Analysis of HIV-1 Matrix-Envelope Cytoplasmic Tail Interactions.
Binding Sites
Cell Membrane
/ metabolism
Cytosol
/ metabolism
Humans
Models, Molecular
Protein Binding
Protein Conformation
Protein Domains
Protein Multimerization
Viral Envelope Proteins
/ chemistry
Viral Matrix Proteins
/ chemistry
Virion
/ physiology
Virus Replication
gag Gene Products, Human Immunodeficiency Virus
/ chemistry
human immunodeficiency virus
Journal
Journal of virology
ISSN: 1098-5514
Titre abrégé: J Virol
Pays: United States
ID NLM: 0113724
Informations de publication
Date de publication:
01 11 2019
01 11 2019
Historique:
received:
27
06
2019
accepted:
30
07
2019
pubmed:
4
8
2019
medline:
11
6
2020
entrez:
4
8
2019
Statut:
epublish
Résumé
The matrix (MA) domains of HIV-1 precursor Gag (PrGag) proteins direct PrGag proteins to plasma membrane (PM) assembly sites where envelope (Env) protein trimers are incorporated into virus particles. MA targeting to PM sites is facilitated by its binding to phosphatidylinositol-(4,5)-bisphosphate [PI(4,5)P2], and MA binding to cellular RNAs appears to serve a chaperone function that prevents MA from associating with intracellular membranes prior to arrival at the PI(4,5)P2-rich PM. Investigations have shown genetic evidence of an interaction between MA and the cytoplasmic tails (CTs) of Env trimers that contributes to Env incorporation into virions, but demonstrations of direct MA-CT interactions have proven more difficult. In direct binding assays, we show here that MA binds to Env CTs. Using MA mutants, matrix-capsid (MACA) proteins, and MA proteins incubated in the presence of inositol polyphosphate, we show a correlation between MA trimerization and CT binding. RNA ligands with high affinities for MA reduced MA-CT binding levels, suggesting that MA-RNA binding interferes with trimerization and/or directly or indirectly blocks MA-CT binding. Rough-mapping studies indicate that C-terminal CT helices are involved in MA binding and are in agreement with cell culture studies with replication-competent viruses. Our results support a model in which full-length HIV-1 Env trimers are captured in assembling PrGag lattices by virtue of their binding to MA trimers.
Identifiants
pubmed: 31375589
pii: JVI.01079-19
doi: 10.1128/JVI.01079-19
pmc: PMC6803273
pii:
doi:
Substances chimiques
Viral Envelope Proteins
0
Viral Matrix Proteins
0
gag Gene Products, Human Immunodeficiency Virus
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, N.I.H., Intramural
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM060170
Pays : United States
Informations de copyright
Copyright © 2019 American Society for Microbiology.
Références
J Virol. 1998 Sep;72(9):7659-63
pubmed: 9696871
J Virol. 1994 Mar;68(3):1689-96
pubmed: 8107229
Biochemistry. 1992 May 5;31(17):4296-303
pubmed: 1567875
J Virol. 2019 May 15;93(11):
pubmed: 30894464
J Mol Biol. 2011 Jul 22;410(4):582-608
pubmed: 21762802
Proc Natl Acad Sci U S A. 2006 Jul 25;103(30):11364-9
pubmed: 16840558
EMBO J. 1998 May 1;17(9):2699-708
pubmed: 9564051
