Properties and structures of the influenza and HIV fusion peptides on lipid membranes: Implications for a role in fusion

Biophysical Journal

Volumn 89, Issue 5, 2005, Pages 3183-3194

  Haque, Md Emdadul ^a   Koppaka, Vishwanath ^b   Axelsen, Paul H ^b   Lentz, Barry R ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; GLYCOPROTEIN GP 41; HEXADECANE; HYBRID PROTEIN; TRYPTOPHAN; VIRUS PROTEIN;

ALPHA HELIX; ARTICLE; BETA SHEET; BILAYER MEMBRANE; HUMAN IMMUNODEFICIENCY VIRUS; INFLUENZA VIRUS; LIPID MEMBRANE; LIPID VESICLE; LIPOPHILICITY; MEMBRANE COMPONENT; MEMBRANE FUSION; NONHUMAN; PARTITION COEFFICIENT; PROTEIN STRUCTURE; VIRUS CELL INTERACTION;

HUMAN IMMUNODEFICIENCY VIRUS; INFLUENZA VIRUS;

EID: 27744577746     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.063032     Document Type: Article

References (80)

1. White, J. M. 1990. Viral and cellular membrane fusion proteins. Annu. Rev. Physiol. 52:675-697.
2. Leikina, E., I. Markovic, L. V. Chernomordik, and M. M. Kozlov. 2000. Delay of influenza hemagglutinin refolding into a fusion-competent conformation by receptor binding: a hypothesis. Biophys. J. 79:1415-1427.
3. Markosyan, R. M., G. B. Melikyan, and F. S. Cohen. 1999. Tension of membranes expressing the hemagglutinin of influenza virus inhibits fusion. Biophys. J. 77:943-952.
4. Dimitrov, D. S., H. Golding, and R. Blumenthal. 1991. Initial stages of HIV-1 envelope glycoprotein-mediated cell fusion monitored by a new assay based on redistribution of fluorescent dyes. AIDS Res. Hum. Retroviruses. 7:799-805.
5. Freed, E. O., D. J. Myers, and R. Risser. 1990. Characterization of the fusion domain of the human immunodeficiency virus type 1 envelope glycoprotein gp41. Proc. Natl. Acad. Sci. USA. 87:4650-4654.
6. Lasky, L. A., G. Nakamura, D. H. Smith, C. Fennie, C. Shimasaki, E. Patzer, P. Berman, T. Gregory, and D. J. Capon. 1987. Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell. 50: 975-985.
7. Dragic, T., V. Litwin, G. P. Allaway, S. R. Martin, Y. Huang, K. A. Nagashirna, C. Cayanan, P. J. Maddon, R. A. Koup, J. P. Moore, and W. A. Paxton. 1996. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature. 381:667-673.
8. Wilkinson, D. 1996. Cofactors provide the entry keys. HIV-1. Curr. Biol. 6:1051-1053.
9. Broder, C. C., and D. S. Dimitrov. 1996. HIV and the 7-transmembrane domain receptors. Pathobiology. 64:171-179.
10. Moore, J. P., B. A. Jameson, R. A. Weiss, and Q. Sattentau. 1993. The HIV-Cell Fusion Reaction. J. Bentz, editor. CRC Press, Boca Raton, FL, Ann Arbor, MI, London, UK, and Tokyo, Japan.
11. Durell, S. R., I. Martin, J. M. Ruysschaert, Y. Shai, and R. Blumenthal. 1997. What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion (review). Mol. Membr. Biol. 14:97-112.
12. Hughson, F. M. 1995. Structural characterization of viral fusion proteins. Curr. Biol. 5:265-274.
13. Moore, J. P., B. A. Jameson, R. A. Weiss, and Q. J. Sattentau. 1993. Viral Fusion Mechanisms. CRC Press, Boca Raton, FL.
14. Gething, M. J., R. W. Doms, D. York, and J. White. 1986. Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus. J. Cell Biol. 102:11-23.
