DOI: 10.1128/jvi.77.6.3624-3633.2003. Potential Role for CD63 in CCR5-Mediated Human Immunodeficiency Virus Type 1 Infection of Macrophages [Penn]

Potential Role for CD63 in CCR5-Mediated Human Immunodeficiency Virus Type 1 Infection of Macrophages

10.1128/jvi.77.6.3624-3633.2003

Crossref journal-article

American Society for Microbiology

Journal of Virology (235)

Abstract

ABSTRACTMacrophages and CD4+lymphocytes are the principal target cells for human immunodeficiency virus type 1 (HIV-1) infection, but the molecular details of infection may differ between these cell types. During studies to identify cellular molecules that could be involved in macrophage infection, we observed inhibition of HIV-1 infection of macrophages by monoclonal antibody (MAb) to the tetraspan transmembrane glycoprotein CD63. Pretreatment of primary macrophages with anti-CD63 MAb, but not MAbs to other macrophage cell surface tetraspanins (CD9, CD81, and CD82), was shown to inhibit infection by several R5 and dualtropic strains, but not by X4 isolates. The block to productive infection was postfusion, as assessed by macrophage cell-cell fusion assays, but was prior to reverse transcription, as determined by quantitative PCR assay for new viral DNA formation. The inhibitory effects of anti-CD63 in primary macrophages could not be explained by changes in the levels of CD4, CCR5, or β-chemokines. Infections of peripheral blood lymphocytes and certain cell lines were unaffected by treatment with anti-CD63, suggesting that the role of CD63 in HIV-1 infection may be specific for macrophages.

Bibliography

von Lindern, J. J., Rojo, D., Grovit-Ferbas, K., Yeramian, C., Deng, C., Herbein, G., Ferguson, M. R., Pappas, T. C., Decker, J. M., Singh, A., Collman, R. G., & OâBrien, W. A. (2003). Potential Role for CD63 in CCR5-Mediated Human Immunodeficiency Virus Type 1 Infection of Macrophages. Journal of Virology, 77(6), 3624â3633.

Authors 12

Jana J. von Lindern (first)
Daniel Rojo (additional)
Kathie Grovit-Ferbas (additional)
Christine Yeramian (additional)
Cheng Deng (additional)
Georges Herbein (additional)
Monique R. Ferguson (additional)
Todd C. Pappas (additional)
Julie M. Decker (additional)
Anjali Singh (additional)
Ronald G. Collman (additional)
William A. O'Brien (additional)

