Destabilization exerted by peptides derived from the membrane-proximal external region of HIV-1 gp41 in lipid vesicles supporting fluid phase coexistence

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 7, 2011, Pages 1797-1805

  Apellániz, Beatriz ^a   García Sáez, Ana ^b   Nir, Shlomo ^c   Nieva, José L ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

HIV gp41; Lipid rafts; Lo Ld coexistence; Lytic pore; Membrane fusion; MPER

Indexed keywords

ASPARAGINYLGLUTAMYLGLUTAMINYLGLUTAMYLLEUCYLLEUCYLGLUTAMYLLEUCYLASPARTYLLYSYLTRYPTOPHANYLALANYLSYRYLLEUCYLTRYPTOPHANYLASPARGINYLTRYPTOPHANYLPHENYLALANINEASPARGINYLISOLEUCYLTHREONYLASPARGINYLTRYPTOPHANYLLEUCYLTRYPTOPHANYLTYROSYLISOLEUCYLLYSINE; GLYCOPROTEIN GP 41; LYSYLLYSYLLYSYLASPARGININETRYPTOPHANYLPHENYLALANYLASPARTYLISOLEUCYLTHREONYLTRYPTOPHANYLLEUCYLTRYPTOPHANYLTYROSYLLEUCYLLYSYLLEUCYLPHENYLALANYLISOLEUCYLMETHIONYLISOLEUCYLVALYLGLYCYLGLYCYLLEUCYLVALYLLYSYLLYSINE; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE PERMEABILITY; CELLULAR DISTRIBUTION; CONCENTRATION PROCESS; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; LIPID BILAYER; MEMBRANE FUSION; MEMBRANE STABILIZATION; MEMBRANE STRUCTURE; MEMBRANE VESICLE; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; VIRUS ENVELOPE;

AMINO ACID SEQUENCE; HIV ENVELOPE PROTEIN GP41; HIV-1; LIPID METABOLISM; MEMBRANE FUSION; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79955797494     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.02.005     Document Type: Article

References (56)