15. Stegmann, T., J. M. Delfino, F. M. Richards, and A. Helenius. 1991. The HA2 subunit of influenza hemagglutinin inserts into the target membrane prior to fusion. J. Biol. Chem. 266:18404-18410.
16. Tsurudome, M., R. Gluck, R. Graf, R. Falchetto, U. Schaller, and J. Brunner. 1992. Lipid interactions of the hemagglutinin HA2 NH2-terminal segment during influenza virus-induced membrane fusion. J. Biol. Chem. 267:20225-20232.
17. Wharton, S. A., S. R. Martin, R. W. Ruigrok, J. J. Skehel, and D. C. Wiley. 1988. Membrane fusion by peptide analogues of influenza virus haemagglutinin. J. Gen. Virol. 69:1847-1857.
18. Lear, J. D., and W. F. DeGrado. 1987. Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. J. Biol. Chem. 262:6500-6505.
19. Murata, M., Y. Sugahara, S. Takahashi, and S. Ohnishi. 1987. pH-dependent membrane fusion activity of a synthetic twenty amino acid peptide with the same sequence as that of the hydrophobic segment of influenza virus hemagglutinin. J: Biochem. (Tokyo). 102:957-962.
20. Kliger, Y., A. Aharoni, D. Rapaport, P. Jones, R. Blumenthal, and Y. Shai. 1997. Fusion peptides derived from the HIV type 1 glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell fusion. Structure- function study. J. Biol. Chem. 272:13496-13505.
21. Martin, I., F. Defrise-Quertain, E. Decroly, M. Vandenbranden, R. Brasseur, and J. M. Ruysschaert. 1993. Orientation and structure of the NH2-terminal HIV-1 gp41 peptide in fused and aggregated liposomes. Biochim. Biophys. Acta. 1145:124-133.
22. Pereira, F. B., F. M. Goni, A. Muga, and J. L. Nieva. 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.
23. Haque, M. E., A. J. McCoy, J. Glenn, J. Lee, and B. R. Lentz. 2001. Effects of hemagglutinin fusion peptide on poly(ethylene glycol)-mediated fusion of phosphatidylcholine vesicles. Biochemistry. 40: 14243-14251.
24. Haque, M. E., and B. R. Lentz. 2002. Influence of gp41 fusion peptide on the kinetics of poly(ethylene glycol)-mediated model membrane fusion. Biochemistry. 41:10866-10876.
25. Nieva, J. L., S. Nir, A. Muga, F. M. Goni, and J. Wilschut. 1994. Interaction of the HIV-1 fusion peptide with phospholipid vesicles: different structural requirements for fusion and leakage. Biochemistry. 33:3201-3209.
26. Gray, C., S. A. Tatulian, S. A. Wharton, and L. K. Tamm. 1996. Effect of the N-terminal glycine on the secondary structure, orientation, and interaction of the influenza hemagglutinin fusion peptide with lipid bilayers. Biophys. J. 70:2275-2286.
27. Matsumoto, T. 1999. Membrane destabilizing activity of influenza virus hemagglutinin-based synthetic peptide: implications of critical glycine residue in fusion peptide. Biophys. Chem. 79:153-162.
28. Pecheur, E. I., I. Martin, A. Bienvenue, J. M. Ruysschaert, and D. Hoekstra. 2000. Protein-induced fusion can be modulated by target membrane lipids through a structural switch at the level of the fusion peptide. J. Biol. Chem. 275:3936-3942.
29. Curtain, C., F. Separovic, K. Nielsen, D. Craik, Y. Zhong, and A. Kirkpatrick. 1999. The interactions of the N-terminal fusogenic peptide of HIV-1 gp41 with neutral phospholipids. Eur. Biophys. J. 28:427-436.
30. Epand, R. M., and R. F. Epand. 1994. Relationship between the infectivity of influenza virus and the ability of its fusion peptide to perturb bilayers. Biochem. Biophys. Res. Commun. 202:1420-1425.
