Inhibition of viral assembly in murine cells by HIV-1 matrix

Hübner, Wolfgang; Chen, Benjamin K

Inhibition of viral assembly in murine cells by HIV-1 matrix

Hübner W, Chen BK (2006)
Virology 352(1): 27-38.

Zeitschriftenaufsatz | Veröffentlicht | Englisch

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DOI

https://doi.org/10.1016/j.virol.2006.04.024

Autor*in

Hübner, Wolfgang^UniBi ; Chen, Benjamin K

Einrichtung

Fakultät für Physik > AG Biomolekulare Photonik

Abstract / Bemerkung

In human cells, the N-terminal matrix (MA) domain of the human immunodeficiency virus type 1 (HIV-1) Gag targets assembly to specific membrane compartments. In murine fibroblasts, membrane targeting of Gag and assembly of HIV-1 are inefficient. These deficiencies are relieved by replacement of HIV-1 MA with murine leukemia virus (MLV) MA in chimeric proviruses. In this study, we examined chimeric HIV-1 carrying tandem MLV and HIV-1 MA domains and found that the addition of MLV MA to the N-terminus of HIV-1 Gag enhanced membrane binding in murine cells, but was not sufficient to stimulate virus production. Removal of HIV MA was required to observe more efficient Gag processing and increased virus production in murine cells. Deletion of the globular head of MA also alleviated the blocks to membrane binding and Gag processing in murine cells, yet did not lead to increased virus production. These MA-dependent, cell-type-specific phenotypes suggest that host factors interact with the globular head of MA to regulate membrane binding and additional membrane-independent step(s) required for assembly.

Stichworte

Murine/genetics; Leukemia Virus; Humans; HIV-1/pathogenicity; HIV-1/metabolism; HIV-1/genetics; HIV-1/chemistry; HIV Antigens/physiology; HIV Antigens/genetics; HIV Antigens/chemistry; gag/physiology; Gene Products; gag/genetics; Gene Products; gag/chemistry; Gene Products; Viral; Gene Expression Regulation; Gene Deletion; Chimera; Cell Membrane/virology; Cell Membrane/metabolism; Cell Line; 3T3 Cells; Animals; Leukemia Virus; Murine/metabolism; Mice; Viral Matrix Proteins/physiology; Viral Proteins/chemistry; Viral Proteins/genetics; Viral Proteins/physiology; Virus Assembly/drug effects; gag Gene Products; Human Immunodeficiency Virus

Erscheinungsjahr

2006

Zeitschriftentitel

Virology

Band

352

Ausgabe

Seite(n)

27-38

ISSN

0042-6822

Page URI

https://pub.uni-bielefeld.de/record/2576961

Zitieren

Hübner W, Chen BK. Inhibition of viral assembly in murine cells by HIV-1 matrix. Virology. 2006;352(1):27-38.

Hübner, W., & Chen, B. K. (2006). Inhibition of viral assembly in murine cells by HIV-1 matrix. Virology, 352(1), 27-38. doi:10.1016/j.virol.2006.04.024

Hübner, Wolfgang, and Chen, Benjamin K. 2006. “Inhibition of viral assembly in murine cells by HIV-1 matrix”. Virology 352 (1): 27-38.

Hübner, W., and Chen, B. K. (2006). Inhibition of viral assembly in murine cells by HIV-1 matrix. Virology 352, 27-38.

Hübner, W., & Chen, B.K., 2006. Inhibition of viral assembly in murine cells by HIV-1 matrix. Virology, 352(1), p 27-38.

W. Hübner and B.K. Chen, “Inhibition of viral assembly in murine cells by HIV-1 matrix”, Virology, vol. 352, 2006, pp. 27-38.

Hübner, W., Chen, B.K.: Inhibition of viral assembly in murine cells by HIV-1 matrix. Virology. 352, 27-38 (2006).

Hübner, Wolfgang, and Chen, Benjamin K. “Inhibition of viral assembly in murine cells by HIV-1 matrix”. Virology 352.1 (2006): 27-38.

Daten bereitgestellt von European Bioinformatics Institute (EBI)

11 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Mice transgenic for equine cyclin T1 and ELR1 are susceptible to equine infectious anemia virus infection.
Du C, Ma J, Liu Q, Li YF, He XJ, Lin YZ, Wang XF, Meng QW, Wang X, Zhou JH., Retrovirology 12(), 2015
PMID: 25928027

Retroviral matrix and lipids, the intimate interaction.
Hamard-Peron E, Muriaux D., Retrovirology 8(), 2011
PMID: 21385335

Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain.
Chukkapalli V, Oh SJ, Ono A., Proc Natl Acad Sci U S A 107(4), 2010
PMID: 20080620

Replication of equine infectious anemia virus in engineered mouse NIH 3T3 cells.
Zhang B, Montelaro RC., J Virol 83(4), 2009
PMID: 19073738

