The present and future of solution NMR in investigating the structure and dynamics of channels and transporters

Current Opinion in Structural Biology

Volumn 23, Issue 4, 2013, Pages 547-554

  Oxenoid, Kirill ^a   Chou, James J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; PROTEIN M2; UNCOUPLING PROTEIN;

BINDING SITE; CHANNEL GATING; MOLECULAR IMAGING; MOLECULAR SIZE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; REVIEW; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TRANSPORT KINETICS;

CRYSTALLOGRAPHY, X-RAY; ION CHANNELS; ION PUMPS; ION TRANSPORT; MITOCHONDRIAL PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SIGNAL TRANSDUCTION; VIRAL MATRIX PROTEINS;

EID: 84881110793     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.03.010     Document Type: Review

References (50)

1. MacKenzie K.R., Prestegard J.H., Engelman D.M. A transmembrane helix dimer: structure and implications. Science 1997, 276:131-133.
2. Call M.E., Schnell J.R., Xu C., Lutz R.A., Chou J.J., Wucherpfennig K.W. The structure of the zetazeta transmembrane dimer reveals features essential for its assembly with the T cell receptor. Cell 2006, 127:355-368.
3. Bocharov E.V., Mineev K.S., Volynsky P.E., Ermolyuk Y.S., Tkach E.N., Sobol A.G., Chupin V.V., Kirpichnikov M.P., Efremov R.G., Arseniev A.S. Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state. J Biol Chem 2008, 283:6950-6956.
4. Call M.E., Wucherpfennig K.W., Chou J.J. The structural basis for intramembrane assembly of an activating immunoreceptor complex. Nat Immunol 2010, 11:1023-1029.
5. 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.
6. Oxenoid K., Chou J.J. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc Natl Acad Sci U S A 2005, 102:10870-10875.
7. Schnell J.R., Chou J.J. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 2008, 451:591-595.
8. Wang J., Pielak R.M., McClintock M.A., Chou J.J. Solution structure and functional analysis of the influenza B proton channel. Nat Struct Mol Biol 2009, 16:1267-1271.
9. Chill J.H., Louis J.M., Miller C., Bax A. NMR study of the tetrameric KcsA potassium channel in detergent micelles. Protein Sci: Publ Protein Soc 2006, 15:684-698.
10. 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.
11. Zhou Y., Cierpicki T., Jimenez R.H., Lukasik 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.
12. Gautier A., Mott H.R., Bostock M.J., Kirkpatrick J.P., Nietlispach D. Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat Struct Mol Biol 2010, 17:768-774.
13. Berardi M.J., Shih W.M., Harrison S.C., Chou J.J. Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 2011, 476:109-113.
14. Pervushin K., Riek R., Wider G., Wuthrich K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci U S A 1997, 94:12366-12371.
15. 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.
16. 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.
17. Loria J.P., Rance M., Palmer A.G. A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J Am Chem Soc 1999, 121:2331-2332.
18. Cady S.D., Schmidt-Rohr K., Wang J., Soto C.S., Degrado W.F., Hong M. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 2010, 463:689-692.
19. Park S.H., Das B.B., Casagrande F., Tian Y., Nothnagel H.J., Chu M., Kiefer H., Maier K., De Angelis A.A., Marassi F.M., et al. Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 2012, 491:779-783.
20. Pinto L.H., Lamb R.A. The M2 proton channels of influenza A and B viruses. J Biol Chem 2006, 281:8997-9000.
21. Bright R.A., Shay D.K., Shu B., Cox N.J., Klimov A.I. Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 2006, 295:891-894.
22. Stouffer A.L., Acharya R., Salom D., Levine A.S., Di Costanzo L., Soto C.S., Tereshko V., Nanda V., Stayrook S., DeGrado W.F. Structural basis for the function and inhibition of an influenza virus proton channel. Nature 2008, 451:596-599.
23. Shimbo K., Brassard D.L., Lamb R.A., Pinto L.H. Ion selectivity and activation of the M2 ion channel of influenza virus. Biophys J 1996, 70:1335-1346.
24. Pielak R.M., Chou J.J. Kinetic analysis of the M2 proton conduction of the influenza virus. J Am Chem Soc 2010, 132:17695-17697.
25. Pielak R.M., Oxenoid K., Chou J.J. Structural investigation of rimantadine inhibition of the AM2-BM2 chimera channel of influenza viruses. Structure 2011, 19:1655-1663.
26. Ohigashi Y., Ma C., Jing X., Balannick V., Pinto L.H., Lamb R.A. An amantadine-sensitive chimeric BM2 ion channel of influenza B virus has implications for the mechanism of drug inhibition. Proc Natl Acad Sci U S A 2009, 106:18775-18779.
