'q-Titration' of long-chain and short-chain lipids differentiates between structured and mobile residues of membrane proteins studied in bicelles by solution NMR spectroscopy

Journal of Magnetic Resonance

Volumn 214, Issue , 2012, Pages 111-118

  Son, Woo Sung ^a   Park, Sang Ho ^a   Nothnagel, Henry J ^a   Lu, George J ^a   Wang, Yan ^a   Zhang, Hua ^a   Cook, Gabriel A ^a   Howell, Stanley C ^a   Opella, Stanley J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CXCR1; Dynamics; Membranes; MerE; MerF; p7; Pf1; Solid state NMR; Vpu

Indexed keywords

CXCR1; MERE; MERF; P7; PF1; SOLID STATE NMR; VPU;

AMIDES; BIOLOGICAL MEMBRANES; DYNAMICS; LIPOSOMES; MEMBRANES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPIDS; SOLID STATE PHYSICS; TITRATION;

PROTEINS;

MEMBRANE PROTEIN;

ALGORITHM; ARTICLE; CHEMISTRY; LIPID BILAYER; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SOLUTION AND SOLUBILITY; ULTRASTRUCTURE;

ALGORITHMS; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; SOLUTIONS;

EID: 84855649990     PISSN: 10907807     EISSN: 10960856     Source Type: Journal    
DOI: 10.1016/j.jmr.2011.10.011     Document Type: Article

References (45)