1. R.C. Aloia, F.C. Jensen, C.C. Curtain, P.W. Mobley, and L.M. Gordon Lipid composition and fluidity of the human immunodeficiency virus Proc. Natl Acad. Sci. USA 85 1988 900 904 (Pubitemid 18073935)
2. R.C. Aloia, H. Tian, and F.C. Jensen Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes Proc. Natl Acad. Sci. USA 90 1993 5181 5185 (Pubitemid 23183001)
3. B. Brugger, B. Glass, P. Haberkant, I. Leibrecht, F.T. Wieland, and H.G. Krausslich The HIV lipidome: a raft with an unusual composition Proc. Natl Acad. Sci. USA 103 2006 2641 2646
4. M. Lorizate, B. Brugger, H. Akiyama, B. Glass, B. Muller, G. Anderluh, F.T. Wieland, and H.G. Krausslich Probing HIV-1 membrane liquid order by Laurdan staining reveals producer cell-dependent differences J. Biol. Chem. 284 2009 22238 22247
5. D.H. Nguyen, and J.E. Hildreth Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts J. Virol. 74 2000 3264 3272 (Pubitemid 30143751)
6. U. Coskun, and K. Simons Membrane rafting: from apical sorting to phase segregation FEBS Lett. 584 2010 1685 1693
7. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
8. T. Baumgart, S.T. Hess, and W.W. Webb Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Nature 425 2003 821 824 (Pubitemid 37351463)
9. D.A. Brown, and E. London Functions of lipid rafts in biological membranes Annu. Rev. Cell Dev. Biol. 14 1998 111 136 (Pubitemid 29001451)
10. A.A. Waheed, and E.O. Freed Lipids and membrane microdomains in HIV-1 replication Virus Res. 143 2009 162 176
11. Z. Liao, D.R. Graham, and J.E. Hildreth Lipid rafts and HIV pathogenesis: virion-associated cholesterol is required for fusion and infection of susceptible cells AIDS Res. Hum. Retroviruses 19 2003 675 687 (Pubitemid 37047093)
12. M. Guyader, E. Kiyokawa, L. Abrami, P. Turelli, and D. Trono Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization J. Virol. 76 2002 10356 10364
13. D.M. Eckert, and P.S. Kim Mechanisms of viral membrane fusion and its inhibition Annu. Rev. Biochem. 70 2001 777 810 (Pubitemid 32662225)
14. S.A. Gallo, C.M. Finnegan, M. Viard, Y. Raviv, A. Dimitrov, S.S. Rawat, A. Puri, S. Durell, and R. Blumenthal The HIV Env-mediated fusion reaction Biochim. Biophys. Acta 1614 2003 36 50 (Pubitemid 36857094)
15. L.V. Chernomordik, and M.M. Kozlov Protein-lipid interplay in fusion and fission of biological membranes Annu. Rev. Biochem. 72 2003 175 207 (Pubitemid 36930445)
16. L.V. Chernomordik, and M.M. Kozlov Mechanics of membrane fusion Nat. Struct. Mol. Biol. 15 2008 675 683 (Pubitemid 351932010)
17. M.M. Kozlov, H.T. McMahon, L.V. Chernomordik, Protein-driven membrane stresses in fusion and fission, Trends Biochem Sci 35 (2010) 699 - 706.
18. K. Salzwedel, J.T. West, and E. Hunter A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity J. Virol. 73 1999 2469 2480 (Pubitemid 29098154)
19. T. Suarez, S. Nir, F.M. Goni, A. Saez-Cirion, and J.L. Nieva The pre-transmembrane region of the human immunodeficiency virus type-1 glycoprotein: a novel fusogenic sequence FEBS Lett. 477 2000 145 149 (Pubitemid 30438873)
20. A. Saez-Cirion, S. Nir, M. Lorizate, A. Agirre, A. Cruz, J. Perez-Gil, and J.L. Nieva Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring J. Biol. Chem. 277 2002 21776 21785 (Pubitemid 34952329)
21. S. Shnaper, K. Sackett, S.A. Gallo, R. Blumenthal, and Y. Shai The C- and the N-terminal regions of glycoprotein 41 ectodomain fuse membranes enriched and not enriched with cholesterol, respectively J. Biol. Chem. 279 2004 18526 18534 (Pubitemid 38623272)
22. S.A. Vishwanathan, and E. Hunter Importance of the membrane-perturbing properties of the membrane-proximal external region of human immunodeficiency virus type 1 gp41 to viral fusion J. Virol. 82 2008 5118 5126 (Pubitemid 351705220)
23. R.F. Epand, B.G. Sayer, and R.M. Epand The tryptophan-rich region of HIV gp41 and the promotion of cholesterol-rich domains Biochemistry 44 2005 5525 5531 (Pubitemid 40489992)
24. R.F. Epand, A. Thomas, R. Brasseur, S.A. Vishwanathan, E. Hunter, and R.M. Epand Juxtamembrane protein segments that contribute to recruitment of cholesterol into domains Biochemistry 45 2006 6105 6114 (Pubitemid 43727103)
25. S.A. Vishwanathan, A. Thomas, R. Brasseur, R.F. Epand, E. Hunter, and R.M. Epand Hydrophobic substitutions in the first residue of the CRAC segment of the gp41 protein of HIV Biochemistry 47 2008 124 130
26. A. Saez-Cirion, J.L. Arrondo, M.J. Gomara, M. Lorizate, I. Iloro, G. Melikyan, and J.L. Nieva Structural and functional roles of HIV-1 gp41 pretransmembrane sequence segmentation Biophys. J. 85 2003 3769 3780 (Pubitemid 37490287)
27. Z.Y. Sun, K.J. Oh, M. Kim, J. Yu, V. Brusic, L. Song, Z. Qiao, J.H. Wang, G. Wagner, and E.L. Reinherz HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane Immunity 28 2008 52 63
28. B. Apellaniz, S. Nir, and J.L. Nieva Distinct mechanisms of lipid bilayer perturbation induced by peptides derived from the membrane-proximal external region of HIV-1 gp41 Biochemistry 48 2009 5320 5331
29. A. Zemel, A. Ben-Shaul, and S. May Perturbation of a lipid membrane by amphipathic peptides and its role in pore formation Eur. Biophys. J. 34 2005 230 242 (Pubitemid 40684805)
