Weak alignment offers new NMR opportunities to study protein structure and dynamics

Protein Science

Volumn 12, Issue 1, 2003, Pages 1-16

  Bax, Ad ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ANISOTROPY; CONFERENCE PAPER; DYNAMICS; HYDROGEL; LIQUID CRYSTAL; MAGNETIC FIELD; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

ANISOTROPY; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS;

EID: 0037215324     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0233303     Document Type: Conference Paper

References (91)

1. Aitio, H., Annila, A., Heikkinen, S., Thulin, E., Drakenberg, T., and Kilpelainen, I. 1999. NMR assignments, secondary structure, and global fold of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea. Protein Sci. 8: 2580-2588.
2. Almond, A. and Axelsen, J.B. 2002. Physical interpretation of residual dipolar couplings in neutral aligned media. J. Am. Chem. Soc. 124: 9986-9987.
3. Annila, A., Aitio, H., Thulin, E., and Drakenberg, T. 1999. Recognition of protein folds via dipolar couplings. J. Biomol. NMR 14: 223-230.
4. Banci, L., Bertini, I., Savellini, G.G., Romagnoli, A., Turano, P., Cremonini, M.A., Luchinat, C., and Gray, H.B. 1997. Pseudocontact shifts as constraints for energy minimization and molecular dynamics calculations on solution structures of paramagnetic metalloproteins. Proteins-Structure Function and Genetics 29: 68-76.
5. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible. Biochemistry 31: 5269-5278.
6. Barrientos, L.G., Dolan, C., and Gronenborn, AM. 2000. Characterization of surfactant liquid crystal phases suitable for molecular alignment and measurement of dipolar couplings. J. Biomol. NMR 16: 329-337.
7. Bax, A. and Tjandra, N. 1997. High-resolution heteronuclear NMR of human ubiquitin in an aqueous liquid crystalline medium. J. Biomol. NMR 10: 289-292.
8. Bax, A., Vuister, G.W., Grzesiek, S., Delaglio, F., Wang, A.C., Tschudin, R., and Zhu, G. 1994. Measurement of homonuclear and heteronuclear J-couplings from quantitative J-correlation. Meth. Enzymol. 239: 79-105.
9. Bewley, C.A. and Clore, G.M. 2000. Determination of the relative orientation of the two halves of the domain-swapped dimer of cyanovirin-N in solution using dipolar couplings and rigid body minimization. J. Am. Chem. Soc. 122: 6009-6016.
10. Biamonti, C., Rios, C.B., Lyons, B.A., and Montelione, G.T. 1994. Multidimensional NMR experiments and analysis techniques for determining homo- and heteronuclear scalar coupling constants in proteins and nucleic acids. Adv. Biophys. Chem. 4: 51-120.
11. Boisbouvier, J., Gans, P., Blackledge, M., Brutscher, B., and Marion, D. 1999. Long-range structural information in NMR studies of paramagnetic molecules from electron spin-nuclear spin cross-correlated relaxation. J. Am. Chem. Soc. 121: 7700-7701.
12. Brunger, A.T. 1993. XPLOR: A System For X-Ray Crystallography and NMR. Yale University Press, New Haven, CT.
13. Brunger, A.T., Clore, G.M., Gronenborn, A.M., Saffrich, R., and Nilges, M. 1993. Assessing the quality of solution nuclear-magnetic-resonance structures by complete cross-validation. Science 261: 328-331.
14. Bystrov, V.F. 1976. Spin-spin couplings and the conformational states of peptide spin systems. Prog. Nucl. Magn. Reson. Spectrosc. 10: 41-81.
15. Chothia, C. 1992. Proteins - 1000 Families for the molecular biologist. Nature 357: 543-544.
16. Chou, J.J., Li, S., and Bax, A. 2000. Study of conformational rearrangement and refinement of structural homology models by the use of dipolar couplings. J. Biomol. NMR 18: 217-227.
