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Science 15 August 1997:
Vol. 277. no. 5328, pp. 959 - 965
DOI: 10.1126/science.277.5328.959
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Reports

Contrasting Genetic Influence of CCR2 and CCR5 Variants on HIV-1 Infection and Disease Progression

Michael W. Smith, * Michael Dean, * Mary Carrington, * Cheryl Winkler, Gavin A. Huttley, Deborah A. Lomb, James J. Goedert, Thomas R. O'Brien, Lisa P. Jacobson, Richard Kaslow, Susan Buchbinder, Eric Vittinghoff, David Vlahov, Keith Hoots, Margaret W. Hilgartner, Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC), ALIVE Study, Stephen J. O'Brien dagger

The critical role of chemokine receptors (CCR5 and CXCR4) in human immunodeficiency virus-type 1 (HIV-1) infection and pathogenesis prompted a search for polymorphisms in other chemokine receptor genes that mediate HIV-1 disease progression. A mutation (CCR2-64I) within the first transmembrane region of the CCR2 chemokine and HIV-1 receptor gene is described that occurred at an allele frequency of 10 to 15 percent among Caucasians and African Americans. Genetic association analysis of five acquired immunodeficiency syndrome (AIDS) cohorts (3003 patients) revealed that although CCR2-64I exerts no influence on the incidence of HIV-1 infection, HIV-1-infected individuals carrying the CCR2-64I allele progressed to AIDS 2 to 4 years later than individuals homozygous for the common allele. Because CCR2-64I occurs invariably on a CCR5-+-bearing chromosomal haplotype, the independent effects of CCR5-Delta 32 (which also delays AIDS onset) and CCR2-64I were determined. An estimated 38 to 45 percent of AIDS patients whose disease progresses rapidly (less than 3 years until onset of AIDS symptoms after HIV-1 exposure) can be attributed to their CCR2-+/+ or CCR5-+/+ genotype, whereas the survival of 28 to 29 percent of long-term survivors, who avoid AIDS for 16 years or more, can be explained by a mutant genotype for CCR2 or CCR5.

M. W. Smith, M. Carrington, C. Winkler, D. A. Lomb, Science Applications International Corp. Frederick, National Cancer Institute, Frederick, MD 21702-1201, USA.
M. Dean, G. A. Huttley, S. J. O'Brien, Laboratory of Genomic Diversity, National Cancer Institute, Frederick, MD 21702-1201, USA.
J. J. Goedert and T. R. O'Brien, Viral Epidemiology Branch, National Cancer Institute-Executive Plaza North, 6130 Executive Boulevard, Bethesda, MD 20892, USA.
L. P. Jacobson, Department of Epidemiology, The Johns Hopkins University School of Hygiene and Public Health, Room E-7008, 615 North Wolfe Street, Baltimore, MD 21205-1999, USA.
R. Kaslow, Department of Epidemiology, University of Alabama at Birmingham, 720 South 20th Street, Tidwell Hall 212C, Birmingham, AL 35294, USA.
S. Buchbinder and E. Vittinghoff, AIDS Office, Department of Public Health, 25 Van Ness Avenue, Suite 500, San Francisco, CA 94102-6033, USA.
D. Vlahov, Department of Epidemiology, The Johns Hopkins School of Hygiene and Public Health, Room E-6008, 615 North Wolfe Street, Baltimore, MD 21205, USA.
K. Hoots, Departments of Pediatrics and Internal Medicine, University of Texas Medical School at Houston, Houston, TX 77030, USA.
M. W. Hilgartner, Division of Pediatric Hematology and Oncology, New York Hospital-Cornell Medical Center, 525 East 68th Street, Payson 695, New York, NY 10021, USA.
*   These authors contributed equally to this study.

dagger    To whom correspondence should be addressed. E-mail: obrien{at}ncifcrf.gov

