Helix conformations in 7TM membrane proteins determined using oriented-sample solid-state NMR with multiple residue-specific 15N labeling

Biophysical Journal

Volumn 94, Issue 1, 2008, Pages 241-250

  Vosegaard, Thomas ^a   Kamihira Ishijima, Miya ^b   Watts, Anthony ^b   Nielsen, Niels Chr ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; MEMBRANE PROTEIN; METHIONINE; VALINE;

ARTICLE; CHEMICAL LABELING; DIPOLE; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE; PROTEIN DETERMINATION; PROTON NUCLEAR MAGNETIC RESONANCE; SOLID STATE;

EID: 37749002195     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.116004     Document Type: Article

References (51)

1. Bernstein, F. C., T. F. Koetzle, G. J. Williams, E. F. Meyer, Jr., M. D. Brice, J. R. Rodgers, O. Kennard, T. Shimanouchi, and M. Tasumi. 1977. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112:535-542.
2. Opella, S. J. 1997. NMR and membrane proteins. Nat. Struct. Biol. 4:845-848.
3. Watts, A., S. K. Straus, S. L. Grage, M. Kamihira, Y. H. Lam, and X. Zhao. 2004. Membrane protein structure determination using solidstate NMR. Methods Mol. Biol. 278:403-473.
4. Nielsen, N., A. Malmendal, and T. Vosegaard. 2004. Techniques and applications of NMR to membrane proteins. Mol. Membr. Biol. 21:129-141.
5. Griffin, R. G. 1998. Dipolar recoupling in MAS spectra of biological solids. Nat. Struct. Biol. 5:508-512.
6. Smith, S. O., J. Hamilton, A. Salmon, and B. J. Bormann. 1994. Rotational resonance NMR determination of intra- and intermolecular distance constraints in dipalmitoylphosphatidylcholine bilayers. Biochemistry. 33:6327-6333.
7. Studelska, D. R., L. M. McDowell, M. Adler, R. D. O'Connor, A. K. Mehta, W. J. Guilford, J. L. Dallas, D. Arnaiz, D. R. Light, and J. Schaefer. 2003. Conformation of a bound inhibitor of blood coagulant factor Xa. Biochemistry. 42:7942-7949.
8. Gröbner, G., I. J. Burnett, C. Glaubitz, G. Choi, A. J. Mason, and A. Watts. 2000. Observations of light-induced structural changes of retinal within rhodopsin. Nature. 405:810-813.
9. Watts, A. 1999. NMR of drugs and ligands bound to membrane receptors. Curr. Opin. Biotechnol. 10:48-53.
10. Watts, A. 2005. Solid-state NMR in drug design and discovery for membrane-embedded targets. Nat. Rev. Drug Discov. 4:555-568.
11. Ketchem, R. R., K. C. Lee, S. Huo, and T. A. Cross. 1996. Macromolecular structural elucidation with solid-state NMR-derived orientational constraints. J. Biomol. NMR. 8:1-14.
12. Glaubitz, C., G. Grobner, and A. Watts. 2000. Structural and orientational information of the membrane embedded M13 coat protein by (13)C-MAS NMR spectroscopy. Biochim. Biophys. Acta. 1463:151-161.
13. Valentine, K. G., S. F. Liu, F. M. Marassi, G. Veglia, S. J. Opella, F. X. Ding, S. H. Wang, B. Arshava, J. M. Becker, and F. Naider. 2001. Structure and topology of a peptide segment of the 6th transmembrane domain of the Saccharomyces cerevisae α-factor receptor in phospholipid bilayers. Biopolymers. 59:243-256.
14. + channel helical bundle combining precise orientational and distance restraints from solid state NMR. Biochemistry. 41:13170-13177.
15. Castellani, F., B. van Rossum, A. Diehl, M. Schubert, K. Rehbein, and H. Oschkinat. 2002. Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature. 420:98-102.
