Abstract
Rhesus macaques (Macaca mulatta) are widely used in developing a strategy for vaccination against human immunodeficiency virus by using simian immunodeficiency virus infection as a model system. Because the genome diversity of major histocompatibility complex (MHC) is well known to control the immune responsiveness to foreign antigens, MHC loci in Indian- and Chinese-origin macaques used in the experiments have been characterized, and it was revealed that the diversity of MHC in macaques was larger than the human MHC. To further characterize the diversity of Mamu-A and Mamu-B loci, we investigated a total of 73 different sequences of Mamu-A, 83 sequences of Mamu-B, and 15 sequences of Mamu-I cDNAs isolated from Burmese-origin macaques. It was found that there were one to five expressing genes in each locus. Among the Mamu-A, Mamu-B, and Mamu-I sequences, 44 (60.2%), 45 (54.2%), and 8 (53.3%), respectively, were novel, and most of the other known alleles were identical to those reported from Chinese- or Indian-origin macaques, demonstrating a genetic mixture between the geographically distinct populations of present day China and India. In addition, it was found that a Mamu haplotype contained at least two highly transcribed Mamu-A genes, because multiple Mamu-A1 cDNAs were obtained from one haplotype. These findings further revealed the diversity and complexity of MHC locus in the rhesus macaques.
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References
Barouch DH, Santra S, Schmitz JE et al (2000) Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290:486–492
Bassinger JW, 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
Campbell KJ, Detmer AM, Karl JA, Wiseman RW, Blasky AJ, Hughes AL, Bimber BN, O'Connor SL, O'Connor DH (2009) Characterization of 47 MHC class I sequences in Filipino cynomolgus macaques. Immunogenetics 61:177–187
Chu F, Lou Z, Chen YW, Liu Y, Gao B, Zong L, Khan AH, Bell JI, Rao Z, Gao GF (2007) First glimpse of the peptide presentation by rhesus macaque MHC class I: crystal structure of Mamu-A*01 complexed with two immunogenic SIV epitopes and insights into CTL escape. J Immunol 178:944–952
Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE (2004) Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14:1501–1515
Friedrich TC, Dodds EJ, Yant LJ et al (2004) Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat Med 10:275–281
Gibbs RA, Rogers J, Katze MG et al (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234
Goulder PJ, Watkins DI (2008) Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat Rev Immunol 8:619–630
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
Kawada M, Tsukamoto T, Yamamoto H, Iwamoto N, Kurihara K, Takeda A, Moriya C, Takeuchi H, Akari H, Matano T (2008) Gag-specific cytotoxic T-lymphocyte-based control of primary simian immunodeficiency virus replication in a vaccine trial. J Virol 82:10199–10206
Kulski JK, Anzai T, Shiina T, Inoko H (2004) Rhesus macaque class I duplicon structures, organization, and evolution within the alpha block of the major histocompatibility complex. Mol Biol Evol 21:2079–2091
Loffredo JT, Maxwell J, Qi Y, Glidden CE, Borchardt GJ, Soma T, Bean AT, Beal DR, Willson 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
Loffredo JT, Bean AT, Beal DR, León 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+ immunodominance may influence the ability of Mamu-B*08-positive macaques to naturally control simian immunodeficiency virus SIVmac239 replication. J Virol 82:1723–1738
Maness NJ, Yant LJ, Chung C, Loffredo JT, Friedrich TC, Piaskowski SM, Furlott J, May GE, Soma T, Leon FJ, Wilson NA, Piontkivsa H, Hughes AL, Sidney J, Sette A, Watkins DI (2008) Comprehensive immunological evolution reveals surprisingly few differences between elite controller and progressor Mamu-B*17-positive simian immunodeficiency virus-infected rhesus macaques. J Virol 82:5245–5254
