Skip to main content

Advertisement

SpringerLink
Log in

Characterization of 47 MHC class I sequences in Filipino cynomolgus macaques

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

Cynomolgus macaques (Macaca fascicularis) provide increasingly common models for infectious disease research. Several geographically distinct populations of these macaques from Southeast Asia and the Indian Ocean island of Mauritius are available for pathogenesis studies. Though host genetics may profoundly impact results of such studies, similarities and differences between populations are often overlooked. In this study we identified 47 full-length MHC class I nucleotide sequences in 16 cynomolgus macaques of Filipino origin. The majority of MHC class I sequences characterized (39 of 47) were unique to this regional population. However, we discovered eight sequences with perfect identity and six sequences with close similarity to previously defined MHC class I sequences from other macaque populations. We identified two ancestral MHC haplotypes that appear to be shared between Filipino and Mauritian cynomolgus macaques, notably a Mafa-B haplotype that has previously been shown to protect Mauritian cynomolgus macaques against challenge with a simian/human immunodeficiency virus, SHIV89.6P. We also identified a Filipino cynomolgus macaque MHC class I sequence for which the predicted protein sequence differs from Mamu-B*17 by a single amino acid. This is important because Mamu-B*17 is strongly associated with protection against simian immunodeficiency virus (SIV) challenge in Indian rhesus macaques. These findings have implications for the evolutionary history of Filipino cynomolgus macaques as well as for the use of this model in SIV/SHIV research protocols.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abegg C, Thierry B (2002) Macaque evolution and dispersal in insular south-east Asia. Biol J Linn Soc Lond 75:555–576 doi:10.1046/j.1095-8312.2002.00045.x

    Article  Google Scholar 

  • Blancher A, Tisseyre P, Dutaur M, Apoil PA, Maurer C, Quesniaux V, Raulf F, Bigaud M, Abbal M (2006) Study of cynomolgus monkey (Macaca fascicularis) MhcDRB (Mafa-DRB) polymorphism in two populations. Immunogenetics 58:269–282 doi:10.1007/s00251-006-0102-9

    Article  PubMed  CAS  Google Scholar 

  • Blancher A, Bonhomme M, Crouau-Roy B, Terao K, Kitano T, Saitou N (2008) Mitochondrial DNA sequence phylogeny of 4 populations of the widely distributed cynomolgus macaque (Macaca fascicularis fascicularis). J Hered 99:254–264 doi:10.1093/jhered/esn003

    Article  PubMed  CAS  Google Scholar 

  • Bonhomme M, Blancher A, Jalil MF, Crouau-Roy B (2007) Factors shaping genetic variation in the MHC of natural non-human primate populations. Tissue Antigens 70:398–411 doi:10.1111/j.1399-0039.2007.00925.x

    Article  PubMed  CAS  Google Scholar 

  • Bonhomme M, Blancher A, Cuartero S, Chikhi L, Crouau-Roy B (2008) Origin and number of founders in an introduced insular primate: estimation from nuclear genetic data. Mol Ecol 17:1009–1019 doi:10.1111/j.1365-294X.2007.03645.x

    Article  PubMed  CAS  Google Scholar 

  • Bontrop RE (2001) Non-human primates: essential partners in biomedical research. Immunol Rev 183:5–9 doi:10.1034/j.1600-065x.2001.1830101.x

    Article  PubMed  CAS  Google Scholar 

  • Bontrop RE, Watkins DI (2005) MHC polymorphism: AIDS susceptibility in non-human primates. Trends Immunol 26:227–233 doi:10.1016/j.it.2005.02.003

    Article  PubMed  CAS  Google Scholar 

  • Capuano SV, 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 71:5831–5844 doi:10.1128/IAI.71.10.5831-5844.2003

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution Int J Org Evolution 39:783–791 doi::10.2307/2408678

    Google Scholar 

  • Florese RH, Wiseman RW, Venzon D, Karl JA, Demberg T, Larsen K, Flanary L, Kalyanaraman VS, Pal R, Titti F, Patterson LJ, Heath MJ, O’Connor DH, 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 26:3312–3321 doi:10.1016/j.vaccine.2008.03.100

    Article  PubMed  CAS  Google Scholar 

  • Goulder PJ, Watkins DI (2008) Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat Rev Immunol 8:619–630 doi:10.1038/nri2357

    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 doi:10.1007/s00251-007-0267-x

