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PMID: 16840558 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly.

Saad JS, Miller J, Tai J, Kim A, Ghanam RH, Summers MF

Abstract

During the late phase of HIV type 1 (HIV-1) replication, newly synthesized retroviral Gag proteins are targeted to the plasma membrane of most hematopoietic cell types, where they colocalize at lipid rafts and assemble into immature virions. Membrane binding is mediated by the matrix (MA) domain of Gag, a 132-residue polypeptide containing an N-terminal myristyl group that can adopt sequestered and exposed conformations. Although exposure is known to promote membrane binding, the mechanism by which Gag is targeted to specific membranes has yet to be established. Recent studies have shown that phosphatidylinositol (PI) 4,5-bisphosphate [PI(4,5)P(2)], a factor that regulates localization of cellular proteins to the plasma membrane, also regulates Gag localization and assembly. Here we show that PI(4,5)P(2) binds directly to HIV-1 MA, inducing a conformational change that triggers myristate exposure. Related phosphatidylinositides PI, PI(3)P, PI(4)P, PI(5)P, and PI(3,5)P(2) do not bind MA with significant affinity or trigger myristate exposure. Structural studies reveal that PI(4,5)P(2) adopts an "extended lipid" conformation, in which the inositol head group and 2'-fatty acid chain bind to a hydrophobic cleft, and the 1'-fatty acid and exposed myristyl group bracket a conserved basic surface patch previously implicated in membrane binding. Our findings indicate that PI(4,5)P(2) acts as both a trigger of the myristyl switch and a membrane anchor and suggest a potential mechanism for targeting Gag to membrane rafts.