1. N. Bloembergen, E.M. Purcell, and RV. Pound Relaxation effects in nuclear magnetic resonance absorption Phys. Rev. 73 1948 679 712
2. 15N NMR spectroscopy J. Magn. Reson. 72 1987 186 190
3. D.R. Bauer, S.J. Opella, D.J. Nelson, and R. Pecora Depolarized light scattering and carbon nuclear resonance measurements of the isotropic rotational correlation time of muscle calcium binding protein J. Am. Chem. Soc. 97 1975 2580 2582
4. C.S. Gangabadage, A. Najda, D. Bogdan, S.S. Wilmenga, and M. Tessari Dependence of the size of a protein-SD complex on degetergent and Na+ concentrations J. Phys. Chem. B 112 2008 4242 4245
5. C. Tian, R.M. Breyer, H.J. Kim, M.D. Karra, D.B. Friedman, A. Karpay, and C.R. Sanders Solution NMR spectroscopy of the human vasopressin V2 receptor, a G protein-coupled receptor J. Am. Chem. Soc. 128 2006 5300
6. C.R. Sanders, and J.P. Schwonek Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR Biochemistry 31 1992 8898 8905
7. T.A. Cross, and S.J. Opella Structural properties of fd coat protein in sodium dodecyl sulfate micelles Biochem. Biophys. Res. Commun. 92 1980 478 484
8. J. Lauterwein, C. Bosch, L.R. Brown, and K. Wuthrich Physicochemical studies of the protein-lipid interactions in melittin-containing micelles Biochim. Biophys. Acta 556 1979 244 264
9. K.J. Glover, J.A. Whiles, G. Wu, N. Yu, R. Deems, J.O. Struppe, R.E. Stark, E.A. Komives, and R.R. Vold Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules Biophys. J. 81 2001 2163 2171 (Pubitemid 32917165)
10. X.O. Shenkarv, A.S. Paramonov, E.N. Lyukmanova, L.N. Shingarova, S.A. Yakimov, M.A. Dubinnyi, V.V. Chupin, M.P. Kirpichnikov, M.J. Blommers, and A.S. Arseniev Lipid-protein nanodiscs as reference medium in detergent screening for high-resolution NMR studies of integral membrane proteins J. Am. Chem. Soc. 132 2010 5628 5629
11. T.K. Ritchie, Y.V. Grinkova, T.H. Bayburt, I.G. Denisov, J.K. Zolnerciks, W.M. Atkins, and S.G. Sligar Reconstitutiion of membrane proteins in phospholipid bilayer nanodiscs Methods Enzymol. 464 2009 211 231
12. T. Raschle, S. Hiller, T.Y. Yu, A.J. Rice, T. Walz, and G. Wagner Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs J. Am. Chem. Soc. 131 2009 17777 17779
13. P.A. McDonnell, and S.J. Opella Effect of detergent concentration on multidimensional solution NMR spectra of membrane proteins in micelles J. Magn. Reson. B102 1993 120 125
14. R.D. Kruger-Koplin, P.L. Sorgen, S.T. Druieger-Koplin, I.O. Rivera-Torres, S.M. Cahill, T.A. Krulwich, and M.E. Girvin An evaluation of detergents for NMR structural studies of membrane proteins J. Biomol. NMR 28 2004 1980 1987
15. H.J. Kim, S.C. Howell, W.D. Van Horn, Y.H. Jeon, and C.R. Sanders Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins Prog. Nucl. Magn. Reson. Spectrosc. 55 2009 335 360
16. S.H. Park, F. Casagrande, B.B. Das, L. Albrecht, M. Chu, and S.J. Opella Local and global dynamics of the G-protein-coupled receptor CXCR1 Biochemistry 2011 2371 2380
17. A. Gautier, J.P. Kirkpatrick, and D. Nietlispach Solution-state NMR spectroscopy of a seven-helix transmembrane protein receptor: backbone assignment, secondary structure, and dynamics Angew. Chem. Int. Ed. Eng. 47 2008 7297 7300
18. A. Gautier, H.R. Mott, M.J. Bostock, J.P. Kirkpatrick, and D. Nietlispach Structure determination of the seven-helx transmembrane receptor sensory rhodopsin II by solution NMR Nat. Struct. Mol. Biol. 17 2010 768 775
19. D. Lee, K.F.A. Walter, A.K. Bruckner, C. Hilty, S. Becker, and C. Griesinger Bilayer in small bicelles revealed by lipid-protein interactions using NMR spectroscopy J. Am. Chem. Soc. 130 2008 13822 13823
20. T.A. Cross, and S.J. Opella Solid-state NMR structural studies of peptides and proteins in membranes Curr. Opin. Struct. Biol. 4 1994 574 581 (Pubitemid 24268991)
21. A. Anderssson, J. Almqvist, F. Hagn., and L. Maler Diffusion and dynamics of penetration in different membrane mimicking media Biochim. Biophys. Acta. - Biomembr. 1161 2004 18 25 (Pubitemid 38201568)
22. J.J. Chou, S. Gaemers, B. Howder, J.M. Louis, and A. Bax A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles J. Biomol. NMR 21 2001 377 382 (Pubitemid 34071393)
23. D.H. Jones, and S.J. Opella Weak alignment of membrane proteins in stressed polyacrylamide gels J. Magn. Reson. 171 2004 258 269
