Modulating alignment of membrane proteins in liquid-crystalline and oriented gel media by changing the size and charge of phospholipid bicelles

Journal of Biomolecular NMR

Volumn 55, Issue 4, 2013, Pages 369-377

  Lorieau, Justin L ^a   Maltsev, Alexander S ^a   Louis, John M ^a   Bax, Ad ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Bicelle; Dipolar coupling; Fusion peptide; NMR; Orthogonal alignment; Saupe matrix

Indexed keywords

HEMAGGLUTININ; MEMBRANE PROTEIN; PHOSPHOLIPID; POLYACRYLAMIDE GEL;

ARTICLE; COVALENT BOND; GEL; HETERONUCLEAR SINGLE QUANTUM COHERENCE; LIQUID; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE ALIGNMENT;

LIQUID CRYSTALS; MEMBRANE PROTEINS; MICELLES; PHOSPHOLIPIDS;

EID: 84877874158     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-013-9720-3     Document Type: Article

References (64)

1. Al-Hashimi HM, Valafar H, Terrell M, Zartler ER, Eidsness MK, Prestegard JH (2000) Variation of molecular alignment as a means of resolving orientational ambiguities in protein structures from dipolar couplings. J Magn Reson 143:402-406
2. Bax A (2003) Weak alignment offers new NMR opportunities to study protein structure and dynamics. Protein Sci 12:1-16 (Pubitemid 36020129)
3. Bax A, Kontaxis G, Tjandra N (2001) Dipolar couplings in macromolecular structure determination. Meth Enzymol 339:127-174 (Pubitemid 32666560)
4. Bertini I, Del Bianco C, Gelis I, Katsaros N, Luchinat C, Parigi G, Peana M, Provenzani A, Zoroddu MA (2004) Experimentally exploring the conformational space sampled by domain reorientation in calmodulin. Proc Natl Acad Sci USA 101:6841-6846 (Pubitemid 38596405)
5. Bertini I, Kursula P, Luchinat C, Parigi G, Vahokoski J, Wilmanns M, Yuan J (2009) Accurate solution structures of proteins from X-ray data and a minimal set of NMR data: calmodulin-peptide complexes as examples. J Am Chem Soc 131:5134-5144
6. Blackledge M (2005) Recent progress in the study of biomolecular structure and dynamics in solution from residual dipolar couplings. Prog Nucl Magn Reson Spectrosc 46:23-61 (Pubitemid 40357061)
7. Briggman KB, Tolman JR (2003) De Novo determination of bond orientations and order parameters from residual dipolar couplings with high accuracy. J Am Chem Soc 125:10164-10165 (Pubitemid 37022214)
8. Cantor CR, Schimmel PR (1980) Biophysical chemistry. Freeman, San Francisco
9. Chou JJ, Gaemers S, Howder B, Louis JM, Bax A (2001) A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles. J Biomol NMR 21:377-382 (Pubitemid 34071393)
10. Chou JJ, Kaufman JD, Stahl SJ, Wingfield PT, Bax A (2002) Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in a stretched polyacrylamide gel. J Am Chem Soc 124:2450-2451 (Pubitemid 34251754)
11. Chou JJ, Baber JL, Bax A (2004) Characterization of phospholipid mixed micelles by translational diffusion. J Biomol NMR 29:299-308 (Pubitemid 38864828)
12. Cierpicki T, Bushweller JH (2004) Charged gels as orienting media for measurement of residual dipolar couplings in soluble and integral membrane proteins. J Am Chem Soc 126:16259-16266 (Pubitemid 39627638)
13. Clore GM, Garrett DS (1999) R-factor, free R, and complete cross-validation for dipolar coupling refinement of NMR structures. J Am Chem Soc 121:9008-9012 (Pubitemid 29477367)
14. Clore GM, Starich MR, Gronenborn AM (1998) Measurement of residual dipolar couplings of marcomolecules aligned in the nematic phase of a colloidal suspension of rod-shaped viruses. J Am Chem Soc 120:10571-10572 (Pubitemid 28500376)
15. Clore GM, Starich MR, Bewley CA, Cai ML, Kuszewski J (1999) Impact of residual dipolar couplings on the accuracy of NMR structures determined from a minimal number of NOE restraints. J Am Chem Soc 121:6513-6514 (Pubitemid 29334638)
16. Cornilescu G, Marquardt JL, Ottiger M, Bax A (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120:6836-6837 (Pubitemid 28347351)
17. De Angelis AA, Opella SJ (2007) Bicelle samples for solid-state NMR of membrane proteins. Nat Protoc 2:2332-2338
18. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRpipe: a multidimensional spectral processing system based on Unix pipes. J Biomol NMR 6:277-293
19. Douglas SM, Chou JJ, Shih WM (2007) DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. Proc Natl Acad Sci USA 104:6644-6648 (Pubitemid 47175554)
20. Gaemers S, Bax A (2001) Morphology of three lyotropic liquid crystalline biological NMR media studied by translational diffusion anisotropy. J Am Chem Soc 123:12343-12352 (Pubitemid 33136071)
21. Ghana R, Walss C, Walmsley JA (1996) Sodium and potassium ion-promoted formation of supramolecular aggregates of 2′-deoxyguanylyl-(3′- 5′)-2′-deoxyguanosine. J Biomol Struct Dyn 14:101-110 (Pubitemid 26313816)
22. Goddard TD, Kneller DG (2008) Sparky 3. University of California, San Francisco
23. Han X, Tamm LK (2000) A host-guest system to study structure-function relationships of membrane fusion peptides. Proc Natl Acad Sci USA 97:13097-13102
24. Hansen MR, Mueller L, Pardi A (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nature Struct Biol 5:1065-1074 (Pubitemid 28546270)
25. Hus JC, Peti W, Griesinger C, Bruschweiler R (2003) Self-consistency analysis of dipolar couplings in multiple alignments of ubiquitin. J Am Chem Soc 125:5596-5597 (Pubitemid 36592859)
26. Hus J-C, Salmon L, Bouvignies G, Lotze J, Blackledge M, Brueschweiler R (2008) 16-fold degeneracy of peptide plane orientations from residual dipolar couplings: analytical treatment and implications for protein structure determination. J Am Chem Soc 130:15927-15937
27. Kamen DE, Cahill SM, Girvin ME (2007) Multiple alignment of membrane proteins for measuring residual dipolar couplings using lanthanide ions bound to a small metal chelator. J Am Chem Soc 129:1846-1847
28. Kay LE, Keifer P, Saarinen T (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J Am Chem Soc 114:10663-10665
29. Lorieau J, Yao LS, Bax A (2008) Liquid crystalline phase of G-tetrad DNA for NMR study of detergent-solubilized proteins. J Am Chem Soc 130:7536-7537 (Pubitemid 351842104)
30. Lorieau JL, Louis JM, Bax A (2010) The complete influenza hemagglutinin fusion domain adopts a tight helical hairpin arrangement at the lipid: water interface. Proc Natl Acad Sci USA 107:11341-11346
31. Lorieau JL, Louis JM, Bax A (2011) Whole-body rocking motion of a fusion peptide in lipid bilayers from size-dispersed (15)N NMR relaxation. J Am Chem Soc 133:14184-14187
32. Losonczi JA, Andrec M, Fischer MWF, Prestegard JH (1999) Order matrix analysis of residual dipolar couplings using singular value decomposition. J Magn Reson 138:334-342 (Pubitemid 129608294)
33. Meier S, Haussinger D, Grzesiek S (2002) Charged acrylamide copolymer gels as media for weak alignment. J Biomol NMR 24:351-356 (Pubitemid 36157540)
34. Meiler J, Prompers JJ, Peti W, Griesinger C, Bruschweiler R (2001) Model-free approach to the dynamic interpretation of residual dipolar couplings in globular proteins. J Am Chem Soc 123:6098-6107 (Pubitemid 32888479)
35. Mueller GA, Choy WY, Yang DW, Forman-Kay JD, Venters RA, Kay LE (2000) Global folds of proteins with low densities of NOEs using residual dipolar couplings: application to the 370-residue maltodextrin-binding protein. J Mol Biol 300:197-212
36. Ottiger M, Bax A (1999) Bicelle-based liquid crystals for NMR-measurement of dipolar couplings at acidic and basic pH values. J Biomol NMR 13:187-191 (Pubitemid 29089229)
37. Peti W, Meiler J, Bruschweiler R, Griesinger C (2002) Model-free analysis of protein backbone motion from residual dipolar couplings. J Am Chem Soc 124:5822-5833 (Pubitemid 34533522)
38. Prestegard JH, Al-Hashimi HM, Tolman JR (2000) NMR structures of biomolecules using field oriented media and residual dipolar couplings. Q Rev Biophys 33:371-424 (Pubitemid 32151707)
39. Ramirez BE, Bax A (1998) Modulation of the alignment tensor of macromolecules dissolved in a dilute liquid crystalline medium. J Am Chem Soc 120:9106-9107 (Pubitemid 28449207)
40. Rodriguez-Castaneda F, Haberz P, Leonov A, Griesinger C (2006) Paramagnetic tagging of diamagnetic proteins for solution NMR. Magn Reson Chem 44:S10-S16 (Pubitemid 44090386)
