Microsecond timescale backbone conformational dynamics in ubiquitin studied with NMR R1ρ relaxation experiments

Protein Science

Volumn 14, Issue 3, 2005, Pages 735-742

  Massi, Francesca ^a   Grey, Michael J ^a   Palmer III, Arthur G ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

15N spin relaxation; Chemical exchange; Multiple quantum relaxation; Protein dynamics

Indexed keywords

UBIQUITIN;

AMINO ACID SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

MAGNETIC RESONANCE SPECTROSCOPY; NITROGEN ISOTOPES; PROTEIN STRUCTURE, TERTIARY; UBIQUITIN;

EID: 14144250990     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041139505     Document Type: Article

References (50)

1. Abragam, A. 1983. Principles of nuclear magnetism. Oxford University Press, Oxford.
2. Beal, R., Deveraux, Q., Xia, G., Rechsteiner, M., and Pickart, C. 1996. Surface hydrophobic residues of multiubiquitin chains essential for proteolytic targeting. Proc. Natl. Acad. Sci. 93: 861-866.
3. 15N random coil chemical-shifts. J. Am. Chem. Soc. 116: 8466-8469.
4. Burch, T.J. and Haas, A.L. 1994. Site-directed mutagenesis of ubiquitin. Differential roles of arginine in the interaction with ubiquitin-activating enzyme. Biochemistry 33: 7300-7308.
5. N CSA-dipolar cross-correlated relaxation. J. Am. Chem. Soc. 122: 5105-5113.
6. Cordier, F. and Grzesiek, S. 2002. Temperature-dependence of protein hydrogen bond properties as studied by high-resolution NMR. J. Mol. Biol. 317: 739-752.
7. de Alba, E., Barber, 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.
8. de Dios, A.C., Pearson, J.G., and Oldfield, E. 1993. Secondary and tertiary structural effects on protein NMR chemical shifts: An ab initio approach. Science 260: 1491-1496.
9. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. 1995. NMRPipe - A multidimentional spectral processing system based on unix pipes. J. Biomol. NMR 6: 277-293.
10. Deverell, C., Morgan, R.E., and Strange, J.H. 1970. Studies of chemical exchange by nuclear magnetic relaxation in rotating frame. Mol. Phys. 18: 553-559.
11. Dittmer, J. and Bodenhausen, G. 2004. Evidence of slow motion in proteins by multiple refocusing of heteronuclear nitrogen/proton multiple quantum coherence in NMR. J. Am. Chem. Soc. 126: 1314-1315.
12. 15N NMR relaxation. Biochemistry 33: 5984-6003.
13. 15N chemical shift anisotropy from NMR relaxation data. Ubiquitin as a test example. J. Am. Chem. Soc. 120: 7109-7110.
14. 15N chemical shift anisotropy in solution. J. Am. Chem. Soc. 120: 10947-10952.
15. Grey, M.J., Wang, C., and Palmer, A.G. 2003. Disulfide bond isomerization in basic pancreatic trypsin inhibitor: Multi-site chemical exchange quantified by CPMG relaxation dispersion and chemical shift modeling. J. Am. Chem. Soc. 125: 14324-14335.
16. 1 field inhomogeneity. Are the biases assumed in heteronuclear relaxation experiments usually underestimated? J. Magn. Reson. 136: 118-126.
17. Haas, A.L. and Siepmann, T.J. 1997. Pathways of ubiquitin conjugation. FASEB J. 11: 1257-1268.
18. Hamilton, K.S., Ellison, M.J., and Shaw, G.S. 2000. Identification of the ubiquitin interfacial residues in a ubiquitin-E2 covalent complex. J. Biomol. NMR 18: 319-327.
19. Hamilton, K.S., Ellison, M.J., Barber, K.R., Williams, R.S., Huzil, J.T., McKenna, S., Ptak, C., Glover, M., and Shaw, G.S. 2001. Structure of a conjugating enzyme-ubiquitin thiolester intermediate reveals a novel role for the ubiquitin tail. Structure 9: 897-904.
20. Hershko, A. and Ciechanover, A. 1998. The ubiquitin system. Annu. Rev. Biochem. 67: 425-479.
21. Hochstrasser, M. 1996. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30: 405-439.
22. 15N transverse relaxation to detect millisecond time-scale motions in perdeuterated proteins: Application to HIV-1 protease. J. Am. Chem. Soc. 120: 10534-10542.
23. James, L.C., Roversi, P., and Tawdik, D.S. 2003. Antibody multispecificity mediated by conformational diversity. Science 299: 1362-1367.
24. Kloibert, K. and Konrat, R. 2000. Differential multiple-quantum relaxation arising from cross-correlated time-modulation of isotropic chemical shifts. J. Biomol. NMR 18: 33-42.
25. 15N chemical shift anisotropy relaxation interference: Unambiguous determination of rotational diffusion tensor and chemical exchange effect in biological macromolecules. J. Am. Chem. Soc. 120: 7905-7915.
26. 15N chemical shift anisotropy in Escherichia coli ribonuclease H in solution. J. Am. Chem. Soc. 121: 10119-10125.
27. Majumdar, A. and Ghose, R. 2004. Probing slow backbone dynamics in proteins using TROSY-based experiments to detect cross-correlated time-modulation of isotropic chemical shifts. J. Biomol. NMR 28: 213-227.
28. 1ρ rotating-frame relaxation with weak radio frequency fields. J. Am. Chem. Soc. 126: 2247-2256.
29. 15N chemical shift anisotropy from NMR relaxation data. Ubiquitin as a test example. J. Am. Chem. Soc. 123: 6098-6107.
30. Mills, J.L. and Szyperski, T. 2002. Protein dynamics in supercooled water: The search for slow motional modes. J. Biomol. NMR 23: 63-67.
31. Miura, T., Klaus, W., Gsell, B., Miyamoto, C., and Senn, H. 1999. Characterization of the binding interface between ubiquitin and class I human ubiquitin-conjugating enzyme 2b by multidimensional heteronuclear NMR spectroscopy in solution. J. Mol. Biol. 290: 213-228.
32. Mosteller, F. and Tukey, J.W. 1977. Data analysis and regression. A second course in statistics. Addison-Wesley, Reading, MA.
33. Mulder, F.A.A., deGraaf, R.A., Kaptein, R., and Boelens, R. 1998. An off-resonance rotating frame relaxation experiment for the investigation of macromolecular dynamics using adiabatic rotations. J. Magn. Reson. 131: 351-357.
34. Palmer, A.G. 2004. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104: 3623-3640.
35. Palmer, A.G., Kroenke, C.D., and Loria, J.P. 2001. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological molecules. