Cellular Immune Responses and Viral Diversity in Individuals Treated during Acute and Early HIV-1 Infection

doi:10.1084/jem.193.2.169

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Published online 8 January 2001.

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© The Rockefeller University Press, 0022-1007/2001/1/169/ $5.00
The Journal of Experimental Medicine, Volume 193, Number 2, January 15, 2001 169-180

Original Article

Cellular Immune Responses and Viral Diversity in Individuals Treated during Acute and Early HIV-1 Infection

Marcus Altfeld^a, Eric S. Rosenberg^a, Raj Shankarappa^d, Joia S. Mukherjee^a, Frederick M. Hecht^c, Robert L. Eldridge^a, Marylyn M. Addo^a, Samuel H. Poon^a, Mary N. Phillips^a, Gregory K. Robbins^a, Paul E. Sax^e, Steve Boswell^f, James O. Kahn^b,c, Christian Brander^a, Philip J.R. Goulder^a, Jay A. Levy^b, James I. Mullins^d, and Bruce D. Walker^a
^a Partners AIDS Research Center and Infectious Disease Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02129
^b Department of Medicine, University of California, San Francisco, California 94143
^c Positive Health Program, University of California at San Francisco, San Francisco, California 94143
^d Department of Microbiology, University of Washington, Seattle, Washington 98195
^e Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts 02115
^f Fenway Community Health Center, Boston, Massachusetts 02116

Correspondence to: Bruce D. Walker, MGH-East, CNY 5212, 149 13th St., Charlestown, MA 02129. Tel:617-724-8332 Fax:617-726-4691 E-mail:bwalker{at}helix.mgh.harvard.edu.

Immune responses induced during the early stages of chronicviral infections are thought to influence disease outcome. UsingHIV as a model, we examined virus-specific cytotoxic T lymphocytes(CTLs), T helper cells, and viral genetic diversity in relationto duration of infection and subsequent response to antiviraltherapy. Individuals with acute HIV-1 infection treated beforeseroconversion had weaker CTL responses directed at fewer epitopesthan persons who were treated after seroconversion. However,treatment-induced control of viremia was associated with thedevelopment of strong T helper cell responses in both groups.After 1 yr of antiviral treatment initiated in acute or earlyinfection, all epitope-specific CTL responses persisted despiteundetectable viral loads. The breadth and magnitude of CTL responsesremained significantly less in treated acute infection thanin treated chronic infection, but viral diversity was also significantlyless with immediate therapy. We conclude that early treatmentof acute HIV infection leads to a more narrowly directed CTLresponse, stronger T helper cell responses, and a less diversevirus population. Given the need for T helper cells to maintaineffective CTL responses and the ability of virus diversificationto accommodate immune escape, we hypothesize that early therapyof primary infection may be beneficial despite induction ofless robust CTL responses. These data also provide rationalefor therapeutic immunization aimed at broadening CTL responsesin treated primary HIV infection.

Key Words: cytotoxic T lymphocytes, T helper cell responses, viral evolution,cytotoxic T lymphocyte epitopes, human leukocyte antigen

