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Science 24 May 2002:
Vol. 296. no. 5572, pp. 1439 - 1443
DOI: 10.1126/science.1069660
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Research Articles

Evidence of HIV-1 Adaptation to HLA-Restricted Immune Responses at a Population Level

Corey B. Moore,1 Mina John,12 Ian R. James,1 Frank T. Christiansen,23 Campbell S. Witt,12 Simon A. Mallal12*

Antigen-specific T cell immunity is HLA-restricted. Human immunodeficiency virus-type 1 (HIV-1) mutations that allow escape from host immune responses may therefore be HLA allele-specific. We analyzed HIV-1 reverse transcriptase sequences from a large HLA-diverse population of HIV-1-infected individuals. Polymorphisms in HIV-1 were most evident at sites of least functional or structural constraint and frequently were associated with particular host HLA class I alleles. Absence of polymorphism was also HLA allele-specific. At a population level, the degree of HLA-associated selection in viral sequence was predictive of viral load. These results support a fundamental role for HLA-restricted immune responses in driving and shaping HIV-1 evolution in vivo.

1 Centre for Clinical Immunology and Biomedical Statistics, Royal Perth Hospital and Murdoch University, Level 2 North Block, Royal Perth Hospital, Wellington Street, WA 6000, Australia.
2 Department of Clinical Immunology and Biochemical Genetics, Royal Perth Hospital.
3 Department of Pathology, University of Western Australia, WA 6009, Australia.
*   To whom correspondence should be addressed. E-mail: mallal{at}prodigal.murdoch.edu.au