16. Zeri, A. C., M. F. Mesleh, A. A. Nevzorov, and S. J. Opella. 2003. Structure of the coat protein in fd filamentous bacteriophage particles determined by solid-state NMR spectroscopy. Proc. Natl. Acad. Sci. USA. 100:6458-6463.
17. Park, S. H., A. A. Mrse, A. A. Nevzorov, M. F. Mesleh, M. Oblatt-Montal, M. Montal, and S. J. Opella. 2003. Three-dimensional structure of the channel-forming trans-membrane domain of virus protein "u" (Vpu) from HIV-1. J. Mol. Biol. 333:409-424.
18. Jaroniec, C. P., C. E. MacPhee, V. S. Bajaj, M. T. McMahon, C. M. Dobson, and R. G. Griffin. 2004. High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. Proc. Natl. Acad. Sci. USA. 101:711-716.
19. Heise, H., W. Hoyer, S. Becker, O. C. Andronesi, D. Riedel, and M. Baldus. 2005. Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solid-state NMR. Proc. Natl. Acad. Sci. USA. 102:15871-15876.
20. Lange, A., K. Giller, S. Hornig, M. F. Martin-Eauclaire, O. Pongs, S. Becker, and M. Baldus. 2006. Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature. 440:959-962.
21. 2+-ATPase. Biochim. Biophys. Acta. 1468:187-198.
22. Harbison, G. S., S. O. Smith, J. A. Pardoen, P. P. Mulder, J. Lugtenburg, J. Herzfeld, R. Mathies, and R. G. Griffin. 1984. Solid-state 13C NMR studies of retinal in bacteriorhodopsin. Biochemistry. 23:2662-2667.
23. Harbison, G. S., S. O. Smith, J. A. Pardoen, C. Winkel, J. Lugtenburg, J. Herzfeld, R. Mathies, and R. G. Griffin. 1984. Dark-adapted bacteriorhodopsin contains 13-cis, 15-syn, and all-trans, 15-anti retinal Schiff bases. Proc. Natl. Acad. Sci. USA. 81:1706-1709.
24. Lakshmi, K. V., M. R. Farrar, J. Raap, J. Lugtenburg, R. G. Griffin, and J. Herzfeld. 1994. Solid state 13C and 15N NMR investigations of the N intermediate of bacteriorhodopsin. Biochemistry. 33:8853-8857.
25. Lewis, B. A., G. S. Harbison, J. Herzfeld, and R. G. Griffin. 1985. NMR structural analysis of a membrane protein: bacteriorhodopsin peptide backbone orientation and motion. Biochemistry. 24:4671-4679.
26. Hatcher, M. E., J. G. Hu, M. Belenky, P. Verdegem, J. Lugtenburg, R. G. Griffin, and J. Herzfeld. 2002. Control of the pump cycle in bacteriorhodopsin: mechanisms elucidated by solid-state NMR of the D85N mutant. Biophys. J. 82:1017-1029.
27. Kamihira, M., T. Vosegaard, A. J. Mason, S. K. Straus, N. C. Nielsen, and A. Watts. 2005. Structural and orientational constraints of bacteriorhodopsin in purple membranes determined by oriented-sample solid-state NMR spectroscopy. J. Struct. Biol. 149:7-16.
28. Saito, H., Y. Kawase, A. Kira, K. Yamamoto, M. Tanio, S. Yamaguchi, S. Tuzi, and A. Naito. 2007. Surface and dynamic structures of bacteriorhodopsin in a 2D crystal, a distorted or disrupted lattice, as revealed by site-directed solid-state C NMR. Photochem. Photobiol. 83:253-262.
29. Kawamura, I., N. Kihara, M. Ohmine, K. Nishimura, S. Tuzi, H. Saito, and A. Naito. 2007. Solid-state NMR studies of two backbone conformations at Tyr185 as a function of retinal configurations in the dark, light, and pressure adapted bacteriorhodopsins. J. Am. Chem. Soc. 129:1016-1017.
30. Park, S. H., S. Prytulla, A. A. De Angelis, J. M. Brown, H. Kiefer, and S. J. Opella. 2006. High-resolution NMR spectroscopy of a GPCR in aligned bicelles. J. Am. Chem. Soc. 128:7402-7403.
