Immobilization of the influenza A M2 transmembrane peptide in virus envelope-mimetic lipid membranes: A solid-state NMR investigation

Biochemistry

Volumn 48, Issue 27, 2009, Pages 6361-6368

  Luo, Wenbin ^a   Cady, Sarah D ^a   Hong, Mei ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BI-LAYER; CHARACTERISTIC LINES; DIPOLAR COUPLINGS; EUKARYOTIC CELLS; HELICAL BUNDLE; HIGH-RESOLUTION SPECTRA; HIGH-SENSITIVITY; INFLUENZA A; LINE-NARROWING; LIPID MEMBRANES; MEMBRANE COMPOSITION; MEMBRANE PROTEINS; MEMBRANE VISCOSITY; NMR SPECTRUM; ORDERS OF MAGNITUDE; PHYSIOLOGICAL TEMPERATURE; PROTON CHANNELS; QUADRUPOLAR COUPLING; ROTATIONAL DIFFUSION; SOLID STATE NMR; SPHINGOMYELIN; STRUCTURE DETERMINATION; TEMPERATURE DEPENDENT; TIME-SCALE; TRANSMEMBRANE; WHOLE-BODY;

AMINES; BIOMIMETICS; CHOLESTEROL; COUPLINGS; CYTOLOGY; DIFFUSION IN SOLIDS; LIPID BILAYERS; LIPIDS; MEMBRANES; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS; SOLID STATE PHYSICS;

CELL MEMBRANES;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CHOLESTEROL; DIMYRISTOYLPHOSPHATIDYLCHOLINE; MEMBRANE PROTEIN; SPHINGOMYELIN;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL MEMBRANE; DIFFUSION; EUKARYOTIC CELL; INFLUENZA VIRUS A; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE MODEL; MOLECULAR DYNAMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN IMMOBILIZATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SENSITIVITY AND SPECIFICITY; SOLID STATE; TEMPERATURE DEPENDENCE; THICKNESS; VIRUS ENVELOPE; VISCOSITY;

CHOLESTEROL; LIPID BILAYERS; MOLECULAR MIMICRY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SPHINGOMYELINS; VIRAL ENVELOPE PROTEINS; VIRAL MATRIX PROTEINS;

EUKARYOTA;

EID: 67650080518     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900716s     Document Type: Article

References (58)

