The N-terminal 12 Residue Long Peptide of HIV gp41 is the Minimal Peptide Sufficient to Induce Significant T-cell-like Membrane Destabilization in Vitro

Journal of Molecular Biology

Volumn 359, Issue 3, 2006, Pages 597-609

  Charloteaux, B ^a   Lorin, A ^a   Crowet, J M ^a   Stroobant, V ^b   Lins, L ^a   Thomas, A ^a   Brasseur, R ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

Author keywords

fusion peptide; HIV 1; membrane fusion; molecular modelling; tilted peptide

Indexed keywords

GLYCOPROTEIN; GP41 PROTEIN; LIPOSOME; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPUTER MODEL; COMPUTER PROGRAM; HUMAN IMMUNODEFICIENCY VIRUS; HYDROPHILICITY; HYDROPHOBICITY; IN VITRO STUDY; MEMBRANE FUSION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RESIDUE ANALYSIS; T LYMPHOCYTE;

EID: 33646786476     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.04.018     Document Type: Article

References (104)

1. Colman P.M., and Lawrence M.C. The structural biology of type I viral membrane fusion. Nature Rev. Mol. Cell Biol. 4 (2003) 309-319
2. Eckert D.M., and Kim P.S. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70 (2001) 777-810
3. Gallo S.A., Finnegan C.M., Viard M., Raviv Y., Dimitrov A., Rawat S.S., et al. The HIV Env-mediated fusion reaction. Biochim. Biophys. Acta 1614 (2003) 36-50
4. Greenberg M., Cammack N., Salgo M., and Smiley L. HIV fusion and its inhibition in antiretroviral therapy. Rev. Med. Virol. 14 (2004) 321-337
5. Jiang S., Zhao Q., and Debnath A.K. Peptide and non-peptide HIV fusion inhibitors. Curr. Pharm. Des. 8 (2002) 563-580
6. Root M.J., and Steger H.K. HIV-1 gp41 as a target for viral entry inhibition. Curr. Pharm. Des. 10 (2004) 1805-1825
7. Weissenhorn W., Dessen A., Calder L.J., Harrison S.C., Skehel J.J., and Wiley D.C. Structural basis for membrane fusion by enveloped viruses. Mol. Membr. Biol. 16 (1999) 3-9
8. White J.M. Membrane fusion. Science 258 (1992) 917-924
9. Buchschacher Jr. G.L., Freed E.O., and Panganiban A.T. Effects of second-site mutations on dominant interference by a human immunodeficiency virus type 1 envelope glycoprotein mutant. J. Virol. 69 (1995) 1344-1348
10. Delahunty M.D., Rhee I., Freed E.O., and Bonifacino J.S. Mutational analysis of the fusion peptide of the human immunodeficiency virus type 1: identification of critical glycine residues. Virology 218 (1996) 94-102
11. Freed E.O., Myers D.J., and Risser R. Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proc. Natl Acad. Sci. USA 87 (1990) 4650-4654
12. Pritsker M., Rucker J., Hoffman T.L., Doms R.W., and Shai Y. Effect of nonpolar substitutions of the conserved Phe11 in the fusion peptide of HIV-1 gp41 on its function, structure, and organization in membranes. Biochemistry 38 (1999) 11359-11371
13. Martin I., Schaal H., Scheid A., and Ruysschaert J.M. Lipid membrane fusion induced by the human immunodeficiency virus type 1 gp41 N-terminal extremity is determined by its orientation in the lipid bilayer. J. Virol. 70 (1996) 298-304
14. Mobley P.W., Waring A.J., Sherman M.A., and Gordon L.M. Membrane interactions of the synthetic N-terminal peptide of HIV-1 gp41 and its structural analogs. Biochim. Biophys. Acta 1418 (1999) 1-18
15. Nir S., and Nieva J.L. Interactions of peptides with liposomes: pore formation and fusion. Prog. Lipid Res. 39 (2000) 181-206
