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Science 12 March 1999:
Vol. 283. no. 5408, pp. 1748 - 1752
DOI: 10.1126/science.283.5408.1748
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Reports

HLA and HIV-1: Heterozygote Advantage and B*35-Cw*04 Disadvantage

Mary Carrington, 1 George W. Nelson, 1 Maureen P. Martin, 1 Teri Kissner, 1 David Vlahov, 2 James J. Goedert, 3 Richard Kaslow, 4 Susan Buchbinder, 5 Keith Hoots, 6 Stephen J. O'Brien 7*

A selective advantage against infectious disease associated with increased heterozygosity at the human major histocompatibility complex [human leukocyte antigen (HLA) class I and class II] is believed to play a major role in maintaining the extraordinary allelic diversity of these genes. Maximum HLA heterozygosity of class I loci (A, B, and C) delayed acquired immunodeficiency syndrome (AIDS) onset among patients infected with human immunodeficiency virus-type 1 (HIV-1), whereas individuals who were homozygous for one or more loci progressed rapidly to AIDS and death. The HLA class I alleles B*35 and Cw*04 were consistently associated with rapid development of AIDS-defining conditions in Caucasians. The extended survival of 28 to 40 percent of HIV-1-infected Caucasian patients who avoided AIDS for ten or more years can be attributed to their being fully heterozygous at HLA class I loci, to their lacking the AIDS-associated alleles B*35 and Cw*04, or to both.

1 Intramural Research Support Program, Science Applications International Corporation Frederick, National Cancer Institute (NCI), Frederick, MD 21702-1201, USA.
2 The Johns Hopkins School of Hygiene and Public Health, Baltimore, MD 21205, USA, for AIDS Linked to Intravenous Experience Cohort.
3 Viral Epidemiology Branch, NCI-Executive Plaza North, Bethesda, MD 20892, USA, for Multicenter Hemophilia Cohort Study.
4 University of Alabama, Birmingham, AL 35294, USA, for Multicenter AIDS Cohort Study.
5 San Francisco City Clinic Cohort, San Francisco, CA 94102, USA, for San Francisco City Cohort.
6 Gulf States Hemophilia Center, University of Texas Health Science Center, Houston, TX 77030, USA, for the Hemophilia Growth and Development Study.
7 Laboratory of Genomic Diversity, NCI, Frederick, MD 21702, USA.
*   To whom correspondence should be addressed. E-mail: obrien{at}mail.ncifcrf.gov

