Oligomeric β-structure of the membrane-bound HIV-1 fusion peptide formed from soluble monomers

Biophysical Journal

Volumn 87, Issue 3, 2004, Pages 1951-1963

  Yang, Jun ^a   Prorok, Mary ^b   Castellino, Francis J ^b   Weliky, David P ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CHOLESTEROL; LIPID; MEMBRANE PROTEIN; MONOMER; OLIGOMER; VIRUS FUSION PROTEIN;

AQUEOUS SOLUTION; ARTICLE; BETA SHEET; CELL FUSION; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE FUSION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN STRUCTURE; SOLID STATE; SOLID STATE NUCLEAR MAGNETIC RESONANCE; TARGET CELL; VIRUS CELL INTERACTION;

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

EID: 4444320707     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.103.028530     Document Type: Article

References (97)

1. 19F NMR structure analysis of membrane-associated peptides. ChemBioChem. 4:1151-1163.
2. Aloia, R. C., H. Tian, and F. C. Jensen. 1993. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl. Acad. Sci. USA. 90:5181-5185.
3. Balbach, J. J., J. Yang, D. P. Weliky, P. J. Steinbach, V. Tugarinov, J. Anglister, and R. Tycko. 2000. Probing hydrogen bonds in the antibody-bound HIV-1 gp120 V3 loop by solid state NMR REDOR measurements. J. Biomol. NMR. 16:313-327.
4. Bennett, A. E., C. M. Rienstra, M. Auger, K. V. Lakshmi, and R. G. Griffin. 1995. Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103:6951-6958.
5. Bentz, J. 2000a. Membrane fusion mediated by coiled coils: a hypothesis. Biophys. J. 78:886-900.
6. Bentz, J. 2000b. Minimal aggregate size and minimal fusion unit for the first fusion pore of influenza hemagglutinin-mediated membrane fusion. Biophys. J. 78:227-245.
7. Blumenthal, R., M. J. Clague, S. R. Durell, and R. M. Epand. 2003. Membrane fusion. Chem. Rev. 103:53-69.
8. Blumenthal, R., D. P. Sarkar, S. Durell, D. E. Howard, and S. J. Morris. 1996. Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J. Cell Biol. 135:63-71.
9. 13C NMR spectra of selectively and uniformly labeled fusion peptides associated with membranes. Magn. Reson. Chem. 42:187-194.
10. Caffrey, M., M. Cai, J. Kaufman, S. J. Stahl, P. T. Wingfield, D. G. Covell, A. M. Gronenborn, and G. M. Clore. 1998. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J. 17:4572-4584.
11. Cantor, C. R., and P. R. Shimmel. 1980. Biophysical Chemistry Part II: Techniques for the Study of Biological Structure and Function. W. H. Freeman, New York.
12. Cavanaugh, J., W. J. Fairbrother, A. G. Palmer, and N. J. Skelton. 1996. Protein NMR Spectroscopy Principles and Practice. Academic Press, San Diego, CA.
13. Chan, D. C., D. Pass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell. 89:263-273.
14. Chang, D. K., and S. F. Cheng. 1998. Determination of the equilibrium micelle-inserting position of the fusion peptide of gp41 of human immunodeficiency virus type 1 at amino acid resolution by exchange broadening of amide proton resonances. J. Biomol. NMR. 12:549-552.
15. Chang, D. K., S. F. Cheng, and W. J. Chien. 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.
16. Chang, D. K., S. F. Cheng, and V. D. Trivedi. 1999. Biophysical characterization of the structure of the amino-terminal region of gp41 of HIV-1. Implications on viral fusion mechanism. J. Biol. Chem. 274:5299-5309.
17. Chang, D. K., W. J. Chien, and S. F. Cheng. 1997b. The FLG motif in the N-terminal region of glucoprotein 41 of human immunodeficiency virus type 1 adopts a type-I beta turn in aqueous solution and serves as the initiation site for helix formation. Eur. J. Biochem. 247:896-905.
18. Chang, C. D., M. Waki, M. Ahmad, J. Meienhofer, E. O. Lundell, and J. D. Haug. 1980. Preparation and properties of N-alpha-9- fluorenylmethyloxycarbonylamino acids bearing tert-butyl side-chain protection. Int. J. Pept. Prot. Res. 15:59-66.
19. 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. 28:427-136.
