Home LiteratureArticle Details
PMID: 8970978 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Differential membrane binding of the human immunodeficiency virus type 1 matrix protein.

Journal of virology ·Vol. 70 ·No. 12 ·1996-12-00 ·Pages 8540-8

Zhou W, Resh MD

Abstract

The human immunodeficiency virus type 1 matrix protein (p17MA) plays a central role at both the early and late stages of the virus life cycle. During viral assembly, the p17MA domain of Pr55gag promotes membrane association, which is essential for the formation of viral particles. When viral infection occurs, the mature p17MA dissociates from the plasma membrane and participates in the nuclear targeting process. Thus, p17MA contains a reversible membrane binding signal to govern its differential subcellular localization and biological functions. We previously identified a membrane binding signal within the amino-terminal 31 amino acids of the matrix domain of human immunodeficiency virus type 1 Gag, consisting of myristate and a highly basic region (W. Zhou, L. J. Parent, J. W. Wills, and M. D. Resh, J. Virol. 68:2556-2569, 1994). Here we show that exposure of this membrane binding signal is regulated in different Gag protein contexts. Within full-length Pr55gag, the membrane targeting signal is exposed and can direct Pr55gag as well as heterologous proteins to the plasma membrane. However, in the context of p17MA alone, this signal is hidden and unable to confer plasma membrane binding. To investigate the molecular mechanism for regulation of membrane binding, a series of deletions within p17MA was generated by sequentially removing alpha-helical regions defined by the nuclear magnetic resonance structure. Removal of the last alpha helix (amino acids 97 to 109) of p17MA was associated with enhancement of binding to biological membranes in vitro and in vivo. Liposome binding experiments indicated that the C-terminal region of p17MA exerts a negative effect on the N-terminal MA membrane targeting domain by sequestering the myristate signal. We propose that mature p17MA adopts a conformation different from that of the p17MA domain within Pr55gag and present evidence to support this hypothesis. It is likely that such a conformational change results in an N-terminal myristyl switch which governs differential membrane binding.