16. Pereira F.B., Goni F.M., Muga A., and Nieva J.L. Permeabilization and fusion of uncharged lipid vesicles induced by the HIV-1 fusion peptide adopting an extended conformation: dose and sequence effects. Biophys. J. 73 (1997) 1977-1986
17. Pereira F.B., Goni F.M., and Nieva J.L. Membrane fusion induced by the HIV type 1 fusion peptide: modulation by factors affecting glycoprotein 41 activity and potential anti-HIV compounds. AIDS Res. Hum. Retroviruses 13 (1997) 1203-1211
18. Rafalski M., Lear J.D., and DeGrado W.F. Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41. Biochemistry 29 (1990) 7917-7922
19. Castano S., and Desbat B. Structure and orientation study of fusion peptide FP23 of gp41 from HIV-1 alone or inserted into various lipid membrane models (mono-, bi- and multibi-layers) by FT-IR spectroscopies and Brewster angle microscopy. Biochim. Biophys. Acta 1715 (2005) 81-95
20. Chang D.K., Cheng S.F., and Chien W.J. The amino-terminal fusion domain peptide of human immunodeficiency virus type 1 gp41 inserts into the sodium dodecyl sulfate micelle primarily as a helix with a conserved glycine at the micelle-water interface. J. Virol. 71 (1997) 6593-6602
21. Schaal H., Klein M., Gehrmann P., Adams O., and Scheid A. Requirement of N-terminal amino acid residues of gp41 for human immunodeficiency virus type 1-mediated cell fusion. J. Virol. 69 (1995) 3308-3314
22. Curtain C., Separovic F., Nielsen K., Craik D., Zhong Y., and Kirkpatrick A. The interactions of the N-terminal fusogenic peptide of HIV-1 gp41 with neutral phospholipids. Eur. Biophys. J. 28 (1999) 427-436
23. Durell S.R., Martin I., Ruysschaert J.M., Shai Y., and Blumenthal R. What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion (review). Mol. Membr. Biol. 14 (1997) 97-112
24. Epand R.M. Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta 1614 (2003) 116-121
25. Gordon L.M., Mobley P.W., Pilpa R., Sherman M.A., and Waring A.J. Conformational mapping of the N-terminal peptide of HIV-1 gp41 in membrane environments using (13)C-enhanced Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 1559 (2002) 96-120
26. 13C-enhanced Fourier transform infrared spectroscopy. Protein Sci. 13 (2004) 1012-1030
27. Kamath S., and Wong T.C. Membrane structure of the human immunodeficiency virus gp41 fusion domain by molecular dynamics simulation. Biophys. J. 83 (2002) 135-143
28. Morris K.F., Gao X., and Wong T.C. The interactions of the HIV gp41 fusion peptides with zwitterionic membrane mimics determined by NMR spectroscopy. Biochim. Biophys. Acta 1667 (2004) 67-81
29. Nieva J.L., Nir S., Muga A., Goni F.M., and Wilschut J. Interaction of the HIV-1 fusion peptide with phospholipid vesicles: different structural requirements for fusion and leakage. Biochemistry 33 (1994) 3201-3209
30. Nieva J.L., and Agirre A. Are fusion peptides a good model to study viral cell fusion?. Biochim. Biophys. Acta 1614 (2003) 104-115
31. Sackett K., and Shai Y. How structure correlates to function for membrane associated HIV-1 gp41 constructs corresponding to the N-terminal half of the ectodomain. J. Mol. Biol. 333 (2003) 47-58
32. 13C FTIR study. J. Mol. Biol. 350 (2005) 790-805
33. Saez-Cirion A., and Nieva J.L. Conformational transitions of membrane-bound HIV-1 fusion peptide. Biochim. Biophys. Acta 1564 (2002) 57-65
34. Waring A.J., Mobley P.W., and Gordon L.M. Conformational mapping of a viral fusion peptide in structure-promoting solvents using circular dichroism and electrospray mass spectrometry. Proteins: Struct. Funct. Genet. Suppl. 2 (1998) 38-49
