Composition and functions of the influenza fusion peptide

Protein and Peptide Letters

Volumn 16, Issue 7, 2009, Pages 766-778

  Cross, Karen J ^a   Langley, William A ^b   Russell, Rupert J ^c   Skehel, John J ^a   Steinhauer, David A ^b  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; ORTHOMYXOVIRUS; PH; PROTEIN CONFORMATION; VIRUS ENTRY;

AMINO ACID SEQUENCE; ANIMALS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE; PROTEIN CONFORMATION; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

ORTHOMYXOVIRIDAE;

EID: 67849097847     PISSN: 09298665     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986609788681715     Document Type: Article

References (73)

1. Harrison, S. C. Viral membrane fusion. Nat. Struct. Mol. Biol., 2008, 15, 690-698
2. Kielian, M.; Rey, F. A. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol., 2006, 4, 67-76.
3. Weissenhorn, W.; Hinz, A.; Gaudin, Y. Virus membrane fusion. FEBS Lett., 2007, 581, 2150-2155
4. Skehel, J. J.; Wiley, D. C. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell, 1998, 95, 871-874
5. Bizebard, T.; Gigant, B.; Rigolet, P.; Rasmussen, B.; Diat, O.; Bosecke, P.; Wharton, S. A.; Skehel, J. J.; Knossow, M. Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature, 1995, 376, 92-94
6. Bullough, P. A.; Hughson, F. M.; Skehel, J. J.; Wiley, D. C. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature, 1994, 371, 37-43.
7. Chen, J.; Lee, K. H.; Steinhauer, D. A.; Stevens, D. J.; Skehel, J. J.; Wiley, D. C. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell, 1998, 95, 409-417
8. Wilson, I. A.; Skehel, J. J.; Wiley, D. C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature, 1981, 289, 366-373
9. Kordyukova, L. V.; Serebryakova, M. V.; Baratova, L. A.; Veit, M. S-acylation of HA of influenza viruses: Mass-spectrometry reveals site-specific attachment of stearic acid to a transmembrane cysteine. J. Virol., 2008, 82, 9288-9292.
10. Schmidt, M. F. Acylation of viral spike glycoproteins: a feature of enveloped RNA viruses. Virology, 1982, 116, 327-338
11. Wiley, D. C.; Wilson, I. A.; Skehel, J. J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature, 1981, 289, 373-378
12. Appleyard, G.; Maber, H. B. Plaque formation by influenza viruses in the presence of trypsin. J. Gen. Virol., 1974, 25, 351-357
13. Klenk, H. D.; Rott, R.; Orlich, M.; Blodorn, J. Activation of influenza A viruses by trypsin treatment. Virology, 1975, 68, 426-439
14. Lazarowitz, S. G.; Choppin, P. W. Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology, 1975, 68, 440-454
15. Garten, W.; Klenk, H. D. Characterization of the carboxypeptidase involved in the proteolytic cleavage of the influenza haemagglutinin. J. Gen. Virol., 1983, 64, 2127-2137
16. Russell, R. J.; Gamblin, S. J.; Haire, L. F.; Stevens, D. J.; Xiao, B.; Ha, Y.; Skehel, J. J. H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. Virology, 2004, 325, 287-296
17. Thoennes, S.; Li, Z. N.; Lee, B. J.; Langley, W. A.; Skehel, J. J.; Russell, R. J.; Steinhauer, D. A. Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion. Virology, 2008, 370, 403-414
18. Daniels, R. S.; Downie, J. C.; Hay, A. J.; Knossow, M.; Skehel, J. J.; Wang, M. L.; Wiley, D. C. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell, 1985,.40, 431-439
19. Steinhauer, D. A.; Wharton, S. A.; Skehel, J. J.; Wiley, D. C.; Hay, A. J. Amantadine selection of a mutant influenza virus containing an acid-stable hemagglutinin glycoprotein: evidence for virusspecific regulation of the pH of glycoprotein transport vesicles. Proc. Natl. Acad. Sci. USA, 1991, 88, 11525-11529
