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Journal of Virology, November 2003, p. 11708-11717, Vol. 77, No. 21
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.21.11708-11717.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Severe CD4+ T-Cell Depletion in Gut Lymphoid Tissue during Primary Human Immunodeficiency Virus Type 1 Infection and Substantial Delay in Restoration following Highly Active Antiretroviral Therapy

Moraima Guadalupe,1 Elizabeth Reay,1 Sumathi Sankaran,1 Thomas Prindiville,2 Jason Flamm,3 Andrew McNeil,2,4 and Satya Dandekar1,2*

Departments of Medical Microbiology & Immunology,1 Internal Medicine, University of California, Davis, California 95616,2 The Permanente Medical Group Inc.,3 CARES, Sacramento, California 961854

Received 7 May 2003/ Accepted 29 July 2003

Gut-associated lymphoid tissue (GALT) harbors the majority of T lymphocytes in the body and is an important target for human immunodeficiency virus type 1 (HIV-1). We analyzed longitudinal jejunal biopsy samples from HIV-1-infected patients, during both primary and chronic stages of HIV-1 infection, prior to and following the initiation of highly active antiretroviral therapy (HAART) to determine the onset of CD4+ T-cell depletion and the effect of HAART on the restoration of CD4+ T cells in GALT. Severe depletion of intestinal CD4+ T cells occurred during primary HIV-1 infection. Our results showed that the restoration of intestinal CD4+ T cells following HAART in chronically HIV-1-infected patients was substantially delayed and incomplete. In contrast, initiation of HAART during early stages of infection resulted in near-complete restoration of intestinal CD4+ T cells, despite the delay in comparison to peripheral blood CD4+ T-cell recovery. DNA microarray analysis of gene expression profiles and flow-cytometric analysis of lymphocyte homing and cell proliferation markers demonstrated that cell trafficking to GALT and not local proliferation contributed to CD4+ T-cell restoration. Evaluation of jejunal biopsy samples from long-term HIV-1-infected nonprogressors showed maintenance of normal CD4+ T-cell levels in both GALT and peripheral blood. Our results demonstrate that near-complete restoration of mucosal immune system can be achieved by initiating HAART early in HIV-1 infection. Monitoring of the restoration and/or maintenance of CD4+ T cells in GALT provides a more accurate assessment of the efficacy of antiviral host immune responses as well as HAART.

* Corresponding author. Mailing address: Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, CA 95616. Phone: (530) 752-6606. Fax: (530) 752-7301. E-mail: sdandekar{at}ucdavis.edu.

Journal of Virology, November 2003, p. 11708-11717, Vol. 77, No. 21
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.21.11708-11717.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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