The hybrid solution/solid-state NMR method for membrane protein structure determination

Comprehensive Biophysics

Volumn 1, Issue , 2012, Pages 182-198

  Veglia, G ^a   Traaseth, N J ^a   Shi, L ^a   Verardi, R ^a   Gopinath, T ^a   Gustavsson, M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Bicelles; Hybrid approach; Membrane proteins; Micelles; NMR; Oriented lipid bilayers; Phospholamban; PISEMA; Sarcolipin; SERCA; Solid state NMR; Solution NMR; Structure calculations

Indexed keywords

EID: 84882738241     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-374920-8.00115-6     Document Type: Chapter

References (182)

1. Sanders C.R., Myers J.K. Disease-related misassembly of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 2004, 33:25-51.
2. Kim H.J., Howell S.C., Van Horn W.D., Jeon Y.H., Sanders C.R. Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins. Prog. NMR Spect. 2009, 55:335-360.
3. Cornea R.L., Thomas D.D. Effects of membrane thickness on the molecular dynamics and enzymatic activity of reconstituted Ca-ATPase. Biochemistry 1994, 33:2912-2920.
4. Reddy L.G., Cornea R.L., Winters D.L., McKenna E., Thomas D.D. Defining the molecular components of calcium transport regulation in a reconstituted membrane system. Biochemistry 2003, 42:4585-4592.
5. 2+-ATPase activity. Cell Calcium 2006, 39:209-216.
6. Cherezov V., Rosenbaum D.M., Hanson M.A., Rasmussen S.G., Thian F.S., Kobilka T.S., Choi H.J., Kuhn P., Weis W.I., Kobilka B.K., Stevens R.C. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 2007, 318:1258-1265.
7. + conduction and selectivity. Science 1998, 280:69-77.
8. Rasmussen S.G., Choi H.J., Rosenbaum D.M., Kobilka T.S., Thian F.S., Edwards P.C., Burghammer M., Ratnala V.R., Sanishvili R., Fischetti R.F., Schertler G.F., Weis W.I., Kobilka B.K. Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 2007, 450:383-387.
9. Toyoshima C., Mizutani T. Crystal structure of the calcium pump with a bound ATP analogue. Nature 2004, 430:529-535.
10. Nath A., Atkins W.M., Sligar S.G. Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 2007, 46:2059-2069.
11. Shi L., Traaseth N.J., Verardi R., Cembran A., Gao J., Veglia G. A refinement protocol to determine structure, topology, and depth of insertion of membrane proteins using hybrid solution and solid-state NMR restraints. J. Biomol. NMR 2009, 44:195-205.
12. Teriete P., Franzin C.M., Choi J., Marassi F.M. Structure of the Na, K-ATPase regulatory protein FXYD1 in micelles. Biochemistry 2007, 46:6774-6783.
13. Traaseth N.J., Shi L., Verardi R., Mullen D.G., Barany G., Veglia G. Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc. Natl. Acad. Sci. USA 2009, 106:10165-10170.
14. Franzin C.M., Teriete P., Marassi F.M. Structural similarity of a membrane protein in micelles and membranes. J. Am. Chem. Soc. 2007, 129:8078-8079.
15. Tamm L.K., Abildgaard F., Arora A., Blad H., Bushweller J.H. Structure, dynamics and function of the outer membrane protein A (OmpA) and influenza hemagglutinin fusion domain in detergent micelles by solution NMR. FEBS Lett. 2003, 555:139-143.
16. Zhou Y., Cierpicki T., Jimenez R.H., LGBRasik S.M., Ellena J.F., Cafiso D.S., Kadokura H., Beckwith J., Bushweller J.H. NMR solution structure of the integral membrane enzyme DsbB: Functional insights into DsbB-catalyzed disulfide bond formation. Mol. Cell 2008, 31:896-908.
17. Page R.C., Kim S., Cross T.A. Transmembrane helix uniformity examined by spectral mapping of torsion angles. Structure 2008, 16:787-797.
18. von Heijne G. Membrane-protein topology. Nat. Rev. Mol. Cell Biol. 2006, 7:909-918.
19. Cross T.A., Opella S.J. Structural properties of fd coat protein in sodium dodecyl sulfate micelles. Biochem. Biophys. Res. Commun. 1980, 92:478-484.
20. Hagen D.S., Weiner J.H., Sykes B.D. Investigation of solvent accessibility of the fluorotyrosyl residues of M13 coat protein in deoxycholate micelles and phospholipid vesicles. Biochemistry 1979, 18:2007-2012.