20. Chen, J.; Skehel, J. J.; Wiley, D. C. N-and C-terminal residues combine in the fusion-pH influenza hemagglutinin HA2, subunit to form an N cap that terminates the triple-stranded coiled coil. Proc. Natl. Acad. Sci. USA, 1999, 96, 8967-8972
21. Kemble, G. W.; Danieli, T.; White, J. M. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell, 1994, 76, 383-391 (Pubitemid 24046699)
22. Nobusawa, E.; Aoyama, T.; Kato, H.; Suzuki, Y.; Tateno, Y.; Nakajima, K. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology, 1991, 182, 475-485
23. Bosch, F. X.; Garten, W.; Klenk, H. D.; Rott, R. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of Avian influenza viruses. Virology, 1981, 113, 725-735
24. Bosch, F. X.; Orlich, M.; Klenk, H. D.; Rott, R. The structure of the hemagglutinin, a determinant for the pathogenicity of influenza viruses. Virology, 1979, 95, 197-207.
25. Klenk, H. D.; Garten, W. Host cell proteases controlling virus pathogenicity. Trends Microbiol., 1994, 2, 39-43.
26. Steinhauer, D. A. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology, 1999, 258, 1-20.
27. Webster, R. G.; Rott, R. Influenza virus A pathogenicity: the pivotal role of hemagglutinin. Cell, 1987, 50, 665-666
28. Stieneke-Grober, A.; Vey, M.; Angliker, H.; Shaw, E.; Thomas, G.; Roberts, C.; Klenk, H. D.; Garten, W. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisinlike endoprotease. EMBO J., 1992, 11, 2407-2414
29. Walker, J. A.; Molloy, S. S.; Thomas, G.; Sakaguchi, T.; Yoshida, T.; Chambers, T. M.; Kawaoka, Y. Sequence specificity of furin, a proprotein-processing endoprotease, for the hemagglutinin of a virulent avian influenza virus. J. Virol., 1994, 68, 1213-1218 (Pubitemid 24022230)
30. Orlich, M.; Linder, D.; Rott, R. Trypsin-resistant protease activation mutants of an influenza virus. J. Gen. Virol., 1995, 76(Pt. 3), 625-633
31. Orlich, M.; Rott, R. Thermolysin activation mutants with changes in the fusogenic region of an influenza virus hemagglutinin. J. Virol., 1994, 68, 7537-7539
32. Steinhauer, D. A.; Wharton, S. A.; Skehel, J. J.; Wiley, D. C. Studies of the membrane fusion activities of fusion peptide mutants of influenza virus hemagglutinin. J. Virol., 1995, 69, 6643-6651
33. Cross, K. J.; Wharton, S. A.; Skehel, J. J.; Wiley, D. C.; Steinhauer, D. A. Studies on influenza haemagglutinin fusion peptide mutants generated by reverse genetics.. EMBO J., 2001, 20, 4432-4442
34. Gething, M. J.; Doms, R. W.; York, D.; White, J. Studies on the mechanism of membrane fusion: site-specific mutagenesis of the hemagglutinin of influenza virus. J. Cell. Biol., 1986, 102, 11-23.
35. Qiao, H.; Armstrong, R. T.; Melikyan, G. B.; Cohen, F. S.; White, J. M. A specific point mutant at position 1 of the influenza hemagglutinin fusion peptide displays a hemifusion phenotype. Mol. Biol. Cell, 1999, 10, 2759-2769
36. Korte, T.; Ludwig, K.; Booy, F. P.; Blumenthal, R.; Herrmann, A. Conformational intermediates and fusion activity of influenza virus hemagglutinin. J. Virol., 1999, 73, 4567-4574
37. Puri, A.; Booy, F. P.; Doms, R. W.; White, J. M.; Blumenthal, R. Conformational changes and fusion activity of influenza virus hemagglutinin of the H2 and H3 subtypes: effects of acid pretreatment. J. Virol., 1990, 64, 3824-3832
38. Durrer, P.; Galli, C.; Hoenke, S.; Corti, C.; Gluck, R.; Vorherr, T.; Brunner, J. H+-induced membrane insertion of influenza virus hemagglutinin involves the HA2 amino-terminal fusion peptide but not the coiled coil region. J. Biol. Chem., 1996, 271, 13417-13421
39. Harter, C.; James, P.; Bachi, T.; Semenza, G.; Brunner, J. Hydrophobic binding of the ectodomain of influenza hemagglutinin to membranes occurs through the "fusion peptide". J. Biol. Chem., 1989, 264, 6459-6464