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J. Virol. 76, 12603-12610
   Abstract »    Full Text »    PDF »
MHC Class I Alleles Influence Set-Point Viral Load and Survival Time in Simian Immunodeficiency Virus-Infected Rhesus Monkeys.
T. Muhl, M. Krawczak, P. ten Haaft, G. Hunsmann, and U. Sauermann (2002)
J. Immunol. 169, 3438-3446
   Abstract »    Full Text »    PDF »
MHC heterozygosity confers a selective advantage against multiple-strain infections.
D. J. Penn, K. Damjanovich, and W. K. Potts (2002)
PNAS 99, 11260-11264
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Favorable and Unfavorable HLA Class I Alleles and Haplotypes in Zambians Predominantly Infected with Clade C Human Immunodeficiency Virus Type 1.
J. Tang, S. Tang, E. Lobashevsky, A. D. Myracle, U. Fideli, G. Aldrovandi, S. Allen, R. Musonda, and R. A. Kaslow (2002)
J. Virol. 76, 8276-8284
   Abstract »    Full Text »    PDF »
Selection following isolation of human immunodeficiency virus type 1 in peripheral blood mononuclear cells and herpesvirus saimiri-transformed T cells is comparable.
N. N. Zheng, C. Vella, P. J. Easterbrook, and R. S. Daniels (2002)
J. Gen. Virol. 83, 1343-1352
   Abstract »    Full Text »    PDF »
Negative selection of thymocytes expressing the D10 TCR.
D. B. Sant'Angelo and C. A. Janeway Jr. (2002)
PNAS 99, 6931-6936
   Abstract »    Full Text »    PDF »
Rhesus Macaque Resistance to Mucosal Simian Immunodeficiency Virus Infection Is Associated with a Postentry Block in Viral Replication.
B. Peng, R. Voltan, L. Lim, Y. Edghill-Smith, S. Phogat, D. S. Dimitrov, K. Arora, M. Leno, S. Than, R. Woodward, et al. (2002)
J. Virol. 76, 6016-6026
   Abstract »    Full Text »    PDF »
HLA-Cw*04 and Hepatitis C Virus Persistence.
C. L. Thio, X. Gao, J. J. Goedert, D. Vlahov, K. E. Nelson, M. W. Hilgartner, S. J. O'Brien, P. Karacki, J. Astemborski, M. Carrington, et al. (2002)
J. Virol. 76, 4792-4797
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Human Leukocyte Antigen Class I Alleles and Cervical Neoplasia: No Heterozygote Advantage.
S. S. Wang, A. Hildesheim, X. Gao, M. Schiffman, R. Herrero, M. C. Bratti, M. E. Sherman, W. A. Barnes, M. D. Greenberg, L. McGowan, et al. (2002)
Cancer Epidemiol. Biomarkers Prev. 11, 419-420
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Magnitude of Functional CD8+ T-Cell Responses to the Gag Protein of Human Immunodeficiency Virus Type 1 Correlates Inversely with Viral Load in Plasma.
B. H. Edwards, A. Bansal, S. Sabbaj, J. Bakari, M. J. Mulligan, and P. A. Goepfert (2002)
J. Virol. 76, 2298-2305
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Human Immunodeficiency Virus Type 1-Hepatitis C Virus Coinfection: Intraindividual Comparison of Cellular Immune Responses against Two Persistent Viruses.
G. M. Lauer, T. N. Nguyen, C. L. Day, G. K. Robbins, T. Flynn, K. McGowan, E. S. Rosenberg, M. Lucas, P. Klenerman, R. T. Chung, et al. (2002)
J. Virol. 76, 2817-2826
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Distribution of Chemokine Receptor CCR2 and CCR5 Genotypes and Their Relative Contribution to Human Immunodeficiency Virus Type 1 (HIV-1) Seroconversion, Early HIV-1 RNA Concentration in Plasma, and Later Disease Progression.
J. Tang, B. Shelton, N. J. Makhatadze, Y. Zhang, M. Schaen, L. G. Louie, J. J. Goedert, E. C. Seaberg, J. B. Margolick, J. Mellors, et al. (2002)
J. Virol. 76, 662-672
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Dominance of CD8 Responses Specific for Epitopes Bound by a Single Major Histocompatibility Complex Class I Molecule during the Acute Phase of Viral Infection.
B. R. Mothe, H. Horton, D. K. Carter, T. M. Allen, M. E. Liebl, P. Skinner, T. U. Vogel, S. Fuenger, K. Vielhuber, W. Rehrauer, et al. (2002)
J. Virol. 76, 875-884
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ALVAC-SIV-gag-pol-env-Based Vaccination and Macaque Major Histocompatibility Complex Class I (A*01) Delay Simian Immunodeficiency Virus SIVmac-Induced Immunodeficiency.
R. Pal, D. Venzon, N. L. Letvin, S. Santra, D. C. Montefiori, N. R. Miller, E. Tryniszewska, M. G. Lewis, T. C. VanCott, V. Hirsch, et al. (2002)
J. Virol. 76, 292-302
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MHC Class I Molecules and Progression to AIDS.
F. Cainelli, E. Concia, S. Vento, M. Carrington, X. Gao, and S. O'Brien (2001)
N. Engl. J. Med. 345, 924-925
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Polymorphisms in HLA Class I Genes Associated with both Favorable Prognosis of Human Immunodeficiency Virus (HIV) Type 1 Infection and Positive Cytotoxic T-Lymphocyte Responses to ALVAC-HIV Recombinant Canarypox Vaccines.
