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Science 27 September 1996:
Vol. 273. no. 5283, pp. 1856 - 1862
DOI: 10.1126/science.273.5283.1856
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Reports

Genetic Restriction of HIV-1 Infection and Progression to AIDS by a Deletion Allele of the CKR5 Structural Gene

Michael Dean, * Mary Carrington, * Cheryl Winkler, Gavin A. Huttley, Michael W. Smith, Rando Allikmets, James J. Goedert, Susan P. Buchbinder, Eric Vittinghoff, Edward Gomperts, Sharyne Donfield, David Vlahov, Richard Kaslow, Alfred Saah, Charles Rinaldo, Roger Detels, Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study, Stephen J. O'Brien dagger

The chemokine receptor 5 (CKR5) protein serves as a secondary receptor on CD4+ T lymphocytes for certain strains of human immunodeficiency virus-type 1 (HIV-1). The CKR5 structural gene was mapped to human chromosome 3p21, and a 32-base pair deletion allele (CKR5Delta 32) was identified that is present at a frequency of sim 0.10 in the Caucasian population of the United States. An examination of 1955 patients included among six well-characterized acquired immunodeficiency syndrome (AIDS) cohort studies revealed that 17 deletion homozygotes occurred exclusively among 612 exposed HIV-1 antibody-negative individuals (2.8 percent) and not at all in 1343 HIV-1-infected individuals. The frequency of CKR5 deletion heterozygotes was significantly elevated in groups of individuals that had survived HIV-1 infection for more than 10 years, and, in some risk groups, twice as frequent as their occurrence in rapid progressors to AIDS. Survival analysis clearly shows that disease progression is slower in CKR5 deletion heterozygotes than in individuals homozygous for the normal CKR5 gene. The CKR5Delta 32 deletion may act as a recessive restriction gene against HIV-1 infection and may exert a dominant phenotype of delaying progression to AIDS among infected individuals.

M. Dean, G. A. Huttley, R. Allikmets, S. J. O'Brien, Laboratory of Genomic Diversity, National Cancer Institute (NCI), Frederick, MD 21702-1201, USA.
M. Carrington, C. Winkler, M. W. Smith, Intramural Research Support Program, Science Applications International Corporation Frederick, NCI, Frederick, MD 21702-1201, USA.
J. J. Goedert, Viral Epidemiology Branch, NCI-Executive Plaza North, 6130 Executive Boulevard, Bethesda, MD 20892, USA.
S. P. Buchbinder and E. Vittinghoff, San Francisco City Clinic, Department of Public Health, 24 Van Ness Avenue, San Francisco, CA 94102-8033, USA.
E. Gomperts, Childrens Hospital Los Angeles, 4650 Sunset Boulevard, Los Angeles, CA 90027, USA.
S. Donfield, New England Research Institute, Incorporated, 9 Galen Street, Watertown, MA 02172, USA.
D. Vlahov, Department of Epidemiology, The Johns Hopkins School of Hygiene and Public Health, 615 North Wolfe Street, Baltimore, MD 21205, USA.
R. Kaslow, Department of Epidemiology, University of Alabama at Birmingham, 720 South 20th Street, Birmingham, AL 35294-0008, USA.
A. Saah, The Johns Hopkins School of Hygiene and Public Health, 615 North Wolfe Street, Baltimore, MD 21205, USA.
C. Rinaldo, University of Pittsburgh School of Public Health, 4200 5th Avenue, Pittsburgh, PA 15213, USA.
R. Detels, University of California, Los Angeles, Schools of Public Health and Medicine, 10833 Le Conte Avenue, Los Angeles, CA 90025-1772, USA.
*   These authors contributed equally to this study.

dagger    To whom correspondence should be addressed.

