E, Hughes AL, Sidney J, Sette A, Wilson NA, Watkins DI (2007) AIDS virus specific CD8+ T lymphocytes against an immunodominant cryptic epitope select for viral escape. J Exp Med 204:2505–2512

    Article  PubMed  CAS  Google Scholar 

  • Maness NJ, Yant LJ, Chung C, Loffredo JT, Friedrich TC, Piaskowski SM, Furlott J, May GE, Soma T, Leon EJ, Wilson NA, Piontkivska H, Hughes AL, Sidney J, Sette A, Watkins DI (2008) Comprehensive immunological evaluation reveals surprisingly few differences between elite controller and progressor Mamu-B*17-positive simian immunodeficiency virus-infected rhesus macaques. J Virol 82:5245–5254

    Article  PubMed  CAS  Google Scholar 

  • Maness NJ, Sacha JB, Piaskowski SM, Weisgrau KL, Rakasz EG, May GE, Buechler MB, Walsh AD, Wilson NA, Watkins DI (2009) Novel translation products from simian immunodeficiency virus SIVmac239 Env-encoding mRNA contain both Rev and cryptic T-cell epitopes. J Virol 83:10280–10285

    Article  PubMed  CAS  Google Scholar 

  • Maness NJ, Walsh AD, Piaskowski SM, Furlott J, Kolar HL, Bean AT, Wilson NA, Watkins DI (2010) CD8+ T cell recognition of cryptic epitopes is a ubiquitous feature of AIDS virus infection. J Virol 84:11569–11574

    Article  PubMed  CAS  Google Scholar 

  • Marthas ML, Lu D, Penedo MC, Hendrickx AG, Miller CJ (2001) Titration of an SIVmac251 stock by vaginal inoculation of Indian and Chinese origin rhesus macaques: transmission efficiency, viral loads, and antibody responses. AIDS Res Hum Retroviruses 17:1455–1466

    Article  PubMed  CAS  Google Scholar 

  • Matano T, Shibata R, Siemon C, Connors M, Lane HC, Martin MA (1998) Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J Virol 72:164–169

    PubMed  CAS  Google Scholar 

  • Matsumura M, Fremont DH, Peterson PA, Wilson IA (1992) Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 257:927–934

    Article  PubMed  CAS  Google Scholar 

  • McDermott AB, O'Connor DH, Fuenger S, Piaskowski S, Martin S, Loffredo J, Reynolds M, Reed J, Furlott J, Jacoby T, Riek C, Dodds E, Krebs K, Davies ME, Schleif WA, Casimiro DR, Shiver JW, Watkins DI (2005) Cytotoxic T-lymphocyte escape does not always explain the transient control of simian immunodeficiency virus SIVmac239 viremia in adenovirus-boosted and DNA-primed Mamu-A*01-positive rhesus macaques. J Virol 79:15556–15566

    Article  PubMed  CAS  Google Scholar 

  • 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 epitopes derived from simian immunodeficiency virus proteins. J Immunol 169:210–219

    PubMed  CAS  Google Scholar 

  • Otting N, Heijmans CM, Noort RC, de Groot NG, Doxiadis GG, van Rood JJ, Watkins DI, Bontrop RE (2005) Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci USA 102:1626–1631

    Article  PubMed  CAS  Google Scholar 

  • Otting N, de Vos-Rouweler AJ, Heijmans CM, de Groot NG, Doxiadis GG, Bontrop RE (2007) MHC class I A region diversity and polymorphism in macaque species. Immunogenetics 59:367–375

    Article  PubMed  CAS  Google Scholar 

  • Otting N, Heijmans CM, van der Wiel M, de Groot NG, Doxiadis GG, Bontrop RE (2008) A snapshot of the Mamu-B genes and their allelic repertoire in rhesus macaques of Chinese origin. Immunogenetics 60:507–514

    Article  PubMed  Google Scholar 

  • Ouyang D, Wang X, He X, Xu L, Shi H, Gao Q, Guo H (2009) Construction of soluble Mamu-b*1703, a class I major histocompatibility complex of Chinese rhesus macaques, monomer and tetramer loaded with a simian immunodeficiency virus peptide. Cell Mol Immunol 6:117–122

    Article  PubMed  CAS  Google Scholar 

  • Sacha JB, Reynolds MR, Buechler MB, Chung C, Jonas AK, Wallace LT, Weiler AM, Lee W, Piaskowski SM, Soma T, Friedrich TC, Wilson NA, Watkins DI (2008) Differential antigen presentation kinetics of CD8+ T-cell epitopes derived from the same viral protein. J Virol 82:9293–9298

    Article  PubMed  CAS  Google Scholar 

  • Sette A, Vitiello A, Reherman B, Fowler P, Nayersina R, Kast WM, Melief CJ, Oseroff C, Yuan L, Ruppert J, Sidney J, del Guercio MF, Southwood S, Kubo RT, Chesnut RW, Grey HM, Chisari FV (1994) The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J Immunol 153:5586–5592

