Conformational mapping of the N-terminal peptide of HIV-1 gp41 in lipid detergent and aqueous environments using 13C-enhanced Fourier transform infrared spectroscopy

Protein Science

Volumn 13, Issue 4, 2004, Pages 1012-1030

  Gordon, Larry M ^a   Mobley, Patrick W ^b   Lee, William ^b   Eskandari, Sepehr ^b   Kaznessis, Yiannis N ^c   Sherman, Mark A ^d   Waring, Alan J ^a,e  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b CALIFORNIA STATE POLYTECHNIC UNIVERSITY   (United States)

^c University of Minnesota   (United States)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid; CD spectroscopy; Computer simulations; Electron microscopy; Fusion; Isotope enhanced FTIR spectroscopy; Prion; Secondary structure

Indexed keywords

AMYLOID; CARBON 13; DETERGENT; GLYCOPROTEIN GP 41; HYBRID PROTEIN; PRION PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; AQUEOUS SOLUTION; ARTICLE; COMPUTER SIMULATION; ELECTRON MICROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS 1; INFRARED SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CARBON ISOTOPES; DETERGENTS; HIV ENVELOPE PROTEIN GP41; HIV-1; LIPIDS; LIPOSOMES; MEMBRANE FUSION; MICELLES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; SODIUM DODECYL SULFATE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 1842611408     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03407704     Document Type: Article

References (77)