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Ortiz, G. M., Hu, J., Goldwitz, J. A., Chandwani, R., Larsson, M., Bhardwaj, N., Bonhoeffer, S., Ramratnam, B., Zhang, L., Markowitz, M. M., Nixon, D. F. (2002). Residual Viral Replication during Antiretroviral Therapy Boosts Human Immunodeficiency Virus Type 1-Specific CD8+ T-Cell Responses in Subjects Treated Early after Infection. J. Virol. 76: 411-415 [Abstract] [Full Text]
Betts, M. R., Ambrozak, D. R., Douek, D. C., Bonhoeffer, S., Brenchley, J. M., Casazza, J. P., Koup, R. A., Picker, L. J. (2001). Analysis of Total Human Immunodeficiency Virus (HIV)-Specific CD4+ and CD8+ T-Cell Responses: Relationship to Viral Load in Untreated HIV Infection. J. Virol. 75: 11983-11991 [Abstract] [Full Text]
Scott, Z. A., Chadwick, E. G., Gibson, L. L., Catalina, M. D., McManus, M. M., Yogev, R., Palumbo, P., Sullivan, J. L., Britto, P., Gay, H., Luzuriaga, K. (2001). Infrequent Detection of HIV-1-Specific, But Not Cytomegalovirus-Specific, CD8+ T Cell Responses in Young HIV-1-Infected Infants. J. Immunol. 167: 7134-7140 [Abstract] [Full Text]
Pacanowski, J., Kahi, S., Baillet, M., Lebon, P., Deveau, C., Goujard, C., Meyer, L., Oksenhendler, E., Sinet, M., Hosmalin, A. (2001). Reduced blood CD123+ (lymphoid) and CD11c+ (myeloid) dendritic cell numbers in primary HIV-1 infection. Blood 98: 3016-3021 [Abstract] [Full Text]
Lifson, J. D., Rossio, J. L., Piatak, M. Jr., Parks, T., Li, L., Kiser, R., Coalter, V., Fisher, B., Flynn, B. M., Czajak, S., Hirsch, V. M., Reimann, K. A., Schmitz, J. E., Ghrayeb, J., Bischofberger, N., Nowak, M. A., Desrosiers, R. C., Wodarz, D. (2001). Role of CD8+ Lymphocytes in Control of Simian Immunodeficiency Virus Infection and Resistance to Rechallenge after Transient Early Antiretroviral Treatment. J. Virol. 75: 10187-10199 [Abstract] [Full Text]
Montefiori, D. C., Hill, T. S., Vo, H. T. T., Walker, B. D., Rosenberg, E. S. (2001). Neutralizing Antibodies Associated with Viremia Control in a Subset of Individuals after Treatment of Acute Human Immunodeficiency Virus Type 1 Infection. J. Virol. 75: 10200-10207 [Abstract] [Full Text]
Novitsky, V., Rybak, N., McLane, M. F., Gilbert, P., Chigwedere, P., Klein, I., Gaolekwe, S., Chang, S. Y., Peter, T., Thior, I., Ndung'u, T., Vannberg, F., Foley, B. T., Marlink, R., Lee, T. H., Essex, M. (2001). Identification of Human Immunodeficiency Virus Type 1 Subtype C Gag-, Tat-, Rev-, and Nef-Specific Elispot-Based Cytotoxic T-Lymphocyte Responses for AIDS Vaccine Design. J. Virol. 75: 9210-9228 [Abstract] [Full Text]
Altfeld, M., Addo, M. M., Eldridge, R. L., Yu, X. G., Thomas, S., Khatri, A., Strick, D., Phillips, M. N., Cohen, G. B., Islam, S. A., Kalams, S. A., Brander, C., Goulder, P. J. R., Rosenberg, E. S., Walker, B. D. (2001). Vpr Is Preferentially Targeted by CTL During HIV-1 Infection. J. Immunol. 167: 2743-2752 [Abstract] [Full Text]
Day, C. L., Shea, A. K., Altfeld, M. A., Olson, D. P., Buchbinder, S. P., Hecht, F. M., Rosenberg, E. S., Walker, B. D., Kalams, S. A. (2001). Relative Dominance of Epitope-Specific Cytotoxic T-Lymphocyte Responses in Human Immunodeficiency Virus Type 1-Infected Persons with Shared HLA Alleles. J. Virol. 75: 6279-6291 [Abstract] [Full Text]
Islam, S. A., Hay, C. M., Hartman, K. E., He, S., Shea, A. K., Trocha, A. K., Dynan, M. J., Reshamwala, N., Buchbinder, S. P., Basgoz, N. O., Kalams, S. A. (2001). Persistence of Human Immunodeficiency Virus Type 1-Specific Cytotoxic T-Lymphocyte Clones in a Subject with Rapid Disease Progression. J. Virol. 75: 4907-4911 [Abstract] [Full Text]
Goulder, P. J.R., Altfeld, M. A., Rosenberg, E. S., Nguyen, T., Tang, Y., Eldridge, R. L., Addo, M. M., He, S., Mukherjee, J. S., Phillips, M. N., Bunce, M., Kalams, S. A., Sekaly, R. P., Walker, B. D., Brander, C. (2001). Substantial Differences in Specificity of HIV-specific Cytotoxic T Cells in Acute and Chronic HIV Infection. JEM 193: 181-194 [Abstract] [Full Text]
Hislop, A. D., Annels, N. E., Gudgeon, N. H., Leese, A. M., Rickinson, A. B. (2002). Epitope-specific Evolution of Human CD8+ T Cell Responses from Primary to Persistent Phases of Epstein-Barr Virus Infection. JEM 195: 893-905 [Abstract] [Full Text]