Membrane protein structure determination in membrana

Accounts of Chemical Research

Volumn 46, Issue 9, 2013, Pages 2182-2190

  Ding, Yi ^a   Yao, Yong ^a   Marassi, Francesca M ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN;

ARTICLE; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

BACTERIAL OUTER MEMBRANE PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS;

EID: 84884224184     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400041a     Document Type: Article

References (55)

1. Mulkidjanian, A. Y.; Galperin, M. Y.; Koonin, E. V. Co-evolution of primordial membranes and membrane proteins Trends Biochem. Sci. 2009, 34, 206-215
2. Cross, T. A.; Sharma, M.; Yi, M.; Zhou, H. X. Influence of solubilizing environments on membrane protein structures Trends Biochem. Sci. 2011, 36, 117-125
3. Hagn, F.; Etzkorn, M.; Raschle, T.; Wagner, G. Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins J. Am. Chem. Soc. 2013, 135, 1919-1925
4. McLaughlin, A. C.; Cullis, P. R.; Hemminga, M. A.; Hoult, D. I.; Radda, G. K.; Ritchie, G. A.; Seeley, P. J.; Richards, R. E. Application of 31P NMR to model and biological membrane systems FEBS Lett. 1975, 57, 213-218
5. Griffin, R. G. Letter: Observation of the effect of water on the 31P nuclear magnetic resonance spectra of dipalmitoyllecithin J. Am. Chem. Soc. 1976, 98, 851-853
6. Seelig, J. Deuterium magnetic resonance: theory and application to lipid membranes Q. Rev. Biophys. 1977, 10, 353-418
7. Macdonald, P. M. Deuterium NMR and the topography of surface electrostatic charge Acc. Chem. Res. 1997, 30, 196-203
8. 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
9. Sharma, M.; Yi, M.; Dong, H.; Qin, H.; Peterson, E.; Busath, D. D.; Zhou, H. X.; Cross, T. A. Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer Science 2010, 330, 509-512
10. Das, B. B.; Nothnagel, H. J.; Lu, G. J.; Son, W. S.; Tian, Y.; Marassi, F. M.; Opella, S. J. Structure determination of a membrane protein in proteoliposomes J. Am. Chem. Soc. 2012, 134, 2047-2056
11. Park, S. H.; Das, B. B.; Casagrande, F.; Tian, Y.; Nothnagel, H. J.; Chu, M.; Kiefer, H.; Maier, K.; De Angelis, A.; Marassi, F. M.; Opella, S. J. Structure of the chemokine receptor CXCR1 in phospholipid bilayers Nature 2012, 491, 779-783
12. Sharif, S.; Kim, S. J.; Labischinski, H.; Schaefer, J. Characterization of peptidoglycan in fem-deletion mutants of methicillin-resistant Staphylococcus aureus by solid-state NMR Biochemistry 2009, 48, 3100-3108
13. Koch, K.; Afonin, S.; Ieronimo, M.; Berditsch, M.; Ulrich, A. In Solid State NMR; Chan, J. C. C., Ed.; Springer: Berlin Heidelberg, 2012; Vol. 306; pp 89-118.
14. Miao, Y.; Qin, H.; Fu, R.; Sharma, M.; Can, T. V.; Hung, I.; Luca, S.; Gor'kov, P. L.; Brey, W. W.; Cross, T. A. M2 proton channel structural validation from full-length protein samples in synthetic bilayers and E. coli membranes Angew. Chem., Int. Ed. 2012, 51, 8383-8386
15. Renault, M.; Tommassen-van Boxtel, R.; Bos, M. P.; Post, J. A.; Tommassen, J.; Baldus, M. Cellular solid-state nuclear magnetic resonance spectroscopy Proc. Natl. Acad. Sci. U. S. A. 2012, 10.1073/pnas.1116478109
16. McDermott, A. Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR Annu. Rev. Biophys. 2009, 38, 385-403