17. Chou, J.J., Gaemers, S., Howder, B., Louis, J.M., and Bax, A. 2001a. A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles. J. Biomol. NMR 21: 377-382.
18. Chou, J.J., Li, S., Klee, C.B., and Bax, A. 2001b. Solution structure of Ca2+-calmodulin reveals flexible hand-like properties of its domains. Nat. Struct. Biol. 8: 990-997.
19. Chou, J.J., Kaufman, J.D., Stahl, S.J., Wingfield, P.T., and Bax, A. 2002. Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel. J. Am. Chem. Soc. 124: 2450-2451.
20. Clore, G.M. 2000. Accurate and rapid docking of protein-protein complexes on the basis of intermolecular nuclear Overhauser enhancement data and dipolar couplings by rigid body minimization. Proc. Natl. Acad. Sci. 97: 9021-9025.
21. Clore. G.M. and Garrett, D.S. 1999. R-factor, free R, and complete crossvalidation for dipolar coupling refinement of NMR structures. J. Am. Chem. Soc. 121: 9008-9012.
22. Clore, G.M., Starich, M.R., and Gronenborn, A.M. 1998. Measurement of residual dipolar couplings of macromolecules aligned in the nematic phase of a colloidal suspension of rod-shaped viruses. J. Am. Chem. Soc. 120: 10571-10572.
23. Clore, G.M., Starich, M.R., Bewley, C.A., Cai, M.L., and 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.
24. Cornilescu, G. and Bax, A. 2000. Measurement of proton, nitrogen, and carbonyl chemical shielding anisotropies in a protein dissolved in a dilute liquid crystalline phase. J. Am. Chem. Soc. 122: 10143-10154.
25. Cornilescu, G., Marquardt, J.L., Ottiger, M., and 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.
26. Cornilescu, G., Delaglio, F., and Bax, A. 1999. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13: 289-302.
27. de Alba, E., Baber, J.L., and Tjandra, N. 1999. The use of residual dipolar coupling in concert with backbone relaxation rates to identify conformational exchange by NMR. J. Am. Chem. Soc. 121: 4282-4283.
28. Delaglio, F., Kontaxis, G., and Bax, A. 2000. Protein structure determination using molecular fragment replacement and NMR dipolar couplings. J. Am. Chem. Soc. 122: 2142-2143.
29. Derrick, J.P. and Wigley, D.B. 1994. The 3rd Igg-binding domain from streptococcal protein-G - An analysis by x-ray crystallography of the structure alone and in a complex with Fab. J. Mol. Biol. 243: 906-918.
30. Dingley, A.J. and Grzesiek, S. 1998. Direct observation of hydrogen bonds in nucleic acid base pairs by intemucleotide (2)J(NN) couplings. J. Am. Chem. Soc. 120: 8293-8297.
31. Drohat, A.C., Tjandra, N., Baldisseri, D.M., and Weber, D.J. 1999. The use of dipolar couplings for determining the solution structure of rat apo-S100B(ββ). Protein Sci. 8: 800-809.
32. Fernandes, M.X., Bernado, P., Pons, M., and de la Torre, J.G. 2001. An analytical solution to the problem of the orientation of rigid particles by planar obstacles. Application to membrane systems and to the calculation of dipolar couplings in protein NMR spectroscopy. J. Am. Chem. Soc. 123: 12037-12047.
33. Gaemers, S. and Bax, A. 2001. Morphology of three lyotropic liquid crystalline biological NMR media studied by translational diffusion anisotropy. J. Am. Chem. Soc. 123: 12343-12352.
34. Gayathri, C., Bothnerby, A.A., Vanzijl, P.C.M., and Maclean, C. 1982. Dipolar magnetic-field effects in NMR-spectra of liquids. Chem. Phys. Lett. 87: 192-196.
35. Gochin, M. 1998. Nuclear magnetic resonance characterization of a paramagnetic DNA-drug complex with high spin cobalt: Assignment of the H-I and P-31 NMR spectra, and determination of electronic, spectroscopic and molecular properties. J. Biomol. NMR 12: 243-257.
