Structural determinants for the membrane insertion of the transmembrane peptide of hemagglutinin from influenza virus

Journal of Chemical Information and Modeling

Volumn 52, Issue 11, 2012, Pages 3001-3012

  Victor, Bruno L ^a   Baptista, António M ^a   Soares, Cláudio M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; ASSOCIATION REACTIONS; CELL MEMBRANES; LIPID BILAYERS; LIPIDS; VIRUSES;

BIOLOGICAL FUNCTIONS; CONFORMATIONAL CHANGE; CRYSTALLOGRAPHIC STRUCTURE; NEUROTRANSMITTER RELEASE; PARALLEL ARRANGEMENT; STRUCTURAL CHARACTERIZATION; STRUCTURAL DETERMINANTS; TRANS-MEMBRANE DOMAINS;

PEPTIDES;

DIMYRISTOYLPHOSPHATIDYLCHOLINE; INFLUENZA VIRUS HEMAGGLUTININ; PEPTIDE FRAGMENT;

ALGORITHM; ARTICLE; CHEMICAL PHENOMENA; CHEMISTRY; CIRCULAR DICHROISM; GENE EXPRESSION REGULATION; INFLUENZA VIRUS A H5N1; LIPID BILAYER; MEMBRANE FUSION; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

ALGORITHMS; AMINO ACID MOTIFS; CIRCULAR DICHROISM; DIMYRISTOYLPHOSPHATIDYLCHOLINE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INFLUENZA A VIRUS, H5N1 SUBTYPE; LIPID BILAYERS; MEMBRANE FUSION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; THERMODYNAMICS;

EID: 84870015416     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci3003396     Document Type: Article

References (51)