20. Delahunty, M. D., I. Rhee, E. O. Freed, and J. S. Bonifacino. 1996. Mutational analysis of the fusion peptide of the human immunodeficiency virus type 1: identification of critical glycine residues. Virology. 218:94-102.
21. Dimitrov, D. S. 2000. Cell biology of virus entry. Cell 101:697-702.
22. 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.
23. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
24. 2 of influenza virus promotes rapid pH dependent membrane fusion. J. Mol. Biol. 286:489-503.
25. Epand, R. F., C. M. Yip, L. V. Chemomordik, D. L. LeDuc, Y. K. Shin, and R. M. Epand. 2001. Self-assembly of influenza hemagglutinin: studies of ectodomain aggregation by in situ atomic force microscopy. Biochim. Biophys. Acta. 1513:167-175.
26. Freed, E. O., E. L. Delwart, G. L. Buchschacher, Jr., and A. T. Panganiban. 1992. A mutation in the human immunodeficiency virus type 1 transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Proc. Natl. Acad. Sci. USA. 89:70-74.
27. 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.
28. Gabrys, C. M., J. Yang, and D. P. Weliky. 2003. Analysis of local conformation of membrane-bound and polycrystalline peptides by two-dimensional slow-spinning rotor-synchronized MAS exchange spectroscopy. J. Biomol. NMR. 26:49-68.
29. Gordon, L. M., C. C. Curtain, Y. C. Zhong, A. Kirkpatrick, P. W. Mobley, and A. J. Waring. 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.
30. 13C-enhanced Fourier transform infrared spectroscopy. Biochim. Biophys. Acta. 1559:96-120.
31. Gullion, T., D. B. Baker, and M. S. Conradi. 1990. New, compensated Carr-Purcell sequences. J. Magn. Reson. 89:479-484.
32. Gullion, T., and J. Schaefer. 1989. Rotational-echo double-resonance NMR. J. Magn. Reson. 81:196-200.
33. Gullion, T., and J. Schaefer. 1991. Elimination of resonance offset effects in rotational-echo, double-resonance NMR. J. Magn. Reson. 92:439-442.
34. Han, X., J. H. Bushweller, D. S. Cafiso, and L. K. Tamm. 2001. Membrane structure and fusion-triggering confonmational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol. 8:715-720.
35. Han, X., and L. K. Tamm. 2000a. A host-guest system to study structure-function relationships of membrane fusion peptides. Proc. Natl. Acad. Sci. USA. 97:13097-13102.
36. Han, X., and L. K. Tamm. 2000b. pH-dependent self-association of influenza hemagglutinin fusion peptides in lipid bilayers. J. Mol. Biol. 304:953-965.
37. 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.
38. Hernandez, L. D., L. R. Hoffman, T. G. Wolfsberg, and J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627-661.
39. Hirsh, D. J., J. Hammer, W. L. Maloy, J. Blazyk, and J. Schaefer. 1996. Secondary structure and location of a magainin analogue in synthetic phospholipid bilayers. Biochemistry. 35:12733-12741.
40. 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.
41. Kamath, S., and T. C. Wong. 2002. Membrane structure of the human immunodeficiency virus gp41 fusion domain by molecular dynamics simulation. Biophys. J. 83:135-143.
42. Ketchem, R. R., W. Hu, and T. A. Cross. 1993. High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science. 261:1457-1460.
43. 2 ectodomain of influenza hemagglutinin. Biochemistry. 37:137-144.
44. 2 domain of the influenza virus hemagglutinin. Biochemistry. 35:5359-5365.
45. 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.
46. Kliger, Y., S. A. Gallo, S. G. Peisajovich, I. Munoz-Barroso, S. Avkin, R. Blumenthal, and Y. Shai. 2001. Mode of action of an antiviral peptide from HIV-1. Inhibition at a post-lipid mixing stage. J. Biol. Chem. 276:1391-1397.
47. 13C NMR cross polarization/magic angle spinning spectroscopic characterization of solid polypeptides. Macromolecules. 16:615-623.
48. Kuhmann, S. E., E. J. Platt, S. L. Kozak, and D. Kabat. 2000. Cooperation of multiple CCR5 coreceptors is required for infections by human immunodeficiency virus type 1. J. Virol. 74:7005-7015.