HIV-1 matrix dependent membrane targeting is regulated by Gag mRNA trafficking.
Jin J, Sturgeon T, Weisz OA, Mothes W, Montelaro RC., PLoS One 4(8), 2009
PMID: 19662089

Analysis of human immunodeficiency virus matrix domain replacements.
Scholz I, Still A, Dhenub TC, Coday K, Webb M, Barklis E., Virology 371(2), 2008
PMID: 17996264

Relief of preintegration inhibition and characterization of additional blocks for HIV replication in primary mouse T cells.
Zhang JX, Diehl GE, Littman DR., PLoS One 3(4), 2008
PMID: 18446227

Inability of human immunodeficiency virus type 1 produced in murine cells to selectively incorporate primer formula.
Wei M, Yang Y, Niu M, Desfosse L, Kennedy R, Musier-Forsyth K, Kleiman L., J Virol 82(24), 2008
PMID: 18842718

Isolation and characterization of mouse-human microcell hybrid cell clones permissive for infectious HIV particle release.
Coskun AK, van Maanen M, Janka D, Stockton D, Stankiewicz P, Yatsenko S, Sutton RE., Virology 362(2), 2007
PMID: 17270231

Sequence of human immunodeficiency virus type 1 (HIV-1) Gag localization and oligomerization monitored with live confocal imaging of a replication-competent, fluorescently tagged HIV-1.
Hübner W, Chen P, Del Portillo A, Liu Y, Gordon RE, Chen BK., J Virol 81(22), 2007
PMID: 17728233

Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses.
Chen P, Hübner W, Spinelli MA, Chen BK., J Virol 81(22), 2007
PMID: 17728240

41 References

Daten bereitgestellt von Europe PubMed Central.

Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone.
Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA., J. Virol. 59(2), 1986
PMID: 3016298

Multiple blocks to human immunodeficiency virus type 1 replication in rodent cells.
Bieniasz PD, Cullen BR., J. Virol. 74(21), 2000
PMID: 11024113

Structure-function studies of the human immunodeficiency virus type 1 matrix protein, p17.
Cannon PM, Matthews S, Clark N, Byles ED, Iourin O, Hockley DJ, Kingsman SM, Kingsman AJ., J. Virol. 71(5), 1997
PMID: 9094619

Distinct modes of human immunodeficiency virus type 1 proviral latency revealed by superinfection of nonproductively infected cell lines with recombinant luciferase-encoding viruses.
Chen BK, Saksela K, Andino R, Baltimore D., J. Virol. 68(2), 1994
PMID: 7507183

Efficient assembly of an HIV-1/MLV Gag-chimeric virus in murine cells.
Chen BK, Rousso I, Shim S, Kim PS., Proc. Natl. Acad. Sci. U.S.A. 98(26), 2001
PMID: 11742097

Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes.
Connor RI, Chen BK, Choe S, Landau NR., Virology 206(2), 1995
PMID: 7531918

Functional exchange of an oncoretrovirus and a lentivirus matrix protein.
Deminie CA, Emerman M., J. Virol. 68(7), 1994
PMID: 8207817

AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly.
Dong X, Li H, Derdowski A, Ding L, Burnett A, Chen X, Peters TR, Dermody TS, Woodruff E, Wang JJ, Spearman P., Cell 120(5), 2005
PMID: 15766529

A large deletion in the matrix domain of the human immunodeficiency virus gag gene redirects virus particle assembly from the plasma membrane to the endoplasmic reticulum.
Facke M, Janetzko A, Shoeman RL, Krausslich HG., J. Virol. 67(8), 1993
PMID: 8331736

HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor.
Feng Y, Broder CC, Kennedy PE, Berger EA., Science 272(5263), 1996
PMID: 8629022

The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein.
Garber ME, Wei P, KewalRamani VN, Mayall TP, Herrmann CH, Rice AP, Littman DR, Jones KA., Genes Dev. 12(22), 1998
PMID: 9832504

Specific incorporation of heat shock protein 70 family members into primate lentiviral virions.
Gurer C, Cimarelli A, Luban J., J. Virol. 76(9), 2002
PMID: 11932435

Matrix-induced inhibition of membrane binding contributes to human immunodeficiency virus type 1 particle assembly defects in murine cells.
Hatziioannou T, Martin-Serrano J, Zang T, Bieniasz PD., J. Virol. 79(24), 2005
PMID: 16306631

Ability of small animal cells to support the postintegration phase of human immunodeficiency virus type-1 replication.
Koito A, Shigekane H, Matsushita S., Virology 305(1), 2003
PMID: 12504551

Efficient particle formation can occur if the matrix domain of human immunodeficiency virus type 1 Gag is substituted by a myristylation signal.
Lee PP, Linial ML., J. Virol. 68(10), 1994
PMID: 7521919

Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains.
Lindwasser OW, Resh MD., J. Virol. 75(17), 2001
PMID: 11483736

The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain.
Maddon PJ, Dalgleish AG, McDougal JS, Clapham PR, Weiss RA, Axel R., Cell 47(3), 1986
PMID: 3094962

A block to human immunodeficiency virus type 1 assembly in murine cells.
Mariani R, Rutter G, Harris ME, Hope TJ, Krausslich HG, Landau NR., J. Virol. 74(8), 2000
PMID: 10729160

Mouse-human heterokaryons support efficient human immunodeficiency virus type 1 assembly.
Mariani R, Rasala BA, Rutter G, Wiegers K, Brandt SM, Krausslich HG, Landau NR., J. Virol. 75(7), 2001
PMID: 11238841

Construction and characterization of a fluorescently labeled infectious human immunodeficiency virus type 1 derivative.
Muller B, Daecke J, Fackler OT, Dittmar MT, Zentgraf H, Krausslich HG., J. Virol. 78(19), 2004
PMID: 15367647

Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus.
Ono A, Freed EO., J. Virol. 73(5), 1999
PMID: 10196310

Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body.
Ono A, Freed EO., J. Virol. 78(3), 2004
PMID: 14722309

Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly.
Ono A, Orenstein JM, Freed EO., J. Virol. 74(6), 2000
PMID: 10684302

Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane.
Ono A, Ablan SD, Lockett SJ, Nagashima K, Freed EO., Proc. Natl. Acad. Sci. U.S.A. 101(41), 2004
PMID: 15465916

Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of gag membrane targeting.
Paillart JC, Gottlinger HG., J. Virol. 73(4), 1999
PMID: 10074105

Human immunodeficiency virus type 1 matrix inhibits and confers cooperativity on gag precursor-membrane interactions.
Perez-Caballero D, Hatziioannou T, Martin-Serrano J, Bieniasz PD., J. Virol. 78(17), 2004
PMID: 15308748

Chimeric human immunodeficiency virus type 1 containing murine leukemia virus matrix assembles in murine cells.
Reed M, Mariani R, Sheppard L, Pekrun K, Landau NR, Soong NW., J. Virol. 76(1), 2002
PMID: 11739711

Efficient HIV-1 replication can occur in the absence of the viral matrix protein.
Reil H, Bukovsky AA, Gelderblom HR, Gottlinger HG., EMBO J. 17(9), 1998
PMID: 9564051

A myristoyl switch regulates membrane binding of HIV-1 Gag.
Resh MD., Proc. Natl. Acad. Sci. U.S.A. 101(2), 2004
PMID: 14707265

A single amino acid substitution within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus.
Rhee SS, Hunter E., Cell 63(1), 1990
PMID: 2170021

Amino acid substitutions within the matrix protein of type D retroviruses affect assembly, transport and membrane association of a capsid.
Rhee SS, Hunter E., EMBO J. 10(3), 1991
PMID: 1705884

The Vif and Gag proteins of human immunodeficiency virus type 1 colocalize in infected human T cells.
Simon JH, Fouchier RA, Southerling TE, Guerra CB, Grant CK, Malim MH., J. Virol. 71(7), 1997
PMID: 9188594

Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly.
Spearman P, Wang JJ, Vander Heyden N, Ratner L., J. Virol. 68(5), 1994
PMID: 8151785

Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism.
Spearman P, Horton R, Ratner L, Kuli-Zade I., J. Virol. 71(9), 1997
PMID: 9261380

Retroviral mRNA nuclear export elements regulate protein function and virion assembly.
Swanson CM, Puffer BA, Ahmad KM, Doms RW, Malim MH., EMBO J. 23(13), 2004
PMID: 15201866

Entropic switch regulates myristate exposure in the HIV-1 matrix protein.
Tang C, Loeliger E, Luncsford P, Kinde I, Beckett D, Summers MF., Proc. Natl. Acad. Sci. U.S.A. 101(2), 2003
PMID: 14699046

Assembly and release of human immunodeficiency virus type 1 Gag proteins containing tandem repeats of the matrix protein coding sequences in the matrix domain.
Wang CT, Chen SS, Chiang CC., Virology 278(1), 2000
PMID: 11112503

Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor.
Yuan X, Yu X, Lee TH, Essex M., J. Virol. 67(11), 1993
PMID: 8411340

Human p32 protein relieves a post-transcriptional block to HIV replication in murine cells.
Zheng YH, Yu HF, Peterlin BM., Nat. Cell Biol. 5(7), 2003
PMID: 12833064

Differential membrane binding of the human immunodeficiency virus type 1 matrix protein.
Zhou W, Resh MD., J. Virol. 70(12), 1996
PMID: 8970978

Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids.
Zhou W, Parent LJ, Wills JW, Resh MD., J. Virol. 68(4), 1994
PMID: 8139035

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