31. Chen, P. S., Jr., T. Y. Toribara, and H. Warner. 1956. Microdetermination of phosphorus. Anal. Chem. 28:1756-1758.
32. Schwenk, E., and N. T. Werthessen. 1952. Studies on the biosynthesis of cholesterol. III. Purification of C(14)-cholesterol from perfusions of livers and other organs. Arch. Biochem. Biophys. 40:334-341.
33. Lentz, B. R., T. J. Carpenter, and D. R. Alford. 1987. Spontaneous fusion of phosphatidylcholine small unilamellar vesicles in the fluid phase. Biochemistry. 26:5389-5397.
34. Hope, M. J., M. B. Bally, G. Webb, and P. R. Cullis. 1985. 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. 812:55-65.
35. Lentz, B. R., G. F. McIntyre, D. J. Parks, J. C. Yates, and D. Massenburg. 1992. Bilayer curvature and certain amphipaths promote poly(ethylene glycol)-induced fusion of dipalmitoylphosphatidylcholine unilamellar vesicles. Biochemistry. 31:2643-2653.
36. Lee, J., and B. R. Lentz. 1997. Outer leaflet-packing defects promote poly(ethylene glycol)-mediated fusion of large unilamellar vesicles. Biochemistry. 36:421-431.
37. Chattopadhyay, A., and E. London. 1987. Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry. 26:39-45.
38. Lewis, B. A., and D. M. Engelman. 1983. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211-217.
39. McIntosh, T. J., and P. W. Holloway. 1987. Determination of the depth of bromine atoms in bilayers formed from bromolipid probes. Biochemistry. 26:1783-1788.
40. Sreerama, N., and R. W. Woody. 2000. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287:252-260.
41. Silvestro, L., and P. H. Axelsen. 1998. Infrared spectroscopy of supported lipid monolayer, bilayer, and multibilayer membranes. Chem. Phys. Lipids. 96:69-80.
42. Axelsen, P. H., W. D. Braddock, H. L. Brockman, C. M. Jones, R. A. Dluhy, B. K. Kaufman, and F. J. Puga II. 1995. Use of internal reflectance infrared spectroscopy for the in-situ study of supported lipid monolayers. Appl. Spectrosc. 49:526-531.
43. Silvestro, L., and P. H. Axelsen. 1999. Fourier transform infrared linked analysis of conformational changes in annexin V upon membrane binding. Biochemistry. 38:113-121.
44. Axelsen, P. H., and M. J. Citra. 1996. Orientational order determination by internal reflection infrared spectroscopy. Prog. Biophys. Mol. Biol. 66:227-253.
45. Silvestro, L., and P. H. Axelsen. 2000. Membrane-induced folding of cecropin A. Biophys. J. 79:1465-1477.
46. Slater, S. J., M. B. Kelly, F. J. Taddeo, C. Ho, E. Rubin, and C. D. Stubbs. 1994. The modulation of protein kinase C activity by membrane lipid bilayer structure. J. Biol. Chem. 269:4866-4871.
47. Rafalski, M., A. Ortiz, A. Rockwell, L. C. van Ginkel, J. D. Lear, W. F. DeGrado, and J. Wilschut. 1991. Membrane fusion activity of the influenza virus hemagglutinin: interaction of HA2 N-terminal peptides with phospholipid vesicles. Biochemistry. 30:10211-10220.
48. Pecheur, E. I., J. Sainte-Marie, A. Bienvenue, and D. Hoekstra. 1999. Peptides and membrane fusion: towards an understanding of the molecular mechanism of protein-induced fusion. J. Membr. Biol. 167:1-17.
49. Koppaka, V., and B. R. Lentz. 1996. Binding of bovine factor Va to phosphatidylcholine membranes. Biophys. J. 70:2930-2937.
