MHC class I characterization of Indonesian cynomolgus macaques
Cynomolgus macaques (Macaca fascicularis) are quickly becoming a useful model for infectious disease and transplantation research. Even though cynomolgus macaques from different geographic regions are used for these studies, there has been limited characterization of full-length major histocompatibility complex (MHC) class I immunogenetics of distinct geographic populations. Here, we identified 48 MHC class I cDNA nucleotide sequences in eleven Indonesian cynomolgus macaques, including 41 novel Mafa-A and Mafa-B sequences. We found seven MHC class I sequences in Indonesian macaques that were identical to MHC class I sequences identified in Malaysian or Mauritian macaques. Sharing of nucleotide sequences between these geographically distinct populations is also consistent with the hypothesis that Indonesia was a source of the Mauritian macaque population. In addition, we found that the Indonesian cDNA sequence Mafa-B*7601 is identical throughout its peptide binding domain to Mamu-B*03, an allele that has been associated with control of Simian immunodeficiency virus (SIV) viremia in Indian rhesus macaques. Overall, a better understanding of the MHC class I alleles present in Indonesian cynomolgus macaques improves their value as a model for disease research, and it better defines the biogeography of cynomolgus macaques throughout Southeast Asia.
KeywordsMHC Immunogenetics Indonesia Macaca fascicularis
This work was supported by 1 R24 RR021745-01A1. PCR-SSP assay development was supported by NIAID Contract number HHSN266200400088C/N01-AI-40088. Support to C.J.P. was made possible through funding for undergraduate research from the UW-Madison Hilldale Fund, and support to A.L.H. was provided by grant number GM43940 from the NIH. This publication was also made possible in part by grant number P51 RR000167 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH), 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 Program grant numbers RR15459-01 and RR020141-01. This publication’s contents are solely the responsibility of the authors and do not necessarily represent the official views of NCRR or NIH.
We thank the Washington Primate Research Center for providing blood samples from animals IN01 through 1N12 and the Cerus Corporation for providing PBMC from animals CE01 through CE30. We thank the MHC typing core at the Wisconsin Primate Research Center for typing the Indonesian cohort for Mamu-B*03. We acknowledge Natasja de Groot and the IMGT for assigning uniform allele nomenclature. Finally, we appreciate many members of the O’Connor lab for helpful discussions.
- Capuano SVr, Croix DA, Pawar S, Zinovik A, Myers A, Lin PL, Bissel S, Fuhrman C, Klein E, Flynn JL (2003) Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect Immun 71:5831–5844PubMedCrossRefGoogle Scholar
- Conlee KM, Hoffeld EH, Stephens ML (2004) A demographic analysis of primate research in the United States. ATLA Supplement 1:315–322Google Scholar
- Evans DT, O’ Connor DH, Jing P, Dzuris JL, Sidney J, da Silva J, Allen TM, Horton H, Venham JE, Rudersdorf RA, Vogel T, Pauza CD, Bontrop RE, DeMars R, Sette A, Hughes AL, Watkins DI (1999) Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nat Med 5:1270–1276PubMedCrossRefGoogle Scholar
- Evans DT, Jing P, Allen TM, O’ Connor DH, Horton H, Venham JE, Piekarczyk M, Dzuris J, Dykhuzen M, Mitchen J, Rudersdorf RA, Pauza CD, Sette A, Bontrop RE, DeMars R, Watkins DI (2000) Definition of five new simian immunodeficiency virus cytotoxic T-lymphocyte epitopes and their restricting major histocompatibility complex class I molecules: evidence for an influence on disease progression. J Virol 74:7400–7410PubMedCrossRefGoogle Scholar
