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PMID: 19935658 Published · ppublish English Journal Article

HIV-1 Nef membrane association depends on charge, curvature, composition and sequence.

Nature chemical biology ·Vol. 6 ·No. 1 ·2010-01-00 ·Pages 46-53

Gerlach H, Laumann V, Martens S, Becker CF, Goody RS, Geyer M

Abstract

Nef-mediated internalization of T-cell receptor molecules from the surface of an infected cell is required for the pathogenicity of HIV and disease progression to AIDS. This function depends on the N-terminal myristoylation of Nef, a lipid modification that targets the protein to membranes. We have analyzed how specific membrane properties and sequence motifs within Nef determine this interaction. Using time-resolved techniques we find that the association with membranes is a biphasic process with a fast rate for an electrostatic-driven protein-liposome interaction and a slow rate for the formation of an amphipathic helix. The rate of myristate insertion into liposomes depends on membrane curvature, while changes in the lipid composition with respect to phosphoinositides, cholesterol or sphingomyelin did not significantly alter the interaction. Moreover, Nef binding to membranes requires negatively charged liposomes, and mutations of basic and hydrophobic residues strongly diminished the association and changed the binding kinetics differently.

MeSH Terms
Amino Acid Motifs Animals COS Cells Cell Membrane/virology Chlorocebus aethiops Cholesterol/chemistry HIV Infections/metabolism Humans Kinetics Lipids/chemistry Liposomes/chemistry Myristic Acids/chemistry Protein Structure, Secondary Receptors, Antigen, T-Cell/metabolism Sphingomyelins/chemistry nef Gene Products, Human Immunodeficiency Virus/metabolism
Chemicals
Lipids Liposomes Myristic Acids Receptors, Antigen, T-Cell Sphingomyelins nef Gene Products, Human Immunodeficiency Virus Cholesterol
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Gerlach Holger
Max-Planck-Institut für molekulare Physiologie, Abteilung Physikalische Biochemie, Dortmund, Germany.
Laumann Vanessa
Martens Sascha
Becker Christian F W
Goody Roger S
Geyer Matthias
References (48)
48 references, click to expand
  1. Biochemical indication for myristoylation-dependent conformational changes in HIV-1 Nef.
    Biochemistry. 2006 Feb 21;45(7):2339-49 PMID: 16475823
  2. HIV-1 pathogenesis.
    Nat Med. 2003 Jul;9(7):853-60 PMID: 12835705
  3. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients.
    Science. 1995 Nov 10;270(5238):988-91 PMID: 7481804
  4. 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
  5. ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif.
    EMBO J. 2005 Jul 6;24(13):2244-53 PMID: 15944734
  6. Membrane phosphatidylserine regulates surface charge and protein localization.
    Science. 2008 Jan 11;319(5860):210-3 PMID: 18187657
  7. Roles of bilayer material properties in function and distribution of membrane proteins.
    Annu Rev Biophys Biomol Struct. 2006;35:177-98 PMID: 16689633
  8. Plasma membrane phosphoinositide organization by protein electrostatics.
    Nature. 2005 Dec 1;438(7068):605-11 PMID: 16319880
  9. Charting HIV's remarkable voyage through the cell: Basic science as a passport to future therapy.
    Nat Med. 2002 Jul;8(7):673-80 PMID: 12091904
  10. How synaptotagmin promotes membrane fusion.
    Science. 2007 May 25;316(5828):1205-8 PMID: 17478680
  11. HIV-1 accessory proteins--ensuring viral survival in a hostile environment.
    Cell Host Microbe. 2008 Jun 12;3(6):388-98 PMID: 18541215
  12. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms.
    Science. 2005 Mar 18;307(5716):1746-52 PMID: 15705808
  13. Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2.
    Mol Cell. 2005 May 27;18(5):519-31 PMID: 15916959
  14. Functional characterization of HIV-1 Nef mutants in the context of viral infection.
    Virology. 2006 Aug 1;351(2):322-39 PMID: 16684552
  15. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane.
    Science. 2006 Dec 1;314(5804):1458-61 PMID: 17095657
  16. Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection.
    N Engl J Med. 1995 Jan 26;332(4):228-32 PMID: 7808489
  17. Trafficking and signaling by fatty-acylated and prenylated proteins.
    Nat Chem Biol. 2006 Nov;2(11):584-90 PMID: 17051234
  18. Extrusion technique to generate liposomes of defined size.
    Methods Enzymol. 2003;367:3-14 PMID: 14611054
  19. How proteins produce cellular membrane curvature.