49. Lapatsanis, L., G. Milias, K. Froussios, and M. Kolovos. 1983. Synthesis of N-2,2,2-(trichloroethoxycarbonyl)-L-amino acids and N-(9-fluorenyl- methoxycarbonyl)-L-amino acids involving succinimidoxy anion as a leaving group in amino-acid protection. Synthesis. 8:671-673.
50. Laue, T. M., B. D. Shah, T. M. Ridgeway, and S. L. Pelletier. 1992. Computer-aided interpretation of analytical sedimentation data for proteins. In Analytical Ultracentrifugation in Biochemistry and Polymer Science. S. E. Harding, A. J. Rowe, and J. C. Horton, editors. Royal Society of Chemistry, Cambridge, UK. 90-125.
51. LeDuc, D. L., Y. K. Shin, R. F. Epand, and R. M. Epand. 2000. Factors determining vesicular lipid mixing induced by shortened constructs of influenza hemagglutinin. Biochemistry. 39:2733-2739.
52. 2 construct of influenza virus hemagglutinin induces cell-cell hemifusion. Biochemistry. 40:8378-8386.
53. Lin, X. X., C. A. Derdeyn, R. Blumenthal, J. West, and E. Hunter. 2003. Progressive truncations C terminal to the membrane-spanning domain of simian immunodeficiency virus Env reduce fusogenicity and increase concentration dependence of Env for fusion. J. Virol. 77:7067-7077.
54. 10-helix contents of a helical peptide. J. Am. Chem. Soc. 120:7039-7048.
55. Macosko, J. C., C. H. Kim, and Y. K. Shin. 1997. The membrane topology of the fusion peptide region of influenza hemagglutinin determined by spin-labeling EPR. J. Mol. Biol. 267:1139-1148.
56. Maddox, M. W., and M. L. Longo. 2002. Conformational partitioning of the fusion peptide of HIV-1 gp41 and its structural analogs in bilayer membranes, Biophys. J. 83:3088-3096.
57. 15N-labeled membrane protein in phospholipid bilayers. Proc. Natl. Acad. Sci. USA. 94:8551-8556.
58. 2-terminal HIV-1 gp41 peptide in fused and aggregated liposomes. Biochim. Biophys. Acta. 1145:124-133.
59. 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.
60. Mittal. A., and J. Bentz. 2001. Comprehensive kinetic analysis of influenza hemagglutinin-mediated membrane fusion: role of sialate binding. Biophys. J. 81:1521-1535.
61. Mobley, P. W., H. F. Lee, C. C. Curtain, A. Kirkpatrick, A. J. Waring, and L. M. Gordon. 1995. The amino-terminal peptide of HIV-1 glycoprotein 41 fuses human erythrocytes. Biochim. Biophys. Acta. 1271:304-314.
62. Mobley, P. W., A. J. Waring, M. A. Sherman, and L. M. Gordon. 1999. Membrane interactions of the synthetic N-terminal peptide of HIV-1 gp41 and its structural analogs. Biochim. Biophys. Acta. 1418:1-18.
63. Morcombe, C. R., and K. W. Zilm. 2003. Chemical shift referencing in MAS solid state NMR. J. Magn. Reson. 162:479-486.
64. Munoz-Barroso, I., S. Durell, K. Sakaguchi, E. Appella, and R. Blumenthal. 1998. Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. J. Cell Biol. 140:315-323.
65. 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.
66. Nieva, J. L., S. Nir, and J. Wilschut. 1998. Destabilization and fusion of zwitterionic large unilamellar lipid vesicles induced by a beta-type structure of the HIV-1 fusion peptide. J. Liposome Res. 8:165-182.
67. Opella, S. J., F. M. Marassi, J. J. Gesell, A. P. Valente, Y. Kim, M. Oblatt-Montal, and M. Montal. 1999. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat. Struct. Biol. 6:374-379.
68. Pecheur, E., 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.
69. Peisajovich, S. G., L. Blank, R. F. Epand, R. M. Epand, and Y. Shai. 2003. On the interaction between gp41 and membranes: the immunodominant loop stabilizes gp41 helical hairpin conformation. J. Mol. Biol. 326:1489-1501.
70. Peisajovich, S. G., R. F. Epand, M. Pritsker, Y. Shai, and R. M. Epand. 2000a. The polar region consecutive to the HIV fusion peptide participates in membrane fusion. Biochemistry. 39:1826-1833.
71. Peisajovich, S. G., O. Samuel, and Y. Shai. 2000b. Paramyxovirus F1 protein has two fusion peptides: implications for the mechanism of membrane fusion. J. Mol. Biol. 296:1353-1365.
72. 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.
