DOI: 10.1128/jvi.73.10.8120-8126.1999. Adaptation of a CCR5-Using, Primary Human Immunodeficiency Virus Type 1 Isolate for CD4-Independent Replication

Adaptation of a CCR5-Using, Primary Human Immunodeficiency Virus Type 1 Isolate for CD4-Independent Replication

10.1128/jvi.73.10.8120-8126.1999

Crossref journal-article

American Society for Microbiology

Journal of Virology (235)

Abstract

ABSTRACTThe gp120 envelope glycoprotein of the human immunodeficiency virus type 1 (HIV-1) promotes virus entry by sequentially binding CD4 and chemokine receptors on the target cell. Primary, clinical HIV-1 isolates require interaction with CD4 to allow gp120 to bind the CCR5 chemokine receptor efficiently. We adapted a primary HIV-1 isolate, ADA, to replicate in CD4-negative canine cells expressing human CCR5. The gp120 changes responsible for the adaptation were limited to alteration of glycosylation addition sites in the V2 loop–V1-V2 stem. The gp120 glycoproteins of the adapted viruses bound CCR5 directly, without prior interaction with CD4. Thus, a major function of CD4 binding in the entry of primary HIV-1 isolates can be bypassed by changes in the gp120 V1-V2 elements, which allow the envelope glycoproteins to assume a conformation competent for CCR5 binding.

Bibliography

Kolchinsky, P., Mirzabekov, T., Farzan, M., Kiprilov, E., Cayabyab, M., Mooney, L. J., Choe, H., & Sodroski, J. (1999). Adaptation of a CCR5-Using, Primary Human Immunodeficiency Virus Type 1 Isolate for CD4-Independent Replication. Journal of Virology, 73(10), 8120â8126.

Authors 8

Peter Kolchinsky (first)
Tajib Mirzabekov (additional)
Michael Farzan (additional)
Enko Kiprilov (additional)
Mark Cayabyab (additional)
Larissa J. Mooney (additional)
Hyeryun Choe (additional)
Joseph Sodroski (additional)