27. Griffin S.D., Beales L.P., Clarke D.S., Worsfold O., Evans S.D., Jaeger J., Harris M.P., Rowlands D.J. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, amantadine. FEBS Lett 2003, 535:34-38.
28. Pervushin K., Tan E., Parthasarathy K., Lin X., Jiang F.L., Yu D., Vararattanavech A., Soong T.W., Liu D.X., Torres J. Structure and inhibition of the SARS coronavirus envelope protein ion channel. PLoS Pathogens 2009, 5:e1000511.
29. Fernandez C., Adeishvili K., Wuthrich K. Transverse relaxation-optimized NMR spectroscopy with the outer membrane protein OmpX in dihexanoyl phosphatidylcholine micelles. Proc Natl Acad Sci U S A 2001, 98:2358-2363.
30. Arora A., Abildgaard F., Bushweller J.H., Tamm L.K. Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat Struct Biol 2001, 8:334-338.
31. Hwang P.M., Choy W.Y., Lo E.I., Chen L., Forman-Kay J.D., Raetz C.R., Prive G.G., Bishop R.E., Kay L.E. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc Natl Acad Sci U S A 2002, 99:13560-13565.
32. Liang B., Tamm L.K. Structure of outer membrane protein G by solution NMR spectroscopy. Proc Natl Acad Sci U S A 2007, 104:16140-16145.
33. Tugarinov V., Kay L.E., Ibraghimov I., Orekhov V.Y. High-resolution four-dimensional 1H-13C NOE spectroscopy using methyl-TROSY, sparse data acquisition, and multidimensional decomposition. J Am Chem Soc 2005, 127:2767-2775.
34. Rosen M.K., Gardner K.H., Willis R.C., Parris W.E., Pawson T., Kay L.E. Selective methyl group protonation of perdeuterated proteins. J Mol Biol 1996, 263:627-636.
35. Song J., Midson C., Blachly-Dyson E., Forte M., Colombini M. The sensor regions of VDAC are translocated from within the membrane to the surface during the gating processes. Biophys J 1998, 74:2926-2944.
36. De Pinto V., Benz R., Palmieri F. Interaction of non-classical detergents with the mitochondrial porin. A new purification procedure and characterization of the pore-forming unit. European journal of biochemistry/FEBS 1989, 183:179-187.
37. Doyle D.A., Morais Cabral J., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 1998, 280:69-77.
38. Cuello L.G., Jogini V., Cortes D.M., Pan A.C., Gagnon D.G., Dalmas O., Cordero-Morales J.F., Chakrapani S., Roux B., Perozo E. Structural basis for the coupling between activation and inactivation gates in K(+) channels. Nature 2010, 466:272-275.
39. Baker K.A., Tzitzilonis C., Kwiatkowski W., Choe S., Riek R. Conformational dynamics of the KcsA potassium channel governs gating properties. Nat Struct Mol Biol 2007, 14:1089-1095.
40. Chill J.H., Louis J.M., Baber J.L., Bax A. Measurement of 15N relaxation in the detergent-solubilized tetrameric KcsA potassium channel. J Biomol NMR 2006, 36:123-136.
41. Imai S., Osawa M., Takeuchi K., Shimada I. Structural basis underlying the dual gate properties of KcsA. Proc Natl Acad Sci U S A 2010, 107:6216-6221.
42. Morrison E.A., DeKoster G.T., Dutta S., Vafabakhsh R., Clarkson M.W., Bahl A., Kern D., Ha T., Henzler-Wildman K.A. Antiparallel EmrE exports drugs by exchanging between asymmetric structures. Nature 2012, 481:45-50.
43. Liu J.J., Horst R., Katritch V., Stevens R.C., Wuthrich K. Biased signaling pathways in beta2-adrenergic receptor characterized by 19F-NMR. Science 2012, 335:1106-1110.
44. Douglas S.M., Chou J.J., Shih W.M. DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. Proc Natl Acad Sci U S A 2007, 104:6644-6648.
45. Jones T.A., Thirup S. Using known substructures in protein model building and crystallography. EMBO J 1986, 5:819-822.
46. Delaglio F., Kontaxis G., Bax A. Protein structure determination using molecular fragment replacement and NMR dipolar couplings. J Am Chem Soc 2000, 122:2142-2143.
47. Raman S., Lange O.F., Rossi P., Tyka M., Wang X., Aramini J., Liu G., Ramelot T.A., Eletsky A., Szyperski T., et al. NMR structure determination for larger proteins using backbone-only data. Science 2010, 327:1014-1018.
48. Chou J.J., Li S.P., Bax A. Study of conformational rearrangement and refinement of structural homology models by the use of heteronuclear dipolar couplings. J Biomol NMR 2000, 18:217-227.
49. Ayala I., Sounier R., Use N., Gans P., Boisbouvier J. An efficient protocol for the complete incorporation of methyl-protonated alanine in perdeuterated protein. J Biomol NMR 2009, 43:111-119.
50. Gans P., Hamelin O., Sounier R., Ayala I., Dura M.A., Amero C.D., Noirclerc-Savoye M., Franzetti B., Plevin M.J., Boisbouvier J. Stereospecific isotopic labeling of methyl groups for NMR spectroscopic studies of high-molecular-weight proteins. Angew Chem 2010, 49:1958-1962.