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J Virol. 1992 August; 66(8): 4966-4971
The matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions.
X Yu,
X Yuan,
Z Matsuda,
T H Lee and
M Essex
Department of Cancer Biology, Harvard School of Public Health, Boston, Massachusetts 02115.
ABSTRACT
Accumulating evidence suggests that the matrix (MA) protein of retroviruses plays a key role in virus assembly by directing the intracellular transport and membrane association of the Gag polyprotein. In this report, we show that the MA protein of human immunodeficiency virus type 1 is also critical for the incorporation of viral Env proteins into mature virions. Several deletions introduced in the MA domain (p17) of human immunodeficiency virus type 1 Gag polyprotein did not greatly affect the synthesis and processing of the Gag polyprotein or the formation of virions. Analysis of the viral proteins revealed normal levels of Gag and Pol proteins in these mutant virions, but the Env proteins, gp120 and gp41, were hardly detectable in the mutant virions. Our data suggest that an interaction between the viral Env protein and the MA domain of the Gag polyprotein is required for the selective incorporation of Env proteins during virus assembly. Such an interaction appears to be very sensitive to conformational changes in the MA domain, as five small deletions in two separate regions of p17 equally inhibited viral Env protein incorporation. Mutant viruses were not infectious in T cells. When mutant and wild-type DNAs were cotransfected into T cells, the replication of wild-type virus was also hindered. These results suggest that the incorporation of viral Env protein is a critical step for replication of retroviruses and can be a target for the design of antiviral strategies.
J Virol. 1992 August; 66(8): 4966-4971
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-
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-
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-
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-
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-
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-
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-
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-
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[Abstract]
[Full Text]
-
Garoff, H., Hewson, R., Opstelten, D.-J. E.
(1998). Virus Maturation by Budding. Microbiol. Mol. Biol. Rev.
62: 1171-1190
[Abstract]
[Full Text]
-
Wang, C.-T., Lai, H.-Y., Li, J.-J.
(1998). Analysis of Minimal Human Immunodeficiency Virus Type 1 gag Coding Sequences Capable of Virus-Like Particle Assembly and Release. J. Virol.
72: 7950-7959
[Abstract]
[Full Text]
-
Salzwedel, K., West, J. T. Jr., Mulligan, M. J., Hunter, E.
(1998). Retention of the Human Immunodeficiency Virus Type 1 Envelope Glycoprotein in the Endoplasmic Reticulum Does Not Redirect Virus Assembly from the Plasma Membrane. J. Virol.
72: 7523-7531
[Abstract]
[Full Text]
-
Morikawa, Y., Zhang, W.-H., Hockley, D. J., Nermut, M. V., Jones, I. M.
(1998). Detection of a Trimeric Human Immunodeficiency Virus Type 1 Gag Intermediate Is Dependent on Sequences in the Matrix Protein, p17. J. Virol.
72: 7659-7663
[Abstract]
[Full Text]
-
Tewari, D., Goldstein, S. L., Notkins, A. L., Zhou, P.
(1998). cDNA Encoding a Single-Chain Antibody to HIV p17 with Cytoplasmic or Nuclear Retention Signals Inhibits HIV-1 Replication. J. Immunol.
161: 2642-2647
[Abstract]
[Full Text]
-
Garnier, L., Ratner, L., Rovinski, B., Cao, S.-X., Wills, J. W.
(1998). Particle Size Determinants in the Human Immunodeficiency Virus Type 1 Gag Protein. J. Virol.
72: 4667-4677
[Abstract]
[Full Text]
-
Kiernan, R. E., Ono, A., Englund, G., Freed, E. O.
(1998). Role of Matrix in an Early Postentry Step in the Human Immunodeficiency Virus Type 1 Life Cycle. J. Virol.
72: 4116-4126
[Abstract]
[Full Text]
-
Accola, M. A., Hoglund, S., Gottlinger, H. G.
(1998). A Putative alpha -Helical Structure Which Overlaps the Capsid-p2 Boundary in the Human Immunodeficiency Virus Type 1 Gag Precursor Is Crucial for Viral Particle Assembly. J. Virol.
72: 2072-2078
[Abstract]
[Full Text]
-
Lama, J., Trono, D.
(1998). Human Immunodeficiency Virus Type 1 Matrix Protein Interacts with Cellular Protein HO3. J. Virol.
72: 1671-1676
[Abstract]
[Full Text]
-
Bunnell, B. A., Morgan, R. A.
(1998). Gene Therapy for Infectious Diseases. Clin. Microbiol. Rev.
11: 42-56
[Abstract]
[Full Text]
-
Ackerson, B., Rey, O., Canon, J., Krogstad, P.
(1998). Cells with High Cyclophilin A Content Support Replication of Human Immunodeficiency Virus Type 1 Gag Mutants with Decreased Ability To Incorporate Cyclophilin A. J. Virol.
72: 303-308
[Abstract]
[Full Text]
-
Yu, G., Shen, F. S., Sturch, S., Aquino, A., Glazer, R. I., Felsted, R. L.
(1995). Regulation of HIV-1 gag Protein Subcellular Targeting by Protein Kinase C. J. Biol. Chem.
270: 4792-4796
[Abstract]
[Full Text]
-
Rousso, I., Mixon, M. B., Chen, B. K., Kim, P. S.
(2000). Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity. Proc. Natl. Acad. Sci. USA
97: 13523-13525
[Abstract]
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Chen, B. K., Rousso, I., Shim, S., Kim, P. S.
(2001). Efficient assembly of an HIV-1/MLV Gag-chimeric virus in murine cells. Proc. Natl. Acad. Sci. USA
98: 15239-15244
[Abstract]
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