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Reappraisal of the historical selective pressures for the CCR5-{Delta}32 mutation.
S R Duncan, S Scott, and C J Duncan (2005)
J. Med. Genet. 42, 205-208
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Potent Anti-R5 Human Immunodeficiency Virus Type 1 Effects of a CCR5 Antagonist, AK602/ONO4128/GW873140, in a Novel Human Peripheral Blood Mononuclear Cell Nonobese Diabetic-SCID, Interleukin-2 Receptor {gamma}-Chain-Knocked-Out AIDS Mouse Model.
H. Nakata, K. Maeda, T. Miyakawa, S. Shibayama, M. Matsuo, Y. Takaoka, M. Ito, Y. Koyanagi, and H. Mitsuya (2005)
J. Virol. 79, 2087-2096
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A subset of human immunodeficiency virus type 1 long-term non-progressors is characterized by the unique presence of ancestral sequences in the viral population.
G. Bello, C. Casado, V. Sandonis, M. Alonso-Nieto, J. L. Vicario, S. Garcia, V. Hernando, C. Rodriguez, J. d. Romero, and C. Lopez-Galindez (2005)
J. Gen. Virol. 86, 355-364
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Evidence for Negative Binding Cooperativity within CCR5-CCR2b Heterodimers.
L. El-Asmar, J.-Y. Springael, S. Ballet, E. U. Andrieu, G. Vassart, and M. Parmentier (2005)
Mol. Pharmacol. 67, 460-469
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R5 Human Immunodeficiency Virus Type 1 Infection of Fetal Thymic Organ Culture Induces Cytokine and CCR5 Expression.
S. K. Choudhary, N. R. Choudhary, K. C. Kimbrell, J. Colasanti, A. Ziogas, D. Kwa, H. Schuitemaker, and D. Camerini (2005)
J. Virol. 79, 458-471
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Inhibition of Human Immunodeficiency Virus Replication by a Dual CCR5/CXCR4 Antagonist.
K. Princen, S. Hatse, K. Vermeire, S. Aquaro, E. De Clercq, L.-O. Gerlach, M. Rosenkilde, T. W. Schwartz, R. Skerlj, G. Bridger, et al. (2004)
J. Virol. 78, 12996-13006
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Medicinal chemistry applied to a synthetic protein: Development of highly potent HIV entry inhibitors.
O. Hartley, H. Gaertner, J. Wilken, D. Thompson, R. Fish, A. Ramos, C. Pastore, B. Dufour, F. Cerini, A. Melotti, et al. (2004)
PNAS 101, 16460-16465
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Recall antigen activation induces prompt release of CCR5 ligands from PBMC: implication in memory responses and immunization.
L. Sun, S. F. Abdelwahab, G. K. Lewis, and A. Garzino-Demo (2004)
Int. Immunol. 16, 1623-1631
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APOBEC3G Genetic Variants and Their Influence on the Progression to AIDS.
P. An, G. Bleiber, P. Duggal, G. Nelson, M. May, B. Mangeat, I. Alobwede, D. Trono, D. Vlahov, S. Donfield, et al. (2004)
J. Virol. 78, 11070-11076
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Prevention of Vaginal SHIV Transmission in Rhesus Macaques Through Inhibition of CCR5.
M. M. Lederman, R. S. Veazey, R. Offord, D. E. Mosier, J. Dufour, M. Mefford, M. Piatak Jr., J. D. Lifson, J. R. Salkowitz, B. Rodriguez, et al. (2004)
Science 306, 485-487
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Entry and Transcription as Key Determinants of Differences in CD4 T-Cell Permissiveness to Human Immunodeficiency Virus Type 1 Infection.
A. Ciuffi, G. Bleiber, M. Munoz, R. Martinez, C. Loeuillet, M. Rehr, M. Fischer, H. F. Gunthard, A. Oxenius, P. Meylan, et al. (2004)
J. Virol. 78, 10747-10754
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Genetics of infectious diseases.
A. J. Frodsham and A. V.S. Hill (2004)
Hum. Mol. Genet. 13, R187-R194
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Spirodiketopiperazine-Based CCR5 Inhibitor Which Preserves CC-Chemokine/CCR5 Interactions and Exerts Potent Activity against R5 Human Immunodeficiency Virus Type 1 In Vitro.
K. Maeda, H. Nakata, Y. Koh, T. Miyakawa, H. Ogata, Y. Takaoka, S. Shibayama, K. Sagawa, D. Fukushima, J. Moravek, et al. (2004)
J. Virol. 78, 8654-8662
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PSC-RANTES Blocks R5 Human Immunodeficiency Virus Infection of Langerhans Cells Isolated from Individuals with a Variety of CCR5 Diplotypes.
T. Kawamura, S. E. Bruce, A. Abraha, M. Sugaya, O. Hartley, R. E. Offord, E. J. Arts, P. A. Zimmerman, and A. Blauvelt (2004)
J. Virol. 78, 7602-7609
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CC-chemokine receptor 5 (CCR5) in hepatitis C--at the crossroads of the antiviral immune response?.
G. Ahlenstiel, R. P. Woitas, J. Rockstroh, and U. Spengler (2004)