MeSH Terms
Animals COS Cells Cell Membrane/metabolism Epitopes Gene Products, gag/genetics,metabolism HIV Antigens/genetics,metabolism HIV-1/genetics,metabolism Humans Myristic Acid Myristic Acids/metabolism Protein Precursors/metabolism Sequence Deletion Signal Transduction Viral Proteins gag Gene Products, Human Immunodeficiency Virus
Chemicals
Epitopes Gene Products, gag HIV Antigens Myristic Acids Protein Precursors Viral Proteins gag Gene Products, Human Immunodeficiency Virus p17 protein, Human Immunodeficiency Virus Type 1 p55 gag precursor protein, Human immunodeficiency virus 1 Myristic Acid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Zhou W
Cell Biology and Genetics Program, Memorial Sloan-Kettering Cancer Center, New York, New York 10021, USA.
Resh M D
References (45)
45 references, click to expand
  1. A simple method for the preparation of homogeneous phospholipid vesicles.
    Biochemistry. 1977 Jun 14;16(12):2806-10 PMID: 889789
  2. Translocation of pp60c-src from the plasma membrane to the cytosol after stimulation by platelet-derived growth factor.
    J Biol Chem. 1993 Sep 15;268(26):19552-8 PMID: 7690037
  3. Highly specific antibody to Rous sarcoma virus src gene product recognizes a novel population of pp60v-src and pp60c-src molecules.
    J Cell Biol. 1985 Feb;100(2):409-17 PMID: 2981886
  4. Failure of a human immunodeficiency virus (HIV) immune globulin to protect chimpanzees against experimental challenge with HIV.
    Proc Natl Acad Sci U S A. 1988 Sep;85(18):6944-8 PMID: 3413127
  5. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins.
    Biochemistry. 1993 Oct 5;32(39):10436-43 PMID: 8399188
  6. Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor.
    J Virol. 1993 Nov;67(11):6387-94 PMID: 8411340
  7. Functional chimeras of the Rous sarcoma virus and human immunodeficiency virus gag proteins.
    J Virol. 1993 Nov;67(11):6487-98 PMID: 8411352
  8. Human immunodeficiency virus type 1 viral protein R localization in infected cells and virions.
    J Virol. 1993 Nov;67(11):6542-50 PMID: 8411357
  9. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells.
    Nature. 1993 Oct 14;365(6447):666-9 PMID: 8105392
  10. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus.
    J Virol. 1994 Jan;68(1):510-6 PMID: 8254763
  11. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids.
    J Virol. 1994 Apr;68(4):2556-69 PMID: 8139035
  12. Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly.
    J Virol. 1994 May;68(5):3232-42 PMID: 8151785
  13. Characterization of human immunodeficiency virus type 1 Pr55gag membrane association in a cell-free system: requirement for a C-terminal domain.
    Proc Natl Acad Sci U S A. 1994 May 10;91(10):4594-8 PMID: 8183954
  14. The nuclear localization signal of the matrix protein of human immunodeficiency virus type 1 allows the establishment of infection in macrophages and quiescent T lymphocytes.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6992-6 PMID: 8041734
  15. The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7311-5 PMID: 8041786
  16. Structural similarity between the p17 matrix protein of HIV-1 and interferon-gamma.
    Nature. 1994 Aug 25;370(6491):666-8 PMID: 8065455
  17. Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein.
    J Mol Biol. 1994 Nov 25;244(2):198-223 PMID: 7966331
  18. Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12253-7 PMID: 7527558
  19. Improved green fluorescence.
    Nature. 1995 Feb 23;373(6516):663-4 PMID: 7854443
  20. HIV-1 infection of nondividing cells: C-terminal tyrosine phosphorylation of the viral matrix protein is a key regulator.
    Cell. 1995 Feb 10;80(3):379-88 PMID: 7859280
  21. Regulation of HIV-1 gag protein subcellular targeting by protein kinase C.
    J Biol Chem. 1995 Mar 3;270(9):4792-6 PMID: 7876252
  22. Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection.
    J Virol. 1995 Jun;69(6):3949-54 PMID: 7745752
  23. Arf proteins: the membrane traffic police?
    Trends Biochem Sci. 1995 Apr;20(4):147-50 PMID: 7770914
  24. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state.
    Nature. 1995 Aug 3;376(6539):444-7 PMID: 7630423
  25. HIV nuclear import is governed by the phosphotyrosine-mediated binding of matrix to the core domain of integrase.
    Cell. 1995 Nov 17;83(4):569-76 PMID: 7585960
  26. Evidence for a second function of the MA sequence in the Rous sarcoma virus Gag protein.
    J Virol. 1996 Feb;70(2):1016-26 PMID: 8551559
  27. The gag gene products of human immunodeficiency virus type 1: alignment within the gag open reading frame, identification of posttranslational modifications, and evidence for alternative gag precursors.
    J Virol. 1988 Nov;62(11):3993-4002 PMID: 3262776
  28. The biology and enzymology of eukaryotic protein acylation.
    Annu Rev Biochem. 1988;57:69-99 PMID: 3052287
  29. In vitro synthesis of pp60v-src: myristylation in a cell-free system.
    Mol Cell Biol. 1988 Oct;8(10):4295-301 PMID: 3141787
  30. Specific and saturable binding of pp60v-src to plasma membranes: evidence for a myristyl-src receptor.
    Cell. 1989 Jul 28;58(2):281-6 PMID: 2546680
  31. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1.
    Proc Natl Acad Sci U S A. 1989 Aug;86(15):5781-5 PMID: 2788277
  32. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells.
    Cell. 1989 Oct 6;59(1):103-12 PMID: 2676191
  33. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):523-7 PMID: 2405382
  34. Immobilon-P transfer membrane: applications and utility in protein biochemical analysis.
    Biotechniques. 1990 Dec;9(6 Suppl):788-805 PMID: 2271178
  35. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3195-9 PMID: 2014240
  36. Regulation by phosphorylation of reversible association of a myristoylated protein kinase C substrate with the plasma membrane.
    Nature. 1991 May 23;351(6324):320-2 PMID: 2034276
  37. Suppression of retroviral MA deletions by the amino-terminal membrane-binding domain of p60src.
    J Virol. 1991 Jul;65(7):3804-12 PMID: 1710290
  38. Assembly and morphology of HIV: potential effect of structure on viral function.
    AIDS. 1991 Jun;5(6):617-37 PMID: 1652977
  39. Form, function, and use of retroviral gag proteins.
    AIDS. 1991 Jun;5(6):639-54 PMID: 1883539
  40. Active nuclear import of human immunodeficiency virus type 1 preintegration complexes.
    Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6580-4 PMID: 1631159
  41. Rapid high resolution western blotting: from gel to image in a single day.
    Biotechniques. 1992 May;12(5):650-4 PMID: 1515130
  42. Lysine residues form an integral component of a novel NH2-terminal membrane targeting motif for myristylated pp60v-src.
    J Cell Biol. 1992 Oct;119(2):415-25 PMID: 1400583
  43. Mutational inactivation of an inhibitory sequence in human immunodeficiency virus type 1 results in Rev-independent gag expression.
    J Virol. 1992 Dec;66(12):7176-82 PMID: 1433510
  44. HIV-1 matrix protein p17 resides in cell nuclei in association with genomic RNA.
    AIDS Res Hum Retroviruses. 1992 Oct;8(10):1795-801 PMID: 1457192
  45. A short amino acid sequence able to specify nuclear location.
    Cell. 1984 Dec;39(3 Pt 2):499-509 PMID: 6096007
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-12-00
Pages
8540-8
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC190946
Subset
IM
Grants
NCI NIH HHS · CA72309 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com