R. A. Kaslow, C. Rivers, J. Tang, T. J. Bender, P. A. Goepfert, R. El Habib, K. Weinhold, M. J. Mulligan, and the NIAID Aids Vaccine Evaluation Group (2001)
J. Virol. 75, 8681-8689
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Paediatric HIV infection: correlates of protective immunity and global perspectives in prevention and management.
P. J. Goulder, P. Jeena, G. Tudor-Williams, and S. Burchett (2001)
Br. Med. Bull. 58, 89-108
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Depletion of circulating natural type 1 interferon-producing cells in HIV-infected AIDS patients.
V. Soumelis, I. Scott, F. Gheyas, D. Bouhour, G. Cozon, L. Cotte, L. Huang, J. A. Levy, and Y.-J. Liu (2001)
Blood 98, 906-912
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Human Leukocyte Antigen Gene Polymorphism and the Histocompatibility Laboratory.
T. M. Williams (2001)
J. Mol. Diagn. 3, 98-104
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Increased Level of Stromal Cell-Derived Factor-1 mRNA in Peripheral Blood Mononuclear Cells from Children with AIDS-related Lymphoma.
S. Sei, D. P. O'Neill, S. K. Stewart, Q.-e. Yang, M. Kumagai, A. M. Boler, M. A. Adde, S. L. Zwerski, L. V. Wood, D. J. Venzon, et al. (2001)
Cancer Res. 61, 5028-5037
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Effect of a Single Amino Acid Change in MHC Class I Molecules on the Rate of Progression to AIDS.
X. Gao, G. W. Nelson, P. Karacki, M. P. Martin, J. Phair, R. Kaslow, J. J. Goedert, S. Buchbinder, K. Hoots, D. Vlahov, et al. (2001)
N. Engl. J. Med. 344, 1668-1675
   Abstract »    Full Text »    PDF »
Host Determinants in HIV Infection and Disease: Part 2: Genetic Factors and Implications for Antiretroviral Therapeutics.
C. M. Hogan and S. M. Hammer (2001)
Ann Intern Med 134, 978-996
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Control of HIV-1 viremia and protection from AIDS are associated with HLA-Bw4 homozygosity.
P. O. Flores-Villanueva, E. J. Yunis, J. C. Delgado, E. Vittinghoff, S. Buchbinder, J. Y. Leung, A. M. Uglialoro, O. P. Clavijo, E. S. Rosenberg, S. A. Kalams, et al. (2001)
PNAS
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Substantial Differences in Specificity of HIV-specific Cytotoxic T Cells in Acute and Chronic HIV Infection.
P. J.R. Goulder, M. A. Altfeld, E. S. Rosenberg, T. Nguyen, Y. Tang, R. L. Eldridge, M. M. Addo, S. He, J. S. Mukherjee, M. N. Phillips, et al. (2001)
J. Exp. Med. 193, 181-194
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In Vivo Attenuation of Simian Immunodeficiency Virus by Disruption of a Tyrosine-Dependent Sorting Signal in the Envelope Glycoprotein Cytoplasmic Tail.
P. N. Fultz, P. J. Vance, M. J. Endres, B. Tao, J. D. Dvorin, I. C. Davis, J. D. Lifson, D. C. Montefiori, M. Marsh, M. H. Malim, et al. (2001)
J. Virol. 75, 278-291
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Genetic restriction of HIV-1 pathogenesis to AIDS by promoter alleles of IL10.
H. D. Shin, C. Winkler, J. C. Stephens, J. Bream, H. Young, J. J. Goedert, T. R. O'Brien, D. Vlahov, S. Buchbinder, J. Giorgi, et al. (2000)
PNAS 97, 14467-14472
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The Influence of HLA Class I Alleles and Heterozygosity on the Outcome of Human T Cell Lymphotropic Virus Type I Infection.
K. J. M. Jeffery, A. A. Siddiqui, M. Bunce, A. L. Lloyd, A. M. Vine, A. D. Witkover, S. Izumo, K. Usuku, K. I. Welsh, M. Osame, et al. (2000)
J. Immunol. 165, 7278-7284
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Clonal Expansions in Acute EBV Infection Are Detectable in the CD8 and not the CD4 Subset and Persist with a Variable CD45 Phenotype.
M. K. Maini, N. Gudgeon, L. R. Wedderburn, A. B. Rickinson, and P. C. L. Beverley (2000)
J. Immunol. 165, 5729-5737
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Science, medicine, and the future: Susceptibility to infection.
D. Kwiatkowski (2000)
BMJ 321, 1061-1065
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Intrinsic Susceptibility of Rhesus Macaque Peripheral CD4+ T Cells to Simian Immunodeficiency Virus In Vitro Is Predictive of In Vivo Viral Replication.
S. Goldstein, C. R. Brown, H. Dehghani, J. D. Lifson, and V. M. Hirsch (2000)
J. Virol. 74, 9388-9395
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Mate Selection and the Evolution of Highly Polymorphic Self/Nonself Recognition Genes.
R. K. Grosberg and M. W. Hart (2000)
Science 289, 2111-2114
   Abstract »    Full Text »


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