21. Kumar A., Ernst R.R., Wuthrich K. A two-dimensional nuclear Overhauser enhancement (2D-NOESY) experiment for the elucidation of complete proton-proton cross relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 1980, 95:1-6.
22. Lauterwein J., Bosch C., Brown L.R., Wuthrich K. Physiochemical studies of the protein-lipid interactions in melittin-containing micelles. Biochim. Biophys. Acta 1979, 556:244-264.
23. Page R.C., Moore J.D., Nguyen H.B., Sharma M., Chase R., Gao F.P., Mobley C.K., Sanders C.R., Ma L., Sonnichsen F.D., Lee S., Howell S.C., Opella S.J., Cross T.A. Comprehensive evaluation of solution nuclear magnetic resonance spectroscopy sample preparation for helical integral membrane proteins. J. Struct. Funct. Genomics 2006, 7:51-64.
24. Poget S.F., Girvin M.E. Solution NMR of membrane proteins in bilayer mimics: Small is beautiful, but sometimes bigger is better. Biochim. Biophys. Acta 2007, 1768:3098-3106.
25. Sanders C.R., Oxenoid K. Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins. Biochim. Biophys. Acta 2000, 1508:129-145.
26. Traaseth N.J., Ha K.N., Verardi R., Shi L., Buffy J.J., Masterson L.R., Veglia G. Structural and dynamic basis of phospholamban and sarcolipin inhibition of Ca(2+)-ATPase. Biochemistry 2008, 47:3-13.
27. Van Horn W.D., Kim H.J., Ellis C.D., Hadziselimovic A., Sulistijo E.S., Karra M.D., Tian C., Sonnichsen F.D., Sanders C.R. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 2009, 324:1726-1729.
28. Buffy J.J., Buck-Koehntop B.A., Porcelli F., Traaseth N.J., Thomas D.D., Veglia G. Defining the intramembrane binding mechanism of sarcolipin to calcium ATPase using solution NMR spectroscopy. J. Mol. Biol. 2006, 358:420-429.
29. 2+-ATPase by tuning phospholamban structural dynamics. J. Biol. Chem. 2007, 282:37205-37214.
30. Traaseth N.J., Thomas D.D., Veglia G. Effects of Ser16 phosphorylation on the allosteric transitions of phospholamban/Ca(2+)-ATPase complex. J. Mol. Biol. 2006, 358:1041-1050.
31. Zamoon J., Mascioni A., Thomas D.D., Veglia G. NMR solution structure and topological orientation of monomeric phospholamban in dodecylphosphocholine micelles. Biophys. J. 2003, 85:2589-2598.
32. Zamoon J., Nitu F., Karim C., Thomas D.D., Veglia G. Mapping the interaction surface of a membrane protein: Unveiling the conformational switch of phospholamban in calcium pump regulation. Proc. Natl. Acad. Sci. USA 2005, 102:4747-4752.
33. Mascioni A., Karim C., Barany G., Thomas D.D., Veglia G. Structure and orientation of sarcolipin in lipid environments. Biochemistry 2002, 41:475-482.
34. Porcelli F., Buck B., Lee D.K., Hallock K.J., Ramamoorthy A., Veglia G. Structure and orientation of pardaxin determined by NMR experiments in model membranes. J. Biol. Chem. 2004, 279:45815-45823.
35. 15N labeling of proteins for NMR studies. J. Biomol. NMR 1995, 5:339-344.
36. Kay L.E., Ikura M., Tschudin R., Bax A. Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. J. Magn. Reson. 1990, 89:496-514.
37. Sprangers R., Velyvis A., Kay L.E. Solution NMR of supramolecular complexes: Providing new insights into function. Nat. Methods 2007, 4:697-703.
38. Xu Y., Liu M., Simpson P.J., Isaacson R., Cota E., Marchant J., Yang D., Zhang X., Freemont P., Matthews S. Automated assignment in selectively methyl-labeled proteins. J. Am. Chem. Soc. 2009, 131:9480-9481.
39. Overhauser A.W. Polarization of nuclei in metals. Phys. Rev. 1953, 92:411-415.
40. Solomon I. Relaxation processes in a system of two spins. Phys. Rev. 1955, 99:559-565.
41. Wuthrich K. NMR of Proteins and Nuclear Acids 1986, Wiley, New York.
42. Traaseth N.J., Verardi R., Veglia G. Asymmetric methyl group labeling as a probe of membrane protein homo-oligomers by NMR spectroscopy. J. Am. Chem. Soc. 2008, 130:2400-2401.