    Nat Rev Mol Cell Biol. 2006 Jan;7(1):9-19 PMID: 16365634
  20. How proteins adapt to a membrane-water interface.
    Trends Biochem Sci. 2000 Sep;25(9):429-34 PMID: 10973056
  21. Cryo-electron tomography of clathrin-coated vesicles: structural implications for coat assembly.
    J Mol Biol. 2007 Jan 19;365(3):892-9 PMID: 17095010
  22. Synaptotagmin activates membrane fusion through a Ca2+-dependent trans interaction with phospholipids.
    Nat Struct Mol Biol. 2007 Oct;14(10):904-11 PMID: 17891149
  23. Mechanism of endophilin N-BAR domain-mediated membrane curvature.
    EMBO J. 2006 Jun 21;25(12):2898-910 PMID: 16763559
  24. Structure--function relationships in HIV-1 Nef.
    EMBO Rep. 2001 Jul;2(7):580-5 PMID: 11463741
  25. Virion incorporation of human immunodeficiency virus type 1 Nef is mediated by a bipartite membrane-targeting signal: analysis of its role in enhancement of viral infectivity.
    J Virol. 1998 Nov;72(11):8833-40 PMID: 9765428
  26. Human immunodeficiency virus type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains.
    Retrovirology. 2007 Oct 01;4:70 PMID: 17908312
  27. Membrane binding kinetics of protein kinase C betaII mediated by the C2 domain.
    Biochemistry. 2001 Nov 6;40(44):13216-29 PMID: 11683630
  28. A general amphipathic alpha-helical motif for sensing membrane curvature.
    Nat Struct Mol Biol. 2007 Feb;14(2):138-46 PMID: 17220896
  29. Domain assembly, surface accessibility and sequence conservation in full length HIV-1 Nef.
    FEBS Lett. 2001 May 11;496(2-3):91-5 PMID: 11356189
  30. Kinetics of interaction of the myristoylated alanine-rich C kinase substrate, membranes, and calmodulin.
    J Biol Chem. 1997 Oct 24;272(43):27167-77 PMID: 9341159
  31. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure.
    Science. 2004 Jan 23;303(5657):495-9 PMID: 14645856
  32. Specific and distinct determinants mediate membrane binding and lipid raft incorporation of HIV-1(SF2) Nef.
    Virology. 2006 Nov 25;355(2):175-91 PMID: 16916529
  33. N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange.
    Biochemistry. 1997 Apr 15;36(15):4675-84 PMID: 9109679
  34. The HIV lipidome: a raft with an unusual composition.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2641-6 PMID: 16481622
  35. Solution structure of a polypeptide from the N terminus of the HIV protein Nef.
    Biochemistry. 1997 May 20;36(20):5970-80 PMID: 9166767
  36. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins.
    Biochim Biophys Acta. 1999 Aug 12;1451(1):1-16 PMID: 10446384
  37. Role of myristoylation and N-terminal basic residues in membrane association of the human immunodeficiency virus type 1 Nef protein.
    J Gen Virol. 2006 Mar;87(Pt 3):563-571 PMID: 16476977
  38. Experimentally determined hydrophobicity scale for proteins at membrane interfaces.
    Nat Struct Biol. 1996 Oct;3(10):842-8 PMID: 8836100
  39. Molecular anatomy of a trafficking organelle.
    Cell. 2006 Nov 17;127(4):831-46 PMID: 17110340
  40. Structure of the anchor-domain of myristoylated and non-myristoylated HIV-1 Nef protein.
    J Mol Biol. 1999 May 28;289(1):123-38 PMID: 10339411
  41. Structural basis of membrane invagination by F-BAR domains.
    Cell. 2008 Mar 7;132(5):807-17 PMID: 18329367
  42. Molecular mechanics of calcium-myristoyl switches.
    Nature. 1997 Sep 11;389(6647):198-202 PMID: 9296500
  43. Curvature of clathrin-coated pits driven by epsin.
    Nature. 2002 Sep 26;419(6905):361-6 PMID: 12353027
  44. Membrane curvature and mechanisms of dynamic cell membrane remodelling.
    Nature. 2005 Dec 1;438(7068):590-6 PMID: 16319878
  45. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1.
    Cell. 2006 Jun 16;125(6):1055-67 PMID: 16777597
  46. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions.
    Trends Biochem Sci. 1995 Jul;20(7):272-6 PMID: 7667880
  47. Kinetic analysis of the interaction of the C1 domain of protein kinase C with lipid membranes by stopped-flow spectroscopy.
    J Biol Chem. 2008 Mar 21;283(12):7885-93 PMID: 18187412
  48. Role of cholesterol and lipid organization in disease.
    Nature. 2005 Dec 1;438(7068):612-21 PMID: 16319881
Article Info
Journal
Nature chemical biology
Abbr.
Nat Chem Biol
ISSN
1552-4469
Published
2010-01-00
Epub
2009-00-22
Pages
46-53
Language
English
Region
United States
NLM ID
101231976
Subset
IM
Databases
PubChem-Substance
85285412, 85285413, 85285414, 85285415, 85285416, 85285417, 85285418, 85285419, 85285420
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