Previous Article | Next Article 
Journal of Virology, December 2006, p. 11710-11722, Vol. 80, No. 23
0022-538X/06/$08.00+0 doi:10.1128/JVI.01038-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
Inhibition of
-Primed Reverse Transcription by Human APOBEC3G during Human Immunodeficiency Virus Type 1 Replication
Fei Guo,1
Shan Cen,1,2
Meijuan Niu,1
Jenan Saadatmand,1,2 and
Lawrence Kleiman1,2,3*
Lady Davis Institute for Medical Research and McGill AIDS Centre, Jewish General Hospital,1
Departments of Medicine,2
Microbiology & Immunology, McGill University, Montreal, Quebec, Canada H3T 1E23
Received 20 June 2006/
Accepted 15 September 2006
Cells are categorized as being permissive or nonpermissive according to their ability to produce infectious human immunodeficiency virus type 1 (HIV-1) lacking the viral protein Vif. Nonpermissive cells express the human cytidine deaminase APOBEC3G (hA3G), and Vif has been shown to bind to APOBEC3G and facilitate its degradation. Vif-negative HIV-1 virions produced in nonpermissive cells incorporate hA3G and have a severely reduced ability to produce viral DNA in newly infected cells. While it has been proposed that the reduction in DNA production is due to hA3G-facilitated deamination of cytidine, followed by DNA degradation, we provide evidence here that a decrease in the synthesis of the DNA by reverse transcriptase may account for a significant part of this reduction. During the infection of cells with Vif-negative HIV-1 produced from 293T cells transiently expressing hA3G, much of the inhibition of early (
50% reduction) and late (
95% reduction) viral DNA production, and of viral infectivity (
95% reduction), can occur independently of DNA deamination. The inhibition of the production of early minus-sense strong stop DNA is also correlated with a similar inability of tRNA3Lys to prime reverse transcription. A similar reduction in tRNA3Lys priming and viral infectivity is also seen in the naturally nonpermissive cell H9, albeit at significantly lower levels of hA3G expression.
* Corresponding author. Mailing address: Lady Davis Institute for Medical Research, Jewish General Hospital, 3755 Cote St. Catherine Rd., Montreal, Quebec, Canada H3T 1E2. Phone: (514) 340-8260. Fax: (514) 340-7502. E-mail:
lawrence.kleiman{at}mcgill.ca.
Published ahead of print on 13 September 2006.
Journal of Virology, December 2006, p. 11710-11722, Vol. 80, No. 23
0022-538X/06/$08.00+0 doi:10.1128/JVI.01038-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Zhen, A., Wang, T., Zhao, K., Xiong, Y., Yu, X.-F.
(2010). A Single Amino Acid Difference in Human APOBEC3H Variants Determines HIV-1 Vif Sensitivity. J. Virol.
84: 1902-1911
[Abstract]
[Full Text]
-
Bulliard, Y., Turelli, P., Rohrig, U. F., Zoete, V., Mangeat, B., Michielin, O., Trono, D.
(2009). Functional Analysis and Structural Modeling of Human APOBEC3G Reveal the Role of Evolutionarily Conserved Elements in the Inhibition of Human Immunodeficiency Virus Type 1 Infection and Alu Transposition. J. Virol.
83: 12611-12621
[Abstract]
[Full Text]
-
Koning, F. A., Newman, E. N. C., Kim, E.-Y., Kunstman, K. J., Wolinsky, S. M., Malim, M. H.
(2009). Defining APOBEC3 Expression Patterns in Human Tissues and Hematopoietic Cell Subsets. J. Virol.
83: 9474-9485
[Abstract]
[Full Text]
-
Chen, G., He, Z., Wang, T., Xu, R., Yu, X.-F.
(2009). A Patch of Positively Charged Amino Acids Surrounding the Human Immunodeficiency Virus Type 1 Vif SLVx4Yx9Y Motif Influences Its Interaction with APOBEC3G. J. Virol.
83: 8674-8682
[Abstract]
[Full Text]
-
Vetter, M. L., D'Aquila, R. T.
(2009). Cytoplasmic APOBEC3G Restricts Incoming Vif-Positive Human Immunodeficiency Virus Type 1 and Increases Two-Long Terminal Repeat Circle Formation in Activated T-Helper-Subtype Cells. J. Virol.
83: 8646-8654
[Abstract]
[Full Text]
-
Guo, F., Saadatmand, J., Niu, M., Kleiman, L.
(2009). Roles of Gag and NCp7 in Facilitating Formula Annealing to Viral RNA in Human Immunodeficiency Virus Type 1. J. Virol.
83: 8099-8107
[Abstract]
[Full Text]
-
Henriet, S., Mercenne, G., Bernacchi, S., Paillart, J.-C., Marquet, R.
