Linker and/or transmembrane regions of influenza A/Group-1, A/Group-2, and type B virus hemagglutinins are packed differently within trimers

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 7, 2011, Pages 1843-1854

  Kordyukova, Larisa V ^a   Serebryakova, Marina V ^b   Polyansky, Anton A ^c   Kropotkina, Ekaterina A ^d   Alexeevski, Andrei V ^a   Veit, Michael ^e   Efremov, Roman G ^c   Filippova, Irina Yu ^a   Baratova, Lyudmila A ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b Federal Agency for Health Care and Social Development   (Russian Federation)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d CHUMAKOV INSTITUTE OF POLIOMYELITIS AND VIRAL ENCEPHALITIDES   (Russian Federation)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Hemagglutinin; Linker and transmembrane region; MALDI TOF MS; Molecular modeling; Phylogenetic groups of influenza virus; Viral membrane

Indexed keywords

BROMELAIN; INFLUENZA VIRUS HEMAGGLUTININ; INFLUENZA VIRUS HEMAGGLUTININ 1; INFLUENZA VIRUS HEMAGGLUTININ 10; INFLUENZA VIRUS HEMAGGLUTININ 11; INFLUENZA VIRUS HEMAGGLUTININ 13; INFLUENZA VIRUS HEMAGGLUTININ 14; INFLUENZA VIRUS HEMAGGLUTININ 16; INFLUENZA VIRUS HEMAGGLUTININ 2; INFLUENZA VIRUS HEMAGGLUTININ 3; INFLUENZA VIRUS HEMAGGLUTININ 4; INFLUENZA VIRUS HEMAGGLUTININ 5; INFLUENZA VIRUS HEMAGGLUTININ 6; INFLUENZA VIRUS HEMAGGLUTININ 7; INFLUENZA VIRUS HEMAGGLUTININ 9; SUBTILISIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; INFLUENZA VIRUS A; INFLUENZA VIRUS B; MEMBRANE STRUCTURE; MICELLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; VIRION; VIRUS ENVELOPE; VIRUS STRAIN; VIRUS TYPING;

AMINO ACID SEQUENCE; BIOPOLYMERS; CRYSTALLOGRAPHY, X-RAY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; INFLUENZA B VIRUS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

CERCOPITHECINE HERPESVIRUS 1; INFLUENZA B VIRUS; ORTHOMYXOVIRIDAE;

EID: 79955798774     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.03.005     Document Type: Article

References (52)