1. Laver, G.; Garman, E. Virology. The origin and control of pandemic influenza Science 2001, 293, 1776-1777 (Pubitemid 32845763)
2. Zambon, M. C. The pathogenesis of influenza in humans Rev. Med. Virol. 2001, 11, 227-241 (Pubitemid 32737646)
3. Nichol, S. T.; Arikawa, J.; Kawaoka, Y. Emerging viral diseases Proc. Natl. Acad. Sci. U. S. A. 2000, 97, 12411-12412
4. Bizebard, T.; Gigant, B.; Rigolet, P.; Rasmussen, B.; Diat, O.; Bosecke, P.; Wharton, S. A.; Skehel, J. J.; Knossow, M. Structure of Influenza-Virus Hemagglutinin Complexed with a Neutralizing Antibody Nature 1995, 376, 92-94
5. Carr, C. M.; Chaudhry, C.; Kim, P. S. Influenza hemagglutinin is spring-loaded by a metastable native conformation Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 14306-14313 (Pubitemid 28041369)
6. Carr, C. M.; Kim, P. S. A Spring-Loaded Mechanism for the Conformational Change of Influenza Hemagglutinin Cell 1993, 73, 823-832 (Pubitemid 23159019)
7. Korte, T.; Ludwig, K.; Huang, Q.; Rachakonda, P. S.; Herrmann, A. Conformational change of influenza virus hemagglutinin is sensitive to ionic concentration Eur. Biophys. J. Biophys. Lett. 2007, 36, 327-335 (Pubitemid 46626200)
8. Madhusoodanan, M.; Lazaridis, T. Investigation of pathways for the low-pH conformational transition in influenza hemagglutinin Biophys. J. 2003, 84, 1926-1939 (Pubitemid 36322955)
9. Stevens, J.; Corper, A. L.; Basler, C. F.; Taubenberger, J. K.; Palese, P.; Wilson, I. A. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus Science 2004, 303, 1866-1870 (Pubitemid 38374878)
10. Takeda, M.; Leser, G. P.; Russell, C. J.; Lamb, R. A. Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 14610-14617 (Pubitemid 37521285)
11. Chang, D. K.; Cheng, S. F.; Trivedi, V. D.; 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 (Pubitemid 30422885)
12. 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 (Pubitemid 43847675)
13. Sammalkorpi, M.; Lazaridis, T. Configuration of influenza hemagglutinin fusion peptide monomers and oligomers in membranes Biochim. Biophys. Acta, Biomembr. 2007, 1768, 30-38 (Pubitemid 44914133)
14. Fuhrmans, M.; Marrink, S. J. Molecular View of the Role of Fusion Peptides in Promoting Positive Membrane Curvature J. Am. Chem. Soc. 2012, 134, 1543-1552
15. Langosch, D.; Hofmann, M.; Ungermann, C. The role of transmembrane domains in membrane fusion Cell. Mol. Life Sci. 2007, 64, 850-864 (Pubitemid 46597757)
16. Schroth-Diez, B.; Ludwig, K.; Baljinnyam, B.; Kozerski, C.; Huang, Q.; Herrmann, A. The role of the transmembrane and of the intraviral domain of glycoproteins in membrane fusion of enveloped viruses Biosci. Rep. 2000, 20, 571-595 (Pubitemid 32523212)
17. Tatulian, S. A.; Tamm, L. K. Secondary structure, orientation, oligomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin Biochemistry 2000, 39, 496-507 (Pubitemid 30077623)
18. Scolari, S.; Engel, S.; Krebs, N.; Plazzo, A. P.; De Almeida, R. F. M.; Prieto, M.; Veit, M.; Herrmann, A. Lateral Distribution of the Transmembrane Domain of Influenza Virus Hemagglutinin Revealed by Time-resolved Fluorescence Imaging J. Biol. Chem. 2009, 284, 15708-15716
19. Chang, D. K.; Cheng, S. F.; Kantchev, E. A. B.; 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
20. Han, X.; Steinhauer, D. A.; Wharton, S. A.; Tamm, L. K. Interaction of mutant influenza virus hemagglutinin fusion peptides with lipid bilayers: Probing the role of hydrophobic residue size in the central region of the fusion peptide Biochemistry 1999, 38, 15052-15059
21. Oostenbrink, C.; Villa, A.; Mark, A. E.; van Gunsteren, W. F. A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 2004, 25, 1656-1676
22. Scott, W. R.; Hunenberger, P. H.; Tironi, I. G.; Marck, A. E.; Billeter, S. R.; Fennen, J.; Torda, A. E.; Huber, T.; Kruger, P.; van Gunsteren, W. F. The GROMOS Biomolecular Simulation Program Package J. Phys. Chem. A 1999, 103, 3596-3607 (Pubitemid 129570863)
23. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 2008, 4, 435-447
24. Hermans, J.; Berendsen, H. J. C.; Vangunsteren, W. F.; Postma, J. P. M. A Consistent Empirical Potential for Water-Protein Interactions Biopolymers 1984, 23, 1513-1518
25. Chiu, S. W.; Clark, M.; Balaji, V.; Subramaniam, S.; Scott, H. L.; Jakobsson, E. Incorporation of Surface-Tension into Molecular-Dynamics Simulation of an Interface-a Fluid-Phase Lipid Bilayer-Membrane Biophys. J. 1995, 69, 1230-1245
26. Barker, J. A.; Watts, R. O. Monte-Carlo Studies of Dielectric Properties of Water-Like Models Mol. Phys. 1973, 26, 789-792
27. Tironi, I. G.; Sperb, R.; Smith, P. E.; Vangunsteren, W. F. A Generalized Reaction Field Method for Molecular-Dynamics Simulations J. Chem. Phys. 1995, 102, 5451-5459
28. Miyamoto, S.; Kollman, P. A. Settle-an Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