35. Wasniewski C.M., Parkanzky P.D., Bodner M.L., and Weliky D.P. Solid-state nuclear magnetic resonance studies of HIV and influenza fusion peptide orientations in membrane bilayers using stacked glass plate samples. Chem. Phys. Lipids 132 (2004) 89-100
36. Yang J., Parkanzky P.D., Khunte B.A., Canlas C.G., Yang R., Gabrys C.M., and Weliky D.P. Solid state NMR measurements of conformation and conformational distributions in the membrane-bound HIV-1 fusion peptide. J. Mol. Graph. Model. 19 (2001) 129-135
37. Yang J., Gabrys C.M., and Weliky D.P. Solid-state nuclear magnetic resonance evidence for an extended beta strand conformation of the membrane-bound HIV-1 fusion peptide. Biochemistry 40 (2001) 8126-8137
38. Yang J., and Weliky D.P. Solid-state nuclear magnetic resonance evidence for parallel and antiparallel strand arrangements in the membrane-associated HIV-1 fusion peptide. Biochemistry 42 (2003) 11879-11890
39. Yang R., Yang J., and Weliky D.P. Synthesis, enhanced fusogenicity, and solid state NMR measurements of cross-linked HIV-1 fusion peptides. Biochemistry 42 (2003) 3527-3535
40. Yang R., Prorok M., Castellino F.J., and Weliky D.P. A trimeric HIV-1 fusion peptide construct which does not self-associate in aqueous solution and which has 15-fold higher membrane fusion rate. J. Am. Chem. Soc. 126 (2004) 14722-14723
41. Gordon L.M., Curtain C.C., Zhong Y.C., Kirkpatrick A., Mobley P.W., and Waring A.J. The amino-terminal peptide of HIV-1 glycoprotein 41 interacts with human erythrocyte membranes: peptide conformation, orientation and aggregation. Biochim. Biophys. Acta 1139 (1992) 257-274
42. Jaroniec C.P., Kaufman J.D., Stahl S.J., Viard M., Blumenthal R., Wingfield P.T., and Bax A. Structure and dynamics of micelle-associated human immunodeficiency virus gp41 fusion domain. Biochemistry 44 (2005) 16167-16180
43. Peisajovich S.G., Epand R.F., Pritsker M., Shai Y., and Epand R.M. The polar region consecutive to the HIV fusion peptide participates in membrane fusion. Biochemistry 39 (2000) 1826-1833
44. Buzon V., Padros E., and Cladera J. Interaction of fusion peptides from HIV gp41 with membranes: a time-resolved membrane binding, lipid mixing, and structural study. Biochemistry 44 (2005) 13354-13364
45. Martin I., Defrise-Quertain F., Decroly E., Vandenbranden M., Brasseur R., and Ruysschaert J.M. Orientation and structure of the NH2-terminal HIV-1 gp41 peptide in fused and aggregated liposomes. Biochim. Biophys. Acta 1145 (1993) 124-133
46. Sackett K., and Shai Y. The HIV-1 gp41 N-terminal heptad repeat plays an essential role in membrane fusion. Biochemistry 41 (2002) 4678-4685
47. Wexler-Cohen Y., Sackett K., and Shai Y. The role of the N-terminal heptad repeat of HIV-1 in the actual lipid mixing step as revealed by its substitution with distant coiled coils. Biochemistry 44 (2005) 5853-5861
48. Maddox M.W., and Longo M.L. Conformational partitioning of the fusion peptide of HIV-1 gp41 and its structural analogs in bilayer membranes. Biophys. J. 83 (2002) 3088-3096
49. Wong T.C. Membrane structure of the human immunodeficiency virus gp41 fusion peptide by molecular dynamics simulation. II. The glycine mutants. Biochim. Biophys. Acta 1609 (2003) 45-54
50. Brasseur R. Tilted peptides: a motif for membrane destabilization (hypothesis). Mol. Membr. Biol. 17 (2000) 31-40
