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Originally published In Press as doi:10.1074/jbc.M000169200 on March 9, 2000

J. Biol. Chem., Vol. 275, Issue 25, 18946-18961, June 23, 2000
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Evolution of Human and Non-human Primate CC Chemokine Receptor 5 Gene and mRNA
POTENTIAL ROLES FOR HAPLOTYPE AND mRNA DIVERSITY, DIFFERENTIAL HAPLOTYPE-SPECIFIC TRANSCRIPTIONAL ACTIVITY, AND ALTERED TRANSCRIPTION FACTOR BINDING TO POLYMORPHIC NUCLEOTIDES IN THE PATHOGENESIS OF HIV-1 AND SIMIAN IMMUNODEFICIENCY VIRUS*,

Srinivas MummidiDagger §, Mike Bamshad§, Seema S. AhujaDagger ||||||, Enrique GonzalezDagger , Pablo M. FeuilletDagger , Kazi BegumDagger , M. Cristina GalvisDagger , Vannessa KosteckiDagger , Anthony J. ValenteDagger , Krishna K. Murthy**, Luis HaroDagger Dagger , Matthew J. Dolan§§, Jonathan S. Allan**, and Sunil K. AhujaDagger ||¶¶

From the Dagger  Departments of Medicine, University of Texas Health Science Center at San Antonio and South Texas Veterans Health Care System, Audie L. Murphy Division, San Antonio, Texas 78229, the  Department of Pediatrics, Eccles Institute of Human Genetics, University of Utah, Salt Lake City, Utah 84112, the ** Department of Virology and Immunology, Southwest Foundation for Biomedical Research, San Antonio, Texas 78228, the Dagger Dagger  Department of Life Sciences, University of Texas, San Antonio, Texas 78249, and the §§ Infectious Diseases Service, Wilford Hall Medical Center, Lackland Air Force Base, San Antonio, Texas 78236

Polymorphisms in CC chemokine receptor 5 (CCR5), the major coreceptor of human immunodeficiency virus 1 (HIV-1) and simian immunodeficiency virus (SIV), have a major influence on HIV-1 transmission and disease progression. The effects of these polymorphisms may, in part, account for the differential pathogenesis of HIV-1 (immunosuppression) and SIV (natural resistance) in humans and non-human primates, respectively. Thus, understanding the genetic basis underlying species-specific responses to HIV-1 and SIV could reveal new anti-HIV-1 therapeutic strategies for humans. To this end, we compared CCR5 structure/evolution and regulation among humans, apes, Old World Monkeys, and New World Monkeys. The evolution of the CCR5 cis-regulatory region versus the open reading frame as well as among different domains of the open reading frame differed from one another. CCR5 cis-regulatory region sequence variation in humans was substantially higher than anticipated. Based on this variation, CCR5 haplotypes could be organized into seven evolutionarily distinct human haplogroups (HH) that we designated HHA, -B, -C, -D, -E, -F, and -G. HHA haplotypes were defined as ancestral to all other haplotypes by comparison to the CCR5 haplotypes of non-human primates. Different human and non-human primate CCR5 haplotypes were associated with differential transcriptional regulation, and various polymorphisms resulted in modified DNA-nuclear protein interactions, including altered binding of members of the NF-kappa B family of transcription factors. We identified novel CCR5 untranslated mRNA sequences that were conserved in human and non-human primates. In some primates, mutations at exon-intron boundaries caused loss of expression of selected CCR5 mRNA isoforms or production of novel mRNA isoforms. Collectively, these findings suggest that the response to HIV-1 and SIV infection in primates may have been driven, in part, by evolution of the elements controlling CCR5 transcription and translation.

* This work was supported in part by a Veterans Administration Merit award, a Veterans Administration Hispanic Research Initiative award (to S. K. A.), by National Institutes of Health Grants RO1-AI43279 and R21-AI46326 (to S. K. A.), RO1-AI41396 (to J. S. A.), and RO1-RR-08122-07 (to K. K. M.), by National Science Foundation Grants SBR-9514733, SBR-9700729, and SBR-9818215, and by National Institutes of Health Grant GM-52290 (to M. B.). This work was also supported by a Robert J. and Helen C. Kleberg Foundation grant (to S. S. A. and S. K. A.)The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains Figs. S1-S3.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) AF246899-AF246925 and AF252551-AF252598.

§ Both authors contributed equally to this work.

|| Supported by the Robert J. and Helen C. Kleberg Foundation.

¶¶ To whom correspondence should be addressed. E-mail: ahujas@uthscsa.edu.

|||| Supported by a Veterans Affairs Career Development Award.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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