1. Hong, M. (2006) Oligomeric structure, dynamics, and orientation of membrane proteins from solid-state NMR. Structure 14, 1731-1740.
2. Hong, M. (2007) Structure, topology, and dynamics of membrane peptides and proteins from solid-state NMR spectroscopy. J. Phys. Chem. B 111, 10340-10351.
3. Reuther, G., Tan, K. T., Vogel, A., Nowak, C., and Arnold, K.; et al. (2006) The lipidated membrane anchor of full length N-Ras protein shows an extensive dynamics as revealed by solid-state NMR spectroscopy. J. Am. Chem. Soc. 128, 13840-13846.
4. Park, S. H., Mrse, A. A., Nevzorov, A. A., De Angelis, A. A., and Opella, S. J. (2006) Rotational diffusion of membrane proteins in aligned phospholipid bilayers by solid-state NMR spectroscopy J. Magn. Reson. 178, 162-165.
5. Hong, M. (2006) Solid-state NMR studies of the structure, dynamics, and assembly of β-sheet membrane peptides and α-helical membrane proteins with antibiotic activities. Acc. Chem. Res. 39, 176-183.
6. 13C Spin Diffusion NMR. J. Am. Chem. Soc. 127, 6402-6408.
7. Huster, D., Xiao, L. S., and Hong, M. (2001) Solid-State NMR Investigation of the dynamics of colicin Ia channel-forming domain. Biochemistry 40, 7662-7674.
8. Tang, M., Waring, A. J., Lehrer, R. I., and Hong, M. (2008) Effects of Guanidinium-Phosphate Hydrogen Bonding on the Membrane-Bound Structure and Activity of an Arginine-Rich Membrane Peptide from Solid-State NMR. Angew. Chem., Int. Ed. 47, 3202-3205.
9. Doherty, T., Waring, A. J., and Hong, M. (2008) Dynamic structure of disulfide-removed linear analogs of tachyplesin-I in the lipid bilayer from solid-state NMR. Biochemistry 47, 1105-1116.
10. Bain, A. D. (2003) Chemical exchange in NMR. Prog. Nucl. Magn. Reson. Spectrosc. 43, 63-103.
11. Saffman, P. G., and Delbruck, M. (1975) Brownian motion in biological membranes. Proc. Natl. Acad. Sci. U.S.A. 72, 3111-3113.
12. 15N solid-state NMR investigation of the dynamics and orientation of a transmembrane helical bundle. J. Am. Chem. Soc. 129, 5719-5729.
13. Pinto, L. H., Holsinger, L. J., and Lamb, R. A. (1992) Influenza virus M2 protein has ion channel activity. Cell 69, 517-528.
14. Pinto, L. H., and Lamb, R. A. (2007) Controlling influenza virus replication by inhibiting its proton flow. Mol. BioSyst. 3, 18-23.
15. Hay, A. J., Wolstenholme, A. J., Skehel, J. J., and Smith, M. H. (1985) The molecular basis of the specific anti-influenza action of amantadine. EMBO J. 4, 3021-3024.
16. Wang, C., Takeuchi, K., Pinto, L. H., and Lamb, R. A. (1993) Ion Channel Activity of Influenza A Virus M2 Protein: Characterization of the Amantadine Block. J. Virol. 67, 5585-5594.
17. Li, C., Qin, H., Gao, F. P., and Cross, T. A. (2007) Solid-state NMR characterization of conformational plasticity within the transmembrane domain of the influenza A M2 proton channel. Biochim. Biophys. Acta 1768, 3162-3170.
18. Kovacs, F. A., and Cross, T. A. (1997) Transmembrane four-helix bundle of influenza A M2 protein channel: Structural implications from helix tilt and orientation. Biophys. J. 73, 2511-2517.
19. Stouffer, A. L., Acharya, R., Salom, D., Levine, A. S., and Di Costanzo, L.; et al. (2008) Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451, 596-599.
20. Schnell, J. R., and Chou, J. J. (2008) Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451, 591-595.
21. Miller, C. (2008) Ion channels: Coughing up flu's proton channels. Nature 451, 532-533.
22. Klenk, H. D., Becht, H., and Rott, R. (1972) Structure of Influenza-Virus Envelope. Virology 47, 579-591.
23. Cady, S. D., Mishanina, T. V., and Hong, M. (2009) Structure of Amantadine-Bound M2 Transmembrane Peptide of Influenza A in Lipid Bilayers from Magic-Angle-Spinning Solid-State NMR: The Role of Ser31 in Amantadine Binding. J. Mol. Biol. 385, 1127-1141.
24. Hong, M., Gross, J. D., Rienstra, C. M., Griffin, R. G., and Kumashiro, K. K.; et al. (1997) Coupling amplification in 2D MAS NMR and its application to torsion angle determination in peptides. J. Magn. Reson. 129, 85-92.
25. 13C-detected N-H dipolar couplings under magic angle spinning J. Magn. Reson. 191, 219-225.
26. Hong, M., and Griffin, R. G. (1998) Resonance assignments for solid peptides by dipolar-mediated C-13/N-15 correlation solid-state NMR. J. Am. Chem. Soc. 120, 7113-7114.
27. Gullion, T., and Schaefer, J. (1989) Rotational-Echo Double-Resonance NMR. J. Magn. Reson. 81, 196-200.
28. Blough, H. A., and Merlie, J. P. (1970) Lipids of Incomplete Influenza Virus. Virology 40, 685-692.
29. Blough, H. A. (1971) Fatty Acid Composition of Individual Phospholipids of Influenza Virus. J. Gen. Virol. 12, 317-320.
30. Edidin, M. (2003) The State of Lipid Rafts: From Model Membranes to Cells. Annu. Rev. Biophys. Biomol. Struct. 32, 257-283.
31. Niemela, P. S., Hyvonen, M. T., and Vattulainen, I. (2009) Atom-scale molecular interactions in lipid raft mixtures. Biochim. Biophys. Acta 1788, 122-135.