51. Lins L., Charloteaux B., Thomas A., and Brasseur R. Computational study of lipid-destabilizing protein fragments: towards a comprehensive view of tilted peptides. Proteins: Struct. Funct. Genet. 44 (2001) 435-447
52. Peuvot J., Schanck A., Lins L., and Brasseur R. Are the fusion processes involved in birth, life and death of the cell depending on tilted insertion of peptides into membranes?. J. Theor. Biol. 198 (1999) 173-181
53. Ducarme P., Rahman M., and Brasseur R. IMPALA: a simple restraint field to simulate the biological membrane in molecular structure studies. Proteins: Struct. Funct. Genet. 30 (1998) 357-371
54. Basyn F., Charloteaux B., Thomas A., and Brasseur R. Prediction of membrane protein orientation in lipid bilayers: a theoretical approach. J. Mol. Graph. Model. 20 (2001) 235-244
55. Basyn F., Spies B., Bouffioux O., Thomas A., and Brasseur R. Insertion of X-ray structures of proteins in membranes. J. Mol. Graph. Model. 22 (2003) 11-21
56. Adam B., Lins L., Stroobant V., Thomas A., and Brasseur R. Distribution of hydrophobic residues is crucial for the fusogenic properties of the Ebola virus GP2 fusion peptide. J. Virol. 78 (2004) 2131-2136
57. Thomas A., Allouche M., Basyn F., Brasseur R., and Kerfelec B. Role of the lid hydrophobicity pattern in pancreatic lipase activity. J. Biol. Chem. 280 (2005) 40074-40083
58. Lins L., Charloteaux B., Heinen C., Thomas A., and Brasseur R. "De novo" design of peptides with specific lipid-binding properties. Biophys. J. 90 (2006) 470-479
59. Pereira F.B., Goni F.M., and Nieva J.L. Liposome destabilization induced by the HIV-1 fusion peptide effect of a single amino acid substitution. FEBS Letters 362 (1995) 243-246
60. Pereira F.B., Valpuesta J.M., Basanez G., Goni F.M., and Nieva J.L. Interbilayer lipid mixing induced by the human immunodeficiency virus type-1 fusion peptide on large unilamellar vesicles: the nature of the nonlamellar intermediates. Chem. Phys. Lipids 103 (1999) 11-20
61. El Kirat K., Lins L., Brasseur R., and Dufrene Y.F. Fusogenic tilted peptides induce nanoscale holes in supported phosphatidylcholine bilayers. Langmuir 21 (2005) 3116-3121
62. Eisenberg D., Weiss R.M., and Terwilliger T.C. The helical hydrophobic moment: a measure of the amphiphilicity of a helix. Nature 299 (1982) 371-374
63. Eisenberg D., Schwarz E., Komaromy M., and Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179 (1984) 125-142
64. Eisenberg D., Weiss R.M., and Terwilliger T.C. The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. Natl Acad. Sci. USA 81 (1984) 140-144
65. Callebaut I., Labesse G., Durand P., Poupon A., Canard L., Chomilier J., et al. Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cell Mol. Life Sci. 53 (1997) 621-645
66. Gaboriaud C., Bissery V., Benchetrit T., and Mornon J.P. Hydrophobic cluster analysis: an efficient new way to compare and analyse amino acid sequences. FEBS Letters 224 (1987) 149-155
67. Lemesle-Varloot L., Henrissat B., Gaboriaud C., Bissery V., Morgat A., and Mornon J.P. Hydrophobic cluster analysis: procedures to derive structural and functional information from 2-D-representation of protein sequences. Biochimie 72 (1990) 555-574
68. Woodcock S., Mornon J.P., and Henrissat B. Detection of secondary structure elements in proteins by hydrophobic cluster analysis. Protein Eng. 5 (1992) 629-635
69. Brasseur R., Lorge P., Goormaghtigh E., Ruysschaert J.M., Espion D., and Burny A. The mode of insertion of the paramyxovirus F1 N-terminus into lipid matrix, an initial step in host cell/virus fusion. Virus Genes 1 (1988) 325-332