43. Karplus M. Vicinal proton coupling in nuclear magnetic resonance. J. Am. Chem. Soc. 1969, 85:2870-2871.
44. Siep S., Balbach J., Kessler H. Determination of the HN-HA coupling constant in large isotopically enriched proteins. Angew. Chem. Int. Ed. Engl. 1992, 31:1609-1611.
45. Cornilescu G., Delaglio F., Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 1999, 13:289-302.
46. Englander S.W., Kallenbach N.R. Hydrogen exchange and structural dynamics of protein and nucleic acids. Q. Rev. Biophys. 1984, 16:521-655.
47. Bodenhausen G., Ruben D.J. Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett. 1980, 60:185-189.
48. Hwang T.L., van Zijl P.C., Mori S. Accurate quantitation of water-amide proton exchange rates using the phase-modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme. J. Biomol. NMR 1998, 11:221-226.
49. Opella S.J., Marassi F.M. Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 2004, 104:3587-3606.
50. Veglia G., Zeri A.C., Ma C., Opella S.J. Deuterium/hydrogen exchange factors measured by solution nuclear magnetic resonance spectroscopy as indicators of the structure and topology of membrane proteins. Biophys. J. 2002, 82:2176-2183.
51. Bax A., Vuister G.W., Grzesiek S., Delaglio F., Wang A.C., Tschudin R., Zhu G. Measurement of homo- and heteronuclear J couplings from quantitative J correlation. Methods Enzymol. 1994, 239:79-105.
52. Hu J.S., Bax A. Chi 1 angle information from a simple two-dimensional NMR experiment that identifies trans 3JNC gamma couplings in isotopically enriched proteins. J. Biomol. NMR 1997, 9:323-328.
53. 13C chemical shifts. J. Biomol. NMR 1996, 7:256-260.
54. MacKenzie K.R., Prestegard J.H., Engelman D.M. A transmembrane helix dimer: Structure and implications. Science 1997, 276:131-133.
55. Oxenoid K., Chou J.J. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc. Natl. Acad. Sci. USA 2005, 102:10870-10875.
56. Traaseth N.J., Buffy J.J., Zamoon J., Veglia G. Structural dynamics and topology of phospholamban in oriented lipid bilayers using multidimensional solid-state NMR. Biochemistry 2006, 45:13827-13834.
57. Crick F.H.C. The packing of α-helices: Simple coiled-coils. Acta Cryst. 1953, 6:689-697.
58. Bowie J.U. Helix packing in membrane proteins. J. Mol. Biol. 1997, 272:780-789.
59. Bowie J.U. Stabilizing membrane proteins. Curr. Opin. Struct. Biol. 2001, 11:397-402.
60. Mackenzie K.R. Folding and stability of alpha-helical integral membrane proteins. Chem. Rev. 2006, 106:1931-1977.
61. MacKenzie K.R., Fleming K.G. Association energetics of membrane spanning alpha-helices. Curr. Opin. Struct. Biol. 2008, 18:412-419.
62. Simmerman H.K., Kobayashi Y.M., Autry J.M., Jones L.R. A leucine zipper stabilizes the pentameric membrane domain of phospholamban and forms a coiled-coil pore structure. J. Biol. Chem. 1996, 271:5941-5946.
63. White S.H., Wimley W.C. Membrane protein folding and stability: Physical principles. Annu. Rev. Biophys. Biomol. Struct. 1999, 28:319-365.
64. Moore D.T., Berger B.W., DeGrado W.F. Protein-protein interactions in the membrane: Sequence, structural, and biological motifs. Structure 2008, 16:991-1001.
65. Walters R.F., DeGrado W.F. Helix-packing motifs in membrane proteins. Proc. Natl. Acad. Sci. USA 2006, 103:13658-13663.
66. Battiste J.L., Wagner G. Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear Overhauser effect data. Biochemistry 2000, 39:5355-5365.
67. Iwahara J., Schwieters C.D., Clore G.M. Ensemble approach for NMR structure refinement against (1)H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule. J. Am. Chem. Soc. 2004, 126:5879-5896.
68. Liang B., Bushweller J.H., Tamm L.K. Site-directed parallel spin-labeling and paramagnetic relaxation enhancement in structure determination of membrane proteins by solution NMR spectroscopy. J. Am. Chem. Soc. 2006, 128:4389-4397.
69. Lindfors H.E., de Koning P.E., Drijfhout J.W., Venezia B., Ubbink M. Mobility of TOAC spin-labelled peptides binding to the Src SH3 domain studied by paramagnetic NMR. J. Biomol. NMR 2008, 41:157-167.
