DOI: 10.1128/jvi.01543-07. Escape from the Dominant HLA-B27-Restricted Cytotoxic T-Lymphocyte Response in Gag Is Associated with a Dramatic Reduction in Human Immunodeficiency Virus Type 1 Replication

Escape from the Dominant HLA-B27-Restricted Cytotoxic T-Lymphocyte Response in Gag Is Associated with a Dramatic Reduction in Human Immunodeficiency Virus Type 1 Replication

10.1128/jvi.01543-07

Crossref journal-article

American Society for Microbiology

Journal of Virology (235)

Abstract

ABSTRACTHuman leukocyte antigen (HLA)-B27-positive subjects are uncommon in their ability to control infection with human immunodeficiency virus type 1 (HIV-1). However, late viral escape from a narrowly directed immunodominant Gag-specific CD8+T-lymphocyte (CTL) response has been linked to AIDS progression in these individuals. Identifying the mechanism of the immune-mediated control may provide critical insights into HIV-1 vaccine development. Here, we illustrate that the CTL escape mutation R264K in the HLA-B27-restricted KK10 epitope in the capsid resulted in a significant defect in viral replication in vitro. The R264K variant was impaired in generating late reverse transcription products, indicating that replication was blocked at a postentry step. Notably, the R264K mutation was associated in vivo with the development of a rare secondary mutation, S173A, which restored viral replication in vitro. Furthermore, infectivity of the R264K variant was rescued by the addition of cyclosporine A or infection of a cyclophilin A-deficient cell line. These data demonstrate a severe functional defect imposed by the R264K mutation during an early step in viral replication that is likely due to the inability of this variant to replicate efficiently in the presence of normal levels of cyclophilin A. We conclude that the impact of the R264K substitution on capsid structure constrains viral escape and enables long-term maintenance of the dominant CTL response against B27-KK10, providing an explanation for the protective effect of HLA-B27 during HIV infection.

Bibliography

Schneidewind, A., Brockman, M. A., Yang, R., Adam, R. I., Li, B., Le Gall, S., Rinaldo, C. R., Craggs, S. L., Allgaier, R. L., Power, K. A., Kuntzen, T., Tung, C.-S., LaBute, M. X., Mueller, S. M., Harrer, T., McMichael, A. J., Goulder, P. J. R., Aiken, C., Brander, C., â¦ Allen, T. M. (2007). Escape from the Dominant HLA-B27-Restricted Cytotoxic T-Lymphocyte Response in Gag Is Associated with a Dramatic Reduction in Human Immunodeficiency Virus Type 1 Replication. Journal of Virology, 81(22), 12382â12393.

Authors 21

Arne Schneidewind (first)
Mark A. Brockman (additional)
Ruifeng Yang (additional)
Rahma I. Adam (additional)
Bin Li (additional)
Sylvie Le Gall (additional)
Charles R. Rinaldo (additional)
Sharon L. Craggs (additional)
Rachel L. Allgaier (additional)
Karen A. Power (additional)
Thomas Kuntzen (additional)
Chang-Shung Tung (additional)
Montiago X. LaBute (additional)
Sandra M. Mueller (additional)
Thomas Harrer (additional)
Andrew J. McMichael (additional)
Philip J. R. Goulder (additional)
Christopher Aiken (additional)
Christian Brander (additional)
Anthony D. Kelleher (additional)
Todd M. Allen (additional)