70. Horth M., Lambrecht B., Khim M.C., Bex F., Thiriart C., Ruysschaert J.M., et al. Theoretical and functional analysis of the SIV fusion peptide. EMBO J. 10 (1991) 2747-2755
71. 2-terminal extremity of simian immunodeficiency virus gp32 and their mode of insertion into the lipid bilayer: an infrared spectroscopy study. J. Virol. 68 (1994) 1139-1148
72. Voneche V., Portetelle D., Kettmann R., Willems L., Limbach K., Paoletti E., et al. Fusogenic segments of bovine leukemia virus and simian immunodeficiency virus are interchangeable and mediate fusion by means of oblique insertion in the lipid bilayer of their target cells. Proc. Natl Acad. Sci. USA 89 (1992) 3810-3814
73. Bradshaw J.P., Darkes M.J., Harroun T.A., Katsaras J., and Epand R.M. Oblique membrane insertion of viral fusion peptide probed by neutron diffraction. Biochemistry 39 (2000) 6581-6585
74. Colotto A., Martin I., Ruysschaert J.M., Sen A., Hui S.W., and Epand R.M. Structural study of the interaction between the SIV fusion peptide and model membranes. Biochemistry 35 (1996) 980-989
75. Luneberg J., Martin I., Nussler F., Ruysschaert J.M., and Herrmann A. Structure and topology of the influenza virus fusion peptide in lipid bilayers. J. Biol. Chem. 270 (1995) 27606-27614
76. 31P NMR. Biochem. Biophys. Res. Commun. 250 (1998) 12-14
77. Martin I., Epand R.M., and Ruysschaert J.M. Structural properties of the putative fusion peptide of fertilin, a protein active in sperm-egg fusion, upon interaction with the lipid bilayer. Biochemistry 37 (1998) 17030-17039
78. Talmud P., Lins L., and Brasseur R. Prediction of signal peptide functional properties: a study of the orientation and angle of insertion of yeast invertase mutants and human apolipoprotein B signal peptide variants. Protein Eng. 9 (1996) 317-321
79. Mingeot-Leclercq M.P., Lins L., Bensliman M., Van Bambeke F., Van Der S.P., Peuvot J., et al. Membrane destabilization induced by beta-amyloid peptide 29-42: importance of the amino-terminus. Chem. Phys. Lipids 120 (2002) 57-74
80. Pillot T., Goethals M., Vanloo B., Talussot C., Brasseur R., Vandekerckhove J., et al. Fusogenic properties of the C-terminal domain of the Alzheimer beta-amyloid peptide. J. Biol. Chem. 271 (1996) 28757-28765
81. Del Angel V.D., Dupuis F., Mornon J.P., and Callebaut I. Viral fusion peptides and identification of membrane-interacting segments. Biochem. Biophys. Res. Commun. 293 (2002) 1153-1160
82. Tamm L.K., and Han X. Viral fusion peptides: a tool set to disrupt and connect biological membranes. Biosci. Rep. 20 (2000) 501-518
83. Galasko D. Cerebrospinal fluid levels of A beta 42 and tau: potential markers of Alzheimer's disease. J. Neural Transm. Suppl 53 (1998) 209-221
84. Gooch M.D., and Stennett D.J. Molecular basis of Alzheimer's disease. Am. J. Health Syst. Pharm. 53 (1996) 1545-1557
85. Shoji M. Cerebrospinal fluid Abeta40 and Abeta42: natural course and clinical usefulness. Front. Biosci. 7 (2002) d997-d1006
86. Fernandez A., and Berry R.S. Proteins with H-bond packing defects are highly interactive with lipid bilayers: implications for amyloidogenesis. Proc. Natl Acad. Sci. USA 100 (2003) 2391-2396
87. Soto C., and Frangione B. Two conformational states of amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neurosci. Letters 186 (1995) 115-118