36. Gonzalez, C., Rullmann, J.A.C., Bonvin, A., Boelens, R., and Kaptein. R. 1991. Toward an NMR R factor. J. Magn. Reson. 91: 659-664.
37. Goto, N.K., Skrynnikov, N.R., Dahlquist, F.W., and Kay, L.E. 2001. What is the average conformation of bacteriophage T4 lysozyme in solution? A domain orientation study using dipolar couplings measured by solution NMR. J. Mol. Biol. 308: 745-764.
38. Hansen, M.R., Mueller. L., and Pardi, A. 1998. Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat. Struct. Biol. 5: 1065-1074.
39. Hu, J.S. and Bax, A. 1997. Determination of phi and chi(1) angles in proteins from C-13-C- 13 three-bond J couplings measured by three-dimensional heteronuclear NMR. How planar is the peptide bond? J. Am. Chem. Soc. 119: 6360-6368.
40. Karplus, M. 1959. Contact electron-spin coupling of nuclear magnetic moments. J. Phys. Chem. 30: 11-15.
41. Karplus, P.A. 1996. Experimentally observed conformation-dependent geometry and hidden strain in proteins. Protein Sci. 5: 1406-1420.
42. Kuszewski, J., Qin, J., Gronenborn, A.M., and Clore, G.M. 1995. The impact of direct refinement against C-13(alpha) and C- 13(beta) chemical-shifts on protein-structure determination by NMR. J. Magn. Reson. Ser. B 106: 92-96.
43. Kuszewski, J., Gronenborn, A.M., and Clore, G.M. 1999. Improving the packing and accuracy of NMR structures with a pseudopotential for the radius of gyration. J. Am. Chem. Soc. 121: 2337-2338.
44. Losonczi, J.A., Andrec, M., Fischer, M.W.F., and Prestegard, J.H. 1999. Order matrix analysis of residual dipolar couplings using singular value decomposition. J. Magn. Reson. 138: 334-342.
45. Mehring, M. 1982. High Resolution NMR in Solids, 2nd Ed. Springer, Berlin, Germany.
46. Meiter, J., Peti, W., and Griesinger, C. 2000. DipoCoup: A versatile program for 3D-structure homology comparison based on residual dipolar couplings and pseudocontact shifts. J. Biomol. NMR 17: 283-294.
47. Nieh, M.P., Glinka, C.J., Krueger, S., Prosser, R.S., and Katsaras, J. 2001. SANS study of the structural phases of magnetically alignable lanthanidedoped phospholipid mixtures. Langmuir 17: 2629-2638.
48. Ottiger, M. and Bax, A. 1998a. Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules. J. Biomol. NMR 12: 361-372.
49. -, 1998b. Determination of relative N-H, N-C′, Ca-C′, and Cα-Hα effective bond lengths in a protein by NMR in a dilute liquid crystalline phase. J. Am. Chem. Soc. 120: 12334-12341.
50. Ottiger, M., Tjandra, N., and Bax, A. 1997. Magnetic field dependent amide N-15 chemical shifts in a protein-DNA complex resulting from magnetic ordering in solution. J. Am. Chem. Soc. 119: 9825-9830.
51. Pelupessy, P., Chiarparin, E., Ghose, R., and Bodenhausen, G. 1999. Efficient determination of angles subtended by C-alpha-H-alpha and N-H-N vectors in proteins via dipole-dipole cross-correlation. J. Biomol. NMR 13: 375-380.
52. Pervushin, K., Ono, A., Fernandez, C., Szyperski, T., Kainosho, M., and Wuthrich, K. 1998. NMR scalar couplings across Watson-Crick base pair hydrogen bonds in DNA observed by transverse relaxation optimized spectroscopy. Proc. Natl. Acad. Sci. 95: 14147-14151.