30. A. Zemel, A. Ben-Shaul, and S. May Modulation of the spontaneous curvature and bending rigidity of lipid membranes by interfacially adsorbed amphipathic peptides J. Phys. Chem. B 112 2008 6988 6996
31. F. Campelo, H.T. McMahon, and M.M. Kozlov The hydrophobic insertion mechanism of membrane curvature generation by proteins Biophys. J. 95 2008 2325 2339
32. B. Apellaniz, J.L. Nieva, P. Schwille, and A.J. Garcia-Saez All-or-none versus graded: single-vesicle analysis reveals lipid composition effects on membrane permeabilization Biophys. J. 99 2010 3619 3628
33. M.J. Hope, M.B. Bally, G. Webb, and P.R. Cullis Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta 812 1985 55 65 (Pubitemid 15159822)
34. S.H. White, W.C. Wimley, A.S. Ladokhin, and K. Hristova Protein folding in membranes: determining energetics of peptide-bilayer interactions Meth. Enzymol. 295 1998 62 87 (Pubitemid 29349909)
35. H. Ellens, J. Bentz, and F.C. Szoka H+- and Ca2+-induced fusion and destabilization of liposomes Biochemistry 24 1985 3099 3106
36. W.C. Wimley, M.E. Selsted, and S.H. White Interactions between human defensins and lipid bilayers: evidence for formation of multimeric pores Protein Sci. 3 1994 1362 1373 (Pubitemid 24314455)
37. A.S. Ladokhin, W.C. Wimley, and S.H. White Leakage of membrane vesicle contents: determination of mechanism using fluorescence requenching Biophys. J. 69 1995 1964 1971
38. A.S. Ladokhin, W.C. Wimley, K. Hristova, and S.H. White Mechanism of leakage of contents of membrane vesicles determined by fluorescence requenching Meth. Enzymol. 278 1997 474 486
39. J.M. Rausch, J.R. Marks, R. Rathinakumar, and W.C. Wimley Beta-sheet pore-forming peptides selected from a rational combinatorial library: mechanism of pore formation in lipid vesicles and activity in biological membranes Biochemistry 46 2007 12124 12139 (Pubitemid 350022368)
40. F. Nicol, S. Nir, and F.C. Szoka Jr. Effect of cholesterol and charge on pore formation in bilayer vesicles by a pH-sensitive peptide Biophys. J. 71 1996 3288 3301 (Pubitemid 26422370)
41. S. Nir, and J.L. Nieva Interactions of peptides with liposomes: pore formation and fusion Prog. Lipid Res. 39 2000 181 206 (Pubitemid 30207061)
42. D.K. Struck, D. Hoekstra, and R.E. Pagano Use of resonance energy transfer to monitor membrane fusion Biochemistry 20 1981 4093 4099
43. M. Lorizate, N. Huarte, A. Saez-Cirion, and J.L. Nieva Interfacial pre-transmembrane domains in viral proteins promoting membrane fusion and fission Biochim. Biophys. Acta 1778 2008 1624 1639
44. L. Shang, L. Yue, and E. Hunter Role of the membrane-spanning domain of human immunodeficiency virus type 1 envelope glycoprotein in cell-cell fusion and virus infection J. Virol. 82 2008 5417 5428 (Pubitemid 351705249)
45. C. Dietrich, L.A. Bagatolli, Z.N. Volovyk, N.L. Thompson, M. Levi, K. Jacobson, and E. Gratton Lipid rafts reconstituted in model membranes Biophys. J. 80 2001 1417 1428 (Pubitemid 32182165)
46. D. Allende, S.A. Simon, and T.J. McIntosh Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores Biophys. J. 88 2005 1828 1837 (Pubitemid 40976196)
47. M. Lorizate, A. Cruz, N. Huarte, R. Kunert, J. Perez-Gil, and J.L. Nieva Recognition and blocking of HIV-1 gp41 pre-transmembrane sequence by monoclonal 4E10 antibody in a Raft-like membrane environment J. Biol. Chem. 281 2006 39598 39606 (Pubitemid 46041919)
48. F. Nicol, S. Nir, and F.C. Szoka Jr. Effect of phospholipid composition on an amphipathic peptide-mediated pore formation in bilayer vesicles Biophys. J. 78 2000 818 829 (Pubitemid 30211839)
49. R. Sougrat, A. Bartesaghi, J.D. Lifson, A.E. Bennett, J.W. Bess, D.J. Zabransky, and S. Subramaniam Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry PLoS Pathog. 3 2007 e63
50. C. Magnus, P. Rusert, S. Bonhoeffer, A. Trkola, and R.R. Regoes Estimating the stoichiometry of human immunodeficiency virus entry J. Virol. 83 2009 1523 1531
51. P. Schon, A.J. Garcia-Saez, P. Malovrh, K. Bacia, G. Anderluh, and P. Schwille Equinatoxin II permeabilizing activity depends on the presence of sphingomyelin and lipid phase coexistence Biophys. J. 95 2008 691 698
52. A. Pokorny, and P.F. Almeida Permeabilization of raft-containing lipid vesicles by delta-lysin: a mechanism for cell sensitivity to cytotoxic peptides Biochemistry 44 2005 9538 9544 (Pubitemid 40962052)
53. A. Vidal, and T.J. McIntosh Transbilayer peptide sorting between raft and nonraft bilayers: comparisons of detergent extraction and confocal microscopy Biophys. J. 89 2005 1102 1108 (Pubitemid 41098992)
54. P. Zhu, J. Liu, J. Bess Jr., E. Chertova, J.D. Lifson, H. Grise, G.A. Ofek, K.A. Taylor, and K.H. Roux Distribution and three-dimensional structure of AIDS virus envelope spikes Nature 441 2006 847 852
55. W. Rawicz, B.A. Smith, T.J. McIntosh, S.A. Simon, and E. Evans Elasticity, strength, and water permeability of bilayers that contain raft microdomain-forming lipids Biophys. J. 94 2008 4725 4736
56. R.F. de Almeida, A. Fedorov, and M. Prieto Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophys. J. 85 2003 2406 2416 (Pubitemid 37210789)