Differential Incorporation of CD45, CD80 (B7-1), CD86 (B7-2), and Major Histocompatibility Complex Class I and II Molecules into Human Immunodeficiency Virus Type 1 Virions and Microvesicles: Implications for Viral Pathogenesis and Immune Regulation

doi:10.1128/JVI.75.13.6173-6182.2001

This Article

	Full Text
	Full Text (PDF)
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by Esser, M. T.
	Articles by Lifson, J. D.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Esser, M. T.
	Articles by Lifson, J. D.

Previous Article | Next Article

Journal of Virology, July 2001, p. 6173-6182, Vol. 75, No. 13
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.13.6173-6182.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Differential Incorporation of CD45, CD80 (B7-1), CD86 (B7-2), and Major Histocompatibility Complex Class I and II Molecules into Human Immunodeficiency Virus Type 1 Virions and Microvesicles: Implications for Viral Pathogenesis and Immune Regulation

Mark T. Esser,¹ David R. Graham,¹ Lori V. Coren,¹ Charles M. Trubey,² Julian W. Bess Jr.,¹ Larry O. Arthur,¹ David E. Ott,¹ and Jeffrey D. Lifson¹^,^*

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

Received 14 December 2000/Accepted 6 April 2001

Human immunodeficiency virus (HIV) infection results in a functional impairment of CD4⁺ T cells long before a quantitative decline in circulating CD4⁺ T cells is evident. The mechanism(s) responsible for this functionalunresponsiveness and eventual depletion of CD4⁺ T cells remains unclear. Both direct effects of cytopathic infectionof CD4⁺ cells and indirect effects in which uninfected "bystander" cellsare functionally compromised or killed have been implicated ascontributing to the immunopathogenesis of HIV infection. BecauseT-cell receptor engagement of major histocompatibility complex(MHC) molecules in the absence of costimulation mediated via CD28binding to CD80 (B7-1) or CD86 (B7-2) can lead to anergy or apoptosis,we determined whether HIV type 1 (HIV-1) virions incorporatedMHC class I (MHC-I), MHC-II, CD80, or CD86. Microvesicles producedfrom matched uninfected cells were also evaluated. HIV infectionincreased MHC-II expression on T- and B-cell lines, macrophages,and peripheral blood mononclear cells (PBMC) but did not significantlyalter the expression of CD80 or CD86. HIV virions derived fromall MHC-II-positive cell types incorporated high levels of MHC-II,and both virions and microvesicles preferentially incorporatedCD86 compared to CD80. CD45, expressed at high levels on cells,was identified as a protein present at high levels on microvesiclesbut was not detected on HIV-1 virions. Virion-associated, hostcell-derived molecules impacted the ability of noninfectious HIVvirions to trigger death in freshly isolated PBMC. These resultsdemonstrate the preferential incorporation or exclusion of hostcell proteins by budding HIV-1 virions and suggest that host cellproteins present on HIV-1 virions may contribute to the overallpathogenesis of HIV-1infection.

^* Corresponding author: Mailing address: Retroviral Pathogenesis Laboratory, AIDS Vaccine Program, SAIC-Frederick, NationalCancer Institute at Frederick, Building 535, Fifth Floor, Frederick,MD 21702-1201. Phone: (301) 846-5019. Fax: (301) 846-5588. E-mail:lifson{at}avpaxp1.ncifcrf.gov.

Journal of Virology, July 2001, p. 6173-6182, Vol. 75, No. 13
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.13.6173-6182.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

