Abstract
Although major histocompatibility complex (MHC) class I molecules are, as a rule, highly polymorphic in mammalian species, those of the New World primate Saguinus oedipus (cotton-top tamarin) exhibit limited polymorphism. We have cloned and sequenced twelve MHC class I cDNAs from this species. Since cloned cotton-top tamarin cell lines express three to six MHC class I molecules, this species must have at least three functional MHC class I loci. There was, however, no evidence of locus-specific substitutions in the tamarin cDNAs. Unlike all other species studied, tamarin MHC class I cDNAs displayed limited nucleotide sequence variation. The sequence similarity between the two most divergent tamarin cDNAs was 95%. To ensure that the polymerase chain reaction (PCR) primers employed in these studies had amplified all of the tamarins' expressed MHC class I genes, we used another set of primers to amplify only exons 2 and 3 from RNA and DNA. PCR of genomic DNA resulted in the amplification of six distinct clones, of which only three were well expressed. Two of these nonexpressed genes were pseudogenes and the other was a nonclassical gene. Southern blot analysis demonstrated that the tamarin has 8–11 MHC class I genes, suggesting we had indeed cloned the majority of these genes. Cotton-top tamarins are, therefore, unique among mammalian species studied to date in that they express MHC class I molecules with limited nucleotide sequence variation.
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Benirschke, K., Anderson, J. M., and Brownshill, L. C.: Marrow chimerism in marmosets. Science 138: 513–515, 1962
Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennet, W. S., Strominger, J. L., and Wiley, D. C.: The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329: 512–518, 1987
Brodsky, F. M., Parham, P., Barnstable, C. J., Crumpton, M. J., and Bodmer, W. F.: Monoclonal antibodies for analysis of the HLA system. Immunol Rev 47: 3–61, 1979
Cann, H. M., Ascanio, L., Paul, P., Marcadet, A., Dausset, J., and Cohen, D.: 80: 1665–1668, 1983 Polymorphic restriction endonuclease fragment segregates with the gene for HLA-B8. Proc Natl Acad Sci USA 1665–1668:
Darden, A. G. and Streilein, J. W.: Syrian hamsters express two monomorphic class I major histocompatibility complex molecules. Immunogenetics 20: 603–622, 1984
Deinhardt, F.: Neoplasms induced by Rous Sarcoma virus in New World monkeys. Nature 10: 443, 1966
Dover, G. A.: Molecular drive: a cohesive mode of species evolution. Nature 299: 117, 1982
Holmes, N. and Parham, P.: Exon shuffling in vivo can generate novel HLA class I molecules. EMBO J 4: 2849, 1985
Hughes, A. L. and Nei, M.: Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170, 1988
Hughes, A. L. and Nei, M.: Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6: 559–579, 1989
Klein, J.: Natural History of the Major Histocompatibility Complex, Wiley, New York, 1986
Klein, J. and Figueroa, F.: Evolution of the major histocompatibility complex. CRC Crit Rev Immunol 6: 295–384, 1987
Lawlor, D. A., Ward, F. E., Ennis, P. D., Jackson, A. P., and Parham, P.: HLA-A and B polymorphism predate the divergence of humans and chimpanzees. Nature 335: 268–271, 1988
Li, W. H. and Tanimura, M.: The molecular clock runs more slowly in man than in apes and monkeys. Nature 326: 93–96, 1987
Mayer, W. E., Jonker, M., Klein, D., Ivanyi, P., van Seventer, G., and Klein, J.: Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO J 7: 2765–2774, 1988
Miller, G., Shope, T., Coope, D., Waters, L., Pagano, J., Bornkamm, G. W., and Henle, W.: Lymphoma in cotton-top marmosets after inoculation with Epstein-Barr virus: tumor incidence, histologic spectrum antibody responses, demonstration of viral DNA, and characterization of viruses. J Exp Med 145: 948–967, 1977
Nei, M. and Gojobori, T.: Simple methods for estimating the numbers of synonymous and nonsynonymous substitutions. Mol Biol Evol 3: 418–426, 1986
Newman, P. J., Gorski, J., White, G. C., Gidwitz, S., Cretney, C. J., and Aster, R. H.: Enzymatic amplification of platelet-specific messenger RNA using the ploymerase chain reaction. J Clin Invest 82: 739–743, 1988
Nikolić-Zugić, J. and Bevan, M. J.: Role of self self-peptides in positively selecting the T-cell repertoire. Nature 344: 61–65, 1990