70. Fernandez C., Hilty C., Wider G., Wuthrich K. Lipid-protein interactions in DHPC micelles containing the integral membrane protein OmpX investigated by NMR spectroscopy. Proc. Natl. Acad. Sci. USA 2002, 99:13533-13537.
71. Petros A.M., Mueller L., Kopple K.D. NMR identification of protein surfaces using paramagnetic probes. Biochemistry 1990, 29:10041-10048.
72. Damberg P., Jarvet J., Graslund A. Micellar systems as solvents in peptide and protein structure determination. Methods Enzymol. 2001, 229:271-285.
73. 19F NMR. Proc. Natl. Acad. Sci. USA 2000, 97:9967-9971.
74. Prosser, R. S.; Evanics, F.; Kitevski, J. L.; Patel, S. The measurement of immersion depth and topology of membrane proteins by solution state NMR. Biochim. Biophys. Acta 2007, 1768, 3044-3051.
75. Bax A., Kontaxis G., Tjandra N. Dipolar coupling in macromolecular structure determination. Methods Enzymol. 2001, 339:127-174.
76. Prestegard J.H. New techniques in structural NMR-anisotropic interactions. Nat. Struct. Biol. 1998, 5:517-522.
77. 31P chemical shift anisotropy. J. Biomol. NMR 2003, 26:297-315.
78. Tycko R., Blanco F.J., Ishii Y. Alignment of biopolymers in strained gels: A new way to create detectable dipole-dipole couplings in high-resolution biomolecular NMR. J. Am. Chem. Soc. 2000, 122:9340-9341.
79. Ma C., Opella S.J. Lanthanide ions bind specifically to an added 'EF-hand' and orient a membrane protein in micelles for solution NMR spectroscopy. J. Magn. Reson. 2000, 146:381-384.
80. Veglia G., Opella S.J. Lanthanide ion binding to adventitious sites aligns membrane proteins in micelles for solution NMR spectroscopy. J. Am. Chem. Soc. 2000, 122:11733-11734.
81. Wohnert J., Franz K.J., Nitz M., Imperiali B., Schwalbe H. Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. J. Am. Chem. Soc. 2003, 125:13338-13339.
82. Park S.H., Son W.S., MGBRhopadhyay R., Valafar H., Opella S.J. Phage-induced alignment of membrane proteins enables the measurement and structural analysis of residual dipolar couplings with dipolar waves and lambda-maps. J. Am. Chem. Soc. 2009, 131:14140-14141.
83. Douglas S.M., Chou J.J., Shih W.M. DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. Proc. Natl. Acad. Sci. USA 2007, 104:6644-6648.
84. Lorieau J., Yao L., Bax A. Liquid crystalline phase of G-tetrad DNA for NMR study of detergent-solubilized proteins. J. Am. Chem. Soc. 2008, 130:7536-7537.
85. 13C NMR relaxation. J. Biomol. NMR 2007, 38:243-253.
86. Cierpicki T., Liang B., Tamm L.K., Bushweller J.H. Increasing the accuracy of solution NMR structures of membrane proteins by application of residual dipolar couplings: High-resolution structure of outer membrane protein A. J. Am. Chem. Soc. 2006, 128:6947-6951.
87. Hiller S., Garces R.G., Malia T.J., Orekhov V.Y., Colombini M., Wagner G. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 2008, 321:1206-1210.
88. Lei S., Traaseth N.J, Verardi R., Gustavsson M., Gao J., Veglia G. Paramagnetic-based NMR restraints lift residual dipolar coupling degeneracy in multidomain detergent-solubilized membrane proteins. J. Am. Chem. Soc 2011, 133:2232-2241.
89. Hong M. Oligomeric structure, dynamics, and orientation of membrane proteins from solid-state NMR. Structure 2006, 14:1731-1740.
90. Senes A., Chadi D.C., Law P.B., Walters R.F., Nanda V., Degrado W.F.E (z) a depth-dependent potential for assessing the energies of insertion of amino acid side-chains into membranes: Derivation and applications to determining the orientation of transmembrane and interfacial helices. J. Mol. Biol. 2007, 366:436-448.
91. Marassi F.M., Opella S.J. NMR structural studies of membrane proteins. Curr. Opin. Struct. Biol. 1998, 8:640-648.
92. Traaseth N.J., Verardi R., Torgersen K.D., Karim C.B., Thomas D.D., Veglia G. Spectroscopic validation of the pentameric structure of phospholamban. Proc. Natl. Acad. Sci. USA 2007, 104:14676-14681.
93. Buffy J.J., Traaseth N.J., Mascioni A., Gor'kov P.L., Chekmenev E.Y., Brey W.W., Veglia G. Two-dimensional solid-state NMR reveals two topologies of sarcolipin in oriented lipid bilayers. Biochemistry 2006, 45:10939-10946.