1. Agirre, A., Flach, C., Goni, F.M., Mendelsohn, R., Valpuesta, J.M., Wu, F., and Nieva, J.L. 2000. Interactions of the HIV-1 fusion peptide with large unilamellar vesicles and monolayers. A cryo-TEM and spectroscopic study. Biochim. Biophys. Acta 1467: 153-164.
2. Aloia, R.C., Jensen, F.C., Curtain, C.C., Mobley, P.W., and Gordon, L.M. 1988. Lipid composition and fluidity of the human immunodeficiency virus type-1. Proc. Natl. Acad. Sci. 85: 900-904.
3. Andersen, H.C. 1980. Molecular dynamics simulations at constant pressure and/or temperature. J. Chem. Phys. 72: 2384-2393.
4. Ashburn, T.T., Auger, M., and Lansbury Jr., P.T. 1992. The structural basis of pancreatic amyloid formation: Isotope-edited spectroscopy in the solid state. J. Am. Chem. Soc. 114: 790-791.
5. Baldwin, M.A. 1999. Stable isotope-labeled peptides in study of protein aggregation. Methods Enzymol. 309: 576-591.
6. Bergeron, L., Sullivan, N., and Sodroski, J. 1992. Target cell-specific determinants of membrane fusion within the human immunodeficiency virus type 1 gp120 third variable region and gp41 amino terminus. J. Virol. 66: 2389-2397.
7. 13C isotope labeling of hydrophobic peptides. Origin of the anomalous intensity distribution in the infrared amide I spectral region of β-sheet structures. J. Am. Chem. Soc. 122: 677-683.
8. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S., and Karplus, M. 1983. CHARMM: A program for macromolecular energy, minimization, and dynamics simulations. J. Comp. Chem. 4: 187-217.
9. Bullough, P.A., Hughson, F.M., Skehel, J.J., and Wiley, D.C. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371: 37-43.
10. Byler, D.M. and Susi, H. 1986. Examination of the secondary structure of protein by deconvolved FTIR spectra. Biopolymers 25: 469-487.
11. Callebaut, I., Tasso, A., Brasseur, R., Burny, A., Portetelle, D., and Mornon, J.P. 1994. Common prevalence of alanine and glycine in mobile reactive centre loops of serpins and viral fusion peptides: Do prions possess a fusion peptide? J. Comput. Aided Mol. Des. 8: 175-191.
12. Chang, D.-K., Cheng, S.-F., and Chien, W.-J. 1997a. 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: 6593-6602.
13. Chang, D.-K., Chien, W.-J., and Cheng, S.-F. 1997b. The FLG motif in the N-terminal region of glucoprotein 41 of human immunodeficiency virus type 1 adopts a type-1 β turn in aqueous solution and serves as the initiation site for helix formation. Eur. J. Biochem. 247: 896-905.
14. Curtain, C.C., Separovic, F., Nielsen, K., Craik, D., Zhong, Y.C., and Kirkpatrick, A. 1999. The interactions of the N-terminal fusogenic peptide of HIV-1 gp41 with neutral phospholipids. Eur. Biophys. J. 28: 427-436.
15. Delahunty, M.D., Rhee, I., Freed, E.O., and Bonifacino, J.S. 1996. Mutational analysis of the fusion peptide of the human immunodeficiency virus type 1: Identification of critical glycine residues. Virology 218: 94-102.
16. Dimitrov, A.S., Xiao, X., Dimitrov, D.S., and Blumenthal, R. 2001. Early intermediates in HIV-1 envelope glycoprotein-mediated fusion triggered by CD4 and co-receptor complexes. J. Biol. Chem. 276: 30335-30341.
17. Dwivedi, A.M. and Krimm, S. 1984. Vibrational analysis of peptides, polypeptides, and proteins. XXIV. Conformation of poly(α-aminoisobutyric acid). Biopolymers 23: 2025-2065.
18. Essman, U., Perera, L., Berkowitz, M.L., Darden, T., Lee, H., and Pedersen, L.G. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103: 8577-8593.
19. Fernandez, A. and Berry, R.S. 2003. Proteins with H-bond packing defects are highly interactive with lipids bilayers: Implications for amyloidogenesis. Proc. Natl. Acad. Sci. 100: 2391-2396.
20. Fodje, M.N. and Al-Karadaghi, S. 2002. Occurrence, conformational features and amino acid propensities for the π-helix. Protein Eng. 15: 353-358.
21. Freed, E.O., Myers, D.J., and Risser, R. 1990. Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proc. Natl. Acad. Sci. 87: 4650-4654.
22. Gallaher, W.R. 1987. Detection of a fusion peptide sequence in the transmembrane protein of the human immunodeficiency virus. Cell 50: 327-328.
23. Gonzalez-Scarano, F., Waxham, M.N., Ross, A.M., and Hoxie, J.A. 1987. Sequence similarities between human immunodeficiency virus gp41 and paramyxovirus fusion proteins. AIDS Res. Hum. Retroviruses 3: 245-252.
24. Goormaghtigh, E., Raussens, V., and Ruysschaert, J.-M. 1999. Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim. Biophys. Acta 1422: 105-185.
25. Gordon, L.M., Curtain, C.C., Zhong, Y.C., Kirkpatrick, A., Mobley, P.W., and Waring, A.J. 1992. The amino terminal peptide of HIV-1 glycoprotein 41 interacts with human erythrocyte membranes: Peptide conformation, orientation and aggregation. Biochim. Biophys. Acta 1139: 257-274.