1. J.J. Skehel, and D.C. Wiley Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin Annu. Rev. Biochem. 69 2000 531 569
2. B.J. Chen, G.P. Leser, E. Morita, and R.A. Lamb Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles J. Virol. 81 2007 7111 7123 (Pubitemid 46986647)
3. G.M. Air Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus Proc. Natl Acad. Sci. U.S.A. 78 1981 7639 7643 (Pubitemid 12186198)
4. E. Nobusawa, T. Aoyama, H. Kato, Y. Suzuki, Y. Tateno, and K. Nakajima Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses Virology 182 1991 475 485
5. R.J. Russell, P.S. Kerry, D.J. Stevens, D.A. Steinhauer, S.R. Martin, S.J. Gamblin, and J.J. Skehel Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion Proc. Natl Acad. Sci. U.S.A. 105 2008 17736 17741
6. Y. Ha, D.J. Stevens, J.J. Skehel, and D.C. Wiley H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes EMBO J. 21 2002 865 875 (Pubitemid 34206160)
7. R.J. Russell, S.J. Gamblin, L.F. Haire, D.J. Stevens, B. Xiao, Y. Ha, and J.J. Skehel H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes Virology 325 2004 287 296 (Pubitemid 38902794)
8. S. Thoennes, Z.N. Li, B.J. Lee, W.A. Langley, J.J. Skehel, R.J. Russell, and D.A. Steinhauer Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion Virology 370 2008 403 414 (Pubitemid 350199676)
9. E.I. Sklyanskaya, M. Shie, Y.S. Komarov, S.S. Yamnikova, and N.V. Kaverin Formation of mixed hemagglutinin trimers in the course of double infection with influenza viruses belonging to different subtypes Virus Res. 10 1988 153 165
10. I.A. Wilson, J.J. Skehel, and D.C. Wiley Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution Nature 289 1981 366 373
11. S.J. Gamblin, L.F. Haire, R.J. Russell, D.J. Stevens, B. Xiao, Y. Ha, N. Vasisht, D.A. Steinhauer, R.S. Daniels, A. Elliot, D.C. Wiley, and J.J. Skehel The structure and receptor binding properties of the 1918 influenza hemagglutinin Science 303 2004 1838 1842 (Pubitemid 38374870)
12. Q. Wang, F. Cheng, M. Lu, X. Tian, and J. Ma Crystal structure of unliganded influenza B virus hemagglutinin J. Virol. 82 2008 3011 3020 (Pubitemid 351329189)
13. J. Liu, D.J. Stevens, L.F. Haire, P.A. Walker, P.J. Coombs, R.J. Russell, S.J. Gamblin, and J.J. Skehel Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957 Proc. Natl Acad. Sci. U.S.A. 106 2009 17175 17180
14. P.A. Bullough, F.M. Hughson, J.J. Skehel, and D.C. Wiley Structure of influenza haemagglutinin at the pH of membrane fusion Nature 371 1994 37 43 (Pubitemid 24277462)
15. J. Chen, K.H. Lee, D.A. Steinhauer, D.J. Stevens, J.J. Skehel, and D.C. Wiley Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation Cell 95 1998 409 417 (Pubitemid 28507328)
16. S.A. Tatulian, and L.K. Tamm Secondary structure, orientation, oligomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin Biochemistry 39 2000 496 507 (Pubitemid 30077623)
17. D.K. Chang, S.F. Cheng, E.A. Kantchev, C.H. Lin, and Y.T. Liu Membrane interaction and structure of the transmembrane domain of influenza hemagglutinin and its fusion peptide complex BMC Biol. 6 2008 2
18. S. Scolari, S. Engel, N. Krebs, A.P. Plazzo, R.F. De Almeida, M. Prieto, M. Veit, and A. Herrmann Lateral distribution of the transmembrane domain of influenza virus hemagglutinin revealed by time-resolved fluorescence imaging J. Biol. Chem. 284 2009 15708 15716
19. Z.N. Li, B.J. Lee, W.A. Langley, K.C. Bradley, R.J. Russell, and D.A. Steinhauer Length requirements for membrane fusion of influenza virus hemagglutinin peptide linkers to transmembrane or fusion peptide domains J. Virol. 82 2008 6337 6348 (Pubitemid 351875112)
20. T. Zurcher, G. Luo, and P. Palese Mutations at palmitylation sites of the influenza virus hemagglutinin affect virus formation J. Virol. 68 1994 5748 5754 (Pubitemid 24258590)
21. T. Sakai, R. Ohuchi, and M. Ohuchi Fatty acids on the A/USSR/77 influenza virus hemagglutinin facilitate the transition from hemifusion to fusion pore formation J. Virol. 76 2002 4603 4611 (Pubitemid 34309595)
22. R. Wagner, A. Herwig, N. Azzouz, and H.D. Klenk Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity J. Virol. 79 2005 6449 6458 (Pubitemid 40617248)
23. B.J. Chen, M. Takeda, and R.A. Lamb Influenza virus hemagglutinin (H3 subtype) requires palmitoylation of its cytoplasmic tail for assembly: M1 proteins of two subtypes differ in their ability to support assembly J. Virol. 79 2005 13673 13684 (Pubitemid 41508179)
24. M. Veit, G. Herrler, M.F. Schmidt, R. Rott, and H.D. Klenk The hemagglutinating glycoproteins of influenza B and C viruses are acylated with different fatty acids Virology 177 1990 807 811 (Pubitemid 20235209)