MeSH Terms
Allosteric Site Binding Sites Cell Membrane/virology Gene Products, gag/chemistry,physiology HIV-1/metabolism Lipids/chemistry Magnetic Resonance Spectroscopy Membrane Microdomains Models, Molecular Phosphatidylinositol 4,5-Diphosphate/metabolism Protein Binding Protein Conformation Protein Structure, Tertiary Virus Assembly
Chemicals
Gene Products, gag Lipids Phosphatidylinositol 4,5-Diphosphate
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Saad Jamil S
Howard Hughes Medical Institute, University of Maryland, Baltimore County, 1000 Hilltop Circle, Baltimore, MD 21250, USA.
Miller Jaime
Tai Janet
Kim Andrew
Ghanam Ruba H
Summers Michael F
References (63)
63 references, click to expand
  1. Relationship between human immunodeficiency virus type 1 Gag multimerization and membrane binding.
    J Virol. 2000 Jun;74(11):5142-50 PMID: 10799589
  2. Structure and function of sphingolipid- and cholesterol-rich membrane rafts.
    J Biol Chem. 2000 Jun 9;275(23):17221-4 PMID: 10770957
  3. Mapping and characterization of the N-terminal I domain of human immunodeficiency virus type 1 Pr55(Gag).
    J Virol. 2000 Aug;74(16):7238-49 PMID: 10906178
  4. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging.
    J Virol. 2000 Sep;74(18):8670-9 PMID: 10954568
  5. Characterization of Rous sarcoma virus Gag particles assembled in vitro.
    J Virol. 2001 Mar;75(6):2753-64 PMID: 11222698
  6. Structural mechanism of endosome docking by the FYVE domain.
    Science. 2001 Mar 2;291(5509):1793-6 PMID: 11230696
  7. RNA is a structural element in retrovirus particles.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5246-51 PMID: 11320254
  8. PI(4,5)P(2) regulation of surface membrane traffic.
    Curr Opin Cell Biol. 2001 Aug;13(4):493-9 PMID: 11454457
  9. Modulation of HIV-like particle assembly in vitro by inositol phosphates.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10875-9 PMID: 11526217
  10. Plasma membrane rafts play a critical role in HIV-1 assembly and release.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13925-30 PMID: 11717449
  11. Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage.
    J Biol Chem. 2002 Mar 15;277(11):8822-6 PMID: 11781329
  12. Nuclear entry and CRM1-dependent nuclear export of the Rous sarcoma virus Gag polyprotein.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3944-9 PMID: 11891341
  13. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells.
    Science. 2002 May 3;296(5569):913-6 PMID: 11988576
  14. Human macrophages accumulate HIV-1 particles in MHC II compartments.
    Traffic. 2002 Oct;3(10):718-29 PMID: 12230470
  15. Myristoylation as a target for inhibiting HIV assembly: unsaturated fatty acids block viral budding.
    Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):13037-42 PMID: 12244217
  16. Characterization of a putative alpha-helix across the capsid-SP1 boundary that is critical for the multimerization of human immunodeficiency virus type 1 gag.
    J Virol. 2002 Nov;76(22):11729-37 PMID: 12388733
  17. Reversible binding of recombinant human immunodeficiency virus type 1 gag protein to nucleic acids in virus-like particle assembly in vitro.
    J Virol. 2002 Nov;76(22):11757-62 PMID: 12388738
  18. Role of myristylation in HIV-1 Gag assembly.
    Biochemistry. 2003 Jun 3;42(21):6408-17 PMID: 12767222
  19. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway.
    J Biol Chem. 2003 Dec 26;278(52):52347-54 PMID: 14561735
  20. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body.
    J Virol. 2004 Feb;78(3):1552-63 PMID: 14722309
  21. Entropic switch regulates myristate exposure in the HIV-1 matrix protein.
    Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):517-22 PMID: 14699046
  22. The stoichiometry of Gag protein in HIV-1.
    Nat Struct Mol Biol. 2004 Jul;11(7):672-5 PMID: 15208690
  23. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane.
    Proc Natl Acad Sci U S A. 2004 Oct 12;101(41):14889-94 PMID: 15465916
  24. Inositol phospholipid arachidonic acid metabolism in GH3 pituitary cells.
    Biochem J. 1986 May 15;236(1):235-42 PMID: 3098231
  25. Polyphosphoinositide micelles and polyphosphoinositide-containing vesicles dissociate endogenous gelsolin-actin complexes and promote actin assembly from the fast-growing end of actin filaments blocked by gelsolin.
    J Biol Chem. 1987 Sep 5;262(25):12228-36 PMID: 3040735
  26. Poorly expressed endogenous ecotropic provirus of DBA/2 mice encodes a mutant Pr65gag protein that is not myristylated.
    J Virol. 1988 Feb;62(2):479-87 PMID: 2826810
  27. 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
  28. 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
  29. Organelle identity and the signposts for membrane traffic.
    Nature. 2005 Dec 1;438(7068):597-604 PMID: 16319879
  30. 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
  31. Four-dimensional heteronuclear triple-resonance NMR spectroscopy of interleukin-1 beta in solution.
    Science. 1990 Jul 27;249(4967):411-4 PMID: 2377896
  32. Form, function, and use of retroviral gag proteins.
    AIDS. 1991 Jun;5(6):639-54 PMID: 1883539
  33. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5181-5 PMID: 8389472
  34. 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
  35. 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
  36. 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
  37. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production.
    J Virol. 1994 Aug;68(8):5311-20 PMID: 8035531
  38. Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein.
    J Mol Biol. 1994 Nov 25;244(2):198-223 PMID: 7966331
  39. Lipid dynamics and peripheral interactions of proteins with membrane surfaces.
    Chem Phys Lipids. 1994 Sep 6;73(1-2):181-207 PMID: 8001181
  40. Reversibility of the binding of cytochrome c to liposomes. Implications for lipid-protein interactions.
    J Biol Chem. 1995 Feb 17;270(7):3197-202 PMID: 7852404
  41. Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1.
    J Virol. 1995 Oct;69(10):6487-97 PMID: 7666550
  42. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):3099-104 PMID: 8610175
  43. The major homology region of the HIV-1 gag precursor influences membrane affinity.
    Biochemistry. 1996 Nov 12;35(45):14268-75 PMID: 8916912
  44. Differential membrane binding of the human immunodeficiency virus type 1 matrix protein.
    J Virol. 1996 Dec;70(12):8540-8 PMID: 8970978
  45. Structure-function studies of the human immunodeficiency virus type 1 matrix protein, p17.
    J Virol. 1997 May;71(5):3474-83 PMID: 9094619
  46. Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism.
    J Virol. 1997 Sep;71(9):6582-92 PMID: 9261380
  47. Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes?
    Biochem Biophys Res Commun. 1997 Nov 7;240(1):1-7 PMID: 9367871
  48. 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. 1998 Mar;72(3):2072-8 PMID: 9499062
  49. The I domain is required for efficient plasma membrane binding of human immunodeficiency virus type 1 Pr55Gag.
    J Virol. 1998 Apr;72(4):2723-32 PMID: 9525590
  50. HIV-1 gag proteins: diverse functions in the virus life cycle.
    Virology. 1998 Nov 10;251(1):1-15 PMID: 9813197
  51. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated.
    J Biol Chem. 1999 Feb 5;274(6):3910-7 PMID: 9920947
  52. Human immunodeficiency virus type 1 protease triggers a myristoyl switch that modulates membrane binding of Pr55(gag) and p17MA.
    J Virol. 1999 Mar;73(3):1902-8 PMID: 9971769
  53. Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of gag membrane targeting.
    J Virol. 1999 Apr;73(4):2604-12 PMID: 10074105
  54. Mass determination of rous sarcoma virus virions by scanning transmission electron microscopy.
    J Virol. 1999 Aug;73(8):7050-5 PMID: 10400808
  55. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly.
    Cell. 2005 Mar 11;120(5):663-74 PMID: 15766529
  56. PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility.
    J Cell Biol. 2005 Apr 11;169(1):151-65 PMID: 15809307
  57. Detailed mapping of the nuclear export signal in the Rous sarcoma virus Gag protein.
    J Virol. 2005 Jul;79(14):8732-41 PMID: 15994767
  58. Role of lipid rafts in virus replication.
    Adv Virus Res. 2005;64:311-58 PMID: 16139599
  59. A novel nuclear export activity in HIV-1 matrix protein required for viral replication.
    Nature. 1999 Dec 9;402(6762):681-5 PMID: 10604476
  60. Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly.
    J Virol. 2000 Mar;74(6):2855-66 PMID: 10684302
  61. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts.
    J Virol. 2000 Apr;74(7):3264-72 PMID: 10708443
  62. Plasma membrane phosphoinositide organization by protein electrostatics.
    Nature. 2005 Dec 1;438(7068):605-11 PMID: 16319880
  63. Interactions of HIV-1 Gag with assembly cofactors.
    Biochemistry. 2006 Apr 4;45(13):4077-83 PMID: 16566581
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2006-07-25
Epub
2006-00-13
Pages
11364-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1544092
Subset
IM
Grants
NIAID NIH HHS · R37 AI030917 · United States
NIGMS NIH HHS · T34 GM008663 · United States
NIAID NIH HHS · AI30917 · United States
NIGMS NIH HHS · GM08663 · United States
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PDB
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