    Article  PubMed  CAS  Google Scholar 

  • Kawamoto Y, Kawamoto S, Matsubayashi K, Nozawa K, Watanabe T, Stanley MA, Perwitasari-Farajallah D (2008) Genetic diversity of longtail macaques (Macaca fascicularis) on the island of Mauritius: an assessment of nuclear and mitochondrial DNA polymorphisms. J Med Primatol 37:45–54

    PubMed  CAS  Google Scholar 

  • Kondo M, Kawamoto Y, Nozawa K, Matsubayashi K, Watanabe T, Griffiths O, Stanley M (1993) Population genetics of crab-eating macaques (Macaca fascicularis) on the island of Mauritius. Am J Primatol 29:167–182 doi:10.1002/ajp.1350290303

    Article  Google Scholar 

  • Koraka P, Benton S, van Amerongen G, Stittelaar KJ, Osterhaus A (2007) Characterization of humoral and cellular immune responses in cynomolgus macaques upon primary and subsequent heterologous infections with dengue viruses. Microbes Infect 9:940–946 doi:10.1016/j.micinf.2007.03.012

    Article  PubMed  CAS  Google Scholar 

  • Krebs KC, Jin Z, Rudersdorf R, Hughes AL, O’Connor DH (2005) Unusually high frequency MHC class I alleles in Mauritian origin cynomolgus macaques. J Immunol 175:5230–5239

    PubMed  CAS  Google Scholar 

  • Lafont BA, Buckler-White A, Plishka R, Buckler C, Martin MA (2003) Characterization of pig-tailed macaque classical MHC class I genes: implications for MHC evolution and antigen presentation in macaques. J Immunol 171:875–885

    PubMed  CAS  Google Scholar 

  • Lawler SH, Sussman RW, Taylor LL (1995) Mitochondrial DNA of the Mauritian macaques (Macaca fascicularis): an example of the founder effect. Am J Phys Anthropol 96:133–141 doi:10.1002/ajpa.1330960203

    Article  PubMed  CAS  Google Scholar 

  • Menninger K, Wieczorek G, Riesen S, Kunkler A, Audet M, Blancher A, Schuurman HJ, Quesniaux V, Bigaud M (2002) The origin of cynomolgus monkey affects the outcome of kidney allografts under neoral immunosuppression. Transplant Proc 34:2887–2888 doi:10.1016/S0041-1345(02)03547-9

    Article  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 doi:10.1073/pnas.0409084102

    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 doi:10.1007/s00251-007-0201-2

    Article  PubMed  CAS  Google Scholar 

  • Otting N, Heijmans C, van der Wiel M, de Groot N, 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 doi:10.1007/s00251-008-0311-5

    Article  PubMed  Google Scholar 

  • Pawar SN, Mattila JT, Sturgeon TJ, Lin PL, Narayan O, Montelaro RC, Flynn JL (2008) Comparison of the effects of pathogenic simian human immunodeficiency virus strains SHIV-89.6P and SHIV-KU2 in cynomolgus macaques. AIDS Res Hum Retroviruses 24:643–654 doi:10.1089/aid.2007.0238

    Article  PubMed  CAS  Google Scholar 

  • Pendley CJ, Becker EA, Karl JA, Blasky AJ, Wiseman RW, Hughes AL, O’Connor SL, O’Connor DH (2008) MHC class I characterization of Indonesian cynomolgus macaques. Immunogenetics 60:339–351 doi:10.1007/s00251-008-0292-4

    Article  PubMed  CAS  Google Scholar 

  • Robinson J, Waller MJ, Parham P, de Groot N, Bontrop R, Kennedy LJ, Stoehr P, Marsh SG (2003) IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic Acids Res 31:311–314 doi:10.1093/nar/gkg070

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sano K, Shiina T, Kohara S, Yanagiya K, Hosomichi K, Shimizu S, Anzai T, Watanabe A, Ogasawara K, Torii R, Kulski JK, Inoko H (2006) Novel cynomolgus macaque MHC-DPB1 polymorphisms in three South-East Asian populations. Tissue Antigens 67:297–306 doi:10.1111/j.1399-0039.2006.00577.x

    Article  PubMed  CAS  Google Scholar 

  • Smith DG, McDonough JW, George DA (2007) Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques. Am J Primatol 69:182–198 doi:10.1002/ajp.20337