26. Gordon, L.M., Horvath, S., Longo, M.L., Zasadzinski, J.A., Taeusch, W., Faull, K., Leung, C., and Waring, A.J. 1996. Conformational and molecular topography of the N-terminal segment of surfactant protein B in structure-promoting environments. Protein Sci. 5: 1662-1675.
27. 13C-enhanced Fourier transform infrared spectroscopy. J. Peptide Res. 55: 330-347.
28. 13C-enhanced Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 1559: 96-120.
29. Gustafsson, M., Thyberg, J., Naslund, J., Eliasson, E., and Johansson, J. 1999. Amyloid fibril formation by pulmonary surfactant protein C. FEBS Lett. 464: 138-142.
30. Halverson, K.J., Sucholeiki, I., Ashburn, T.T., and Lansbury Jr., P.T. 1991. Location of β-sheet-forming sequences in amyloid proteins by FTIR. J. Am. Chem. Soc. 113: 6701-6703.
31. Haris, P.I. and Chapman, D. 1995. The conformational analysis of peptides using Fourier transform IR spectroscopy. Biopolymers 37: 251-263.
32. Henry, G.D. and Sykes, B.D. 1994. Methods to study membrane protein structure in solution. Methods Enzymol. 239: 515-535.
33. Hoover, W.H. 1985. Canonical dynamics: Equilibrium phase-space distributions. Phys. Rev. A 31: 1695-1697.
34. Jiang, S., Zhao, Q., and Debnath, A.K. 2002. Peptide and non-peptide HIV fusion inhibitors. Curr. Pharm. Des. 8: 563-580.
35. Johansson, J. 2001. Membrane properties and amyloid fibril formation of lung surfactant protein C. Biochem. Soc. Trans. 29: 601-606.
36. Johansson, J., Szyperski, T., Curstedt, T., and Wuthrich, K. 1994. The NMR structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich α-helix. Biochemistry 33: 6015-6023.
37. Jorgensen, W.L., Chandrasekhar, J., Medura, J.D., Impey, R.W., and Klein, M.L. 1983. Comparison of simple potential function for simulating liquid water. J. Chem. Phys. 79: 926-935.
38. Kabsch, W. and Sander, C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
39. Kamath, S. and Wong, T.C. 2002. Membrane structure of the Human Immunodeficiency Virus gp41 fusion domain by molecular dynamics simulation. Biophys. J. 83: 135-143.
40. Kaznessis, Y.N., Kim, S., and Larson, R.G. 2002. Specific mode of interaction between components of model pulmonary surfactants using computer simulations. J. Mol. Biol. 322: 569-582.
41. Kliger, Y., Aharoni, A., Rapaport, D., Jones, P., Blumenthal, R., and Shai, Y. 1997. Fusion peptides derived from the HIV type 1 glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell fusion. J. Biol. Chem. 272: 13496-13505.
42. Kovacs, H., Mark, A.E., Johansson, J., and van Gusteren, W.F. 1995. The effect of environment on the stability of an integral membrane helix: Molecular dynamics simulations of surfactant protein C in chloroform, methanol and water. J. Mol. Biol. 247: 808-822.
43. Krimm, S. and Bandekar, J. 1986. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem. 38: 181-364.
44. Lorenzo, A. and Yankner, B.A. 1994. β-amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc. Natl. Acad. Sci. 91: 12243-12247.
45. Lu, M., Blacklow, S.C., and Kim, P.S. 1995. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2: 1075-1082.
46. Ludlam, C.F.C., Arkin, I.T., Liu, X.-M., Rothman, M.S., Rath, P., Aimoto, S., Smith, S.O., Engelman, D.M., and Rothschild, K.J. 1996. Fourier transform infrared spectroscopy and site-directed isotope labeling as a probe of local secondary structure in the transmembrane domain of phospholamban. Biophys. J. 70: 1728-1736.
47. MacKerell, A. 1995. Molecular dynamics simulation analysis of a sodium dodecyl sulfate micelle in aqueous solution: Decreased fluidity of the micelle hydrophobic interior. J. Phys. Chem. 99: 1846-1855.
48. Maddox, M.W. and Longo, M.L. 2002. Conformational partitioning of the fusion peptide of HIV-1 gp41 and its structural analogs in bilayer membranes. Biophys. J. 83: 3088-3096.
49. 2-terminal HIV-1 gp41 peptide in fused and aggregated liposomes. Biochim. Biophys. Acta 1145: 124-133.
50. Martin, I., Schaal, H., Scheid, A., and Ruysschaert, J.-M. 1996. 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: 298-304.
51. McCune, J.M., Rabin, L.B., Feinberg, M.B., Lieberman, M., Kosek, J.C., Reyes, G.R., and Weisman, I.L. 1988. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 53: 55-67.
52. + lymphocytes. Biochim. Biophys. Acta 1139: 251-256.
53. Mobley, P.W., Lee, H.-F., Curtain, C.C., Kirkpatrick, A., Waring, A.J., and Gordon, L.M. 1995. The amino-terminal peptide of HIV-1 glycoprotein 41 fuses human erythrocytes. Biochim. Biophys. Acta 1271: 304-315.