- Florese R, Wiseman RW, Venzon D, Karl JA, Demberg T, Larsen K, Flanary L, Kalyanaraman VS, Pal R, Titti F, Patterson LJ, Heath MJ, O’Connor D, Cafaro A, Ensoli B, Robert-Guroff M (2008) Comparative study of Tat vaccine regimens in Mauritian cynomolgus and Indian rhesus macaques: Influence of Mauritian MHC haplotypes on susceptibility/resistance to SHIV89.6P infection. Vaccine (in press)Google Scholar
- Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, Mardis ER, Remington KA, Strausberg RL, Venter JC, Wilson RK, Batzer MA, Bustamante CD, Eichler EE, Hahn MW, Hardison RC, Makova KD, Miller W, Milosavljevic A, Palermo RE, Siepel A, Sikela JM, Attaway T, Bell S, Bernard KE, Buhay CJ, Chandrabose MN, Dao M, Davis C, Delehaunty KD, Ding Y, Dinh HH, Dugan-Rocha S, Fulton LA, Gabisi RA, Garner TT, Godfrey J, Hawes AC, Hernandez J, Hines S, Holder M, Hume J, Jhangiani SN, Joshi V, Khan ZM, Kirkness EF, Cree A, Fowler RG, Lee S, Lewis LR, Li Z, Liu YS, Moore SM, Muzny D, Nazareth LV, Ngo DN, Okwuonu GO, Pai G, Parker D, Paul HA, Pfannkoch C, Pohl CS, Rogers YH, Ruiz SJ, Sabo A, Santibanez J, Schneider BW, Smith SM, Sodergren E, Svatek AF, Utterback TR, Vattathil S, Warren W, White CS, Chinwalla AT, Feng Y, Halpern AL, Hillier LW, Huang X, Minx P, Nelson JO, Pepin KH, Qin X, Sutton GG, Venter E, Walenz BP, Wallis JW, Worley KC, Yang SP, Jones SM, Marra MA, Rocchi M, Schein JE, Baertsch R, Clarke L, Csuros M, Glasscock J, Harris RA, Havlak P, Jackson AR, Jiang H, Liu Y, Messina DN, Shen Y, Song HX, Wylie T, Zhang L, Birney E, Han K, Konkel MK, Lee J, Smit AF, Ullmer B, Wang H, Xing J, Burhans R, Cheng Z, Karro JE, Ma J, Raney B, She X, Cox MJ, Demuth JP, Dumas LJ, Han SG, Hopkins J, Karimpour-Fard A, Kim YH, Pollack JR, Vinar T, Addo-Quaye C, Degenhardt J, Denby A, Hubisz MJ, Indap A, Kosiol C, Lahn BT, Lawson HA, Marklein A, Nielsen R, Vallender EJ, Clark AG, Ferguson B, Hernandez RD, Hirani K, Kehrer-Sawatzki H, Kolb J, Patil S, Pu LL, Ren Y, Smith DG, Wheeler DA, Schenck I, Ball EV, Chen R, Cooper DN, Giardine B, Hsu F, Kent WJ, Lesk A, Nelson DL, O, brien WE, Prufer K, Stenson PD, Wallace JC, Ke H, Liu XM, Wang P, Xiang AP, Yang F, Barber GP, Haussler D, Karolchik D, Kern AD, Kuhn RM, Smith KE, Zwieg AS (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234PubMedCrossRefGoogle Scholar
- Lawler JV, Endy TP, Hensley LE, Garrison A, Fritz EA, Lesar M, Baric RS, Kulesh DA, Norwood DA, Wasieloski LP, Ulrich MP, Slezak TR, Vitalis E, Huggins JW, Jahrling PB, Paragas J (2006) Cynomolgus macaque as an animal model for severe acute respiratory syndrome. PLoS Med 3:677–686CrossRefGoogle Scholar
- Liu C, Noorchashm H, Sutter JA, Naji M, Prak EL, Boyer J, Green T, Rickels MR, Tomaszewski JE, Koeberlein B, Wang Z, Paessler ME, Velidedeoglu E, Rostami SY, Yu M, Barker CF, Naji A (2007) B lymphocyte-directed immunotherapy promotes long-term islet allograft survival in nonhuman primates. Nat Med 13:1295–1298PubMedCrossRefGoogle 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 2:1152CrossRefGoogle Scholar
- Loudon JE, Howells ME, Guentes A (2006) The importance of integrative anthropology: a preliminary investigation employing primatological and cultural anthropological data collection methods in assessing human-monkey co-existence in Bali, Indonesia. Ecological and Environmental Anthropology 2:2–13Google Scholar
- Negri DR, Borghi M, Baroncelli S, Macchia I, Buffa V, Sernicola L, Leone P, Titti F, Cara A (2006) Identification of a cytotoxic T-lymphocyte (CTL) epitope recognized by Gag-specific CTLs in cynomolgus monkeys infected with simian/human immunodeficiency virus. J Gen Virol 87:3385–3392PubMedCrossRefGoogle Scholar
- Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In S Krawetz & S Misener (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology (365–386). Totowa, NJ: Humana PressGoogle Scholar
- Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, Racz P, Tenner-Racz K, Dalesandro M, Scallon BJ, Ghrayeb J, Forman MA, Montefiori DC, Rieber EP, Letvin NL, Reimann KA (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857–860PubMedCrossRefGoogle Scholar