Membrane Interaction of Retroviral Gag Proteins

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2014 May 9

PMID 24808894

Citations 43

Authors

Robert A Dick

Volker M Vogt

Affiliations

Soon will be listed here.

Abstract

Assembly of an infectious retroviral particle relies on multimerization of the Gag polyprotein at the inner leaflet of the plasma membrane. The three domains of Gag common to all retroviruses - MA, CA, and NC - provide the signals for membrane binding, assembly, and viral RNA packaging, respectively. These signals do not function independently of one another. For example, Gag multimerization enhances membrane binding and is more efficient when NC is interacting with RNA. MA binding to the plasma membrane is governed by several principles, including electrostatics, recognition of specific lipid head groups, hydrophobic interactions, and membrane order. HIV-1 uses many of these principles while Rous sarcoma virus (RSV) appears to use fewer. This review describes the principles that govern Gag interactions with membranes, focusing on RSV and HIV-1 Gag. The review also defines lipid and membrane behavior, and discusses the complexities in determining how lipid and membrane behavior impact Gag membrane binding.

Citing Articles

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References

Shkriabai N, Datta S, Zhao Z, Hess S, Rein A, Kvaratskhelia M . Interactions of HIV-1 Gag with assembly cofactors. Biochemistry. 2006; 45(13):4077-83. DOI: 10.1021/bi052308e. View

Lingappa J, Hill R, Wong M, Hegde R . A multistep, ATP-dependent pathway for assembly of human immunodeficiency virus capsids in a cell-free system. J Cell Biol. 1997; 136(3):567-81. PMC: 2134302. DOI: 10.1083/jcb.136.3.567. View

Hogue I, Hoppe A, Ono A . Quantitative fluorescence resonance energy transfer microscopy analysis of the human immunodeficiency virus type 1 Gag-Gag interaction: relative contributions of the CA and NC domains and membrane binding. J Virol. 2009; 83(14):7322-36. PMC: 2704781. DOI: 10.1128/JVI.02545-08. View

Ono A, Orenstein J, Freed E . Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J Virol. 2000; 74(6):2855-66. PMC: 111776. DOI: 10.1128/jvi.74.6.2855-2866.2000. View

Silvius J, Bhagatji P, Leventis R, Terrone D . K-ras4B and prenylated proteins lacking "second signals" associate dynamically with cellular membranes. Mol Biol Cell. 2005; 17(1):192-202. PMC: 1345658. DOI: 10.1091/mbc.e05-05-0408. View

Charlier L, Louet M, Chaloin L, Fuchs P, Martinez J, Muriaux D . Coarse-grained simulations of the HIV-1 matrix protein anchoring: revisiting its assembly on membrane domains. Biophys J. 2014; 106(3):577-85. PMC: 3944987. DOI: 10.1016/j.bpj.2013.12.019. View

Buboltz J, Feigenson G . A novel strategy for the preparation of liposomes: rapid solvent exchange. Biochim Biophys Acta. 1999; 1417(2):232-45. DOI: 10.1016/s0005-2736(99)00006-1. View

Redfern D, Gericke A . pH-dependent domain formation in phosphatidylinositol polyphosphate/phosphatidylcholine mixed vesicles. J Lipid Res. 2004; 46(3):504-15. DOI: 10.1194/jlr.M400367-JLR200. View

Pelchen-Matthews A, Kramer B, Marsh M . Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol. 2003; 162(3):443-55. PMC: 2172706. DOI: 10.1083/jcb.200304008. View

10.

Nadaraia-Hoke S, Bann D, Lochmann T, Gudleski-ORegan N, Parent L . Alterations in the MA and NC domains modulate phosphoinositide-dependent plasma membrane localization of the Rous sarcoma virus Gag protein. J Virol. 2013; 87(6):3609-15. PMC: 3592118. DOI: 10.1128/JVI.03059-12. View

11.

Chan J, Dick R, Vogt V . Rous sarcoma virus gag has no specific requirement for phosphatidylinositol-(4,5)-bisphosphate for plasma membrane association in vivo or for liposome interaction in vitro. J Virol. 2011; 85(20):10851-60. PMC: 3187501. DOI: 10.1128/JVI.00760-11. View

12.

Konyakhina T, Wu J, Mastroianni J, Heberle F, Feigenson G . Phase diagram of a 4-component lipid mixture: DSPC/DOPC/POPC/chol. Biochim Biophys Acta. 2013; 1828(9):2204-14. PMC: 3738200. DOI: 10.1016/j.bbamem.2013.05.020. View

13.

Heberle F, Wu J, Goh S, Petruzielo R, Feigenson G . Comparison of three ternary lipid bilayer mixtures: FRET and ESR reveal nanodomains. Biophys J. 2010; 99(10):3309-18. PMC: 2980711. DOI: 10.1016/j.bpj.2010.09.064. View

14.

Heberle F, Feigenson G . Phase separation in lipid membranes. Cold Spring Harb Perspect Biol. 2011; 3(4). PMC: 3062215. DOI: 10.1101/cshperspect.a004630. View

15.

Saad J, Miller J, Tai J, Kim A, Ghanam R, Summers M . Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc Natl Acad Sci U S A. 2006; 103(30):11364-9. PMC: 1544092. DOI: 10.1073/pnas.0602818103. View

16.

Reil H, Bukovsky A, Gelderblom H, Gottlinger H . Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J. 1998; 17(9):2699-708. PMC: 1170610. DOI: 10.1093/emboj/17.9.2699. View

17.

Balla T . Imaging and manipulating phosphoinositides in living cells. J Physiol. 2007; 582(Pt 3):927-37. PMC: 2075240. DOI: 10.1113/jphysiol.2007.132795. View

18.

Gamble T, Yoo S, Vajdos F, von Schwedler U, Worthylake D, Wang H . Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science. 1997; 278(5339):849-53. DOI: 10.1126/science.278.5339.849. View

19.

Murray P, Li Z, Wang J, Tang C, Honig B, Murray D . Retroviral matrix domains share electrostatic homology: models for membrane binding function throughout the viral life cycle. Structure. 2005; 13(10):1521-31. DOI: 10.1016/j.str.2005.07.010. View

20.

Batonick M, Favre M, Boge M, Spearman P, Honing S, Thali M . Interaction of HIV-1 Gag with the clathrin-associated adaptor AP-2. Virology. 2005; 342(2):190-200. DOI: 10.1016/j.virol.2005.08.001. View