94. De Angelis A.A., Opella S.J. Bicelle samples for solid-state NMR of membrane proteins. Nat. Protoc. 2007, 2:2332-2338.
95. Prosser R.S., Evanics F., Kitevski J.L., Al-Abdul-Wahid M.S. Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins. Biochemistry 2006, 45:8453-8465.
96. Gor'kov P.L., Chekmenev E.Y., Li C., Cotten M., Buffy J.J., Traaseth N.J., Veglia G., Brey W.W. Using low-E resonators to reduce RF heating in biological samples for static solid-state NMR up to 900 MHz. J. Magn. Reson. 2007, 185:77-93.
97. Park S.H., Prytulla S., De Angelis A.A., Brown J.M., Kiefer H., Opella S.J. High-resolution NMR spectroscopy of a GPCR in aligned bicelles. J. Am. Chem. Soc. 2006, 128:7402-7403.
98. Cook G.A., Opella S.J. NMR studies of p7 protein from hepatitis C virus. Eur. Biophys. J. 2010, 39:1097-1104.
99. De Angelis A.A., Howell S.C., Nevzorov A.A., Opella S.J. Structure determination of a membrane protein with two trans-membrane helices in aligned phospholipid bicelles by solid-state NMR spectroscopy. J. Am. Chem. Soc. 2006, 128:12256-12267.
100. Waugh J.S. Uncoupling of local field spectra in nuclear magnetic resonance: Determination of atomic positions in solids. Proc. Natl. Acad. Sci. USA 1976, 73:1394-1397.
101. Muller L., Kumar A., Baumann T., Ernst R.R. Transient oscillations in NMR cross-polarization experiments in solids. Phys. Rev. Lett. 1974, 32:1402-1406.
102. Opella S.J., Yesinowski J.P., Waugh J.S. Nuclear magnetic resonance description of molecular motion and phase separations of cholesterol in lecithin dispersions. Proc. Natl. Acad. Sci. USA 1976, 73:3812-3815.
103. Allen T.W., Andersen O.S., Roux B. Structure of gramicidin a in a lipid bilayer environment determined using molecular dynamics simulations and solid-state NMR data. J. Am. Chem. Soc. 2003, 125:9868-9877.
104. Bertram R., Quine J.R., Chapman M.S., Cross T.A. Atomic refinement using orientational restraints from solid-state NMR. J. Magn. Reson. 2000, 147:9-16.
105. Ketchem R., Roux B., Cross T. High-resolution polypeptide structure in a lamellar phase lipid environment from solid state NMR derived orientational constraints. Structure 1997, 5:1655-1669.
106. Kim S., Quine J.R., Cross T.A. Complete cross-validation and R-factor calculation of a solid-state NMR derived structure. J. Am. Chem. Soc. 2001, 123:7292-7298.
107. Quine J.R., Brenneman M.T., Cross T.A. Protein structural analysis from solid-state NMR-derived orientational constraints. Biophys. J. 1997, 72:2342-2348.
108. Quine J.R., Cross T.A., Chapman M.S., Bertram R. Mathematical aspects of protein structure determination with NMR orientational restraints. Bull. Math. Biol. 2004, 66:1705-1730.
109. Shi L., Cembran A., Gao J., Veglia G. Tilt and azimuthal angles of a transmembrane peptide: A comparison between molecular dynamics calculations and solid-state NMR data of sarcolipin in lipid membranes. Biophys. J. 2009, 96:3648-3662.
110. Fu R., Truong M., Saager R.J., Cotten M., Cross T.A. High-resolution heteronuclear correlation spectroscopy in solid state NMR of aligned samples. J. Magn. Reson. 2007, 188:41-48.
111. Ketchem R.R., Hu W., Cross T.A. High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science 1993, 261:1457-1460.
112. 15N-labeled membrane protein in phospholipid bilayers. Proc. Natl. Acad. Sci. USA 1997, 94:8551-8556.
113. Marassi F.M., Opella S.J. Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints. Protein Sci. 2003, 12:403-411.
114. McDonnell P.A., Shon K., Kim Y., Opella S. J. fd coat protein structure in membrane environments. J. Mol. Biol. 1993, 233:447-463.
115. Nevzorov A.A., Park S.H., Opella S.J. Three-dimensional experiment for solid-state NMR of aligned protein samples in high field magnets. J. Biomol. NMR 2007, 37:113-116.
116. Opella S.J., Marassi F.M., Gesell J.J., Valente A.P., Kim Y., Oblatt-Montal M., Montal M. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat. Struct. Biol 1999, 6:374-379.