17. Judge, P. J.; Watts, A. Recent contributions from solid-state NMR to the understanding of membrane protein structure and function Curr. Opin. Chem. Biol. 2011, 15, 690-695
18. Franks, W. T.; Linden, A. H.; Kunert, B.; van Rossum, B. J.; Oschkinat, H. Solid-state magic-angle spinning NMR of membrane proteins and protein-ligand interactions Eur. J. Cell Biol. 2012, 91, 340-348
19. Hong, M.; Zhang, Y.; Hu, F. Membrane protein structure and dynamics from NMR spectroscopy Annu. Rev. Phys. Chem. 2012, 63, 1-24
20. Reif, B. Ultra-high resolution in MAS solid-state NMR of perdeuterated proteins: implications for structure and dynamics J. Magn. Reson. 2012, 216, 1-12
21. Shi, L.; Ladizhansky, V. Magic angle spinning solid-state NMR experiments for structural characterization of proteins Methods Mol. Biol. 2012, 895, 153-165
22. Goncalves, J.; Eilers, M.; South, K.; Opefi, C. A.; Laissue, P.; Reeves, P. J.; Smith, S. O. Magic angle spinning nuclear magnetic resonance spectroscopy of G protein-coupled receptors Methods Enzymol. 2013, 522, 365-389
23. Opella, S. J.; Marassi, F. M. Structure determination of membrane proteins by NMR spectroscopy Chem. Rev. 2004, 104, 3587-3606
24. Murray, D. T.; Das, N.; Cross, T. A. Solid state NMR strategy for characterizing native membrane protein structures Acc. Chem. Res. 2013, 10.1021/ar3003442
25. Bartra, S. S.; Styer, K. L.; O'Bryant, D. M.; Nilles, M. L.; Hinnebusch, B. J.; Aballay, A.; Plano, G. V. Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer membrane protein Infect. Immun. 2008, 76, 612-622
26. Vogt, J.; Schulz, G. E. The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence Structure 1999, 7, 1301-1309
27. Yamashita, S.; Lukacik, P.; Barnard, T. J.; Noinaj, N.; Felek, S.; Tsang, T. M.; Krukonis, E. S.; Hinnebusch, B. J.; Buchanan, S. K. Structural insights into Ail-mediated adhesion in Yersinia pestis Structure 2011, 19, 1672-1682
28. Plesniak, L. A.; Mahalakshmi, R.; Rypien, C.; Yang, Y.; Racic, J.; Marassi, F. M. Expression, refolding, and initial structural characterization of the Y. pestis Ail outer membrane protein in lipids Biochim. Biophys. Acta 2011, 1808, 482-489
29. Mahalakshmi, R.; Franzin, C. M.; Choi, J.; Marassi, F. M. NMR structural studies of the bacterial outer membrane protein OmpX in oriented lipid bilayer membranes Biochim. Biophys. Acta 2007, 1768, 3216-3224
30. Mahalakshmi, R.; Marassi, F. M. Orientation of the Escherichia coli outer membrane protein OmpX in phospholipid bilayer membranes determined by solid-state NMR Biochemistry 2008, 47, 6531-6538
31. Kleinschmidt, J. H.; Tamm, L. K. Secondary and tertiary structure formation of the beta-barrel membrane protein OmpA is synchronized and depends on membrane thickness J. Mol. Biol. 2002, 324, 319-330
32. 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
33. Shen, Y.; Lange, O.; Delaglio, F.; Rossi, P.; Aramini, J. M.; Liu, G.; Eletsky, A.; Wu, Y.; Singarapu, K. K.; Lemak, A.; Ignatchenko, A.; Arrowsmith, C. H.; Szyperski, T.; Montelione, G. T.; Baker, D.; Bax, A. Consistent blind protein structure generation from NMR chemical shift data Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 4685-4690
34. Raman, S.; Lange, O. F.; Rossi, P.; Tyka, M.; Wang, X.; Aramini, J.; Liu, G.; Ramelot, T. A.; Eletsky, A.; Szyperski, T.; Kennedy, M. A.; Prestegard, J.; Montelione, G. T.; Baker, D. NMR structure determination for larger proteins using backbone-only data Science 2010, 327, 1014-1018