73. Pereira, F. B., F. M. Goni, and J. L. Nieva. 1995. Liposome destabilization induced by the HIV-1 fusion peptide effect of a single amino acid substitution. FEBS Lett. 362:243-246.
74. Pritsker, M., J. Rucker, T. L. Hoffman, R. W. Doms, and Y. Shai. 1999. Effect of nonpolar substitutions of the conserved Phel1 in the fusion peptide of HIV-1 gp41 on its function, structure, and organization in membranes. Biochemistry. 38:11359-11371.
75. 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.
76. Ramamoorthy, A., F. M. Marassi, M. Zasloff, and S. J. Opella. 1995. 3-Dimensional solid-state NMR spectroscopy of a peptide oriented in membrane bilayers. J. Biomol. NMR. 6:329-334.
77. Sackett, K., and Y. Shai. 2002. The HIV-1 gp41 N-terminal heptad repeat plays an essential role in membrane fusion. Biochemistry. 41:4678-4685.
78. 13C NMR. Magn. Reson. Chem. 24:835-852.
79. Schaal, H., M. Klein, P. Gehrmann, O. Adams, and A. Scheid. 1995. Requirement of N-terminal amino acid residues of gp41 for human immunodeficiency virus type 1-mediated cell fusion. J. Virol. 69: 3308-3314.
80. 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.
81. Slepushkin, V. A., G. B. Melikyan, M. S. Sidorova, V. M. Chumakov, S. M. Andreev, R. A. Manulyan, and E. V. Karamov. 1990. Interaction of human immunodeficiency virus (HIV-1) fusion peptides with artificial lipid membranes. Biochem. Biophys. Res. Commun. 172:952-957.
82. Steinfeld, J. I., J. S. Francisco, and W. L. Hase. 1999. Chemical Kinetics and Dynamics. Prentice Hall, Upper Saddle River, NJ.
83. Struck, D. K., D. Hoekstra, and R. E. Pagano. 1981. Use of resonance energy transfer to monitor membrane fusion. Biochemistry. 20: 4093-4099.
84. Suarez, T., W. R. Gallaher, A. Agirre, F. M. Goni, and J. L. Nieva. 2000. Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J. Virol. 74:8038-8047.
85. Tan, K., J. Liu, J. Wang, S. Shen, and M. Lu. 1997. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. USA. 94:12303-12308.
86. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature. 387:426-430.
87. Weliky, D. P., A. E. Bennett, A. Zvi, J. Anglister, P. J. Steinbach, and R. Tycko. 1999. Solid-state NMR evidence for an antibody-dependent conformation of the V3 loop of HIV-1 gp120. Nat. Struct. Biol. 6: 141-145.
88. 15N chemical-shift referencing in biomolecular NMR. J. Biomol. NMR. 6:135-140.
89. Wong, T. C. 2003. Membrane structure of the human immunodeficiency virus gp41 fusion peptide by molecular dynamics simulation II. The glycine mutants. Biochim. Biophys. Acta. 1609:45-54.
90. Yang, J. 2003. Solid-state nuclear magnetic resonance structural studies of the HIV-1 fusion peptide in the membrane environment. PhD thesis. Michigan State University, East Lansing, MI.
91. Yang, J., C. M. Gabrys, and D. P. Weliky. 2001a. Solid-state nuclear magnetic resonance evidence for an extended beta strand conformation of the membrane-bound HIV-1 fusion peptide. Biochemistry. 40: 8126-8137.
92. Yang, Z. N., T. C. Mueser, J. Kaufman, S. J. Stahl, P. T. Wingfield, and C. C. Hyde. 1999. The crystal structure of the SIV gp41 ectodomain at 1.47 Å resolution. J. Struct. Biol. 126:131-144.
93. Yang, J., P. D. Parkanzky, M. L. Bodner, C. G. Duskin, and D. P. Weliky. 2002. Application of REDOR subtraction for filtered MAS observation of labeled backbone carbons of membrane-bound fusion peptides. J. Magn. Reson. 159:101-110.
94. Yang, J., P. D. Parkanzky, B. A. Khunte, C. G. Canlas, R. Yang, C. M. Gabrys, and D. P. Weliky. 2001b. Solid state NMR measurements of conformation and conformational distributions in the membrane-bound HIV-1 fusion peptide. J. Mol. Graph. Model. 19:129-135.
95. 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.
96. Yang. R., J. Yang, and D. P. Weliky. 2003. Synthesis, enhanced fusogenicity, and solid state NMR measurements of cross-linked HIV-1 fusion peptides. Biochemistry. 42:3527-3535.
97. Zhang, H. Y., S. Neal, and D. S. Wishart. 2003. RefDB: a database of uniformly referenced protein chemical shifts. J. Biomol. NMR. 25: 173-195.