Oligomeric Structure, Dynamics, and Orientation of Membrane Proteins from Solid-State NMR

Structure

Volumn 14, Issue 12, 2006, Pages 1731-1740

  Hong, Mei ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ALPHA HELIX; ANISOTROPY; ATOM; BETA SHEET; CONCENTRATION (PARAMETERS); CONFORMATION; DIFFUSION; DYNAMICS; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SOLID STATE; STRUCTURE ANALYSIS;

ANIMALS; ANISOTROPY; CELL MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MODELS, MOLECULAR; PEPTIDES; POTASSIUM; POTASSIUM CHANNELS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEINS;

EID: 33845217043     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2006.10.002     Document Type: Review

References (80)

1. Afonin S., Glaser R.W., Berditchevskaia M., Wadhwani P., Guhrs K.H., Mollmann U., Perner A., and Ulrich A.S. 4-fluorophenylglycine as a label for 19F NMR structure analysis of membrane-associated peptides. ChemBioChem 4 (2003) 1151-1163
2. Afonin S., Durr U.H., Glaser R.W., and Ulrich A.S. 'Boomerang'-like insertion of a fusogenic peptide in a lipid membrane revealed by solid-state 19F NMR. Magn. Reson. Chem. 42 (2004) 195-203
3. Aisenbrey C., and Bechinger B. Investigations of polypeptide rotational diffusion in aligned membranes by 2H and 15N solid-state NMR spectroscopy. J. Am. Chem. Soc. 126 (2004) 16676-16683
4. Aisenbrey C., and Bechinger B. Tilt and rotational pitch angle of membrane-inserted polypeptides from combined 15N and 2H solid-state NMR spectroscopy. Biochemistry 43 (2004) 10502-10512
5. Antzutkin O.N., and Tycko R. High-order multiple quantum excitation in 13C nuclear magnetic resonance spectroscopy of organic solids. J. Chem. Phys. 110 (1999) 2749-2752
6. Antzutkin O.N., Balbach J.J., Leapman R.D., Rizzo N.W., Reed J., and Tycko R. Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of β-sheets in Alzheimer's β-amyloid fibrils. Proc. Natl. Acad. Sci. USA 97 (2000) 13045-13050
7. Baldus M. Solid-state NMR spectroscopy: molecular structure and organization at the atomic level. Angew. Chem. Int. Ed. Engl. 45 (2006) 1186-1188
8. Barre P., Zschornig O., Arnold K., and Huster D. Structural and dynamical changes of the bindin B18 peptide upon binding to lipid membranes. A solid-state NMR study. Biochemistry 42 (2003) 8377-8386
9. Bechinger B., Aisenbrey C., and Bertani P. The alignment, structure and dynamics of membrane-associated polypeptides by solid-state NMR spectroscopy. Biochim. Biophys. Acta 1666 (2004) 190-204
10. Bockmann A. Structural and dynamic studies of proteins by high-resolution solid-state NMR. C. R. Chim. 9 (2006) 381-392
11. Buffy J.J., Hong T., Yamaguchi S., Waring A., Lehrer R.I., and Hong M. Solid-state NMR investigation of the depth of insertion of protegin-1 in lipid bilayers using paramagnetic Mn2+. Biophys. J. 85 (2003) 2363-2373
12. Buffy J.J., Waring A.J., Lehrer R.I., and Hong M. Immobilization and aggregation of antimicrobial peptide protegrin in lipid bilayers investigated by solid-state NMR. Biochemistry 42 (2003) 13725-13734
13. Buffy J.J., Waring A.J., and Hong M. Determination of peptide oligomerization in lipid membranes with magic-angle spinning spin diffusion NMR. J. Am. Chem. Soc. 127 (2005) 4477-4483
14. Cady, S.D., and Hong, M. (2006). Determining the orientation of rotationally diffusing membrane proteins using powder samples and magic-angle spinning: a 2H, 13C, and 15N solid-state NMR investigation of a transmembrane helical bundle. In Rocky Mountain Conference on Analytical Chemistry: Breckenridge, CO.