117. Park S.H., Mrse A.A., Nevzorov A.A., Mesleh M.F., Oblatt-Montal M., Montal M., Opella S.J. Three-dimensional structure of the channel-forming trans-membrane domain of virus protein 'u' (Vpu) from HIV-1. J. Mol. Biol. 2003, 333:409-424.
118. Thiriot D.S., Nevzorov A.A., Zagyanskiy L., Wu C.H., Opella S.J. Structure of the coat protein in Pf1 bacteriophage determined by solid-state NMR spectroscopy. J. Mol. Biol. 2004, 341:869-879.
119. Valentine K.G., Liu S.F., Marassi F.M., Veglia G., Opella S.J., Ding F.X., Wang S.H., Arshava B., Becker J.M., Naider F. Structure and topology of a peptide segment of the 6th transmembrane domain of the Saccharomyces cerevisiae alpha-factor receptor in phospholipid bilayers. Biopolymers 2001, 59:243-256.
120. Zeri A.C., Mesleh M.F., Nevzorov A.A., Opella S.J. Structure of the coat protein in fd filamentous bacteriophage particles determined by solid-state NMR spectroscopy. Proc. Natl. Acad. Sci. USA 2003, 100:6458-6463.
121. 15N]-labeled membrane proteins in oriented lipid bilayers. J. Biomol. NMR 2002, 22:225-247.
122. Marassi F., Gesell J.J., Opella J.S. Recent developments in multidimensional NMR methods for structural studies of membrane proteins. Biol. Magn. Reson 1999, 16:121-145.
123. Nevzorov A.A. Mismatched Hartmann-Hahn conditions cause proton-mediated intermolecular magnetization transfer between dilute low-spin nuclei in NMR of static solids. J. Am. Chem. Soc. 2008, 130:11282-11283.
124. Nevzorov A.A. High-resolution local field spectroscopy with internuclear correlations. J. Magn. Reson. 2009, 201:111-114.
125. Xu J., Struppe J., Ramamoorthy A. Two-dimensional homonuclear chemical shift correlation established by the cross-relaxation driven spin diffusion in solids. J. Chem. Phys. 2008, 128:052308.
126. Mascioni A., Eggimann B.L., Veglia G. Determination of helical membrane protein topology using residual dipolar couplings and exhaustive search algorithm: Application to phospholamban. Chem. Phys. Lipids 2004, 132:133-144.
127. Mesleh M.F., Veglia G., DeSilva T.M., Marassi F.M., Opella S.J. Dipolar waves as NMR maps of protein structure. J. Am. Chem. Soc. 2002, 124:4206-4207.
128. Mesleh M.F., Opella S.J. Dipolar waves as NMR maps of helices in proteins. J. Magn. Reson. 2003, 163:288-299.
129. Mesleh M.F., Lee S., Veglia G., Thiriot D.S., Marassi F.M., Opella S.J. Dipolar waves map the structure and topology of helices in membrane proteins. J. Am. Chem. Soc. 2003, 125:8928-8935.
130. Walsh J.D., Wang Y.X. Periodicity, planarity, residual dipolar coupling, and structures. J. Magn. Reson. 2005, 174:152-162.
131. Marassi F.M., Opella S.J. A solid-state NMR index of helical membrane protein structure and topology. J. Magn. Reson. 2000, 144:150-155.
132. Wang J., Denny J., Tian C., Kim S., Mo Y., Kovacs F., Song Z., Nishimura K., Gan Z., Fu R., Quine J.R., Cross T.A. Imaging membrane protein helical wheels. J. Magn. Reson. 2000, 144:162-167.
133. Kim S., Cross T.A. Uniformity, ideality, and hydrogen bonds in transmembrane alpha-helices. Biophys. J. 2002, 83:2084-2095.
134. Tjandra N., Bax A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 1997, 278:1111-1114.
135. Kuszewski J., Gronenborn A.M., Clore G.M. Improving the quality of NMR and crystallographic protein structures by means of a conformational database potential derived from structure databases. Protein Sci. 1996, 5:1067-1080.
136. Kuszewski J., Gronenborn A.M., Clore G.M. Improvements and extensions in the conformational database potential for the refinement of NMR and X-ray structures of proteins and nucleic acids. J. Magn. Reson. 1997, 125:171-177.
137. Schwieters C.D., Kuszewski J.J., Tjandra N., Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 2003, 160:65-73.
138. Im W., Brooks C.L. De novo folding of membrane proteins: An exploration of the structure and NMR properties of the fd coat protein. J. Mol. Biol. 2004, 337:513-519.