35. Veshtort, M.; Griffin, R. G. Proton-driven spin diffusion in rotating solids via reversible and irreversible quantum dynamics J. Chem. Phys. 2011, 135 134509
36. Schaefer, J. "Development of REDOR rotational-echo double-resonance NMR" by Terry Gullion and Jacob Schaefer [J. Magn. Reson. 81 (1989) 196-200] J. Magn. Reson. 2011, 213, 421-422
37. Sengupta, I.; Nadaud, P. S.; Helmus, J. J.; Schwieters, C. D.; Jaroniec, C. P. Protein fold determined by paramagnetic magic-angle spinning solid-state NMR spectroscopy Nat. Chem. 2012, 4, 410-417
38. Wylie, B. J.; Sperling, L. J.; Nieuwkoop, A. J.; Franks, W. T.; Oldfield, E.; Rienstra, C. M. Ultrahigh resolution protein structures using NMR chemical shift tensors Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 16974-16979
39. Saito, H.; Ando, I.; Ramamoorthy, A. Chemical shift tensor-the heart of NMR: Insights into biological aspects of proteins Prog. Nucl. Magn. Reson. Spectrosc. 2010, 57, 181-228
40. Li, D.-W.; Bruschweiler, R. Certification of molecular dynamics trajectories with NMR chemical shifts J. Phys. Chem. Lett. 2010, 1, 246-248
41. Tian, Y.; Opella, S. J.; Marassi, F. M. Improved chemical shift prediction by Rosetta conformational sampling J. Biomol. NMR 2012, 54, 237-243
42. Das, R.; Baker, D. Macromolecular modeling with Rosetta Annu. Rev. Biochem. 2008, 77, 363-382
43. Marassi, F. M.; Ramamoorthy, A.; Opella, S. J. Complete resolution of the solid-state NMR spectrum of a uniformly 15N-labeled membrane protein in phospholipid bilayers Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 8551-8556
44. 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
45. 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
46. Marassi, F. M. A simple approach to membrane protein secondary structure and topology based on NMR spectroscopy Biophys. J. 2001, 80, 994-1003
47. Tian, Y.; Schwieters, C. D.; Opella, S. J.; Marassi, F. M. AssignFit: A program for simultaneous assignment and structure refinement from solid-state NMR spectra J. Magn. Reson. 2012, 214, 42-50
48. De Angelis, A. A.; Howell, S. C.; Opella, S. J. Assigning solid-state NMR spectra of aligned proteins using isotropic chemical shifts J. Magn. Reson. 2006, 183, 329-332
49. Tian, F.; Song, Z.; Cross, T. A. Orientational constraints derived from hydrated powder samples by two-dimensional PISEMA J. Magn. Reson. 1998, 135, 227-231
50. Lewis, B. A.; Harbison, G. S.; Herzfeld, J.; Griffin, R. G. NMR structural analysis of a membrane protein: Bacteriorhodopsin peptide backbone orientation and motion Biochemistry 1985, 24, 4671-4679
51. Marassi, F. M.; Das, B. B.; Lu, G. J.; Nothnagel, H. J.; Park, S. H.; Son, W. S.; Tian, Y.; Opella, S. J. Structure determination of membrane proteins in five easy pieces Methods 2011, 55, 363-369
52. Griffin, R. G. Dipolar recoupling in MAS spectra of biological solids Nat. Struct. Biol. 1998, 5 (Suppl) 508-512
53. Tycko, R. Solid-state NMR studies of amyloid fibril structure Annu. Rev. Phys. Chem. 2011, 62, 279-299
54. Bauer, A. J.; Gieschler, S.; Lemberg, K. M.; McDermott, A. E.; Stockwell, B. R. Functional model of metabolite gating by human voltage-dependent anion channel 2 Biochemistry 2011, 50, 3408-3410
55. 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. U. S. A. 2002, 99, 13533-13537