15. Chekmenev E.Y., Hu J., Gor'kov P.L., Brey W.W., Cross T.A., Ruuge A., and Smirnov A.I. 15N and 31P solid-state NMR study of transmembrane domain alignment of M2 protein of influenza A virus in hydrated cylindrical lipid bilayers confined to anodic aluminum oxide nanopores. J. Magn. Reson. 173 (2005) 322-327
16. De Angelis A.A., Nevzorov A.A., Park S.H., Howell S.C., Mrse A.A., and Opella S.J. High-resolution NMR spectroscopy of membrane proteins in aligned bicelles. J. Am. Chem. Soc. 126 (2004) 15340-15341
17. deAzevedo E.R., Bonagamba T.J., Hu W., and Schmidt-Rohr K. Centerband-only detection of exchange: efficient analysis of dynamics in solids by NMR. J. Am. Chem. Soc. 121 (1999) 8411-8412
18. deAzevedo E.R., Bonagamba T.J., Hu W., and Schmidt-Rohr K. Principle of centerband-only detection of the exchange and extension to a four-time CODEX. J. Chem. Phys. 112 (2000) 8988-9001
19. Doherty T., Waring A.J., and Hong M. Membrane-bound conformation and topology of the antimicrobial peptide tachyplesin-I by solid-state NMR. Biochemistry (2006)
20. Gaemers S., and Bax A. Morphology of three lyotropic liquid crystalline biological NMR media studied by translational diffusion anisotropy. J. Am. Chem. Soc. 123 (2001) 12343-12352
21. Glaser R.W., Grune M., Wandelt C., and Ulrich A.S. Structure analysis of a fusogenic peptide sequence from the sea urchin fertilization protein bindin. Biochemistry 38 (1999) 2560-2569
22. Glaser R.W., Sachse C., Durr U.H., Wadhwani P., and Ulrich A.S. Orientation of the antimicrobial peptide PGLa in lipid membranes determined from 19F-NMR dipolar couplings of 4-CF3-phenylglycine labels. J. Magn. Reson. 168 (2004) 153-163
23. Glaser R.W., Sachse C., Durr U.H., Wadhwani P., Afonin S., Strandberg E., and Ulrich A.S. Concentration-dependent realignment of the antimicrobial peptide PGLa in lipid membranes observed by solid-state 19F-NMR. Biophys. J. 88 (2005) 3392-3397
24. Grage S.L., and Ulrich A.S. Orientation-dependent (19)F dipolar couplings within a trifluoromethyl group are revealed by static multipulse NMR in the solid state. J. Magn. Reson. 146 (2000) 81-88
25. Harroun T.A., Koslowsky M., Nieh M.P., de Lannoy C.F., Raghunathan V.A., and Katsaras J. Comprehensive examination of mesophases formed by DMPC and DHPC mixtures. Langmuir 21 (2005) 5356-5361
26. Hiller M., Krabben L., Vinothkumar K.R., Castellani F., van Rossum B.J., Kuhlbrandt W., and Oschkinat H. Solid-state magic-angle spinning NMR of outer-membrane protein G from Escherichia coli. ChemBioChem 6 (2005) 1679-1684
27. Hong M., and Doherty T. Orientation determination of membrane-disruptive proteins using powder samples and rotational diffusion: a simple solid-state NMR approach. Chem. Phys. Lett. 432 (2006) 296-300
28. Howard K.P., Liu W., Crocker E., Nanda V., Lear J., Degrado W.F., and Smith S.O. Rotational orientation of monomers within a designed homo-oligomer transmembrane helical bundle. Protein Sci. 14 (2005) 1019-1024
29. Huster D. Investigations of the structure and dynamics of membrane-associated peptides by magic angle spinning NMR. Prog. NMR Spectrosc. 46 (2005) 79-107
30. Huster D., and Gawrisch K. NOESY NMR crosspeaks between lipid headgroups and hydrocarbon chains: spin diffusion or molecular disorder?. J. Am. Chem. Soc. 121 (1999) 1992-1993
