Immunogenetics 33: 79-89, 1991
Original articles
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genetics
© Springer-Verlag 1991
Unusually limited nucleotide sequence variation of the expre
major histocompatibility complex class I genes of a New Wo
primate species (Saguinus oedipus)
David I. Watkins 1, Theodore L. Garber 2, Zheng W. Chen 1, Gary Toukatly t, Austin L. Hughes 3, and N
L. Letvin x
1 Harvard Medical School, New England Regional Primate Research Center, Southborough, MA 01772, USA
2 Texas A&M University, College of Veterinary Medicine, College Station, TX 77843, USA
3 Center for Demographic and Population Genetics, The University of Texas Health Science Center at Houston, Houston, TX 77225, USA
Received September 17, 1990
Abstract. Although major histocompatibility complex
(MHC) class I molecules are, as a rule, highly polymor-
phic in mammalian species, those of the New World
primate Saguinus oedipus (cotton-top tamarin) exhibit
limited polymorphism. We have cloned and sequenced
twelve MHCclass I cDNAs from thisspecies. 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 displayedlimited 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.
* The nucleotide sequence data reported in this paper have been submit-
ted to the GenBank nucleotide sequence database and have been assign-
ed the accession numbers M38403-15.
Address correspondence and offprint requests to: D.I. Watkins.
Introduction
The products of the major histocompatibility complex
(MHC) class I loci are among the most polymorphic
molecules in the animal kingdom (Klein 1986). The
crystal structure of a human MHC class I molecule
suggests that pepfides bind to a groove in the top of the
molecule (Bjorkman et al. 1987). Bound peptide frag-
ments are then presented to cytotoxic T lymphocytes
(Townsend et al. 1985). Overdominant selective pres-
sures at the peptide-binding groove are largely responsible
for the extreme diversity of these molecules (Hughes and
Nei 1988).
Only 11 different MHC class I molecules have been
defined in the cotton-top tamarin (Watkins et al. 1988a
and data not shown). One of these MHC class I molecules
is expressed by the lymphocytes of every tamarin ex-
amined to date. To understand the molecular basis of this
limited MHC class I polymorphism, twelve cDNAs en-
coding tamarin MHC class I molecules and two
pseudogenes have been sequenced. We have previously
reported that these cDNAs are related to the human
nonclassical genes
HLA-G and
HLA-F (Watkinset al.
1990b). In the present studies we have analyzed the extent
of nucleotide sequence variation of the tamarins' MHC
class I genes.
Materials and methods
Animals. Heparinized blood was obtained by venipuncture from healthy
cotton-top tamarins originally housed at the New England Regional
Primate Research Center, Southborough, Massachusetts (#779-76), the
University of Bristol, Bristol, England (#46-85), and at a colony in