54. Mobley, P.W., Waring, A.J., Sherman, M.A., and Gordon, L.M. 1999. Membrane interactions of the synthetic N-terminal peptide of HIV-1 gp41 and its structural analogs. Biochim. Biophys. Acta 1418: 1-18.
55. Mobley, P.W., Pilpa, R., Brown, C., Waring, A.J., and Gordon, L.M. 2001. Membrane-perturbing domains of HIV Type 1 glycoprotein 41. AIDS Res. Hum. Retroviruses 17: 311-327.
56. Moore, W.H. and Krimm, S. 1976a. Vibrational analysis of peptides, polypeptides, and proteins. I. Polyglycine I. Biopolymers 15: 2439-2464.
57. -. 1976b. Vibrational analysis of peptides, polypeptides, and proteins. II. β-poly(L-alanine) and β-poly(L-alanylglycine). Biopolymers 15: 2465-2483.
58. Myers, G., Korber, B., Berzofsky, J.A., Smith, R.F., and Pavalakis, G.N. 1991. Human retroviruses and AIDS 1991: A compilation and analysis of nucleic acid and amino acid sequences, p. II-81. Los Alamos National Laboratory, Los Alamos, NM.
59. Nieva, J.L., Nir, S., Muga, A., Goni, F.M., and Wilschut, J. 1994. Interaction of the HIV-1 fusion peptide with phospholipid vesicles: Different structural requirements for fusion and leakage. Biochemistry 33: 3201-3209.
60. Nieva, J.L., Goni, F.M., Mason, A.L., Mock, A.R., Muga, A., Saez, A., and Gallaher, W.R. 2000. Similarities of prion protein to fusion/entry proteins of HIV and ebola: Membrane interactions of its putative fusion domain. Biophys. J. 78: 412A.
61. Pereira, F.B., Goni, F.M., and Nieva, J.L. 1995. Liposome destabilization induced by the HIV-1 fusion peptide: Effect of a single amino acid substitution. FEBS Lett. 362: 243-246.
62. -. 1997. 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: 1977-1986.
63. Pillot, T., Lins, L., Goethals, M., Vanloo, B., Baert, J., Vandekerckhove, J., Rosseneu, M., and Brasseur, R. 1997. The 118-135 peptide of the human prion protein forms amyloid fibrils and induces liposome fusion. J. Mol. Biol. 274: 381-393.
64. Rafalski, M., Lear, J.D., and DeGrado, W.F. 1990. Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41. Biochemistry 29: 7917-7922.
65. Ryckaert, J.P., Ciccotti, G., and Berendesen, H.J.C. 1977. Numerical integration of the cartesian equations of motion for a system with constraints: Molecular dynamics of n-alkanes. J. Comp. Phys. 23: 327-341.
66. Saez-Cirion, A. and Nieva, J.L. 2002. Conformational transitions of membrane-bound HIV-1 fusion peptide. Biochim. Biophys. Acta 1564: 57-65.
67. Schaal, H., Klein, M., Gehrmann, P., Adams, O., and Scheid, A. 1995. Requirement of N-terminal amino acid residues of gp41 for human immunodeficiency virus type 1-mediated cell fusion. J. Virol. 69: 3308-3314.
68. Slepushkin, V.A., Melikyan, G.B., Sidorova, M.V., Chumakov, V.M., Andreev, S.M., Manukyan, R.A., and Karamov, E.V. 1990. Interaction of human immunodeficiency virus (HIV-1) fusion peptide with artificial lipid membranes. Biochem. Biophys. Res. Commun. 172: 952-957.
69. Slepushkin, V.A., Andreev, S.M., Sidorova, M.V., Melikyan, G.B., Grigoriev, V.B., Chumakov, V.M., Grinfeldt, A.E., Manukyan, R.A., and Karamov, E.V. 1992. Investigation of human immunodeficiency virus fusion peptides. Analysis of interrelations between their structure and function. AIDS Res. Hum. Retroviruses 8: 9-18.
70. Surewicz, W.K. and Mantsch, H.H. 1988. New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. Biophys. Acta 952: 115-130.
71. Tadesse, L., Nazarbaghi, R., and Walters, L. 1991. Isotopically-enhanced infrared spectroscopy: A novel method for examining secondary structure at specific sites in conformationally heterogeneous peptides. J. Am. Chem. Soc. 113: 7036-7037.
72. Tamm, L.K. and Han, X. 2000. Viral fusion peptides: A tool set to disrupt and connect biological membranes. Biosci. Rep. 20: 501-518.
73. Tenidis, K., Waldner, M., Bernhagen, J., Fischle, W., Bergmann, M., Weber, M., Merkle, M.-L., Voelter, W., Brunner, H., and Kapurniotu, A. 2000. Identification of a penta- and hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties. J. Mol. Biol. 295: 1055-1071.
74. Vidal, P., Chaloin, L., Heitz, A., Van Mau, N., Mery, J., Divita, G., and Heitz, F. 1998. Interactions of primary amphipathic vector peptides with membranes. Conformational consequences and influence on cellular localization. J. Membr. Biol. 162: 259-264.
75. Weaver, T.M. 2000. The π-helix translates structure into function. Protein Sci. 9: 201-206.
76. Weissenhorn, W., Dessen, A., Harrison, S.C., Skehel, J.J., and Wiley, D.C. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387: 426-430.
77. Yang, J., Gabrys, C.M., and Weliky, D.P. 2001. Solid-state nuclear magnetic resonance evidence for an extended β strand conformation of the membrane-bound HIV-1 fusion peptide. Biochemistry 40: 8126-8137.