24. T. Cierpicki, and J. Bushweller Charged gels as orienting media for measurement of residual dipolar couplings in soluble and integral membrane proteins J. Am. Chem. Soc. 126 2004 16259 16266 (Pubitemid 39627638)
25. T.A. Cross, J.A. DiVerdi, and S.J. Opella Strategy for nitrogen NMR of biopolymers J. Am. Chem. Soc. 104 1982 1759 1761
26. M. Meselson, and F. Stahl The replication of DNA in escherichia coli Proc. Natl. Acad. Sci. 44 1958 671 682
27. R.S. Prosser, F. Evanics, J.L. Kitevski, and M.S. Al-Abdul-Wahid Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins Biochemistry 2006 8453 8465 (Pubitemid 44078865)
28. C.R. Sanders, B. Hare, K.P. Howard, and J.H. Prestegard Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules Prog. NMR Spectrosc. 26 1994 421 444 (Pubitemid 124003831)
29. C.R. Sanders 2nd, and J.H. Prestegard Magnetically orientable phospholipid bilayers containing small amounts of a bile salt analogue, CHAPSO Biophys. J. 58 1990 447 460 (Pubitemid 20249672)
30. S.H. Park, and S.J. Opella Triton X-100 as the 'short-chain lipid' improves the magnetic alignment and stability of membrane proteins in phosphatidylcholine bilayers for oriented-sample solid-state NMR spectroscopy J. Am. Chem. Soc. 132 2010 12552 12553
31. S. Mori, C. Abeygunawardana, M. Johnson, and P. VanZijl Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation J. Magn. Reson. B 108 1995 94 98
32. M.J. Bogusky, P. Leighton, R.A. Schiksnis, A. Khoury, P. Lu, and S.J. Opella 15N NMR spectroscopy of proteins in solution J. Magn. Reson. 86 1990 11 29
33. A.A. DeAngelis, A.A. Nevzorov, S.H. Park, S.C. Howell, A.A. Mrse, and S.J. Opella High-resolution NMR spectroscopy of membrane proteins in aligned bicelles J. Am. Chem. Soc. 126 2004 15340 15341 (Pubitemid 39577443)
34. S.H. Park, A.A. De Angelis, A.A. Nevzorov, C.H. Wu, and S.J. Opella Three-dimensional structure of the transmembrane domain of Vpu from HIV-1 in aligned phospholipid bicelles Biophys. J. 91 2006 3032 3042 (Pubitemid 44526493)
35. G.A. Cook, H. Zhang, S.H. Park, Y. Wang, and S.J. Opella Comparative NMR studies demonstrate profound differences between two viroporins: p7 of HCV and Vpu of HIV-1 Biochimica et Biophysica Acta 1808 2011 554 560
36. G.A. Cook, H. Zhang, S.H. Park, Y. Wang, S.J. Opella, Biochimica et Biophysica Acta 1808, Comparative NMR Studies Demonstrate Profound Differences Between the Viroporins: p7 of HCV and Vpu of HIV-1, 2010, pp. 554-560.
37. S.C. Howell, M.F. Mesleh, and S.J. Opella NMR structure determination of a membrane protein with two transmembrane helices in micelles: MerF of the bacterial mercury detoxification system Biochemistry 44 2005 5196 5206 (Pubitemid 40471234)
38. C.R. Sanders, and F. Sonnichsen Solution NMR of membrane proteins: practice and challenges Magn. Reson. Chem. S 2006 24 40
39. S.F. Poget, and M.E. Girvin Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better Biochim. Biophys. Acta 2007 3098 3106 (Pubitemid 350236093)
40. R.C. Page, J.D. Moore, H.B. Nguyen, M. Sharma, R. Chase, F.P. Gao, C.K. Mobley, C.R. Sanders, L. Ma, F.D. Sonnichsen, S. Lee, S.C. Howell, S.J. Opella, and T.A. Cross Comprehensive evaluation of solution nuclear magnetic resonance spectroscopy sample preparation for helical integral membrane proteins J. Struct. Funct. Genomics 7 2006 51 64 (Pubitemid 44273863)
41. A.A. De Angelis, A.A. Nevzorov, S.H. Park, S.C. Howell, A.A. Mrse, and S.J. Opella High-resolution NMR spectroscopy of membrane proteins in aligned bicelles J. Am. Chem. Soc. 126 2004 15340 15341 (Pubitemid 39577443)
42. G.A. Cook, and S.J. Opella Secondary structure, dynamics, and architecture of the p7 membrane protein from hepatitis C virus by NMR spectroscopy Biochimica et Biophysica Acta 1808 2011 1448 1453
43. M. Piotto, V. Saudek, and V. Sklenar Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solution J. Biomol. NMR 2 1992 661 665
44. F. Delaglio, S. Grzesiek, G. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimeensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
45. A. Pines, M.G. Gibby, and J.S. Waugh Proton-enhanced nuclear induction spectroscopy - method for high-resolution NMR of dilute spins in solids J. Chem. Phys. 56 1972 1776 1777