31. Huster D., Arnold K., and Gawrisch K. Investigation of lipid organization in biological membranes by two-dimensional nuclear Overhauser enhancement spectroscopy. J. Phys. Chem. 103 (1999) 243-251
32. Huster D., Yao X.L., and Hong M. Membrane protein topology probed by 1H spin diffusion from lipids using solid-state NMR spectroscopy. J. Am. Chem. Soc. 124 (2002) 874-883
33. Huster D., Vogel A., Katzka C., Scheidt H.A., Binder H., Dante S., Gutberlet T., Zschornig O., Waldmann H., and Arnold K. Membrane insertion of a lipidated ras peptide studied by FTIR, solid-state NMR, and neutron diffraction spectroscopy. J. Am. Chem. Soc. 125 (2003) 4070-4079
34. Kamihira M., Vosegaard T., Mason A.J., Straus S.K., Nielsen N.C., and Watts A. Structural and orientational constraints of bacteriorhodopsin in purple membranes determined by oriented-sample solid-state NMR spectroscopy. J. Struct. Biol. 149 (2005) 7-16
35. Ketchem R.R., Hu W., and Cross T.A. High resolution conformation of Gramicidine A in a lipid bilayer by solid-state NMR. Science 261 (1993) 1457-1460
36. Lange A., Giller K., Hornig S., Martin-Eauclaire M.F., Pongs O., Becker S., and Baldus M. Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440 (2006) 959-962
37. Liu W., Crocker E., Siminovitch D.J., and Smith S.O. Role of side-chain conformational entropy in transmembrane helix dimerization of glycophorin A. Biophys. J. 84 (2003) 1263-1271
38. Liu W., Crocker E., Constantinescu S.N., and Smith S.O. Helix packing and orientation in the transmembrane dimer of gp55-P of the spleen focus forming virus. Biophys. J. 89 (2005) 1194-1202
39. Lorigan G.A., Dave P.C., Tiburu E.K., Damodaran K., Abu-Baker S., Karp E.S., Gibbons W.J., and Minto R.E. Solid-state NMR spectroscopic studies of an integral membrane protein inserted into aligned phospholipid bilayer nanotube arrays. J. Am. Chem. Soc. 126 (2004) 9504-9505
40. Luca S., White J.F., Sohal A.K., Filippov D.V., van Boom J.H., Grisshammer R., and Baldus M. The conformation of neurotensin bound to its G protein-coupled receptor. Proc. Natl. Acad. Sci. USA 100 (2003) 10706-10711
41. Ludtke S.J., He K., Heller W.T., Harroun T.A., Yang L., and Huang H.W. Membrane pores induced by magainin. Biochemistry 35 (1996) 13723-13728
42. Mani R., Cady S.D., Tang M., Waring A.J., Lehrer R.I., and Hong M. Membrane-dependent oligomeric structure and pore formation of a β-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR. Proc. Natl. Acad. Sci. USA 103 (2006) 16242-16247
43. Mani R., Tang M., Wu X., Buffy J.J., Waring A.J., Sherman M.A., and Hong M. Membrane-bound dimer structure of a β-hairpin antimicrobial peptide from rotational-echo double-resonance solid-state NMR. Biochemistry 45 (2006) 8341-8349
44. Marassi F.M., and Opella S.J. Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints. Protein Sci. 12 (2003) 403-411
45. Mascioni A., and Veglia G. Theoretical analysis of residual dipolar coupling patterns in regular secondary structures of proteins. J. Am. Chem. Soc. 125 (2003) 12520-12526
46. McDermott A.E. Structural and dynamic studies of proteins by solid-state NMR spectroscopy: rapid movement forward. Curr. Opin. Struct. Biol. 14 (2004) 554-561
47. Mesleh M.F., Lee S., Veglia G., Thiriot D.S., Marassi F.M., and Opella S.J. Dipolar waves map the structure and topology of helices in membrane proteins. J. Am. Chem. Soc. 125 (2003) 8928-8935
48. Opella S.J., and Marassi F.M. Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 104 (2004) 3587-3606
49. Opella S.J., Marassi F.M., Gesell J.J., Valente A.P., Kim Y., Oblatt-Montal M., and Montal M. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat. Struct. Biol. 6 (1999) 374-379
50. Park S.H., and Opella S.J. Tilt angle of a trans-membrane helix is determined by hydrophobic mismatch. J. Mol. Biol. 350 (2005) 310-318
51. Park S.H., Mrse A.A., Nevzorov A.A., Mesleh M.F., Oblatt-Montal M., Montal M., and Opella S.J. Three-dimensional structure of the channel-forming trans-membrane domain of virus protein "u" (Vpu) from HIV-1. J. Mol. Biol. 333 (2003) 409-424
52. Park S.H., Mrse A.A., Nevzorov A.A., De Angelis A.A., and Opella S.J. Rotational diffusion of membrane proteins in aligned phospholipid bilayers by solid-state NMR spectroscopy. J. Magn. Reson. 178 (2006) 162-165
53. Park S.H., Prytulla S., De Angelis A.A., Brown J.M., Kiefer H., and Opella S.J. High-resolution NMR spectroscopy of a GPCR in aligned bicelles. J. Am. Chem. Soc. 128 (2006) 7402-7403
54. Prosser R.S., Hwang J.S., and Vold R.R. Magnetically aligned phospholipid bilayers with positive ordering: a new model membrane system. Biophys. J. 74 (1998) 2405-2418
55. Prosser R.S., Luchette P.A., and Westerman P.W. Using O2 to probe membrane immersion depth by 19F NMR. Proc. Natl. Acad. Sci. USA 97 (2000) 9967-9971
56. Prosser R.S., Evanics F., Kitevski J.L., and Al-Abdul-Wahid M.S. Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins. Biochemistry 45 (2006) 8453-8465
57. Saffman P.G., and Delbruck M. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA 72 (1975) 3111-3113
58. Salgado J., Grage S.L., Kondejewski L.H., Hodges R.S., McElhaney R.N., and Ulrich A.S. Membrane-bound structure and alignment of the antimicrobial β-sheet peptide gramicidin S derived from angular and distance constraints by solid-state 19F-NMR. J. Biomol. NMR 21 (2001) 191-208
59. Sanders C.R., Hare B.J., Howard K.P., and Prestegard J.H. Magnetically oriented phospholipid micelles as a tool for the study of membrane associated molecules. Prog. NMR Spectrosc. 26 (1994) 421-444
60. Schmidt-Rohr K., and Hong M. Measurements of carbon to amide-proton distances by C-H dipolar recoupling with 15N NMR detection. J. Am. Chem. Soc. 125 (2003) 5648-5649
61. Smith S.O., Kawakami T., Liu W., Ziliox M., and Aimoto S. Helical structure of phospholamban in membrane bilayers. J. Mol. Biol. 313 (2001) 1139-1148
62. Smith S.O., Song D., Shekar S., Groesbeek M., Ziliox M., and Aimoto S. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry 40 (2001) 6553-6558
63. Smith S.O., Smith C., Shekar S., Peersen O., Ziliox M., and Aimoto S. Transmembrane interactions in the activation of the Neu receptor tyrosine kinase. Biochemistry 41 (2002) 9321-9332
64. Song Z., Kovacs F.A., Wang J., Denny J.K., Shekar S.C., Quine J.R., and Cross T.A. Transmembrane domain of M2 protein from influenza A virus studied by solid-state 15N polarization inversion spin exchange at magic angle NMR. Biophys. J. 79 (2000) 767-775
65. Strandberg, E., Tremouilhac, P., Wadhwani, P., and Ulrich, A.S. (2006). Realignment of membrane-bound antimicrobial peptides studied by solid-state 2H- and 19F-NMR. In Rocky Mountain Conference on Analytical Chemistry: Breckenridge, CO.