Matano T, Kobayashi M, Igarashi H et al (2004) Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trail. J Exp Med 199:1709–1718
Mothe BR, Weinfurter J, Wang C, Rehrauer W, Wilson N, Allen TM, Allison DB, Watkins DI (2003) Expression of the major histocompatibility complex class I molecule Mamu-A*01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 77:2736–2740
Otting N, Hejimans CMC, Noort RC, de Groot NG, Gaby GMD, van Rood JJ, Watkins DI, Bontrop RE (2004) Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci USA 102:1626–1631
Otting N, de Vos-Rouweler AJM, Heijmans CMC, de Groot NG, Doxiadis GGM, Bontrop RE (2007) MHC class I A region diversity and polymorphism in macaque species. Immunogenetics 59:367–375
Otting N, Heijimans CMC, van der Wiel M, de Groot NG, Doxiadis GGM, Bontrop RE (2008) A snapshot of the Mamu-B genes and their allelic repertoire in rhesus macaques of Chinese origin. Immunogenetics 60:507–514
Otting N, Doxiadis GG, Bontrop RE (2009) Definition of Mafa-A and -B haplotypes in pedigreed cynomolgus macaques (Macaca fascicularis). Immunogenetics 61:745–753
Reynolds MR, Weiler AM, Weisgrau KL et al (2008) Macaques vaccinated with live-attenuated SIV control replication of heterologous virus. J Exp Med 205:2537–2550
Robinson J, Waller MJ, Parham P, de Groot N, Bontrop R, Kennedy LJ, Stoehr P, Marsh SGE (2003) IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic Acids Res 31:311–314
Ronser C, Kruse PH, Lűbke T, Walter L (2010) Rhesus macaque MHC class I molecules show differential subcellular localizations. Immunogenetics 62:149–158
Schmitz JE, Kuroda MJ, Santra S et al (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857–860
Sidney J, Dzuris JL, Newman MJ, Johnson PR, 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
Stewart CB, Disotell TR (1998) Primate evolution—in and out of Africa. Curr Biol 8:R582–R588
Tanaka-Takahashi Y, Yasunami M, Naruse T, Hinohara K, Matano T, Mori K, Miyazawa M, Honda M, Yasutomi Y, Nagai Y, Kimura A (2007) Reference strand-mediated conformation analysis-based typing of multiple alleles in the rhesus macaque MHC class I Mamu-A and Mamu-B loci. Electrophoresis 28:918–924
Timmins RJ, Richardson M, Chhangani A, Yongcheng L (2008) Macaca mulatta. In: IUCN 2009. IUCN red list of threatened species. Version 2009.1. <www.iucnredlist.org>.
Tsukamoto T, Dohki S, Ueno T, Kawada M, Takeda A, Yasunami M, Naruse T, Kimura A, Takiguchi M, Matano T (2008) Determination of a major histocompatibility complex class I restricting simian immunodeficiency virus Gag241-249 epitope. AIDS 22:993–998
Urvater JA, Otting N, Loehrke JH, Rudersdorf R, Slukvin II, Piekarczyk MS, Goios TG, Hughes AL, Bontrop RE, Watkins DI (2000) Mamu-I: A novel primate MHC class I B-related locus with unusually low variability. J Immunol 164:1386–1398
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
Yasutomi Y, Reimann K, Lord C, Miller M, Letvin N (1993) Simian immunodeficiency virus-specific CD8+ lymphocyte response in acutely infected rhesus monkeys. J Virol 67:1707–1711
Acknowledgments
We thank Miss Yukiko Ueda for technical assistance. This work was supported in part by research grants from the Ministry of Health, Labor and Welfare, Japan; the Japan Health Science Foundation; the program of Founding Research Centers for Emerging and Reemerging Infection Disease; Grant-in-Aids for Scientific research from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan; and research grants from Heiwa Nakajima Foundation, Japan and from Life Science Institute of Seizon-Kagaku Foundation, Japan.
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Naruse, T.K., Chen, Z., Yanagida, R. et al. Diversity of MHC class I genes in Burmese-origin rhesus macaques. Immunogenetics 62, 601–611 (2010). https://doi.org/10.1007/s00251-010-0462-z
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DOI: https://doi.org/10.1007/s00251-010-0462-z