Proc Natl Acad Sci U S A. 2014 Jun 3;111(22):8233-8
pubmed: 24843179
Curr Biol. 1997 Oct 1;7(10):729-38
pubmed: 9368755
J Virol. 2011 Feb;85(4):1594-603
pubmed: 21123373
J Virol. 1996 Jan;70(1):341-51
pubmed: 8523546
J Virol. 2000 Apr;74(8):3548-54
pubmed: 10729129
Cell. 2014 Nov 20;159(5):1096-1109
pubmed: 25416948
J Virol. 2007 Feb;81(3):1472-8
pubmed: 17108052
Nature. 2018 Aug;560(7719):509-512
pubmed: 30069050
J Mol Biol. 2018 Jul 6;430(14):2113-2127
pubmed: 29752967
Methods Enzymol. 2014;539:53-66
pubmed: 24581438
Virology. 2011 Aug 15;417(1):137-46
pubmed: 21676426
MBio. 2014 Dec 09;5(6):e02202
pubmed: 25491356
Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):517-22
pubmed: 14699046
Rapid Commun Mass Spectrom. 2013 Jul 30;27(14):1660-8
pubmed: 23754800
J Virol. 2009 Dec;83(23):12196-203
pubmed: 19776118
Science. 2013 Dec 20;342(6165):1484-90
pubmed: 24179160
J Virol. 2004 Apr;78(7):3429-35
pubmed: 15016865
Trends Microbiol. 2014 Jul;22(7):372-8
pubmed: 24933691
PLoS Pathog. 2013;9(11):e1003739
pubmed: 24244165
AIDS Res Hum Retroviruses. 2000 Aug 10;16(12):1141-7
pubmed: 10954889
J Virol. 1999 Mar;73(3):1902-8
pubmed: 9971769
J Virol. 2013 Jun;87(12):7155-9
pubmed: 23552424
J Virol. 2016 May 27;90(12):5657-5664
pubmed: 27030269
J Mol Biol. 2007 Jan 19;365(3):812-24
pubmed: 17097677
J Virol. 1997 Jun;71(6):4409-18
pubmed: 9151831
Virology. 2009 May 10;387(2):466-72
pubmed: 19327811
J Mol Biol. 2011 Jul 22;410(4):653-66
pubmed: 21762806
J Mol Biol. 2007 Feb 16;366(2):574-85
pubmed: 17188710
Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):417-8
pubmed: 14707265
J Virol. 1993 Dec;67(12):7067-76
pubmed: 7693966
J Virol. 2008 Mar;82(5):2405-17
pubmed: 18094158
Biochem Biophys Res Commun. 2003 Jun 6;305(3):761-70
pubmed: 12763058
J Virol. 2015 Apr;89(7):3988-4001
pubmed: 25631074
J Virol. 2001 Jan;75(2):759-71
pubmed: 11134289
Nature. 2015 Jan 22;517(7535):505-8
pubmed: 25363765
Proc Natl Acad Sci U S A. 2004 Oct 12;101(41):14889-94
pubmed: 15465916
J Virol. 1995 Mar;69(3):1984-9
pubmed: 7853546
J Biol Chem. 2013 Jan 4;288(1):666-76
pubmed: 23135280
Nat Struct Mol Biol. 2013 Dec;20(12):1352-7
pubmed: 24154805
J Virol. 1992 Aug;66(8):4966-71
pubmed: 1629961
J Virol. 1998 Dec;72(12):9621-7
pubmed: 9811695
Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):3099-104
pubmed: 8610175
Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1600-5
pubmed: 20080620
RNA. 2001 Apr;7(4):576-84
pubmed: 11345436
Structure. 2017 Nov 7;25(11):1708-1718.e5
pubmed: 29056482
J Mol Biol. 2009 Mar 27;387(2):376-89
pubmed: 19356593
J Biol Chem. 2005 May 6;280(18):17664-70
pubmed: 15734744
EMBO J. 1996 Nov 1;15(21):5783-8
pubmed: 8918455
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
Retrovirology. 2011 May 14;8:37
pubmed: 21569545
EMBO J. 2007 Apr 18;26(8):2218-26
pubmed: 17396149
J Mol Biol. 2015 Mar 27;427(6 Pt B):1413-1427
pubmed: 25659909
J Mol Biol. 2007 Jan 19;365(3):799-811
pubmed: 17098251
Elife. 2018 May 31;7:
pubmed: 29848441
Virology. 2009 Feb 5;384(1):233-41
pubmed: 19059618
J Virol. 2006 Mar;80(5):2405-17
pubmed: 16474147