66. Tian F., Song Z., and Cross T.A. Orientational constraints derived from hydrated powder samples by two-dimensional PISEMA. J. Magn. Reson. 135 (1998) 227-231
67. Toke O., Maloy W.L., Kim S.J., Blazyk J., and Schaefer J. Secondary structure and lipid contact of a peptide antibiotic in phospholipid bilayers by REDOR. Biophys. J. 87 (2004) 662-674
68. Toke O., O'Connor R.D., Weldeghiorghis T.K., Maloy W.L., Glaser R.W., Ulrich A.S., and Schaefer J. Structure of (KIAGKIA)3 aggregates in phospholipid bilayers by solid-state NMR. Biophys. J. 87 (2004) 675-687
69. Tuzi S., Hasegawa J., Kawaminami R., Naito A., and Saito H. Regio-selective detection of dynamic structure of transmembrane alpha-helices as revealed from (13)C NMR spectra of [3-13C]Ala-labeled bacteriorhodopsin in the presence of Mn2+ ion. Biophys. J. 81 (2001) 425-434
70. Ulrich A.S., Otter M., Glabe C.G., and Hoekstra D. Membrane fusion is induced by a distinct peptide sequence of the sea urchin fertilization protein bindin. J. Biol. Chem. 273 (1998) 16748-16755
71. van Dam L., Karlsson G., and Edwards K. Direct observation and characterization of DMPC/DHPC aggregates under conditions relevant for biological solution NMR. Biochim. Biophys. Acta 1664 (2004) 241-256
72. van Dam L., Karlsson G., and Edwards K. Morphology of magnetically aligning DMPC/DHPC aggregates-perforated sheets, not disks. Langmuir 22 (2006) 3280-3285
73. Vogel A., Katzka C.P., Waldmann H., Arnold K., Brown M.F., and Huster D. Lipid modifications of a Ras peptide exhibit altered packing and mobility versus host membrane as detected by 2H solid-state NMR. J. Am. Chem. Soc. 127 (2005) 12263-12272
74. Wang J., Kim S., Kovacs F., and Cross T.A. Structure of the the transmembrane region of the M2 protein H+ channel. Protein Sci. 10 (2001) 2241-2250
75. Yamaguchi S., Huster D., Waring A., Lehrer R.I., Tack B.F., Kearney W., and Hong M. Orientation and dynamics of an antimicrobial peptide in the lipid bilayer by solid-state NMR. Biophys. J. 81 (2001) 2203-2214
76. Yamaguchi S., Waring A., Hong T., Lehrer R., and Hong M. Solid-State NMR investigations of peptide-lipid interaction and orientation of a β-sheet antimicrobial peptide, protegrin. Biochemistry 41 (2002) 9852-9862
77. Yang J., and Weliky D.P. Solid-state nuclear magnetic resonance evidence for parallel and antiparallel strand arrangements in the membrane-associated HIV-1 fusion peptide. Biochemistry 42 (2003) 11879-11890
78. Yang J., Gabrys C.M., and Weliky D.P. Solid-state nuclear magnetic resonance evidence for an extended β strand conformation of the membrane-bound HIV-1 fusion peptide. Biochemistry 40 (2001) 8126-8137
79. Yang J., Prorok M., Castellino F.J., and Weliky D.P. Oligomeric β-structure of the membrane-bound HIV-1 fusion peptide formed from soluble monomers. Biophys. J. 87 (2004) 1951-1963
80. Yen Y., and Pines A. Multiple-quantum NMR in solids. J. Chem. Phys. 78 (1983) 3579-3582