53. Peti, W., Meiler, J., Bruschweiler, R., and Griesinger, C. 2002. Model-free analysis of protein backbone motion from residual dipolar couplings. J. Am. Chem. Soc. 124: 5822-5833.
54. Prosser, R.S., Losonczi, J.A., and Shiyanovskaya, I.V. 1998. Use of a novel aqueous liquid crystalline medium for high-resolution NMR of macromolecules in solution. J. Am. Chem. Soc. 120: 11010-11011.
55. Ramirez, B.E. and Bax, A. 1998. Modulation of the alignment tensor of macromolecules dissolved in a dilute liquid crystalline medium. J. Am. Chem. Soc. 120: 9106-9107.
56. Ramirez, B.E., Voloshin, O.N., Camerini-Otero, R.D., and Bax, A. 2000. Solution structure of DinI provides insight into its mode of RecA inactivation. Protein Sci. 9: 2161-2169.
57. Reif, B., Hennig, M., and Griesinger, C. 1997. Direct measurement of angles between bond vectors in high-resolution NMR. Science 276: 1230-1233.
58. Rohl, C.A. and Baker, D. 2002. De novo determination of protein backbone structure from residual dipolar couplings using Rosetta. J. Am. Chem. Soc. 124: 2723-2729.
59. Ruckert, M. and Otting, G. 2000. Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J. Am. Chem. Soc. 122: 7793-7797.
60. Sanders, C.R. and Prestegard, J.H. 1990. Magnetically orientable phospholipidbilayers containing small amounts of a bile-salt analog, chapso. Biophys. J. 58: 447-460.
61. Sanders, C.R. and Schwonek, J.P. 1992. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 31: 8898-8905.
62. Sanders, C.R., Hare, B.J., Howard, K.P., and Prestegard, J.H. 1994. Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules. Prog. Nucl. Magn. Reson. Spectrosc. 26: 421-444.
63. Sass, H.J., Musco, G., Stahl, S.J., Wingfield, P.T., and 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.
64. Saupe, A. and Englert, G. 1963. High-resolution nuclear magnetic resonance spectra of oriented molecules. Phys. Rev. Lett. 11: 462-464.
65. Shortle, D. and Ackerman, M.S. 2001. Persistence of native-like topology in a denatured protein in 8 M urea. Science 293: 487-489.
66. Sitkoff, D. and Case, D.A. 1998. Theories of chemical shift anisotropies in proteins and nucleic acids. Prog. Nucl. Magn. Reson. Spectrosc. 32: 165-190.
67. Skrynnikov, N.R., Goto, N.K., Yang, D.W., Choy, W.Y., Tolman, J.R., Mueller, G.A., and Kay, L.E. 2000. Orienting domains in proteins using dipolar couplings measured by liquid-state NMR: Differences in solution and crystal forms of maltodextrin binding protein loaded with beta-cyclodextrin. J. Mol. Biol. 295: 1265-1273.
68. Spera, S. and Bax, A. 1991. Empirical correlation between protein backbone conformation and C-alpha and C-beta C-13 nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. 113: 5490-5492.
69. Struppe, J. and Vold, R.R. 1998. Dilute bicellar solutions for structural NMR work. J. Magn. Reson. 135: 541-546.
70. Thomas, P.D., Basus, V.J., and James, T.L. 1991. Protein solution structure determination using distances from 2-dimensional nuclear overhauser effect experiments - Effect of approximations on the accuracy of derived structures. Proc. Natl. Acad. Sci. 88: 1237-1241.
71. Tjandra, N. and Bax, A. 1997. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278: 1111-1114.
72. Tjandra, N., Grzesiek, S., and Bax, A. 1996. Magnetic field dependence of nitrogen-proton J splittings in N-15-enriched human ubiquitin resulting from relaxation interference and residual dipolar coupling. J. Am. Chem. Soc. 118: 6264-6272.
73. Tjandra, N., Omichinski, J.G., Gronenborn, A.M., Clore. G.M., and Bax, A. 1997. Use of dipolar H1-N15 and H1-C13 couplings in the structure determination of magnetically oriented macromolecules in solution. Nat. Struct. Biol. 4: 732-738.