29. Smith, K. C.; Honig, B. Evaluation of the Conformational Free-Energies of Loops in Proteins Proteins: Struct., Funct., Genet. 1994, 18, 119-132 (Pubitemid 24055075)
30. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690
31. Machuqueiro, M.; Campos, S. R. R.; Soares, C. M.; Baptista, A. M. Membrane-Induced Conformational Changes of Kyotorphin Revealed by Molecular Dynamics Simulations J. Phys. Chem. B 2010, 114, 11659-11667
32. DeLano, W. L. The Pymol Molecular Graphics System, 0.90; DeLano Scientific LLC: San Carlos, CA, 2003.
33. Hofmann, M. W.; Weise, K.; Ollesch, J.; Agrawal, P.; Stalz, H.; Stelzer, W.; Hulsbergen, F.; de Groot, H.; Gerwert, K.; Reed, J.; Langosch, D. De novo design of conformationally flexible transmembrane peptides driving membrane fusion Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 14776-14781 (Pubitemid 39410751)
34. Lorin, A.; Charloteaux, B.; Fridmann-Sirkis, Y.; Thomas, A.; Shai, Y.; Brasseur, R. Mode of membrane interaction and fusogenic properties of a de Novo transmembrane model peptide depend on the length of the hydrophobic core J. Biol. Chem. 2007, 282, 18388-18396 (Pubitemid 47100240)
35. 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
36. Sternberg, M.; Ali, S. N.; Helmer-Citterich, M.; Gherardini, P. F.; Fleming, K.; Kelley, L. A.; Wass, M. N. Evolution of protein structure and function Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2009, 153A, S47
37. Holt, A.; Killian, J. A. Orientation and dynamics of transmembrane peptides: the power of simple models Eur. Biophys. J. Biophys. Lett. 2010, 39, 609-621
38. Yau, W. M.; Wimley, W. C.; Gawrisch, K.; White, S. H. The preference of tryptophan for membrane interfaces Biochemistry 1998, 37, 14713-14718 (Pubitemid 28487579)
39. Armstrong, R. T.; Kushnir, A. S.; White, J. M. The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition J. Cell Biol. 2000, 151, 425-437
40. Armstrong, R. T.; Kushnir, A. S.; White, J. M. Length requirements of the influenza hemagglutinin transmembrane domain for membranefusion: 17 amino acids yield full fusion, but 15 amino acids yield only hemifusion Mol. Biol. Cell 1999, 10, 299A
41. Neumann, S.; Langosch, D. Conserved conformational dynamics of membrane fusion protein transmembrane domains and flanking regions indicated by sequence statistics Proteins: Struct., Funct., Bioinf. 2011, 79, 2418-2427
42. Tatulian, S. A.; Hinterdorfer, P.; Baber, G.; Tamm, L. K. Influenza Hemagglutinin Assumes a Tilted Conformation during Membrane-Fusion as Determined by Attenuated Total-Reflection Ftir Spectroscopy EMBO J. 1995, 14, 5514-5523
43. Killian, J. A.; dePlanque, M.; vanderWel, P.; Koeppe, R. E.; Greathouse, D. V. Induction of non-bilayer structures by alpha-helical peptides in a model membranes of diacylphosphatidylcholine and diacylphosphatidylethanolamine Biophys. J. 1996, 70, Wp267
44. van der Wel, P. C. A.; Pott, T.; Morein, S.; Greathouse, D. V.; Koeppe, R. E.; Killian, J. A. Tryptophan-anchored transmembrane peptides promote formation of nonlamellar phases in phosphatidylethanolamine model membranes in a mismatch-dependent manner Biochemistry 2000, 39, 3124-3133 (Pubitemid 30159419)
45. Lee, M. T.; Hung, W. C.; Chen, F. Y.; Huang, H. W. Mechanism and kinetics of pore formation in membranes by water-soluble amphipathic peptides Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 5087-5092 (Pubitemid 351738514)
46. Strandberg, E.; Ozdirekcan, S.; Rijkers, D. T. S.; van der Wel, P. C. A.; Koeppe, R. E.; Liskamp, R. M. J.; Killian, J. A. Tilt angles of transmembrane model peptides in oriented and non-oriented lipid bilayers as determined by H-2 solid-state NMR Biophys. J. 2004, 86, 3709-3721 (Pubitemid 38780249)
47. Thomson, J. D.; Higgins, D. G.; Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice Nucleic Acids Res. 1994, 22, 4673-4680 (Pubitemid 24354800)
48. Harrison, S. C. Viral membrane fusion Nat. Struct. Mol. Biol. 2008, 15, 690-698 (Pubitemid 351932011)
49. Martens, S.; McMahon, H. T. Mechanisms of membrane fusion: disparate players and common principles Nat. Rev. Mol. Cell Biol. 2008, 9, 543-556 (Pubitemid 351881838)
50. White, J. M.; Delos, S. E.; Brecher, M.; Schornberg, K. Structures and mechanisms of viral membrane fusion proteins: Multiple variations on a common theme Crit. Rev. Biochem. Mol. Biol. 2008, 43, 189-219 (Pubitemid 351883153)
51. Kordyukova, L. V.; Serebryakova, M. V.; Polyansky, A. A.; Kropotkina, E. A.; Alexeevski, A. V.; Veit, M.; Efremov, R. G.; Filippova, I. Y.; Baratova, L. A. Linker and/or transmembrane regions of influenza A/Group-1, A/Group-2, and type B virus hemagglutinins are packed differently within trimers Biochim. Biophys. Acta, Biomembr. 2011, 1808, 1843-1854