(2009). Tumultuous Relationship between the Human Immunodeficiency Virus Type 1 Viral Infectivity Factor (Vif) and the Human APOBEC-3G and APOBEC-3F Restriction Factors. Microbiol. Mol. Biol. Rev.
73: 211-232
[Abstract]
[Full Text]
-
Malim, M. H
(2009). APOBEC proteins and intrinsic resistance to HIV-1 infection. Phil Trans R Soc B
364: 675-687
[Abstract]
[Full Text]
-
Chiu, Y.-L., Greene, W. C
(2009). APOBEC3G: an intracellular centurion. Phil Trans R Soc B
364: 689-703
[Abstract]
[Full Text]
-
Tan, L., Sarkis, P. T. N., Wang, T., Tian, C., Yu, X.-F.
(2009). Sole copy of Z2-type human cytidine deaminase APOBEC3H has inhibitory activity against retrotransposons and HIV-1. FASEB J.
23: 279-287
[Abstract]
[Full Text]
-
Wei, M., Yang, Y., Niu, M., Desfosse, L., Kennedy, R., Musier-Forsyth, K., Kleiman, L.
(2008). Inability of Human Immunodeficiency Virus Type 1 Produced in Murine Cells To Selectively Incorporate Primer Formula. J. Virol.
82: 12049-12059
[Abstract]
[Full Text]
-
Bennett, R. P., Salter, J. D., Liu, X., Wedekind, J. E., Smith, H. C.
(2008). APOBEC3G Subunits Self-associate via the C-terminal Deaminase Domain. J. Biol. Chem.
283: 33329-33336
[Abstract]
[Full Text]
-
Watashi, K., Khan, M., Yedavalli, V. R. K., Yeung, M. L., Strebel, K., Jeang, K.-T.
(2008). Human Immunodeficiency Virus Type 1 Replication and Regulation of APOBEC3G by Peptidyl Prolyl Isomerase Pin1. J. Virol.
82: 9928-9936
[Abstract]
[Full Text]
-
Lee, Y. N., Malim, M. H., Bieniasz, P. D.
(2008). Hypermutation of an Ancient Human Retrovirus by APOBEC3G. J. Virol.
82: 8762-8770
[Abstract]
[Full Text]
-
Armitage, A. E., Katzourakis, A., de Oliveira, T., Welch, J. J., Belshaw, R., Bishop, K. N., Kramer, B., McMichael, A. J., Rambaut, A., Iversen, A. K. N.
(2008). Conserved Footprints of APOBEC3G on Hypermutated Human Immunodeficiency Virus Type 1 and Human Endogenous Retrovirus HERV-K(HML2) Sequences. J. Virol.
82: 8743-8761
[Abstract]
[Full Text]
-
Land, A. M., Ball, T. B., Luo, M., Pilon, R., Sandstrom, P., Embree, J. E., Wachihi, C., Kimani, J., Plummer, F. A.
(2008). Human Immunodeficiency Virus (HIV) Type 1 Proviral Hypermutation Correlates with CD4 Count in HIV-Infected Women from Kenya. J. Virol.
82: 8172-8182
[Abstract]
[Full Text]
-
Nguyen, D. H., Hu, J.
(2008). Reverse Transcriptase- and RNA Packaging Signal-Dependent Incorporation of APOBEC3G into Hepatitis B Virus Nucleocapsids. J. Virol.
82: 6852-6861
[Abstract]
[Full Text]
-
Knoepfel, S. A., Salisch, N. C., Huelsmann, P. M., Rauch, P., Walter, H., Metzner, K. J.
(2008). Comparison of G-to-A Mutation Frequencies Induced by APOBEC3 Proteins in H9 Cells and Peripheral Blood Mononuclear Cells in the Context of Impaired Processivities of Drug-Resistant Human Immunodeficiency Virus Type 1 Reverse Transcriptase Variants. J. Virol.
82: 6536-6545
[Abstract]
[Full Text]
-
Gallois-Montbrun, S., Holmes, R. K., Swanson, C. M., Fernandez-Ocana, M., Byers, H. L., Ward, M. A., Malim, M. H.
(2008). Comparison of Cellular Ribonucleoprotein Complexes Associated with the APOBEC3F and APOBEC3G Antiviral Proteins. J. Virol.
82: 5636-5642
[Abstract]
[Full Text]
-
Langlois, M.-A., Neuberger, M. S.
(2008). Human APOBEC3G Can Restrict Retroviral Infection in Avian Cells and Acts Independently of both UNG and SMUG1. J. Virol.
82: 4660-4664
[Abstract]
[Full Text]
-
Dang, Y., Siew, L. M., Wang, X., Han, Y., Lampen, R., Zheng, Y.-H.