25. L.V. Kordyukova, M.V. Serebryakova, L.A. Baratova, and M. Veit S acylation of the hemagglutinin of influenza viruses: mass spectrometry reveals site-specific attachment of stearic acid to a transmembrane cysteine J. Virol. 82 2008 9288 9292
26. M.V. Serebryakova, L.V. Kordyukova, L.A. Baratova, and S.G. Markushin Mass spectrometric sequencing and acylation character analysis of C-terminal anchoring segment from Influenza A hemagglutinin Eur. J. Mass Spectrom. 12 2006 51 62 (Pubitemid 43587048)
27. Iu.A. Smirnova, L.V. Kordiukova, M.V. Serebriakova, I.Iu. Filippova, E.N. Lysogorskaia, and L.A. Baratova Flu virion as a substrate for proteolytic enzymes Bioorg. Khim. 34 2008 409 415
28. L.V. Kordyukova, M.V. Serebryakova, L.A. Baratova, and M. Veit Site-specific attachment of palmitate or stearate to cytoplasmic versus transmembrane cysteines is a common feature of viral spike proteins Virology 398 2010 49 56
29. N.D. Rawlings, F.R. Morton, C.Y. Kok, J. Kong, and A.J. Barrett MEROPS: the peptidase database Nucleic Acids Res. 36 2008 320 325
30. A.D. Rowan, D.J. Buttle, and A.J. Barrett The cysteine proteinases of the pineapple plant Biochem. J. 266 1990 869 875 (Pubitemid 20103724)
31. Y. Choe, F. Leonetti, D.C. Greenbaum, F. Lecaille, M. Bogyo, D. Brömme, J.A. Ellman, and C.S. Craik Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities J. Biol. Chem. 281 2005 12824 12832
32. A. Berger, and I. Schechter Mapping the active site of papain with the aid of peptide substrates and inhibitors Philos. Trans. R. Soc. Lond. B Biol. Sci. 257 1970 249 264
33. M. Meldal, I. Svendsen, K. Breddam, and F.I. Auzanneau Portion-mixing peptide libraries of quenched fluorogenic substrates for complete subsite mapping of endoprotease specificity Proc. Natl Acad. Sci. U.S.A. 91 1994 3314 3318 (Pubitemid 24130227)
34. R.J. Siezen, and J.A. Leunissen Subtilases: the superfamily of subtilisin-like serine proteases Protein Sci. 6 1997 501 523 (Pubitemid 27120048)
35. B. Ruan, V. London, K.E. Fisher, D.T. Gallagher, and P.N. Bryan Engineering substrate preference in subtilisin: structural and kinetic analysis of a specificity mutant Biochemistry 47 2008 6628 6636 (Pubitemid 351874289)
36. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
37. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
38. G.L. Peterson A simplification of the protein assay method of Lowry et al. which is more generally applicable Anal. Biochem. 83 1977 346 356 (Pubitemid 8269786)
39. C.M. Brand, and J.J. Skehel Crystalline antigen from the influenza virus envelope Nat. New Biol. 238 1972 145 147
40. D.L. Gibbons, and M. Kielian Molecular dissection of the Semliki Forest virus homotrimer reveals two functionally distinct regions of the fusion protein J. Virol. 76 2002 1194 1205 (Pubitemid 34066423)
41. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797 (Pubitemid 38832724)
42. A.A. Polyansky, P.E. Edgar, and R.G. Volynsky Structural, dynamic, and functional aspects of helix association in membranes: a computational view Adv. Protein Chem. Struct. Biol. 83 2011 129 161 10.1016/B978-0-12-381262-9.00004-5
43. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
44. T.V. Pyrkov, A.O. Chugunov, N.A. Krylov, D.E. Nolde, and R.G. Efremov PLATINUM: a web tool for analysis of hydrophobic/hydrophilic organization of biomolecular complexes Bioinformatics 25 2009 1201 1202
45. J. Sui, W.C. Hwang, S. Perez, G. Wei, D. Aird, L.M. Chen, E. Santelli, B. Stec, G. Cadwell, M. Ali, H. Wan, A. Murakami, A. Yammanuru, T. Han, N.J. Cox, L.A. Bankston, R.O. Donis, R.C. Liddington, and W.A. Marasco Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses Nat. Struct. Mol. Biol. 16 2009 265 273
46. A. Ridder, P. Skupjen, S. Unterreitmeier, and D. Langosch Tryptophan supports interaction of transmembrane helices J. Mol. Biol. 354 2005 894 902 (Pubitemid 41735510)
47. N. Sal-Man, D. Gerber, I. Bloch, and Y. Shai Specificity in transmembrane helix-helix interactions mediated by aromatic residues J. Biol. Chem. 282 2007 19753 19761 (Pubitemid 47100067)
48. R.M. Johnson, K. Hecht, and C.M. Deber Aromatic and cation-pi interactions enhance helix-helix association in a membrane environment Biochemistry 46 2007 9208 9214 (Pubitemid 47255035)
49. M. Veit, and M.F. Schmidt Timing of palmitoylation of influenza virus hemagglutinin FEBS Lett. 336 1993 243 247
50. R. Tsutsumi, Y. Fukata, and M. Fukata Discovery of protein-palmitoylating enzymes Pflugers Arch. 456 2008 1199 1206
51. O. Rocks, M. Gerauer, N. Vartak, S. Koch, Z.P. Huang, M. Pechlivanis, J. Kuhlmann, L. Brunsveld, A. Chandra, B. Ellinger, H. Waldmann, and P.I. Bastiaens The palmitoylation machinery is a spatially organizing system for peripheral membrane proteins Cell 141 2010 458 471
52. The PyMOL Molecular Graphics System, Version 1.2r3pre, Schrodinger, LLC.