J. Antimicrob. Chemother. 53, 895-898
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Induction of Autoantibodies to CCR5 in Macaques and Subsequent Effects upon Challenge with an R5-Tropic Simian/Human Immunodeficiency Virus.
B. Chackerian, L. Briglio, P. S. Albert, D. R. Lowy, and J. T. Schiller (2004)
J. Virol. 78, 4037-4047
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The Differential Sensitivity of Human and Rhesus Macaque CCR5 to Small-Molecule Inhibitors of Human Immunodeficiency Virus Type 1 Entry Is Explained by a Single Amino Acid Difference and Suggests a Mechanism of Action for These Inhibitors.
E. Billick, C. Seibert, P. Pugach, T. Ketas, A. Trkola, M. J. Endres, N. J. Murgolo, E. Coates, G. R. Reyes, B. M. Baroudy, et al. (2004)
J. Virol. 78, 4134-4144
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Roles of substrate availability and infection of resting and activated CD4+ T cells in transmission and acute simian immunodeficiency virus infection.
Z.-Q. Zhang, S. W. Wietgrefe, Q. Li, M. D. Shore, L. Duan, C. Reilly, J. D. Lifson, and A. T. Haase (2004)
PNAS 101, 5640-5645
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Patterns of ethnic diversity among the genes that influence AIDS.
C. Winkler, P. An, and S. J. O'Brien (2004)
Hum. Mol. Genet. 13, R9-19
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Persistent GB Virus C Infection and Survival in HIV-Infected Men.
C. F. Williams, D. Klinzman, T. E. Yamashita, J. Xiang, P. M. Polgreen, C. Rinaldo, C. Liu, J. Phair, J. B. Margolick, D. Zdunek, et al. (2004)
N. Engl. J. Med. 350, 981-990
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Role for CCR5{Delta}32 Protein in Resistance to R5, R5X4, and X4 Human Immunodeficiency Virus Type 1 in Primary CD4+ Cells.
L. Agrawal, X. Lu, J. Qingwen, Z. VanHorn-Ali, I. V. Nicolescu, D. H. McDermott, P. M. Murphy, and G. Alkhatib (2004)
J. Virol. 78, 2277-2287
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Mapping a locus for susceptibility to HIV-1-associated nephropathy to mouse chromosome 3.
A. G. Gharavi, T. Ahmad, R. D. Wong, R. Hooshyar, J. Vaughn, S. Oller, R. Z. Frankel, L. A. Bruggeman, V. D. D'Agati, P. E. Klotman, et al. (2004)
PNAS 101, 2488-2493
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Association of Homozygous Wild-Type Glutathione S-Transferase M1 Genotype with Increased Breast Cancer Risk.
N. Roodi, W. D. Dupont, J. H. Moore, and F. F. Parl (2004)
Cancer Res. 64, 1233-1236
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Fraction of Cases of Acquired Immunodeficiency Syndrome Prevented by the Interactions of Identified Restriction Gene Variants.
M. J. Silverberg, M. W. Smith, J. S. Chmiel, R. Detels, J. B. Margolick, C. R. Rinaldo, S. J. O'Brien, and A. Munoz (2004)
Am. J. Epidemiol. 159, 232-241
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Immune Failure in the Absence of Profound CD4+ T-Lymphocyte Depletion in Simian Immunodeficiency Virus-Infected Rapid Progressor Macaques.
V. M. Hirsch, S. Santra, S. Goldstein, R. Plishka, A. Buckler-White, A. Seth, I. Ourmanov, C. R. Brown, R. Engle, D. Montefiori, et al. (2004)
J. Virol. 78, 275-284
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Evaluating plague and smallpox as historical selective pressures for the CCR5-{Delta}32 HIV-resistance allele.
A. P. Galvani and M. Slatkin (2003)
PNAS 100, 15276-15279
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Relationship between In Vitro Human Immunodeficiency Virus Type 1 Replication Rate and Virus Load in Plasma.
T. B. Campbell, K. Schneider, T. Wrin, C. J. Petropoulos, and E. Connick (2003)
J. Virol. 77, 12105-12112
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CCR5 Expression Influences the Progression of Human Breast Cancer in a p53-dependent Manner.
S. Manes, E. Mira, R. Colomer, S. Montero, L. M. Real, C. Gomez-Mouton, S. Jimenez-Baranda, A. Garzon, R. A. Lacalle, K. Harshman, et al. (2003)
J. Exp. Med. 198, 1381-1389
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Quantification of CCR5 mRNA in Human Lymphocytes and Macrophages by Real-Time Reverse Transcriptase PCR Assay.
J.-P. Lai, J.-H. Yang, S. D. Douglas, X. Wang, E. Riedel, and W.-Z. Ho (2003)
Clin. Vaccine Immunol. 10, 1123-1128
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Macrophage HIV-1 infection and the gastrointestinal tract reservoir.
P. D. Smith, G. Meng, J. F. Salazar-Gonzalez, and G. M. Shaw (2003)
J. Leukoc. Biol. 74, 642-649
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