32. Gambin, Y., Lopez-Esparza, R., Reffay, M., Sierecki, E., and Gov, N. S.; et al. (2006) Lateral mobility of proteins in lipid membranes revisited. Proc. Natl. Acad. Sci. U.S.A. 103, 2098-2102.
33. Lindblom, G., Oradd, G., and Filippov, A. (2006) Lipid lateral diffusion in bilayers with phosphatidylcholine, sphingomyelin and cholesterol: An NMR study of dynamics and lateral phase separation. Chem. Phys. Lipids 141, 179-184.
34. 2H NMR study of molecular motion in collagen fibrils. Nature 284, 531-534.
35. 13C labeled biomolecules: J-decoupled REDOR. J. Am. Chem. Soc. 121, 10237-10238.
36. Pinto, L. H., Dieckmann, G. R., Gandhi, C. S., Papworth, C. G., and Braman, J.; et al. (1997) A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc. Natl. Acad. Sci. U.S.A. 94, 11301-11306.
37. Cady, S. D., and Hong, M. (2008) Amantadine-Induced Conformational and Dynamical Changes of the Influenza M2 Transmembrane Proton Channel. Proc. Natl. Acad. Sci. U.S.A. 105, 1483-1488.
38. Khurana, E., Dal Peraro, M., DeVane, R., Vemparala, S., and DeGrado, W. F.; et al. (2009) Molecular dynamics calculations suggest a conduction mechanism for the M2 proton channel from influenza A virus. Proc. Natl. Acad. Sci. U.S.A. 106, 1069-1074.
39. Cristian, L., Lear, J. D., and DeGrado, W. F. (2003) Use of thiol-disulfide equilibria to measure the energetics of assembly of transmembrane helices in phospholipid bilayers. Proc. Natl. Acad. Sci. U.S.A. 100, 14772-14777.
40. Schroeder, C., Heider, H., Möncke-Buchner, E., and Lin, T. I. (2005) The influenza virus ion channel and maturation cofactor M2 is a cholesterol-binding protein. Eur. Biophys. J. 34, 52-66.
41. Ma, C., Polishchuk, A. L., Ohigashi, Y., Stouffer, A. L., and Schön, A. (2009) Identification of the Functional Core of the Influenza A Virus A/M2 Proton-Selective Ion Channel. Proc. Natl. Acad. Sci. U.S.A. (in press).
42. + channel. Protein Sci. 10, 2241-2250.
43. Hu, J., Asbury, T., Achuthan, S., Li, C., and Bertram, R.; et al. (2007) Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from Influenza A virus. Biophys. J. 92, 4335-4343.
44. Duong-Ly, K. C., Nanda, V., DeGrado, W. F., and Howard, K. P. (2005) The conformation of the pore region of the M2 proton channel depends on lipid bilayer environment. Protein Sci. 14, 856-861.
45. Hu, J., Fu, R., Nishimura, K., Zhang, L., and Zhou, H.-X.; et al. (2006) Histidines, heart of the hydrogen ion channel from influenza A virus: Toward an understanding of conductance and proton selectivity. Proc. Natl. Acad. Sci. U.S.A. 103, 6865-6870.
46. Howard, K. P., Lear, J. D., and DeGrado, W. F. (2002) Sequence determinants of the energetics of folding of a transmembrane four-helix-bundle protein. Proc. Natl. Acad. Sci. U.S.A. 99, 8568-8572.
47. Salom, D., Hill, B. R., Lear, J. D., and DeGrado, W. F. (2000) pH-dependent tetramerization and amantadine binding of the transmembrane helix of M2 from the influenza A virus. Biochemistry 39, 14160-14170.
48. Luo, W., Mani, R., and Hong, M. (2007) Sidechain conformation and gating of the M2 transmembrane peptide proton channel of influenza A virus from solid-state NMR. J. Phys. Chem. 111, 10825-10832.
49. 1H-Driven Spin Diffusion NMR Spectroscopy. J. Am. Chem. Soc. 128, 7242-7451.
50. DeGrado, W. F., Gratkowski, H., and Lear, J. D. (2003) How do helix-helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo-oligomeric helical bundles. Protein Sci. 12, 647-665.
51. Yang, J., Prorok, M., Castellino, F. J., and Weliky, D. P. (2004) Oligomeric β-structure of the membrane-bound HIV-1 fusion peptide formed from soluble monomers. Biophys. J. 87, 1951-1963.
52. Hiller, M., Krabben, L., Vinothkumar, K. R., Castellani, F., and van Rossum, B. J.; et al. (2005) Solid-state magic-angle spinning NMR of outer-membrane protein G from Escherichia coli. ChemBioChem 6, 1679-1684.
53. Schneider, R., Ader, C., Lange, A., Giller, K., and Hornig, S.; et al. (2008) Solid-state NMR spectroscopy applied to a chimeric potassium channel in lipid bilayers. J. Am. Chem. Soc. 130, 7427-7435.
54. 2H NMR of aligned membranes. J. Mol. Biol. 372, 50-66.
55. Lewis, B. A., Harbison, G. S., Herzfeld, J., and Griffin, R. G. (1985) NMR structural analysis of a membrane protein: Bacteriorhodopsin peptide backbone orientation and motion. Biochemistry 24, 4671-4679.
56. Kates, M., Kushwaha, S. C., and Sprott, G. D. (1982) Lipids of purple membrane from extreme halophiles and of methanogenic bacteria. Methods Enzymol. 88, 98-111.
57. Bunge, A., Muller, P., Stöckl, M., Herrmann, A., and Huster, D. (2008) Characterization of the ternary mixture of sphingomyelin, POPC, and cholesterol: Support for an inhomogeneous lipid distribution at high temperatures. Biophys. J. 94, 2680-2690.
58. Leser, G. P., and Lamb, R. A. (2005) Influenza virus assembly and budding in raft-derived microdomains: A quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology 342, 215-227.