References 61 Referenced 67

10.1126/science.272.5270.1955
10.1128/JVI.74.23.10984-10993.2000
10.1128/JVI.72.5.4485-4491.1998
10.1128/JVI.76.3.1004-1014.2002
10.1006/viro.1996.0206
10.1016/S0092-8674(00)81313-6
10.1016/0042-6822(91)90904-P
De Clercq, E., and D. Schols. 2001. Inhibition of HIV infection by CXCR4 and CCR5 chemokine receptor antagonists. Antivir. Chem. Chemother. 12(Suppl. 1): 19-31. / Antivir. Chem. Chemother. (2001)
deParseval, A., D. L. Lerner, P. Borrow, B. J. Willett, and J. H. Elder. 2001. Blocking of feline immunodeficiency virus infection by a monoclonal antibody to CD9 is via inhibition of virus release rather than interference with receptor binding. J. Virol. 71 : 5742-5749. / J. Virol. (2001)
10.1089/aid.1998.14.129
10.1006/viro.1999.9747
10.1016/S0092-8674(00)81314-8
10.1038/381667a0
10.1073/pnas.86.9.3337
10.1128/jvi.71.5.3588-3596.1997
10.1128/jvi.66.3.1394-1401.1992
10.1126/science.3014648
10.1126/science.1905842
10.1073/pnas.98.2.658
Imai, T., K. Fukudome, S. Takagi, M. Nagira, M. Furuse, N. Fukuhara, M. Nishimura, Y. Hinuma, and O. Yoshie. 1992. C33 antigen recognized by monoclonal antibodies inhibitory to human T cell leukemia virus type 1-induced syncytium formation is a member of a new family of transmembrane proteins including CD9, CD37, CD53, and CD63. J. Immunol. 149 : 2879-2886. (10.4049/jimmunol.149.9.2879) / J. Immunol. (1992)
10.1016/S0166-0934(99)00056-7
Koenig, S., H. E. Gendelman, J. M. Orenstein, M. C. Dal Canto, G. H. Pezeshkpour, M. Yungbluth, F. Janotta, A. Aksamit, M. Martin, and A. S. Fauci. 1986. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. J. Acquir. Immune Defic. Syndr. 5 : 1089-1093. / J. Acquir. Immune Defic. Syndr. (1986)
10.1128/JVI.76.4.1802-1815.2002
10.1126/science.274.5287.602
10.1038/6523
10.1128/JVI.74.11.5016-5023.2000
10.1089/088922201300343690
10.1073/pnas.090521697
10.1096/fasebj.11.6.9194523
Mannion, B. A., F. Berditchevski, S. K. Kraeft, L. B. Chen, and M. E. Hemler. 1996. Transmembrane-4 superfamily proteins CD81 (TAPA-1), CD82, CD63, and CD53 specifically associated with integrin α4β1 (CD49d/CD29). J. Immunol. 157 : 2039-2047. (10.4049/jimmunol.157.5.2039) / J. Immunol. (1996)
10.1099/0022-1317-74-1-129
Meltzer, M. S., and H. E. Gendelman. 1992. Mononuclear phagocytes as targets, tissue reservoirs, and immunoregulatory cells in human immunodeficiency virus disease. Curr. Top. Microbiol. Immunol. 181 : 239-263. / Curr. Top. Microbiol. Immunol. (1992)
10.1016/0167-5699(90)90086-O
10.1016/S0021-9258(18)49980-2
10.1128/JVI.74.7.3264-3272.2000
10.1182/blood-2001-11-0087
10.4049/jimmunol.168.8.4121
10.1006/excr.2002.5522
10.1038/348069a0
10.1126/science.276.5320.1857
10.1089/aid.1993.9.1157
10.1126/science.282.5390.938
10.1128/JVI.72.4.2855-2864.1998
10.1128/JVI.76.10.4709-4722.2002
10.1172/JCI115559
10.1002/eji.1830261117
10.1128/JVI.72.6.4633-4642.1998
10.1126/science.2981429
Skubitz, K. M., K. D. Campbell, J. Iida, and A. P. Skubitz. 1996. CD63 associates with tyrosine kinase activity and CD11/CD18, and transmits an activation signal in neutrophils. J. Immunol. 157 : 3617-3626. (10.4049/jimmunol.157.8.3617) / J. Immunol. (1996)
10.1073/pnas.221375398
10.1128/AAC.45.12.3538-3543.2001
10.1128/JVI.75.15.6776-6785.2001
10.1111/1523-1747.ep12525402
10.1006/viro.1997.8606
10.1084/jem.190.5.591
10.1128/AAC.46.6.1896-1905.2002
10.1073/pnas.83.18.7089
10.1006/exmp.1999.2299
10.1128/JVI.73.9.7117-7125.1999
10.1056/NEJM199812173392502
10.1126/science.8356453

Dates

Type	When
Created	22 years, 6 months ago (Feb. 27, 2003, 6:28 p.m.)
Deposited	2 years, 4 months ago (April 25, 2023, 5:09 p.m.)
Indexed	4 months, 1 week ago (April 18, 2025, 6:06 a.m.)
Issued	22 years, 5 months ago (March 15, 2003)
Published	22 years, 5 months ago (March 15, 2003)
Published Print	22 years, 5 months ago (March 15, 2003)

Funders 0

None

BibTeX

@article{von_Lindern_2003, title={Potential Role for CD63 in CCR5-Mediated Human Immunodeficiency Virus Type 1 Infection of Macrophages}, volume={77}, ISSN={1098-5514}, url={http://dx.doi.org/10.1128/jvi.77.6.3624-3633.2003}, DOI={10.1128/jvi.77.6.3624-3633.2003}, number={6}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={von Lindern, Jana J. and Rojo, Daniel and Grovit-Ferbas, Kathie and Yeramian, Christine and Deng, Cheng and Herbein, Georges and Ferguson, Monique R. and Pappas, Todd C. and Decker, Julie M. and Singh, Anjali and Collman, Ronald G. and O’Brien, William A.}, year={2003}, month=mar, pages={3624–3633} }

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