Sato, K., Aoki, J., Misawa, N., Daikoku, E., Sano, K., Tanaka, Y., Koyanagi, Y. (2008). Modulation of Human Immunodeficiency Virus Type 1 Infectivity through Incorporation of Tetraspanin Proteins. J. Virol. 82: 1021-1033 [Abstract] [Full Text]
Monde, K., Maeda, Y., Tanaka, Y., Harada, S., Yusa, K. (2007). Gp120 V3-dependent Impairment of R5 HIV-1 Infectivity Due to Virion-incorporated CCR5. J. Biol. Chem. 282: 36923-36932 [Abstract] [Full Text]
Harman, A. N., Wilkinson, J., Bye, C. R., Bosnjak, L., Stern, J. L., Nicholle, M., Lai, J., Cunningham, A. L. (2006). HIV Induces Maturation of Monocyte-Derived Dendritic Cells and Langerhans Cells. J. Immunol. 177: 7103-7113 [Abstract] [Full Text]
Wahl, S. M., Greenwell-Wild, T., Vazquez, N. (2006). HIV accomplices and adversaries in macrophage infection. J. Leukoc. Biol. 80: 973-983 [Abstract] [Full Text]
Chertova, E., Chertov, O., Coren, L. V., Roser, J. D., Trubey, C. M., Bess, J. W. Jr., Sowder, R. C. II, Barsov, E., Hood, B. L., Fisher, R. J., Nagashima, K., Conrads, T. P., Veenstra, T. D., Lifson, J. D., Ott, D. E. (2006). Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages.. J. Virol. 80: 9039-9052 [Abstract] [Full Text]
Saini, M., Potash, M. J. (2006). Novel Activities of Cyclophilin A and Cyclosporin A during HIV-1 Infection of Primary Lymphocytes and Macrophages. J. Immunol. 177: 443-449 [Abstract] [Full Text]
Booth, A. M., Fang, Y., Fallon, J. K., Yang, J.-M., Hildreth, J. E.K., Gould, S. J. (2006). Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane.. JCB 172: 923-935 [Abstract] [Full Text]
Kolegraff, K., Bostik, P., Ansari, A. A. (2006). Characterization and role of lentivirus-associated host proteins.. Exp. Biol. Med. 231: 252-263 [Abstract] [Full Text]
Kovacs, B., Parry, R. V., Ma, Z., Fan, E., Shivers, D. K., Freiberg, B. A., Thomas, A. K., Rutherford, R., Rumbley, C. A., Riley, J. L., Finkel, T. H. (2005). Ligation of CD28 by Its Natural Ligand CD86 in the Absence of TCR Stimulation Induces Lipid Raft Polarization in Human CD4 T Cells. J. Immunol. 175: 7848-7854 [Abstract] [Full Text]
Chan, L., Nesbeth, D., MacKey, T., Galea-Lauri, J., Gaken, J., Martin, F., Collins, M., Mufti, G., Farzaneh, F., Darling, D. (2005). Conjugation of Lentivirus to Paramagnetic Particles via Nonviral Proteins Allows Efficient Concentration and Infection of Primary Acute Myeloid Leukemia Cells. J. Virol. 79: 13190-13194 [Abstract] [Full Text]
Holm, G. H., Gabuzda, D. (2005). Distinct Mechanisms of CD4+ and CD8+ T-Cell Activation and Bystander Apoptosis Induced by Human Immunodeficiency Virus Type 1 Virions. J. Virol. 79: 6299-6311 [Abstract] [Full Text]
Roy, J., Martin, G., Giguere, J.-F., Belanger, D., Petrin, M., Tremblay, M. J. (2005). HIV Type 1 Can Act as an APC upon Acquisition from the Host Cell of Peptide-Loaded HLA-DR and CD86 Molecules. J. Immunol. 174: 4779-4788 [Abstract] [Full Text]
Ouellet, M., Mercier, S., Pelletier, I., Bounou, S., Roy, J., Hirabayashi, J., Sato, S., Tremblay, M. J. (2005). Galectin-1 Acts as a Soluble Host Factor That Promotes HIV-1 Infectivity through Stabilization of Virus Attachment to Host Cells. J. Immunol. 174: 4120-4126 [Abstract] [Full Text]
Morcock, D. R., Thomas, J. A., Gagliardi, T. D., Gorelick, R. J., Roser, J. D., Chertova, E. N., Bess, J. W. Jr., Ott, D. E., Sattentau, Q. J., Frank, I., Pope, M., Lifson, J. D., Henderson, L. E., Crise, B. J. (2005). Elimination of Retroviral Infectivity by N-Ethylmaleimide with Preservation of Functional Envelope Glycoproteins. J. Virol. 79: 1533-1542 [Abstract] [Full Text]
Beausejour, Y., Tremblay, M. J. (2004). Interaction between the Cytoplasmic Domain of ICAM-1 and Pr55Gag Leads to Acquisition of Host ICAM-1 by Human Immunodeficiency Virus Type 1. J. Virol. 78: 11916-11925 [Abstract] [Full Text]
Chandrashekran, A., Gordon, M. Y., Casimir, C. (2004). Targeted retroviral transduction of c-kit+ hematopoietic cells using novel ligand display technology. Blood 104: 2697-2703 [Abstract] [Full Text]
Giguere, J.-F., Bounou, S., Paquette, J.-S., Madrenas, J., Tremblay, M. J. (2004). Insertion of Host-Derived Costimulatory Molecules CD80 (B7.1) and CD86 (B7.2) into Human Immunodeficiency Virus Type 1 Affects the Virus Life Cycle. J. Virol. 78: 6222-6232 [Abstract] [Full Text]