40. Gray, C.; Tatulian, S. A.; Wharton, S. A.; Tamm, L. K. Effect of the N-terminal glycine on the secondary structure, orientation, and interaction of the influenza hemagglutinin fusion peptide with lipid bilayers. Biophys. J., 1996, 70, 2275-2286
41. Han, X.; Steinhauer, D. A.; Wharton, S. A.; Tamm, L. K. Interaction of mutant influenza virus hemagglutinin fusion peptides withlipid bilayers: probing the role of hydrophobic residue size in the central region of the fusion peptide. Biochemistry, 1999, 38, 15052-15059
42. Lear, J. D.; DeGrado, W. F. Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. J. Biol. Chem., 1987, 262, 6500-6505
43. Murata, M.; Sugahara, Y.; Takahashi, S.; Ohnishi, S. 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., 1987, 102, 957-962
44. Rafalski, M.; Ortiz, A.; Rockwell, A.; van Ginkel, L. C.; Lear, J. D.; DeGrado, W. F.; Wilschut, J. Membrane fusion activity of the influenza virus hemagglutinin: interaction of HA2 N-terminal peptides with phospholipid vesicles. Biochemistry, 1991, 30, 10211-10220
45. Wharton, S. A.; Martin, S. R.; Ruigrok, R. W.; Skehel, J. J.; Wiley, D. C. Membrane fusion by peptide analogues of influenza virus haemagglutinin. J. Gen. Virol., 1988, 69, 1847-1857
46. Burger, K. N.; Wharton, S. A.; Demel, R. A.; Verkleij, A. J. The interaction of synthetic analogs of the N-terminal fusion sequence of influenza virus with a lipid monolayer. Comparison of fusionactive and fusion-defective analogs. Biochim. Biophys. Acta, 1991, 1065, 121-129
47. Brasseur, R. Tilted peptides: a motif for membrane destabilization. hypothesis,. Mol. Membr. Biol, 2000, 17, 31-40.
48. Han, X.; Bushweller, J. H.; Cafiso, D. S.; Tamm, L. K. Membrane structure and fusion-triggering conformational change of the fusion domain from influenza hemagglutinin. Nat. Struct. Biol., 2001, 8, 715-720
49. Han, X.; Tamm, L. K. A host-guest system to study structurefunction relationships of membrane fusion peptides. Proc. Natl. Acad. Sci. USA, 2000, 97, 13097-13102
50. Hsu, C. H.; Wu, S. H.; Chang, D. K.; Chen, C. Structural characterizations of fusion peptide analogs of influenza virus hemagglutinin. Implication of the necessity of a helix-hinge-helix motif in fusion activity. J. Biol. Chem., 2002, 277, 22725-22733
51. Lai, A. L.; Park, H.; White, J. M.; Tamm, L. K. Fusion peptide of influenza hemagglutinin requires a fixed angle boomerang structure for activity. J. Biol. Chem., 2006, 281, 5760-5770
52. Lai, A. L.; Tamm, L. K. Locking the kink in the influenza hemagglutinin fusion domain structure. J. Biol. Chem., 2007, 282, 23946-23956
53. Li, Y.; Han, X.; Lai, A. L.; Bushweller, J. H.; Cafiso, D. S.; Tamm, L. K. Membrane structures of the hemifusion-inducing fusion peptide mutant G1S and the fusion-blocking mutant G1V of influenza virus hemagglutinin suggest a mechanism for pore opening in membrane fusion. J. Virol., 2005, 79, 12065-12076
54. Chang, D. K.; Cheng, S. F.; Deo Trivedi, V.; Yang, S. H. The amino-terminal region of the fusion peptide of influenza virus hemagglutinin HA2 inserts into sodium dodecyl sulfate micelle with residues 16-18 at the aqueous boundary at acidic pH. Oligomerization and the conformational flexibility. J. Biol. Chem., 2000, 275, 19150-19158
55. Skehel, J. J.; Cross, K.; Steinhauer, D.; Wiley, D. C. Influenza fusion peptides. Biochem. Soc. Trans, 2001, 29, 623-626
56. Lau, W. L.; Ege, D. S.; Lear, J. D.; Hammer, D. A.; DeGrado, W. F. Oligomerization of fusogenic peptides promotes membrane fusion by enhancing membrane destabilization. Biophys. J., 2004, 86, 272-284