References 80 Referenced 272

10.1128/jvi.70.6.3536-3544.1996
10.1128/JVI.72.1.303-308.1998
10.1073/pnas.88.24.11047
10.1128/JVI.79.21.13239-13249.2005
10.1128/JVI.78.13.7069-7078.2004
10.1038/35030124
10.1097/00002030-200312050-00005
10.1016/j.it.2006.09.007
10.1038/nature01200
10.1371/journal.pmed.0030403
10.1089/aid.2005.21.395
10.1038/415335a
10.1073/pnas.0408773102
10.1128/jvi.70.7.4220-4227.1996
10.1093/emboj/20.6.1300
10.1016/j.jviromet.2005.08.003
10.1097/00002030-199408000-00014
10.1086/345482
10.1074/jbc.274.27.19434
10.1038/sj.gt.3300895
10.1074/jbc.M506314200
10.1128/JVI.00465-07
10.1128/JVI.80.8.3712-3720.2006
10.1128/jvi.76.5.2298-2305.2002
10.1128/JVI.78.16.8927-8930.2004
10.1128/JVI.79.2.869-875.2005
10.1128/JVI.76.11.5667-5677.2002
10.1128/JVI.78.5.2187-2200.2004
10.1006/viro.1996.0421
10.1016/0092-8674(91)90123-G
10.1038/nm998
10.1128/JVI.78.5.2581-2585.2004
10.1016/S0092-8674(00)81823-1
10.1038/nm1333
10.1074/jbc.M505920200
10.1128/JVI.01847-06
10.1126/science.273.5272.231
10.1038/35085576
10.1084/jem.185.8.1423
10.1038/nri1417
10.1038/nm0297-212
10.1128/JVI.79.1.176-183.2005
10.1084/jem.20040511
10.1038/nm0496-405
10.1093/aje/126.2.310
10.1084/jem.193.3.375
10.1038/nature03113
10.1038/nm1520
10.1128/jvi.68.7.4650-4655.1994
10.1038/nm992
10.1128/JVI.01231-06
J. Exp. Med.
10.1128/JVI.80.7.3617-3623.2006
10.1128/JVI.78.7.3233-3243.2004
10.1084/jem.20040432
10.1073/pnas.050567397
10.1128/JVI.77.4.2736-2740.2003
Nietfeld, W., M. Bauer, M. Fevrier, R. Maier, B. Holzwarth, R. Frank, B. Maier, Y. Riviere, and A. Meyerhans. 1995. Sequence constraints and recognition by CTL of an HLA-B27-restricted HIV-1 gag epitope. J. Immunol.154:2189-2197. (10.4049/jimmunol.154.5.2189) / J. Immunol. (1995)
10.1038/336484a0
10.1128/JVI.77.2.882-890.2003
10.1038/nm0502-493
10.1128/JVI.77.16.9029-9040.2003
10.1128/JVI.78.24.13901-13910.2004
10.1128/JVI.79.18.12100-12105.2005
10.1073/pnas.94.5.1890
10.1128/jvi.68.4.2362-2370.1994
10.4049/jimmunol.178.5.2746
10.1126/science.283.5403.857
10.1128/JVI.00708-07
10.1038/372363a0
10.1084/jem.20041006
10.1038/nm910
10.1093/infdis/172.1.88
10.1097/00002030-200002180-00003
Winkelstein, W., Jr., M. Samuel, N. S. Padian, and J. A. Wiley. 1987. Selected sexual practices of San Francisco heterosexual men and risk of infection by the human immunodeficiency virus. JAMA257:1470-1471. / JAMA (1987)
10.1128/jvi.70.9.5799-5806.1996
10.1128/JVI.02634-06
10.1128/JVI.80.10.5074-5077.2006
10.1128/JVI.00068-06
10.1128/JVI.80.6.3122-3125.2006

Dates

Type	When
Created	18 years ago (Sept. 5, 2007, 9:01 p.m.)
Deposited	2 years, 3 months ago (May 13, 2023, 9:41 p.m.)
Indexed	2 months ago (July 2, 2025, 2:13 p.m.)
Issued	17 years, 9 months ago (Nov. 15, 2007)
Published	17 years, 9 months ago (Nov. 15, 2007)
Published Print	17 years, 9 months ago (Nov. 15, 2007)

Funders 0

None

BibTeX

@article{Schneidewind_2007, title={Escape from the Dominant HLA-B27-Restricted Cytotoxic T-Lymphocyte Response in Gag Is Associated with a Dramatic Reduction in Human Immunodeficiency Virus Type 1 Replication}, volume={81}, ISSN={1098-5514}, url={http://dx.doi.org/10.1128/jvi.01543-07}, DOI={10.1128/jvi.01543-07}, number={22}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={Schneidewind, Arne and Brockman, Mark A. and Yang, Ruifeng and Adam, Rahma I. and Li, Bin and Le Gall, Sylvie and Rinaldo, Charles R. and Craggs, Sharon L. and Allgaier, Rachel L. and Power, Karen A. and Kuntzen, Thomas and Tung, Chang-Shung and LaBute, Montiago X. and Mueller, Sandra M. and Harrer, Thomas and McMichael, Andrew J. and Goulder, Philip J. R. and Aiken, Christopher and Brander, Christian and Kelleher, Anthony D. and Allen, Todd M.}, year={2007}, month=nov, pages={12382–12393} }

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