    Article  PubMed  CAS  Google Scholar 

  • Southwick CH, Siddiqi MF (1994) Population status of nonhuman primates in Asia, with emphasis on rhesus macaques in India. Am J Primatol 34:51–59 doi:10.1002/ajp.1350340110

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599 doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 doi:10.1093/nar/22.22.4673

    Article  PubMed  CAS  Google Scholar 

  • Tosi AJ, Coke CS (2007) Comparative phylogenetics offer new insights into the biogeographic history of Macaca fascicularis and the origin of the Mauritian macaques. Mol Phylogenet Evol 42:498–504 doi:10.1016/j.ympev.2006.08.002

    Article  PubMed  CAS  Google Scholar 

  • Uda A, Tanabayashi K, Yamada YK, Akari H, Lee YJ, Mukai R, Terao K, Yamada A (2004) Detection of 14 alleles derived from the MHC class I A locus in cynomolgus monkeys. Immunogenetics 56:155–163 doi:10.1007/s00251-004-0683-0

    Article  PubMed  CAS  Google Scholar 

  • Uda A, Tanabayashi K, Fujita O, Hotta A, Terao K, Yamada A (2005) Identification of the MHC class I B locus in cynomolgus monkeys. Immunogenetics 57:189–197 doi:10.1007/s00251-005-0782-6

    Article  PubMed  CAS  Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167 doi:10.1046/j.1365-2699.2000.00489.x

    Article  Google Scholar 

  • Walsh GP, Tan EV, dela Cruz EC, Abalos RM, Villahermosa LG, Young LJ, Cellona RV, Nazareno JB, Horwitz MA (1996) The Philippine cynomolgus monkey (Macaca fascicularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med 2:430–436 doi:10.1038/nm0496-430

    Article  PubMed  CAS  Google Scholar 

  • Warfield KL, Swenson DL, Olinger GG, Kalina WV, Aman MJ, Bavari S (2007) Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. J Infect Dis 196:S430–S437 doi:10.1086/520583

    Article  PubMed  CAS  Google Scholar 

  • Wiseman RW, O’Connor DH (2007) Major histocompatibility complex-defined macaques in transplantation research. Transplant Rev 21:17–25 doi:10.1016/j.trre.2007.01.001

    Article  Google Scholar 

  • Wiseman RW, Wojcechowskyj JA, Greene JM, Blasky AJ, Gopon T, Soma T, Friedrich TC, O’Connor SL, O’Connor DH (2007) Simian immunodeficiency virus SIVmac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius. J Virol 81:349–361 doi:10.1128/JVI.01841-06

    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 doi:10.1128/JVI.80.10.5074-5077.2006

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Natasja de Groot, Nel Otting, and the IMGT Non-human Primate Nomenclature Committee for naming the Mafa-A and Mafa-B sequences. We thank Claire O’Leary for editorial assistance and other members of the O’Connor laboratory for helpful discussions. This work was supported by 1 R24 RR021745-01A1. 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. Partial support was provided by NIH grant GM43940 to A.L.H. This publication’s contents are solely the responsibility of the authors and do not necessarily represent the official views of NCRR or NIH.

Author information

Authors and Affiliations

  1. Wisconsin National Primate Research Center, University of Wisconsin—Madison, Madison, WI, 53706, USA

    Kevin J. Campbell, Ann M. Detmer, Julie A. Karl, Roger W. Wiseman, Alex J. Blasky, Benjamin N. Bimber & David H. O’Connor

  2. Department of Biological Sciences, University of South Carolina, Columbus, SC, 29208, USA

    Austin L. Hughes

  3. Department of Pathology and Laboratory Medicine, University of Wisconsin—Madison, Madison, WI, 53706, USA

    Shelby L. O’Connor & David H. O’Connor

  4. University of Wisconsin—Madison, 555 Science Drive, Madison, WI, 53711, USA

    David H. O’Connor

Authors
  1. Kevin J. Campbell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ann M. Detmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie A. Karl
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roger W. Wiseman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alex J. Blasky
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Austin L. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Benjamin N. Bimber
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shelby L. O’Connor
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. David H. O’Connor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David H. O’Connor.

Additional information

Kevin J. Campbell and Ann M. Detmer contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Campbell, K.J., Detmer, A.M., Karl, J.A. et al. Characterization of 47 MHC class I sequences in Filipino cynomolgus macaques. Immunogenetics 61, 177–187 (2009). https://doi.org/10.1007/s00251-008-0351-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-008-0351-x

Keywords

Search

Navigation