50. Lentz, B. R. 1993. Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. Chem. Phys. Lipids. 64: 99-116.
51. Stubbs, C. D., C. Ho, and S. J. Slater. 1995. Fluorescence techniques for probing water penetration into lipid bilayers. J. Fluo. 5.
52. Clague, M.-J., J. R. Knutson, R. Blumenthal, and A. Herrmann. 1991. Interaction of influenza hemagglutinin amino-terminal peptide with phospholipid vesicles: a fluorescence study. Biochemistry. 30:5491-5497.
53. Zhelev, D. V., N. Stoicheva, P. Scherrer, and D. Needham. 2001. Interaction of synthetic HA2 influenza fusion peptide analog with model membranes. Biophys. J. 81:285-304.
54. Luneberg, J., I. Martin, F. Nussler, J. M. Ruysschaert, and A. Herrmann. 1995. Structure and topology of the influenza virus fusion peptide in lipid bilayers. J. Biol. Chem. 270:27606-27614.
55. Burger, K. N., S. A. Wharton, R. A. Demel, and A. J. Verkleij. 1991. The interaction of synthetic analogs of the N-terminal fusion sequence of influenza virus with a lipid monolayer. Comparison of fusion-active and fusion-defective analogs. Biochim. Biophys. Acta. 1065: 121-129.
56. Takahashi, S. 1990. Conformation of membrane fusion-active 20-residue peptides with or without lipid bilayers. Implication of alpha-helix formation for membrane fusion. Biochemistry. 29:6257-6264.
57. Murata, M., S. Takahashi, S. Kagiwada, A. Suzuki, and S. Ohnishi. 1992. pH-dependent membrane fusion and vesiculation of phospholipid large unilamellar vesicles induced by amphiphilic anionic and cationic peptides. Biochemistry. 31:1986-1992.
58. Ishiguro, R., N. Kimura, and S. Takahashi. 1993. Orientation of fusion-active synthetic peptides in phospholipid bilayers: determination by Fourier transform infrared spectroscopy. Biochemistry. 32:9792-9797.
59. Ishiguro, R., M. Matsumoto, and S. Takahashi. 1996. Interaction of fusogenic synthetic peptide with phospholipid bilayers: orientation of the peptide alpha-helix and binding isotherm. Biochemistry. 35:4976-4983.
60. Luneberg, J., I. Martin, F. Nussler, J. M. Ruysschaert, and A. Herrmann. 1995. Structure and topology of the influenza virus fusion peptide in lipid bilayers. J. Biol. Chem. 270:27606-27614.
61. Rafalski, M., J. D. Lear, and W. F. DeGrado. 1990. Phospholipid interactions of synthetic peptides representing the N- terminus of HIV gp41. Biochemistry. 29:7917-7922.
62. Chang, D. K., S. F. Cheng, and W. J. Chien. 1997. The amino-terminal fusion domain peptide of human immunodeficiency virus type 1 Gp41 inserts into the sodium dodecyl sulfate micelle primarily as helix with a conserved glycine at the micelle-water interface. J. Virol. 71:6593-6602.
63. Bodner, M. L., C. M. Gabrys, P. D. Parkanzky, J. Yang, C. A. Duskin, and D. P. Weliky. 2004. Temperature dependence and resonance assignment of 13C NMR spectra of selectively and uniformly labeled fusion peptides associated with membranes. Magn. Reson. Chem. 42:187-194.
64. Krimm, S., and J. Bandekar. 1986. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem. 38:181-364.
65. Wimley, W. C., K. Hristova, A. S. Ladokhin, L. Silvestro, P. H. Axelsen, and S. H. White. 1998. Folding of beta-sheet membrane proteins: a hydrophobic hexapeptide model. J. Mol. Biol. 277:1091-1110.
66. Slepushkin, V. A., S. M. Andreev, M. V. Sidorova, G. B. Melikyan, V. B. Grigoriev, V. M. Chumakov, A. E. Grinfeldt, R. A. Manukyan, and E. V. Karamov. 1992. Investigation of human immunodeficiency virus fusion peptides. Analysis of interrelations between their structure and function. AIDS Res. Hum. Retroviruses. 8:9-18.