    PubMed  CAS  Google Scholar 

  • 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 57:53–68

    Article  PubMed  CAS  Google Scholar 

  • Sidney J, Dzuris JL, Newman MJ, Johnson RP, Kaur A, Amitinder K, Walker CM, Appella E, Mothe B, Watkins DI, Sette A (2000) Definition of the Mamu A*01 peptide binding specificity: application to the identification of wild-type and optimized ligands from simian immunodeficiency virus regulatory proteins. J Immunol 165:6387–6399

    PubMed  CAS  Google Scholar 

  • 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(7):451–464

    Article  PubMed  CAS  Google Scholar 

  • Trichel AM, Rajakumar PA, Murphey-Corb M (2002) Species-specific variation in SIV disease progression between Chinese and Indian subspecies of rhesus macaque. J Med Primatol 31:171–178

    Article  PubMed  CAS  Google Scholar 

  • Vogel TU, Friedrich TC, O'Connor DH, Rehrauer W, Dodds EJ, Hickman H, Hildebrand W, Sidney J, Sette A, Hughes A, Horton H, Vielhuber K, Rudersdorf R, De Souza IP, Reynolds MR, Allen TM, Wilson N, Watkins DI (2002) Escape in one of two cytotoxic T-lymphocyte epitopes bound by a high-frequency major histocompatibility complex class I molecule, Mamu-A*02: a paradigm for virus evolution and persistence? J Virol 76:11623–11636

    Article  PubMed  CAS  Google Scholar 

  • Wilson NA, Reed J, Napoe GS, Piaskowski S, Szymanski A, Furlott J, Gonzalez EJ, Yant LJ, Maness NJ, May GE, Soma T, Reynolds MR, Rakasz E, Rudersdorf R, McDermott AB, O'Connor DH, Friedrich TC, Allison DB, Patki A, Picker LJ, Burton DR, Lin J, Huang L, Patel D, Heindecker G, Fan J, Citron M, Horton M, Wang F, Liang X, Shiver JW, Casimiro DR, Watkins DI (2006) Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239. J Virol 80:5875–5885

    Article  PubMed  CAS  Google Scholar 

  • Wilson NA, Keele BF, Reed JS, Piaskowski SM, MacNair CE, Bett AJ, Liang X, Wang F, Thoryk E, Heidecker GJ, Citron MP, Huang L, Lin J, Vitelli S, Ahn CD, Kaizu M, Maness NJ, Reynolds MR, Friedrich TC, Loffredo JT, Rakasz EG, Erickson S, Allison DB, Piatak MJ, Lifson JD, Shiver JW, Casimiro DR, Shaw GM, Hahn BH, Watkins DI (2009) Vaccine-induced cellular responses control simian immunodeficiency virus replication after heterologous challenge. J Virol 83:6508–6521

    Article  PubMed  CAS  Google Scholar 

  • Wiseman RW, Karl JA, Bimber BN, O'Leary CE, Lank SM, Tuscher JJ, Detmer AM, Bouffard P, Levenkova N, Turcotte CL, Szekeres EJ, Wright C, Harkins T, O'Connor DH (2009) Major histocompatibility complex genotyping with massively parallel pyrosequencing. Nat Med 15:1322–1326

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Bassinger S, Montoya GD, Chavez L, Jones CE, Holder-Lockyer B, Masten B, Williams TM, Prilliman KR (2008) Allelic diversity within the high frequency Mamu-A2*05/Mane-A2*05 (Mane-A*06)/Mafa-A2*05 family of macaque MHC-A loci. Tissue Antigens 72:29–38

    Article  PubMed  CAS  Google Scholar 

  • Yant LJ, Friedrich TC, Johnson RC, May GE, Maness NJ, Enz AM, Lifson JD, O'Connor DH, Carrington M, Watkins DI (2006) The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 80:5074–5077

    Article  PubMed  CAS  Google Scholar 

  • Zhumabayeva B, Chenchik A, Siebert PD (1999) RecA-mediated affinity capture: a method for full-length cDNA cloning. Biotechniques 27:834–836, 838, 840 passim

    PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by NIH grants R37 AI052056, R01 A1049120, R01 AI076114, R24 RR015371, R24 RR016038, and R21 AI081590 to D.I.W. and grant P51 RR000167 from the National Center for Research Resources, a component of the National Institutes of Health (to the Wisconsin National Primate Research Center, University of Wisconsin-Madison). This research was conducted in part at a facility constructed with support from Research Facilities Improvement grants RR15459-01 and RR020141-01.

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  1. Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, 585 Science Drive, Madison, WI, 53711, USA

    Nicholas James Maness, Andrew D. Walsh, Richard A. Rudersdorf, Priscilla A. Erickson, Shari M. Piaskowski, Nancy A. Wilson & David I. Watkins

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  1. Nicholas James Maness
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  2. Andrew D. Walsh
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  3. Richard A. Rudersdorf
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  4. Priscilla A. Erickson
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  7. David I. Watkins
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Correspondence to Nicholas James Maness.

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Maness, N.J., Walsh, A.D., Rudersdorf, R.A. et al. Chinese origin rhesus macaque major histocompatibility complex class I molecules promiscuously present epitopes from SIV associated with molecules of Indian origin; implications for immunodominance and viral escape. Immunogenetics 63, 587–597 (2011). https://doi.org/10.1007/s00251-011-0538-4

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