31. Etzkorn, M., S. Martell, O. C. Andronesi, K. Seidel, M. Engelhard, and M. Baldus. 2007. Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew. Chem. Int. Ed. 46:459-462.
32. 15N]-labeled membrane proteins in oriented lipid bilayers. J. Biomol. NMR. 22:225-247.
33. Henzler Wildman, K. A., D. K. Lee, and A. Ramamoorthy. 2003. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry. 42:6545-6558.
34. 31P solid-state NMR spectroscopy. Concepts Magn. Reson. 18A:130-145.
35. Aisenbrey, C., C. Sizun, J. Koch, M. Herget, R. Abele, B. Bechinger, and R. Tampe. 2006. Structure and dynamics of membrane-associated ICP47, a viral inhibitor of the MHC I antigen-processing machinery. J. Biol. Chem. 281:30365-30372.
36. 31P solid-state NMR investigations of the Pf3 coat protein in oriented phospholipid bilayers. FEBS J. 273:817-828.
37. Grobner, G., A. Taylor, P. T. Williamson, G. Choi, C. Glaubitz, J. A. Watts, W. J. de Grip, and A. Watts. 1997. Macroscopic orientation of natural and model membranes for structural studies. Anal. Biochem. 254:132-138.
38. Kamihira, M., and A. Watts. 2006. Functionally relevant coupled dynamic profile of bacteriorhodopsin and lipids in purple membranes. Biochemistry. 45:4304-4313.
39. Wu, C. H., A. Ramamoorthy, and S. J. Opella. 1994. High-resolution heteronuclear dipolar solid-state NMR spectroscopy. J. Magn. Reson. A. 109:270-272.
40. Levitt, M. H. 1991. J. Chem. Phys. 94:30-38.
41. Marassi, F. M., and S. J. Opella. 2000. A solid-state NMR index of helical membrane protein structure and topology. J. Magn. Reson. 144:150-155.
42. Wang, J., J. Denny, C. Tian, S. Kim, Y. Mo, F. Kovacs, Z. Song, K. Nishimura, Z. Gan, R. Fu, J. R. Quine, and T. A. Cross. 2000. Imaging membrane protein helical wheels. J. Magn. Reson. 144:162-167.
43. Toyoshima, C., M. Nakasako, H. Nomura, and H. Ogawa. 2000. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature. 405:647-655.
44. Luecke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:899-911.
45. Kim, S., and T. A. Cross. 2002. Uniformity, ideality, and hydrogen bonds in transmembrane α-helices. Biophys. J. 83:2084-2095.
46. Bak, M., J. T. Rasmussen, and N. C. Nielsen. 2000. SIMPSON: a general simulation program for solid-state NMR spectroscopy. J. Magn. Reson. 147:296-330.
47. Vosegaard, T., A. Malmendal, and N. C. Nielsen. 2002. The flexibility of SIMPSON and SIMMOL for numerical simulations in solid- and liquid-state NMR spectroscopy. Monatsh. Chem. 133:1555-1574.
48. Bak, M., R. Schultz, T. Vosegaard, and N. C. Nielsen. 2002. Specification and visualization of anisotropic interaction tensors in polypeptides and numerical simulations in biological solid-state NMR. J. Magn. Reson. 154:28-45.
49. Pervushin, K., R. Riek, G. Wider, and K. Wuthrich. 1997. 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. USA. 94:12366-12371.
50. Flaux, J., E. B. Bertelsen, A. L. Horwich, and K. Wütrich. 2002. Nature. 418:207-211.
51. Palczewski, K., T. Kumasaka, T. Hori, C. A. Behnke, H. Motoshima, B. A. Fox, I. Le Trong, D. C. Teller, T. Okada, R. E. Stenkamp, M. Yamamoto, and M. Miyano. 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science. 289:739-745.