139. Lee J., Chen J., Brooks C.L., Im W. Application of solid-state NMR restraint potentials in membrane protein modeling. J. Magn. Reson. 2008, 193:68-76.
140. Nilges M., Clore G.M., Gronenborn A.M. Determination of three-dimensional structures of proteins from interproton distance data by dynamical simulated annealing from a random array of atoms: Circumventing problems associated with folding. FEBS Lett. 1988, 239:129-136.
141. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., Karplus M. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 1983, 4:187-217.
142. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., Skeel R.D., Kalé L., Schulten K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 2005, 26:1781-1802.
143. Verardi R., Shi L., Traaseth NJ., Walsh N., Veglia G. Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method. Proc. Natl. Acad. Sci. USA 2011, 108:9101-9106.
144. Robia S.L., Flohr N.C., Thomas D.D. Phospholamban pentamer quaternary conformation determined by in-gel fluorescence anisotropy. Biochemistry 2005, 44:4302-4311.
145. Robia S.L., Campbell K.S., Kelly E.M., Hou Z., Winters D.L., Thomas D.D. Forster transfer recovery reveals that phospholamban exchanges slowly from pentamers but rapidly from the SERCA regulatory complex. Circ. Res. 2007, 101:1123-1129.
146. Liu W., Fei J.Z., Kawakami T., Smith S.O. Structural constraints on the transmembrane and juxtamembrane regions of the phospholamban pentamer in membrane bilayers: Gln29 and Leu52. Biochim. Biophys. Acta 2007, 1768:2971-2978.
147. Smith S.O., Kawakami T., Liu W., Ziliox M., Aimoto S. Helical structure of phospholamban in membrane bilayers. J. Mol. Biol. 2001, 313:1139-1148.
148. Hughes E., Middleton D.A. Solid-state NMR reveals structural changes in phospholamban accompanying the functional regulation of Ca2+-ATPase. J. Biol. Chem. 2003, 278:20835-20842.
149. Hughes E., Clayton J.C., Middleton D.A. Cytoplasmic residues of phospholamban interact with membrane surfaces in the presence of SERCA: A new role for phospholipids in the regulation of cardiac calcium cycling?. Biochim. Biophys. Acta 2009, 1788:559-566.
150. 13C solid-state NMR spectroscopic study. Biochemistry 2006, 45:13312-13322.
151. Abu-Baker S., Lu J.X., Chu S., Brinn C.C., Makaroff C.A., Lorigan G.A. Side chain and backbone dynamics of phospholamban in phospholipid bilayers utilizing (2)H and (15)N solid-state NMR spectroscopy. Biochemistry 2007, 46:11695-11706.
152. 15N solid-state NMR spectroscopy. Protein Sci. 2007, 16:2345-2349.
153. Kirby T.L., Karim C.B., Thomas D.D. Electron paramagnetic resonance reveals a large-scale conformational change in the cytoplasmic domain of phospholamban upon binding to the sarcoplasmic reticulum Ca-ATPase. Biochemistry 2004, 43:5842-5852.
154. Nesmelov Y.E., Karim C.B., Song L., Fajer P.G., Thomas D.D. Rotational dynamics of phospholamban determined by multifrequency electron paramagnetic resonance. Biophys. J. 2007, 93:2805-2812.
155. Traaseth N.J., Veglia G. Probing excited states and activation energy for the integral membrane protein phospholamban by NMR CPMG relaxation dispersion experiments. Biochim. Biophys. Acta 2010, 1798:77-81.
156. Masterson, L.R.; Yu, T.; Shi, L.; Wang, Y.; Gustavsson, M.; Mueller, M. M.; Veglia, G. cAMP-dependent protein kinase A selects the excited state of the membrane substrate phospholamban. J. Mol. Biol.2011, in-press. PMID 21741980.
157. Dvinskikh S.V., Yamamoto K., Ramamoorthy A. Heteronuclear isotropic mixing separated local field NMR spectroscopy. J. Chem. Phys. 2006, 125:34507.
158. Nevzorov A.A., Opella S.J. Selective averaging for high-resolution solid-state NMR spectroscopy of aligned samples. J. Magn. Reson. 2007, 185:59-70.
159. Wu C.H., Ramamoorthy A., Opella S.J. Three-dimensional solid-state NMR experiment that correlates the chemical shift and dipolar coupling frequencies of two heteronuclei. J. Magn. Res. B 1995, 107:88-90.
160. Wu C.H., Ramamoorthy A., Opella S.J. High-resolution heteronuclear dipolar solid-state NMR spectroscopy. J. Magn. Res. 1994, 109:270-272.