67. Terletskaya, Y. T., I. O. Trikash, E. S. Serdyuk, and S. M. Andreev. 1995. Fusion of negatively charged liposomes induced by peptides of the N-terminal fragment of HIV-1 transmembrane protein. Biochemistry (Mosc.). 60:1309-1314.
68. Gordon, L. M., C. C. Curtain, Y. C. Zhong, A. Kirkpatrick, P. W. Mobley, and A. J. Waring. 1992. The ammo-terminal peptide of HIV-1 glycoprotein 41 interacts with human erythrocyte membranes: peptide conformation, orientation and aggregation. Biochim. Biophys. Acta. 1139:257-274.
69. Martin, I., H. Schaal, A. Scheid, and J. M. Ruysschaert. 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.
70. Yang, J., C. M. Gabrys, and D. P. Weliky. 2001. Solid-state nuclear magnetic resonance evidence for an extended beta strand conformation of the membrane-bound HIV-1 fusion peptide. Biochemistiy. 40:8126-8137.
71. Koppaka, V., L. Silvestro, J. A. Engler, C. G. Brouillette, and P. H. Axelsen. 1999. The structure of human lipoprotein A-I. Evidence for the "belt" model. J. Biol. Chem. 274:14541-14544.
72. Han, X., J. H. Bushweller, D. S. Cafiso, and L. K. Tamm. 2001. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 8:715-720.
73. Vaccaro, L., K. J. Cross, J. Kleinjung, S. K. Straus, D. J. Thomas, S. A. Wharton, J. J. Skehel, and F. Fraternali. 2005. Plasticity of influenza haemagglutinin fusion peptides and their interaction with lipid bilayers. Biophys. J. 88:25-36.
74. Yang, J., and D. P. Weliky. 2003. Solid-state nuclear magnetic resonance evidence for parallel and antiparallel strand arrangements in the membrane-associated HIV-1 fusion peptide. Biochemistry. 42:11879-11890.
75. Clodi, K., K. O. Kliche, S. Zhao, D. Weidner, T. Schenk, U. Consoli, S. Jiang, V. Snell, and M. Andreeff. 2000. Cell-surface exposure of phosphatidylserine correlates with the stage of fludarabine-induced apoptosis in chronic lymphocytic leukemia and expression of apoptosis-regulating genes. Cytometry. 40:19-25.
76. Mourdjeva, M., D. Kyurkchiev, A. Mandinova, I. Altankova, I. Kehayov, S. Kyurkchiev, K. Clodi, K. O. Kliche, S. Zhao, D. Weidner, T. Schenk, U. Consoli, et al. 2005. Dynamics of membrane translocation of phosphatidylserine during apoptosis detected by a monoclonal antibody. Cell-surface exposure of phosphatidylserine correlates with the stage of fludarabine-induced apoptosis in chronic lymphocytic leukemia and expression of apoptosis-regulating genes. Apoptosis. 10:209-217.
77. Colotto, A., I. Martin, J. M. Ruysschaert, A. Sen, S. W. Hui, and R. M. Epand. 1996. Structural study of the interaction between the SIV fusion peptide and model membranes. Biochemistry. 35:980-989.
78. Chen, Z., and R. P. Rand. 1998. Comparative study of the effects of several n-alkanes on phospholipid hexagonal phases. Biophys. J. 74: 944-952.
79. Malinin, V. S., P. Frederik, and B. R. Lentz. 2002. Osmotic and curvature stress affect PEG-induced fusion of lipid vesicles but not mixing of their lipids. Biophys. J. 82:2090-2100.
80. Malinin, V., and B. R. Lentz. 2004. Energetics of vesicle fusion intermediates: comparison of calculations with observed effects of osmotic and curvature stresses. Biophys. J. 86:2951-2964.