57. Wharton, S. A.; Skehel, J. J.; Wiley, D. C. Studies of influenza haemagglutinin-mediated membrane fusion. Virology, 1986, 149, 27-35.
58. Carr C.M.; Chaudhry, C.; Kim P.S. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc. Natl. Acad. Sci. USA, 1997, 94, 14306-14313.
59. Ruigrok, R. W.; Martin, S. R.; Wharton, S. A.; Skehel, J. J.; Bayley, P. M.; Wiley, D. C. Conformational changes in the hemagglutinin of influenza virus which accompany heat-induced fusion of virus with liposomes. Virology, 1986, 155, 484-497
60. Walker, J. A.; Kawaoka, Y. Importance of conserved amino acids at the cleavage site of the haemagglutinin of a virulent avian influenza A virus. J. Gen. Virol., 1993, 74, 311-314
61. Lin, Y. P.; Wharton, S. A.; Martin, J.; Skehel, J. J.; Wiley, D. C.; Steinhauer, D. A. Adaptation of egg-grown and transfectant influenza viruses for growth in mammalian cells: selection of hemagglutinin mutants with elevated pH of membrane fusion. Virology, 1997, 233, 402-410
62. Verhoeyen, M.; Fang, R.; Jou, W. M.; Devos, R.; Huylebroeck, D.; Saman, E.; Fiers, W. Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75. Nature, 1980, 286, 771-776
63. Yewdell, J. W.; Taylor, A.; Yellen, A.; Caton, A.; Gerhard, W.; Bachi, T. Mutations in or near the fusion peptide of the influenza virus hemagglutinin affect an antigenic site in the globular region. J. Virol., 1993, 67, 933-942
64. Korte, T.; Epand, R. F.; Epand, R. M.; Blumenthal, R. Role of the Glu residues of the influenza hemagglutinin fusion peptide in the pH dependence of fusion activity. Virology, 2001, 289, 353-361
65. Nobusawa, E.; Hishida, R.; Murata, M.; Kawasaki, K.; Ohnishi, S.; Nakajima, K. The role of acidic residues in the "fusion segment" of influenza A virus hemagglutinin in low-pH-dependent membrane fusion. Arch. Virol., 1995, 140, 865-875
66. Neumann, G.; Watanabe, T.; Ito, H.; Watanabe, S.; Goto, H.; Gao, P.; Hughes, M.; Perez, D. R.; Donis, R.; Hoffmann, E.; Hobom, G.; Kawaoka, Y. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. USA, 1999, 96, 9345-9350
67. Li, Z. N.; Lee, B. J.; Langley, W. A.; Bradley, K. C.; Russell, R. J.; Steinhauer, D. A. Length requirements for membrane fusion of influenza virus hemagglutinin peptide linkers to transmembrane or fusion peptide domains. J. Virol., 2008, 82, 6337-6348
68. Li, Z. N.; Mueller, S. N.; Ye, L.; Bu, Z.; Yang, C.; Ahmed, R.; Steinhauer, D. A. Chimeric influenza virus hemagglutinin proteins containing large domains of the Bacillus anthracis protective antigen: protein characterization, incorporation into infectious influenza viruses, and antigenicity. J. Virol., 2005, 79, 10003-10012
69. Melikyan, G. B.; Markosyan, R. M.; Roth, M. G.; Cohen, F. S. A point mutation in the transmembrane domain of the hemagglutinin of influenza virus stabilizes a hemifusion intermediate that can transit to fusion. Mol. Biol. Cell, 2000, 11, 3765-3775
70. Chang, D. K.; Cheng, S. F.; Kantchev, E. A.; Lin, C. H.; Liu, Y. T. Membrane interaction and structure of the transmembrane domain of influenza hemagglutinin and its fusion peptide complex. BMC Biol., 2008, 6, 2.
71. Bentz, J. Minimal aggregate size and minimal fusion unit for the first fusion pore of influenza hemagglutinin-mediated membrane fusion. Biophys. J., 2000, 78, 227-245
72. Blumenthal, R.; Sarkar, D. P.; Durell, S.; Howard, D. E.; Morris, S. J. Dilation of the influenza hemagglutinin fusion pore revealed by the kinetics of individual cell-cell fusion events. J. Cell. Biol., 1996, 135, 63-71.
73. Danieli, T.; Pelletier, S. L.; Henis, Y. I.; White, J. M. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J. Cell. Biol., 1996, 133, 559-569