References 78 Referenced 139

10.1126/science.272.5270.1955
Allan J. Lee T. H. McLane M. F. Sodroski J. Haseltine W. Essex M. Identification of the major envelope glycoprotein product of HTLV-III.Science 228 1983 1322 1323 / Science / Identification of the major envelope glycoprotein product of HTLV-III by Allan J. (1983)
10.1126/science.1925547
10.1126/science.2309120
10.1126/science.6189183
10.1093/emboj/16.10.2599
Bugelski P. J. Ellens H. Hart T. K. Kirsh R. L. Soluble CD4 and dextran sulfate mediate release of gp120 from HIV-1: implications for clinical trials.J. Acquir. Immune Defic. Syndr. 4 1991 923 924 / J. Acquir. Immune Defic. Syndr. / Soluble CD4 and dextran sulfate mediate release of gp120 from HIV-1: implications for clinical trials by Bugelski P. J. (1991)
10.1128/JVI.73.2.976-984.1999
10.1016/S0092-8674(00)80205-6
10.1128/jvi.71.4.2705-2714.1997
10.1016/S0092-8674(00)81313-6
10.1128/jvi.66.6.3531-3537.1992
Clavel F. HIV-2, the West African AIDS virus.AIDS 1 1987 135 140 / AIDS / HIV-2, the West African AIDS virus by Clavel F. (1987)
10.1038/nm1196-1244
10.1038/312763a0
10.1038/331082a0
10.1038/381661a0
Denisova G. Raviv D. Mondor I. Sattentau Q. J. Gershoni J. M. Conformational transitions in CD4 due to complexation with HIV-envelope glycoprotein gp120.J. Immunol. 158 1997 1157 1164 (10.4049/jimmunol.158.3.1157) / J. Immunol. / Conformational transitions in CD4 due to complexation with HIV-envelope glycoprotein gp120 by Denisova G. (1997)
10.1146/annurev.iy.08.040190.003013
10.1016/S0092-8674(00)81314-8
10.1038/381667a0
10.1128/JVI.72.1.512-519.1998
10.1097/00002030-199305000-00005
10.1073/pnas.94.26.14742
10.1016/S0092-8674(00)81393-8
10.1016/S0092-8674(00)80577-2
10.7326/0003-4819-100-1-92
10.1126/science.272.5263.872
10.1038/331076a0
10.1128/jvi.67.7.3818-3825.1993
10.1126/science.6200936
10.1073/pnas.88.6.2189
10.1128/jvi.64.5.2416-2420.1990
10.1038/331078a0
10.1126/science.3873705
10.1089/aid.1990.6.1209
10.1038/312767a0
Korber B. Foley B. Kuiken C. Pillai S. Sodroski J. Numbering positions in HIV relative to HXB2 p. IV-27–35.In B. Korber C. Brander B. Haynes R. Koup J. Moore and B. Walker (ed.) Human retroviruses and AIDS 1998. 1998 Los Alamos National Laboratory Los Alamos N.Mex
Korber B. Foley B. Leitner T. McCutchan F. Hahn B. Mellors J. Myers G. Kuiken C. Human retroviruses and AIDS 1997. 1997 Los Alamos National Laboratory Los Alamos N.Mex (10.2172/607510)
10.1038/31405
10.1016/S0021-9258(18)86956-3
10.1126/science.2412295
10.1016/0092-8674(86)90590-8
10.1128/jvi.71.3.2522-2527.1997
10.1126/science.278.5342.1470
Mirzabekov T. N. Bannert M. Farzan W. Hofmann P. Kolchinsky L. Wu R. Wyatt and J. Sodroski. Enhanced expression native purification and characterization of CCR5 a principal HIV-1 coreceptor. J. Biol. Chem. in press.
10.1126/science.2251501
10.1089/aid.1992.8.443
10.1128/jvi.65.3.1133-1140.1991
10.1128/jvi.70.3.1863-1872.1996
10.1128/jvi.68.1.469-484.1994
10.1006/viro.1995.1361
10.1128/jvi.64.12.5701-5707.1990
10.1016/0042-6822(81)90642-5
10.1126/science.280.5371.1949
10.1126/science.2984774
10.1016/S0042-6822(95)80094-8
10.1128/jvi.67.12.7383-7393.1993
10.1084/jem.174.2.407
Schenten D. L. Marcon G. Karlsson C. Parolin T. Kodama N. Gerard and J. Sodroski. Effects of soluble CD4 on simian immunodeficiency virus infection of CD4-positive and CD4-negative cells. Submitted for publication.
10.1111/j.1365-3083.1995.tb03528.x
10.1126/science.3500514
10.1128/jvi.71.9.7136-7139.1997
10.1016/0092-8674(87)90542-3
10.1038/328728a0
10.1128/jvi.69.7.4413-4422.1995
10.1128/JVI.72.6.4694-4703.1998
10.1128/jvi.66.9.5516-5524.1992
10.1128/jvi.67.7.3978-3988.1993
10.1038/331084a0
10.1038/384184a0
10.1038/387426a0
10.1128/jvi.67.5.2566-2574.1993
10.1128/jvi.68.2.1029-1039.1994
10.1038/384179a0
10.1128/jvi.67.8.4557-4565.1993
10.1128/jvi.69.9.5723-5733.1995
10.1038/31514

Dates

Type	When
Created	5 years, 7 months ago (Dec. 31, 2019, 1:19 p.m.)
Deposited	1 year, 11 months ago (Sept. 24, 2023, 11:08 a.m.)
Indexed	4 months, 2 weeks ago (April 8, 2025, 10:44 p.m.)
Issued	25 years, 10 months ago (Oct. 1, 1999)
Published	25 years, 10 months ago (Oct. 1, 1999)
Published Print	25 years, 10 months ago (Oct. 1, 1999)

Funders 0

None

BibTeX

@article{Kolchinsky_1999, title={Adaptation of a CCR5-Using, Primary Human Immunodeficiency Virus Type 1 Isolate for CD4-Independent Replication}, volume={73}, ISSN={1098-5514}, url={http://dx.doi.org/10.1128/jvi.73.10.8120-8126.1999}, DOI={10.1128/jvi.73.10.8120-8126.1999}, number={10}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={Kolchinsky, Peter and Mirzabekov, Tajib and Farzan, Michael and Kiprilov, Enko and Cayabyab, Mark and Mooney, Larissa J. and Choe, Hyeryun and Sodroski, Joseph}, year={1999}, month=oct, pages={8120–8126} }

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