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Polymorphism in the Interleukin-4 Promoter Affects Acquisition of Human Immunodeficiency Virus Type 1 Syncytium-Inducing Phenotype.
E. E. Nakayama, Y. Hoshino, X. Xin, H. Liu, M. Goto, N. Watanabe, H. Taguchi, A. Hitani, A. Kawana-Tachikawa, M. Fukushima, et al. (2000)
J. Virol. 74, 5452-5459
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Unusual Polymorphisms in Human Immunodeficiency Virus Type 1 Associated with Nonprogressive Infection.
L. Alexander, E. Weiskopf, T. C. Greenough, N. C. Gaddis, M. R. Auerbach, M. H. Malim, S. J. O'Brien, B. D. Walker, J. L. Sullivan, and R. C. Desrosiers (2000)
J. Virol. 74, 4361-4376
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Variant genotypes of Fcgamma RIIIA influence the development of Kaposi's sarcoma in HIV-infected men.
T. L. nbecher, C. B. Foster, S. Zhu, D. Venzon, S. M. Steinberg, K. Wyvill, J. A. Metcalf, S. S. Cohen, J. Kovacs, R. Yarchoan, et al. (2000)
Blood 95, 2386-2390
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International Union of Pharmacology. XXII. Nomenclature for Chemokine Receptors.
P. M. Murphy, M. Baggiolini, I. F. Charo, C. A. Hebert, R. Horuk, K. Matsushima, L. H. Miller, J. J. Oppenheim, and C. A. Power (2000)
Pharmacol. Rev. 52, 145-176
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Cloning of a Novel Chemoattractant Receptor Activated by Leukotriene B4 and Used by Human Immunodeficiency Virus Type 1 to Infect CD4-positive Immune Cells . A Therapeutic Connection to Asthma?.
C. OWMAN, A. SABIRSH, A. GARZINO-DEMO, and F. COCCHI (2000)
Am. J. Respir. Crit. Care Med. 161, S56-61
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5' Nuclease Assays for the Loci CCR5-+/{Delta}32, CCR2-V64I, and SDF1-G801A Related to Pathogenesis of AIDS.
C.-C. Yuan, R. J. Peterson, C.-D. Wang, F. Goodsaid, and D. J. Waters (2000)
Clin. Chem. 46, 24-30
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Multiple Charged and Aromatic Residues in CCR5 Amino-terminal Domain Are Involved in High Affinity Binding of Both Chemokines and HIV-1 Env Protein.
C. Blanpain, B. J. Doranz, J. Vakili, J. Rucker, C. Govaerts, S. S. W. Baik, O. Lorthioir, I. Migeotte, F. Libert, F. Baleux, et al. (1999)
J. Biol. Chem. 274, 34719-34727
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A Polymorphism in the Regulatory Region of the CC-Chemokine Receptor 5 Gene Influences Perinatal Transmission of Human Immunodeficiency Virus Type 1 to African-American Infants.
L. G. Kostrikis, A. U. Neumann, B. Thomson, B. T. Korber, P. McHardy, R. Karanicolas, L. Deutsch, Y. Huang, J. F. Lew, K. McIntosh, et al. (1999)
J. Virol. 73, 10264-10271
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Genotyping of the CCR5 Chemokine Receptor by Isothermal NASBA Amplification and Differential Probe Hybridization.
J. W. Romano, S. Tetali, E. M. Lee, R. N. Shurtliff, X. P. Wang, S. Pahwa, M. H. Kaplan, and C. C. Ginocchio (1999)
Clin. Vaccine Immunol. 6, 959-965
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Race-specific HIV-1 disease-modifying effects associated with CCR5 haplotypes.
E. Gonzalez, M. Bamshad, N. Sato, S. Mummidi, R. Dhanda, G. Catano, S. Cabrera, M. McBride, X.-H. Cao, G. Merrill, et al. (1999)
PNAS 96, 12004-12009
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Search for the Mechanism of Genetic Variation in the pro Gene of Human Immunodeficiency Virus.
I. M. Rouzine and J. M. Coffin (1999)
J. Virol. 73, 8167-8178
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Characterization of V3 Sequence Heterogeneity in Subtype C Human Immunodeficiency Virus Type 1 Isolates from Malawi: Underrepresentation of X4 Variants.
L.-H. Ping, J. A. E. Nelson, I. F. Hoffman, J. Schock, S. L. Lamers, M. Goodman, P. Vernazza, P. Kazembe, M. Maida, D. Zimba, et al. (1999)
J. Virol. 73, 6271-6281
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Reduced Risk of AIDS Lymphoma in Individuals Heterozygous for the CCR5-{{Delta}}32 Mutation.
M. Dean, L. P. Jacobson, G. McFarlane, J. B. Margolick, F. J. Jenkins, O. M. Z. Howard, H.-F. Dong, J. J. Goedert, S. Buchbinder, E. Gomperts, et al. (1999)
Cancer Res. 59, 3561-3564
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Naturally Occurring CCR5 Extracellular and Transmembrane Domain Variants Affect HIV-1 Co-receptor and Ligand Binding Function.
O. M. Z. Howard, A.-K. Shirakawa, J. A. Turpin, A. Maynard, G. J. Tobin, M. Carrington, J. J. Oppenheim, and M. Dean (1999)
J. Biol. Chem. 274, 16228-16234
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Simian Immunodeficiency Virus Disease Course Is Predicted by the Extent of Virus Replication during Primary Infection.
S. I. Staprans, P. J. Dailey, A. Rosenthal, C. Horton, R. M. Grant, N. Lerche, and M. B. Feinberg (1999)
J. Virol. 73, 4829-4839