161. Yamamoto K., Lee D.K., Ramamoorthy A. Broadband-PISEMA solid-state NMR spectroscopy. Chem. Phys. Lett. 2005, 407:289-293.
162. Qian C., Fu R., Gor'kov P., Brey W.W., Cross T.A., Gan Z. (14)N polarization inversion spin exchange at magic angle (PISEMA). J. Magn. Reson. 2009, 196:96-99.
163. Ramamoorthy A., Wei Y., Dong-KGBR L. PISEMA solid-state NMR spectroscopy. Annu. Rep. NMR Spectrosc. 2004, 52:1-52.
164. Bielecki A., Kolbert A.C., de Groot H.J.M., Griffin R.G., Levitt M.H. Frequency-switched Lee-Goldburg sequences in solids. Adv. Magn. Reson. 1990, 14:111.
165. 13C NMR of liquid crystals with different proton homonuclear dipolar decoupling methods. J. Magn. Res. 1999, 138:28-35.
166. Vinogradov E., Madhu P.K., Vega S. High-resolution proton solid-state NMR spectroscopy by phase-modulated Lee-Goldberg experiment. Chem. Phys. Lett. 1999, 314:443-450.
167. Hartmann S.R., Hahn E.L. Nuclear double resonance in the rotating frame. Phys. Rev. 1962, 128:2042.
168. Fung B.M., Khitrin A.K., Ermolaev K. An improved broadband decoupling sequence for liquid crystals and solids. J. Magn. Reson. 2000, 142:97-101.
169. Bennett A.E., Rienstra C.M., Auger M., Lakshmi K.V., Griffin R.G. Heteronuclear decoupling in rotating solids. J. Chem. Phys. 1995, 103:6951-6958.
170. Gopinath T., Veglia G. Sensitivity enhancement in static solid-state NMR experiments via single- and multiple-quantum dipolar coherences. J. Am. Chem. Soc. 2009, 131:5754-5756.
171. Gopinath T., Verardi R., Traaseth N.J, Veglia G. Sensitivity enhancement of separated local field experiments: application to membrane proteins. J. Phys. Chem. B. 2010, 114:5089-5095.
172. Fu R., Gordon E.D., Hibbard D.J., Cotten M. High resolution heteronuclear correlation NMR spectroscopy of an antimicrobial peptide in aligned lipid bilayers: Peptide-water interactions at the water-bilayer interface. J. Am. Chem. Soc. 2009, 131:10830-10831.
173. Marassi F.M., Gesell J.J., Valente A.P., Kim Y., Oblatt-Montal M., Montal M., Opella S.J. Dilute spin-exchange assignment of solid-state NMR spectra of oriented proteins: Acetylcholine M2 in bilayers. J. Biomol. NMR 1999, 14:141-148.
174. Gopinath T., Traaseth N.J., Mote K., Veglia G. Sensitivity enhanced heteronuclear correlation spectroscopy in multidimensional solid-state NMR of oriented systems via chemical shift coherences. J. Am. Chem. Soc. 2010, 132:5357-5363.
175. Gopinath T., Veglia G. Improved resolution in dipolar NMR spectra using constant time evolution PISEMA experiment. Chem. Phys. Lett. 2010, 494:104-110.
176. Bax A., Mehlkopf A.F., Smidt J. Homonuclear broadband-decoupled absorption spectra, with linewidths which are independent of the transverse relaxation rate. J. Magn. Reson. 1979, 35:167-169.
177. Suter D., Ernst R.R. Spin diffusion in resolved solid-state NMR spectra. Phys. Rev. B Condens. Matter 1985, 32:5608-5627.
178. 13C cross polarization-magic-angle spinning. J. Magn. Reson. 1982, 47:462-475.
179. Robyr P., Meier B.H., Ernst R.R. RF-driven spin diffusion in solids. Chem. Phys. Lett. 1989, 162:417-423.
180. Traaseth N.J., Gopinath T., Veglia G. On the performance of spin diffusion NMR techniques in oriented solids: prospects for resonance assignments and distance measurements from separated local field experiments. J. Phys. Chem. B 2010, 114:13872-13880.
181. Lewandowski J.R., De Paepe G., Eddy M.T., Griffin R.G. (15)N-(15)N proton assisted recoupling in magic angle spinning NMR. J. Am. Chem. Soc. 2009, 131:5769-5776.
182. Tamm L.K., Lai A.L., Li Y. Combined NMR and EPR spectroscopy to determine structures of viral fusion domains in membranes. Biochim. Biophys. Acta 2007, 1768:3052-3060.