74. Tolman, J.R., Flanagan, J.M., Kennedy, M.A., and Prestegard. J.H. 1995. Nuclear magnetic dipole interactions in field-oriented proteins - Information for structure determination in solution. Proc. Natl. Acad. Sci. 92: 9279-9283.
75. Tolman, J.R., Flanagan, J.M., Kennedy, M.A., and Prestegard, J.H. 1997. NMR evidence for slow collective motions in cyanometmyoglobin. Nat. Struct. Biol. 4: 292-297.
76. Tycko, R., Blanco, F.J., and 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.
77. Ulmer, T.S., Werner, J.M., and Campbell, I.D. 2002. SH3-SH2 domain orientation in Src kinases: NMR studies of Fyn. Structure 10: 901-911.
78. Vijay-Kumar, S., Bugg, C.E., and Cook. W.J. 1987. Structure of ubiquitin refined at 1.8 A resolution. J. Mol. Biol. 194: 531-544.
79. Vold, R.R. and Prosser, R.S. 1996. Magnetically oriented phospholipid bilayered micelles for structural studies of polypeptides. Does the ideal bicelle exist? J. Magn. Reson. Ser. B 113: 267-271.
80. Vold, R.R., Prosser, R.S., and Deese, A.J. 1997. Isotropic solutions of phospholipid bicelles: A new membrane mimetic for high-resolution NMR studies of polypeptides. J. Biomol. NMR 9: 329-335.
81. Voloshin, O.N., Ramirez, B.E., Bax, A., and Camerini-Otero, R.D. 2001. A model for the abrogation of the SOS response by an SOS protein: A negatively charged helix in DinI mimics DNA in its interaction with RecA. Genes & Dev. 15: 415-427.
82. Vuister, G.W., Tessari, M., Karimi-Nejad, Y., and Whitehead, B. 1999. Pulse sequences for measuring coupling constants. In Biological magnetic resonance (eds. R. Krishna and L. Berliner), Vol. 16, pp. 195-257. Kluwer, Dordrecht, The Netherlands.
83. Wang, Y.X., Jacob, J., Cordier, F., Wingfield, P., Stahl, S.J., Lee-Huang, S., Torchia, D., Grzesiek, S., and Bax, A. 1999. Measurement of (3h)J(NC′) connectivities across hydrogen bonds in a 30 kDa protein. J. Biomol. NMR 14: 181-184.
84. 2+-bound calmodulin: An analysis of disorder and implications for functionally relevant plasticity. J. Mol. Biol. 301: 1237-1256.
85. Wishart, D.S., Sykes, B.D., and Richards, F.M. 1991. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222: 311-333.
86. Withka, J.M., Srinivasan, J., and Bolton, P.H. 1992. Problems with, and alternatives to, the NMR R-factor. J. Magn. Reson. 98: 611-617.
87. Wooton, J.B., Savitsky, G.B., Jacobus, J., Bayerlein, A.L., and Emsley, J.W. 1979. Methyl group geometry. J. Chem. Phys. 70: 438-442.
88. Yang, D.W., Konrat, R., and Kay, L.E. 1997. A multidimensional NMR experiment for measurement of the protein dihedral angle psi based on cross-correlated relaxation between (Hα-13Cα)-H1 dipolar and C-13′ (carbonyl) chemical shift anisotropy mechanisms. J. Am. Chem. Soc. 119: 11938-11940.
89. Zweckstetter, M. and Bax, A. 2000. Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J. Am. Chem. Soc. 122: 3791-3792.
90. -, 2001a. Characterization of molecular alignment in aqueous suspensions of Pfl bacteriophage. J. Biomol. NMR 20: 365-377.
91. - . 2001b. Single-step determination of protein substructures using dipolar couplings: Aid to structural genomics. J. Am. Chem. Soc. 123: 9490-9491.