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Parallel Human Immunodeficiency Virus Type 1-Specific CD8+ T-Lymphocyte Responses in Blood and Mucosa during Chronic Infection.
F. J. Ibarrondo, P. A. Anton, M. Fuerst, H. L. Ng, J. T. Wong, J. Matud, J. Elliott, R. Shih, M. A. Hausner, C. Price, et al. (2005)
J. Virol. 79, 4289-4297
   Abstract »    Full Text »    PDF »
Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA.
A. Leslie, D. Kavanagh, I. Honeyborne, K. Pfafferott, C. Edwards, T. Pillay, L. Hilton, C. Thobakgale, D. Ramduth, R. Draenert, et al. (2005)
J. Exp. Med. 201, 891-902
   Abstract »    Full Text »    PDF »
Immunologic Pressure within Class I-Restricted Cognate Human Immunodeficiency Virus Epitopes during Highly Active Antiretroviral Therapy.
J. P. Casazza, M. R. Betts, B. J. Hill, J. M. Brenchley, D. A. Price, D. C. Douek, and R. A. Koup (2005)
J. Virol. 79, 3653-3663
   Abstract »    Full Text »    PDF »
Mutations in the RNase H Primer Grip Domain of Murine Leukemia Virus Reverse Transcriptase Decrease Efficiency and Accuracy of Plus-Strand DNA Transfer.
J. L. Mbisa, G. N. Nikolenko, and V. K. Pathak (2005)
J. Virol. 79, 419-427
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HIV-specific Cytotoxic T Cells from Long-Term Survivors Select a Unique T Cell Receptor.
T. Dong, G. Stewart-Jones, N. Chen, P. Easterbrook, X. Xu, L. Papagno, V. Appay, M. Weekes, C. Conlon, C. Spina, et al. (2004)
J. Exp. Med. 200, 1547-1557
   Abstract »    Full Text »    PDF »
Fitness Costs Limit Viral Escape from Cytotoxic T Lymphocytes at a Structurally Constrained Epitope.
F. W. Peyerl, H. S. Bazick, M. H. Newberg, D. H. Barouch, J. Sodroski, and N. L. Letvin (2004)
J. Virol. 78, 13901-13910
   Abstract »    Full Text »    PDF »
A Dominant Role for CD8+-T-Lymphocyte Selection in Simian Immunodeficiency Virus Sequence Variation.
D. H. O'Connor, A. B. McDermott, K. C. Krebs, E. J. Dodds, J. E. Miller, E. J. Gonzalez, T. J. Jacoby, L. Yant, H. Piontkivska, R. Pantophlet, et al. (2004)
J. Virol. 78, 14012-14022
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T Cell Cross-Reactivity and Conformational Changes during TCR Engagement.
J. K. Lee, G. Stewart-Jones, T. Dong, K. Harlos, K. Di Gleria, L. Dorrell, D. C. Douek, P. A. van der Merwe, E. Y. Jones, and A. J. McMichael (2004)
J. Exp. Med. 200, 1455-1466
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Determinants of Human Immunodeficiency Virus Type 1 Escape from the Primary CD8+ Cytotoxic T Lymphocyte Response.
N. A. Jones, X. Wei, D. R. Flower, M. Wong, F. Michor, M. S. Saag, B. H. Hahn, M. A. Nowak, G. M. Shaw, and P. Borrow (2004)
J. Exp. Med. 200, 1243-1256
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Between-Host Evolution of Cytotoxic T-Lymphocyte Epitopes in Human Immunodeficiency Virus Type 1: an Approach Based on Phylogenetically Independent Comparisons.
H. Piontkivska and A. L. Hughes (2004)
J. Virol. 78, 11758-11765
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Predicting the Impact of a Nonsterilizing Vaccine against Human Immunodeficiency Virus.
M. P. Davenport, R. M. Ribeiro, D. L. Chao, and A. S. Perelson (2004)
J. Virol. 78, 11340-11351
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A Robust Measure of HIV-1 Population Turnover Within Chronically Infected Individuals.
G. Achaz, S. Palmer, M. Kearney, F. Maldarelli, J. W. Mellors, J. M. Coffin, and J. Wakeley (2004)
Mol. Biol. Evol. 21, 1902-1912
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Consequences of Cytotoxic T-Lymphocyte Escape: Common Escape Mutations in Simian Immunodeficiency Virus Are Poorly Recognized in Naive Hosts.
T. C. Friedrich, A. B. McDermott, M. R. Reynolds, S. Piaskowski, S. Fuenger, I. P. de Souza, R. Rudersdorf, C. Cullen, L. J. Yant, L. Vojnov, et al. (2004)
J. Virol. 78, 10064-10073
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From the Cover: Quantifiable cytotoxic T lymphocyte responses and HLA-related risk of progression to AIDS.
A. Scherer, J. Frater, A. Oxenius, J. Agudelo, D. A. Price, H. F. Gunthard, M. Barnardo, L. Perrin, B. Hirschel, R. E. Phillips, et al. (2004)
PNAS 101, 12266-12270
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Frequent Transmission of Cytotoxic-T-Lymphocyte Escape Mutants of Human Immunodeficiency Virus Type 1 in the Highly HLA-A24-Positive Japanese Population.
T. Furutsuki, N. Hosoya, A. Kawana-Tachikawa, M. Tomizawa, T. Odawara, M. Goto, Y. Kitamura, T. Nakamura, A. D. Kelleher, D. A. Cooper, et al. (2004)
J. Virol. 78, 8437-8445
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Selection, Transmission, and Reversion of an Antigen-Processing Cytotoxic T-Lymphocyte Escape Mutation in Human Immunodeficiency Virus Type 1 Infection.
T. M. Allen, M. Altfeld, X. G. Yu, K. M. O'Sullivan, M. Lichterfeld, S. Le Gall, M. John, B. R. Mothe, P. K. Lee, E. T. Kalife, et al. (2004)
J. Virol. 78, 7069-7078
   Abstract »    Full Text »    PDF »
Antiretroviral Drug Resistance Mutations Sustain or Enhance CTL Recognition of Common HIV-1 Pol Epitopes.
R. D. Mason, M. I. Bowmer, C. M. Howley, M. Gallant, J. C. E. Myers, and M. D. Grant (2004)
J. Immunol. 172, 7212-7219
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Migration of Antigen-Specific T Cells Away from CXCR4-Binding Human Immunodeficiency Virus Type 1 gp120.
D. M. Brainard, W. G. Tharp, E. Granado, N. Miller, A. K. Trocha, X.-H. Ren, B. Conrad, E. F. Terwilliger, R. Wyatt, B. D. Walker, et al. (2004)
J. Virol. 78, 5184-5193
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Immune Selection for Altered Antigen Processing Leads to Cytotoxic T Lymphocyte Escape in Chronic HIV-1 Infection.
R. Draenert, S. Le Gall, K. J. Pfafferott, A. J. Leslie, P. Chetty, C. Brander, E. C. Holmes, S.-C. Chang, M. E. Feeney, M. M. Addo, et al. (2004)
J. Exp. Med. 199, 905-915
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Positive Selection Detection in 40,000 Human Immunodeficiency Virus (HIV) Type 1 Sequences Automatically Identifies Drug Resistance and Positive Fitness Mutations in HIV Protease and Reverse Transcriptase.
L. Chen, A. Perlina, and C. J. Lee (2004)
J. Virol. 78, 3722-3732
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Consistent Cytotoxic-T-Lymphocyte Targeting of Immunodominant Regions in Human Immunodeficiency Virus across Multiple Ethnicities.
N. Frahm, B. T. Korber, C. M. Adams, J. J. Szinger, R. Draenert, M. M. Addo, M. E. Feeney, K. Yusim, K. Sango, N. V. Brown, et al. (2004)
J. Virol. 78, 2187-2200
   Abstract »    Full Text »    PDF »
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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Comparative Study of Adaptive Molecular Evolution in Different Human Immunodeficiency Virus Groups and Subtypes.
M. Choisy, C. H. Woelk, J.-F. Guegan, and D. L. Robertson (2004)
J. Virol. 78, 1962-1970
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Impaired Processing and Presentation of Cytotoxic-T-Lymphocyte (CTL) Epitopes Are Major Escape Mechanisms from CTL Immune Pressure in Human Immunodeficiency Virus Type 1 Infection.
Y. Yokomaku, H. Miura, H. Tomiyama, A. Kawana-Tachikawa, M. Takiguchi, A. Kojima, Y. Nagai, A. Iwamoto, Z. Matsuda, and K. Ariyoshi (2004)
J. Virol. 78, 1324-1332
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Unifying the Epidemiological and Evolutionary Dynamics of Pathogens.
B. T. Grenfell, O. G. Pybus, J. R. Gog, J. L. N. Wood, J. M. Daly, J. A. Mumford, and E. C. Holmes (2004)
Science 303, 327-332
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Human Immunodeficiency Virus Type 1 Superinfection Was Not Detected following 215 Years of Injection Drug User Exposure.
R. Tsui, B. L. Herring, J. D. Barbour, R. M. Grant, P. Bacchetti, A. Kral, B. R. Edlin, and E. L. Delwart (2004)
J. Virol. 78, 94-103
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