O'Brien, S. J., Wildt, D. E., Goldman, D., Merril, C. R., and Bush, M.: The cheetah is depauperate in genetic variation. Science 221: 459–462, 1983
O'Brien, S. J., Roelke, M. E., Marker, L., Newman, A., Windler, C. A., Meltzer, D., Colly, L., Evermann, J. F., Bush, M., and Wildt, D. E.: Genetric basis for species vulnerability in the cheetah. Science 227: 1428–1434, 1985
Ohlen, C., Kling, G., Hoglund, P., Hansson, M., Scangos, G., Bieberich, C., Jay, G., and Karre, K.: Prevention of allogeneic bone marrow graft rejection by H-2 transgene in donor mice. Science 246: 666–668, 1989
Parham, P., Lomen, C. E., Lawlor, D. A., Ways, J. P., Holmes, N., Coppin, H. L., Salter, R. D., Wan, A. M., and Ennis, P. D.: Nature of polymorphism in HLA-A, -B, and -C molecules. Proc Natl Acad Sci USA 85: 4005–4009, 1988
Parham, P., Lawlor, D. A., Lomen, C. E., and Ennis, P. D.: Diversity and diversification of HLA-B, B,C alleles. J Immunol 142: 3937–3950, 1989
Picus, J., Aldrich, W. R., and Letvin, N. L.: A naturally occurring bone-marrow-chimeric primate. Transplantation 39: 297–302, 1985
Rada, C., Lorenzi, R., Powis, S. J., van den Bogaerde, J., Parham, P., and Howard, J. C.: Concerted evolution of class I genes in the major histocompatibility complex of murine rodents. Proc Natl Acad Sci USA 87: 2167–2171, 1990
Sanger, F., Nicklen, S., and Coulson, A. R.: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467, 1977
Sood, A. K., Pereira, D., and Weissman, S. M.: Isolation and partial nucleotide sequence of a cDNA clone for human histocompatibility antigen HLA-B by use of an oligodeoxynucleotide primer. Proc Natl Acad Sci USA 78: 616–620, 1981
Townsend, A. R. M., Gotch, F. M., and Davey, J.: Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell 42: 457–467, 1985
Watkins, D. I., Hodi, F. S., and Letvin, N. L.: A primate species with limited major histocompatibility complex class I polymorphism. Proc Natl Acad Sci USA 85: 7714–7718, 1988a
Watkins, D. I., Kannagi, M., Stone, M. E., and Letvin, N. L.: Major histocompatibility complex class I molecules of nonhuman primates. Eur J Immunol 18: 1425–1432, 1988b
Watkins, D. I., Shadduck, J. A., Hodi, F. S., Stone, M. E., and Letvin, N. L.: Use of cDNA probes specific for the human MHC class II beta loci for tissue-typing nonhuman primates at their class II beta loci. Transplantation 47: 172–173, 1989
Watkins, D. I., Letvin, N. L., Hughes, A. L., and Tedder, T. F.: Molecular cloning of cDNAs that encode MHC class I molecules from a New World primate (Saguinus oedipus): natural selection acts at positions that may affect peptide presentation to T cells. J Immunol 144: 1136–1143, 1990a
Watkins, D. I., Chen, Z. W., Hughes, A. L., Evans, M. G., Tedder, T. F., and Letvin, N. L.: Evolution of the MHC class I genes of a New World primate from ancestral homologues of human nonclassical genes. Nature 346: 60–63, 1990b
Watkins, D. I., Chen, Z. W., Hughes, A. L., Lagos, A., Lewis, A. M., Shadduck, J. A., and Letvin, N. L.: Syrian hamsters express diverse MHC class I gene products. J Immunol, 145: 3483–3490, 1990c
Weiss, E., Golden, L., Zahut, R., Mellor, A., Fahrner, K., Kvist, S., and Flavell, R. A.: The DNA sequence of the H-2Kb gene: evidence for gene conversion as a mechanism for the generation of polymorphism in histocompatibility antigens. EMBO J 2: 453–462, 1983
Wolfe, L. G. and Deinhardt, F.: Overview of viral oncology studies in Saquinus and Callithrix species. Primate Med 10: 96–118, 1978
Zijlstra, M., Bix, M., Simister, N. E., Loring, J. M., Raulet, D. H., and Jaenisch, R.: Beta 2-microglobulin deficient mice lack CD4–8+ cytolytic T cells. Nature 344: 742–746, 1990
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The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers M38403-15.
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Watkins, D.I., Garber, T.L., Chen, Z.W. et al. Unusually limited nucleotide sequence variation of the expressed major histocompatibility complex class I genes of a New World primate species (Saguinus oedipus). Immunogenetics 33, 79–89 (1991). https://doi.org/10.1007/BF00210819
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DOI: https://doi.org/10.1007/BF00210819