(2008). Human Cytidine Deaminase APOBEC3H Restricts HIV-1 Replication. J. Biol. Chem.
283: 11606-11614
[Abstract]
[Full Text]
-
Bennett, R. P., Presnyak, V., Wedekind, J. E., Smith, H. C.
(2008). Nuclear Exclusion of the HIV-1 Host Defense Factor APOBEC3G Requires a Novel Cytoplasmic Retention Signal and Is Not Dependent on RNA Binding. J. Biol. Chem.
283: 7320-7327
[Abstract]
[Full Text]
-
Iwatani, Y., Chan, D. S.B., Wang, F., Maynard, K. S., Sugiura, W., Gronenborn, A. M., Rouzina, I., Williams, M. C., Musier-Forsyth, K., Levin, J. G.
(2007). Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res
35: 7096-7108
[Abstract]
[Full Text]
-
Wiegand, H. L., Cullen, B. R.
(2007). Inhibition of Alpharetrovirus Replication by a Range of Human APOBEC3 Proteins. J. Virol.
81: 13694-13699
[Abstract]
[Full Text]
-
Miyagi, E., Opi, S., Takeuchi, H., Khan, M., Goila-Gaur, R., Kao, S., Strebel, K.
(2007). Enzymatically Active APOBEC3G Is Required for Efficient Inhibition of Human Immunodeficiency Virus Type 1. J. Virol.
81: 13346-13353
[Abstract]
[Full Text]
-
Wang, T., Tian, C., Zhang, W., Luo, K., Sarkis, P. T. N., Yu, L., Liu, B., Yu, Y., Yu, X.-F.
(2007). 7SL RNA Mediates Virion Packaging of the Antiviral Cytidine Deaminase APOBEC3G. J. Virol.
81: 13112-13124
[Abstract]
[Full Text]
-
Li, X.-Y., Guo, F., Zhang, L., Kleiman, L., Cen, S.
(2007). APOBEC3G Inhibits DNA Strand Transfer during HIV-1 Reverse Transcription. J. Biol. Chem.
282: 32065-32074
[Abstract]
[Full Text]
-
Guo, F., Cen, S., Niu, M., Yang, Y., Gorelick, R. J., Kleiman, L.
(2007). The Interaction of APOBEC3G with Human Immunodeficiency Virus Type 1 Nucleocapsid Inhibits tRNA3Lys Annealing to Viral RNA. J. Virol.
81: 11322-11331
[Abstract]
[Full Text]
-
Niewiadomska, A. M., Tian, C., Tan, L., Wang, T., Sarkis, P. T. N., Yu, X.-F.
(2007). Differential Inhibition of Long Interspersed Element 1 by APOBEC3 Does Not Correlate with High-Molecular-Mass-Complex Formation or P-Body Association. J. Virol.
81: 9577-9583
[Abstract]
[Full Text]
-
Henriet, S., Sinck, L., Bec, G., Gorelick, R. J., Marquet, R., Paillart, J.-C.
(2007). Vif is a RNA chaperone that could temporally regulate RNA dimerization and the early steps of HIV-1 reverse transcription. Nucleic Acids Res
35: 5141-5153
[Abstract]
[Full Text]
-
Luo, K., Wang, T., Liu, B., Tian, C., Xiao, Z., Kappes, J., Yu, X.-F.
(2007). Cytidine Deaminases APOBEC3G and APOBEC3F Interact with Human Immunodeficiency Virus Type 1 Integrase and Inhibit Proviral DNA Formation. J. Virol.
81: 7238-7248
[Abstract]
[Full Text]
-
Mbisa, J. L., Barr, R., Thomas, J. A., Vandegraaff, N., Dorweiler, I. J., Svarovskaia, E. S., Brown, W. L., Mansky, L. M., Gorelick, R. J., Harris, R. S., Engelman, A., Pathak, V. K.
(2007). Human Immunodeficiency Virus Type 1 cDNAs Produced in the Presence of APOBEC3G Exhibit Defects in Plus-Strand DNA Transfer and Integration. J. Virol.
81: 7099-7110
[Abstract]
[Full Text]
-
Kinomoto, M., Kanno, T., Shimura, M., Ishizaka, Y., Kojima, A., Kurata, T., Sata, T., Tokunaga, K.
(2007). All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res
35: 2955-2964
[Abstract]
[Full Text]
-
Gallois-Montbrun, S., Kramer, B., Swanson, C. M., Byers, H., Lynham, S., Ward, M., Malim, M. H.
(2007). Antiviral Protein APOBEC3G Localizes to Ribonucleoprotein Complexes Found in P Bodies and Stress Granules. J. Virol.
81: 2165-2178
[Abstract]
[Full Text]