Hammarstedt, M., Garoff, H. (2004). Passive and Active Inclusion of Host Proteins in Human Immunodeficiency Virus Type 1 Gag Particles during Budding at the Plasma Membrane. J. Virol. 78: 5686-5697 [Abstract] [Full Text]
Holm, G. H., Zhang, C., Gorry, P. R., Peden, K., Schols, D., De Clercq, E., Gabuzda, D. (2004). Apoptosis of Bystander T Cells Induced by Human Immunodeficiency Virus Type 1 with Increased Envelope/Receptor Affinity and Coreceptor Binding Site Exposure. J. Virol. 78: 4541-4551 [Abstract] [Full Text]
Yung, E., Sorin, M., Wang, E.-J., Perumal, S., Ott, D., Kalpana, G. V. (2004). Specificity of Interaction of INI1/hSNF5 with Retroviral Integrases and Its Functional Significance. J. Virol. 78: 2222-2231 [Abstract] [Full Text]
Nguyen, D. G., Booth, A., Gould, S. J., Hildreth, J. E. K. (2003). Evidence That HIV Budding in Primary Macrophages Occurs through the Exosome Release Pathway. J. Biol. Chem. 278: 52347-52354 [Abstract] [Full Text]
Mansharamani, M., Graham, D. R. M., Monie, D., Lee, K. K., Hildreth, J. E. K., Siliciano, R. F., Wilson, K. L. (2003). Barrier-to-Autointegration Factor BAF Binds p55 Gag and Matrix and Is a Host Component of Human Immunodeficiency Virus Type 1 Virions. J. Virol. 77: 13084-13092 [Abstract] [Full Text]
Trubey, C. M., Chertova, E., Coren, L. V., Hilburn, J. M., Hixson, C. V., Nagashima, K., Lifson, J. D., Ott, D. E. (2003). Quantitation of HLA Class II Protein Incorporated into Human Immunodeficiency Type 1 Virions Purified by Anti-CD45 Immunoaffinity Depletion of Microvesicles. J. Virol. 77: 12699-12709 [Abstract] [Full Text]
Gummuluru, S., Rogel, M., Stamatatos, L., Emerman, M. (2003). Binding of Human Immunodeficiency Virus Type 1 to Immature Dendritic Cells Can Occur Independently of DC-SIGN and Mannose Binding C-Type Lectin Receptors via a Cholesterol-Dependent Pathway. J. Virol. 77: 12865-12874 [Abstract] [Full Text]
Gould, S. J., Booth, A. M., Hildreth, J. E. K. (2003). The Trojan exosome hypothesis. Proc. Natl. Acad. Sci. USA 100: 10592-10597 [Abstract] [Full Text]
Pelchen-Matthews, A., Kramer, B., Marsh, M. (2003). Infectious HIV-1 assembles in late endosomes in primary macrophages. JCB 162: 443-455 [Abstract] [Full Text]
Graham, D. R. M., Chertova, E., Hilburn, J. M., Arthur, L. O., Hildreth, J. E. K. (2003). Cholesterol Depletion of Human Immunodeficiency Virus Type 1 and Simian Immunodeficiency Virus with {beta}-Cyclodextrin Inactivates and Permeabilizes the Virions: Evidence for Virion-Associated Lipid Rafts. J. Virol. 77: 8237-8248 [Abstract] [Full Text]
LaBonte, J. A., Madani, N., Sodroski, J. (2003). Cytolysis by CCR5-Using Human Immunodeficiency Virus Type 1 Envelope Glycoproteins Is Dependent on Membrane Fusion and Can Be Inhibited by High Levels of CD4 Expression. J. Virol. 77: 6645-6659 [Abstract] [Full Text]
Briggs, J. A. G., Wilk, T., Fuller, S. D. (2003). Do lipid rafts mediate virus assembly and pseudotyping?. J. Gen. Virol. 84: 757-768 [Abstract] [Full Text]
Giguere, J.-F., Paquette, J.-S., Bounou, S., Cantin, R., Tremblay, M. J. (2002). New Insights into the Functionality of a Virion-Anchored Host Cell Membrane Protein: CD28 Versus HIV Type 1. J. Immunol. 169: 2762-2771 [Abstract] [Full Text]
Chertova, E., Bess, J. W. Jr., Crise, B. J., Sowder II, R. C., Schaden, T. M., Hilburn, J. M., Hoxie, J. A., Benveniste, R. E., Lifson, J. D., Henderson, L. E., Arthur, L. O. (2002). Envelope Glycoprotein Incorporation, Not Shedding of Surface Envelope Glycoprotein (gp120/SU), Is the Primary Determinant of SU Content of Purified Human Immunodeficiency Virus Type 1 and Simian Immunodeficiency Virus. J. Virol. 76: 5315-5325 [Abstract] [Full Text]
Bounou, S., Leclerc, J. E., Tremblay, M. J. (2002). Presence of Host ICAM-1 in Laboratory and Clinical Strains of Human Immunodeficiency Virus Type 1 Increases Virus Infectivity and CD4+-T-Cell Depletion in Human Lymphoid Tissue, a Major Site of Replication In Vivo. J. Virol. 76: 1004-1014 [Abstract] [Full Text]

J. Bacteriol.	Mol. Cell. Biol.	Microbiol. Mol. Biol. Rev.

Clin. Vaccine Immunol.	ALL ASM JOURNALS