Partial Activation and Induction of Apoptosis in CD4+ and CD8+ T Lymphocytes by Conformationally Authentic Noninfectious Human Immunodeficiency Virus Type 1

doi:10.1128/JVI.75.3.1152-1164.2001

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Journal of Virology, February 2001, p. 1152-1164, Vol. 75, No. 3
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.3.1152-1164.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Partial Activation and Induction of Apoptosis in CD4⁺ and CD8⁺ T Lymphocytes by Conformationally Authentic Noninfectious Human Immunodeficiency Virus Type 1

Mark T. Esser,¹ Julian W. Bess Jr.,¹ Kalachar Suryanarayana,¹^, Elena Chertova,¹ Darlene Marti,² Mary Carrington,² Larry O. Arthur,¹ and Jeffrey D. Lifson¹^,^*

AIDS Vaccine Program¹ and Intramural Research Support Program,² SAIC-Frederick, National Cancer Institute Frederick Cancer Research and Development Center, Frederick, Maryland 21702-1201

Received 23 August 2000/Accepted 6 November 2000

Increased levels of apoptosis are seen in human immunodeficiency virus (HIV) infection, and this has been proposed as an importantmechanism contributing to HIV pathogenesis. However, interpretationof in vitro studies aimed at understanding HIV-related apoptosishas been complicated by the use of high concentrations of recombinantproteins or by direct cytopathic effects of replicating virus.We have developed an inactivation procedure that destroys retroviralinfectivity while preserving the structural and functional integrityof the HIV surface proteins. These noninfectious virions interactauthentically with target cells, providing a powerful tool todissect mechanisms of HIV pathogenesis that do or do not requireviral replication. Noninfectious CXCR4-tropic HIV-1 virions, butnot microvesicles, partially activated freshly isolated CD4⁺ and CD8⁺ peripheral blood mononuclear cell T lymphocytes to express FasLand Fas, but not CD69 or CD25 (interleukin-2 receptor alpha) andeventually die via apoptosis starting 4 to 6 days postexposure.These effects required conformationally intact virions, as heat-denaturedvirions or equivalent amounts of recombinant gp120 did not induceapoptosis. The maximal apoptotic effect was dependent on majorhistocompatibility complex (MHC) class II proteins being presenton the virion, but was not MHC restricted. The results suggestthat the immunopathogenesis of HIV infection may not depend solelyon direct cytopathic effects of HIV replication, but that effectsdue to noninfectious HIV-1 virions may also contributeimportantly.

^* Corresponding author, Mailing address: Building 535, Room 509, Retroviral Pathogenesis Laboratory, AIDS Vaccine Program, SAIC-Frederick,National Cancer Institute at Frederick, Frederick, MD 21702. Phone:(301) 846 5019. Fax: (301) 846 5588. E-mail: lifson{at}avpvx1.ncifcrf.gov.

This paper is dedicated in loving memory of KalacharSuryanarayana.

Deceased.

Journal of Virology, February 2001, p. 1152-1164, Vol. 75, No. 3
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.3.1152-1164.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

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