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Definition of the Stage of Host Cell Genetic Restriction of Replication of Human Immunodeficiency Virus Type 1 in Monocytes and Monocyte-Derived Macrophages by Using Twins.
H. M. Naif, S. Li, M. Alali, J. Chang, C. Mayne, J. Sullivan, and A. L. Cunningham (1999)
J. Virol. 73, 4866-4881
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The Role of the C-C Chemokine Receptor 2 Gene Polymorphism V64I (CCR2-64I) in Sarcoidosis in a Japanese Population.
N. HIZAWA, E. YAMAGUCHI, K. FURUYA, E. JINUSHI, A. ITO, and Y. KAWAKAMI (1999)
Am. J. Respir. Crit. Care Med. 159, 2021-2023
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New Class I and II HLA Alleles Strongly Associated with Opposite Patterns of Progression to AIDS.
H. Hendel, S. Caillat-Zucman, H. Lebuanec, M. Carrington, S. O'Brien, J.-M. Andrieu, F. Schachter, D. Zagury, J. Rappaport, C. Winkler, et al. (1999)
J. Immunol. 162, 6942-6946
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Polymorphism in chemokine promoter affects HIV-1 disease progression.
H. Liu, D. Chao, E. E. Nakayama, H. Taguchi, M. Goto, X. Xin, J.-k. Takamatsu, H. Saito, Y. Ishikawa, T. Akaza, et al. (1999)
PNAS 96, 4581-4585
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Chemokine and Chemokine Receptor Gene Variants and Risk of Non-Hodgkin's Lymphoma in Human Immunodeficiency Virus-1-Infected Individuals.
C. S. Rabkin, Q.-e. Yang, J. J. Goedert, G. Nguyen, H. Mitsuya, and S. Sei (1999)
Blood 93, 1838-1842
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HLA and HIV-1: Heterozygote Advantage and B*35-Cw*04 Disadvantage.
M. Carrington, G. W. Nelson, M. P. Martin, T. Kissner, D. Vlahov, J. J. Goedert, R. Kaslow, S. Buchbinder, K. Hoots, and S. J. O'Brien (1999)
Science 283, 1748-1752
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CCR2-64I Polymorphism Is Not Associated with Altered CCR5 Expression or Coreceptor Function.
R. Mariani, S. Wong, L. C. F. Mulder, D. A. Wilkinson, A. L. Reinhart, G. LaRosa, R. Nibbs, T. R. O'Brien, N. L. Michael, R. I. Connor, et al. (1999)
J. Virol. 73, 2450-2459
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Conserved CTL Epitopes Shared Between HIV-Infected Human Long-Term Survivors and Chimpanzees.
S. S. Balla-Jhagjhoorsingh, G. Koopman, P. Mooij, T. G. M. Haaksma, V. J. P. Teeuwsen, R. E. Bontrop, and J. L. Heeney (1999)
J. Immunol. 162, 2308-2314
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Coreceptor Specificity of Temporal Variants of Simian Immunodeficiency Virus Mne.
J. T. Kimata, J. J. Gosink, V. N. KewalRamani, L. M. Rudensey, D. R. Littman, and J. Overbaugh (1999)
J. Virol. 73, 1655-1660
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Combined Genotypes of CCR5, CCR2, SDF1, and HLA Genes Can Predict the Long-Term Nonprogressor Status in Human Immunodeficiency Virus-1-Infected Individuals.
M. Magierowska, I. Theodorou, P. Debre, F. Sanson, B. Autran, Y. Riviere, D. Charron, F. ALT, I. S. Groups, and D. Costagliola (1999)
Blood 93, 936-941
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Genetic Acceleration of AIDS Progression by a Promoter Variant of CCR5.
M. P. Martin, M. Dean, M. W. Smith, C. Winkler, B. Gerrard, N. L. Michael, B. Lee, R. W. Doms, J. Margolick, S. Buchbinder, et al. (1998)
Science 282, 1907-1911
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An HIV-Resistant Allele Is Exceptionally Frequent in New Guinean Highlanders.
B. Su, R. Chakraborty, L. Jin, J. Xiao, and D. Lu (1998)
JAMA 280, 1830
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Differential Tropism and Replication Kinetics of Human Immunodeficiency Virus Type 1 Isolates in Thymocytes: Coreceptor Expression Allows Viral Entry, but Productive Infection of Distinct Subsets Is Determined at the Postentry Level.
L. Pedroza-Martins, K. B. Gurney, B. E. Torbett, and C. H. Uittenbogaart (1998)
J. Virol. 72, 9441-9452
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Potential Contributions of Viral Envelope and Host Genetic Factors in a Human Immunodeficiency Virus Type 1-Infected Long-Term Survivor.
K. Grovit-Ferbas, J. Ferbas, V. Gudeman, S. Sadeghi, M. B. Goetz, J. V. Giorgi, I. S. Y. Chen, and W. A. O'Brien (1998)
J. Virol. 72, 8650-8658
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HIV-1 Tat protein mimicry of chemokines.
A. Albini, S. Ferrini, R. Benelli, S. Sforzini, D. Giunciuglio, M. G. Aluigi, A. E. I. Proudfoot, S. Alouani, T. N. C. Wells, G. Mariani, et al. (1998)
PNAS 95, 13153-13158
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Patterns of HIV-1 evolution in individuals with differing rates of CD4 T cell decline.
R. B. Markham, W.-C. Wang, A. E. Weisstein, Z. Wang, A. Munoz, A. Templeton, J. Margolick, D. Vlahov, T. Quinn, H. Farzadegan, et al. (1998)
PNAS 95, 12568-12573
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