88. Ravault S., Soubias O., Saurel O., Thomas A., Brasseur R., and Milon A. Fusogenic Alzheimer's peptide fragment Abeta (29-42) in interaction with lipid bilayers: secondary structure, dynamics, and specific interaction with phosphatidyl ethanolamine polar heads as revealed by solid-state NMR. Protein Sci. 14 (2005) 1181-1189
89. Decaffmeyer M., Lins L., Charloteaux B., Vaneyck M.H., Thomas A., and Brasseur R. Rational design of complementary peptides to the betaAmyloid 29-42 fusion peptide: an application of PepDesign. in the press. Biochim. Biophys. Acta (2006)
90. Ugolini S., Mondor I., and Sattentau Q.J. HIV-1 attachment: another look. Trends Microbiol. 7 (1999) 144-149
91. Bernstein H.B., Tucker S.P., Kar S.R., McPherson S.A., McPherson D.T., Dubay J.W., et al. Oligomerization of the hydrophobic heptad repeat of gp41. J. Virol. 69 (1995) 2745-2750
92. Chen S.S., Lee S.F., Hao H.J., and Chuang C.K. Mutations in the leucine zipper-like heptad repeat sequence of human immunodeficiency virus type 1 gp41 dominantly interfere with wild-type virus infectivity. J. Virol. 72 (1998) 4765-4774
93. Dubay J.W., Roberts S.J., Brody B., and Hunter E. Mutations in the leucine zipper of the human immunodeficiency virus type 1 transmembrane glycoprotein affect fusion and infectivity. J. Virol. 66 (1992) 4748-4756
94. Lu M., Ji H., and Shen S. Subdomain folding and biological activity of the core structure from human immunodeficiency virus type 1 gp41: implications for viral membrane fusion. J. Virol. 73 (1999) 4433-4438
95. Poumbourios P., Wilson K.A., Center R.J., El Ahmar W., and Kemp B.E. Human immunodeficiency virus type 1 envelope glycoprotein oligomerization requires the gp41 amphipathic alpha-helical/leucine zipper-like sequence. J. Virol. 71 (1997) 2041-2049
96. Shugars D.C., Wild C.T., Greenwell T.K., and Matthews T.J. Biophysical characterization of recombinant proteins expressing the leucine zipper-like domain of the human immunodeficiency virus type 1 transmembrane protein gp41. J. Virol. 70 (1996) 2982-2991
97. Wild C., Dubay J.W., Greenwell T., Baird Jr. T., Oas T.G., McDanal C., et al. Propensity for a leucine zipper-like domain of human immunodeficiency virus type 1 gp41 to form oligomers correlates with a role in virus- induced fusion rather than assembly of the glycoprotein complex. Proc. Natl Acad. Sci. USA 91 (1994) 12676-12680
98. Han X., Bushweller J.H., Cafiso D.S., and Tamm L.K. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nature Struct. Biol. 8 (2001) 715-720
99. Creighton T.E. In: Creighton T.E. (Ed). Proteins: Structures and Molecular Properties, Library of Congress Cataloging-in-Publication Data. 2nd edit (1997), W. H. Freeman and Company, New York 507
100. Lins L., Ducarme P., Breukink E., and Brasseur R. Computational study of nisin interaction with model membrane. Biochim. Biophys. Acta 1420 (1999) 111-120
101. Vogt B., Ducarme P., Schinzel S., Brasseur R., and Bechinger B. The topology of lysine-containing amphipathic peptides in bilayers by circular dichroism, solid-state NMR, and molecular modeling. Biophys. J. 79 (2000) 2644-2656
102. Aloia R.C., Tian H., and Jensen F.C. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl Acad. Sci. USA 90 (1993) 5181-5185
103. Barlett G.R. Colorimetric assay methods for free and phosphorylated glyceric acids. J. Biol. Chem. 65 (1959) 2146-2156
104. 2+-induced fusion and destabilization of liposomes. Biochemistry 24 (1985) 3099-3106