41. Ruan K, Tolman JR (2005) Composite alignment media for the measurement of independent sets of NMR residual dipolar couplings. J Am Chem Soc 127:15032-15033 (Pubitemid 41547363)
42. Ruan K, Briggman KB, Tolman JR (2008) De novo determination of internuclear vector orientations from residual dipolar couplings measured in three independent alignment media. J Biomol NMR 41:61-76
43. Ruckert M, Otting G (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J Am Chem Soc 122:7793-7797
44. Sanders CR, Schwonek JP (1992) Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 31:8898-8905
45. Sass J, Cordier F, Hoffmann A, Rogowski M, Cousin A, Omichinski JG, Lowen H, Grzesiek S (1999) Purple membrane induced alignment of biological macromolecules in the magnetic field. J Am Chem Soc 121:2047-2055 (Pubitemid 29152418)
46. Sass H-J, Musco G, Stahl SJ, Wingfield PT, Grzesiek S (2000) Solution NMR of proteins within polyacrylamide gels: diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes. J Biomol NMR 18:303-309 (Pubitemid 32065084)
47. Saupe A, Englert G (1963) High-resolution nuclear magnetic resonance spectra of oriented molecules. Phys Rev Lett 11:462-464
48. Shortle D, Ackerman MS (2001) Persistence of native-like topology in a denatured protein in 8 M urea. Science 293:487-489 (Pubitemid 32679075)
49. Struppe J, Whiles JA, Vold RR (2000) Acidic phospholipid bicelles: a versatile model membrane system. Biophys J 78:281-289 (Pubitemid 30207137)
50. Su XC, Otting G (2010) Paramagnetic labelling of proteins and oligonucleotides for NMR. J Biomol NMR 46:101-112
51. Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111-1114 (Pubitemid 27517889)
52. Tolman JR (2002) A novel approach to the retrieval of structural and dynamic information from residual dipolar couplings using several oriented media in biomolecular NMR spectroscopy. J Am Chem Soc 124:12020-12030
53. Tolman JR, Ruan K (2006) NMR residual dipolar couplings as probes of biomolecular dynamics. Chem Rev 106:1720-1736 (Pubitemid 43792777)
54. Tolman JR, Flanagan JM, Kennedy MA, Prestegard JH (1995) Nuclear magnetic dipole interactions in field-oriented proteins - information for structure determination in solution. Proc Natl Acad Sci USA 92:9279-9283
55. Tycko R, Blanco FJ, Ishii Y (2000) Alignment of biopolymers in strained gels: a new way to create detectable dipole-dipole couplings in high-resolution biomolecular NMR. J Am Chem Soc 122:9340-9341
56. Ulmer TS, Ramirez BE, Delaglio F, Bax A (2003) Evaluation of backbone proton positions and dynamics in a small protein by liquid crystal NMR spectroscopy. J Am Chem Soc 125:9179-9191 (Pubitemid 36903834)
57. Vold RR, Prosser RS (1996) Magnetically oriented phospholipid bilayered micelles for structural studies of polypeptides. Does the ideal bicelle exist? J Magn Reson, Ser B 113:267-271 (Pubitemid 126758778)
58. Vold RR, Prosser RS, Deese AJ (1997) Isotropic solutions of phospholipid bicelles: a new membrane mimetic for high-resolution NMR studies of polypeptides. J Biomol NMR 9:329-335 (Pubitemid 127505395)
59. Wohnert J, Franz KJ, Nitz M, Imperiali B, Schwalbe H (2003) Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. J Am Chem Soc 125:13338-13339 (Pubitemid 37352103)
60. Yao LS, Bax A (2007) Modulating protein alignment in a liquid-crystalline medium through conservative mutagenesis. J Am Chem Soc 129:11326-11327 (Pubitemid 47555539)
61. Yao L, Vogeli B, Torchia DA, Bax A (2008) Simultaneous NMR study of protein structure and dynamics using conservative mutagenesis. J Phys Chem B 112:6045-6056
62. Yao LS, Ying JF, Bax A (2009) Improved accuracy of N-15-H-1 scalar and residual dipolar couplings from gradient-enhanced IPAP-HSQC experiments on protonated proteins. J Biomol NMR 43:161-170
63. Zhang Q, Sun XY, Watt ED, Al-Hashimi HM (2006) Resolving the motional modes that code for RNA adaptation. Science 311:653-656 (Pubitemid 43191308)
64. Zidek L, Padrta P, Chmelik J, Sklenar V (2003) Internal consistency of NMR data obtained in partially aligned biomacromolecules. J Magn Reson 162:385-395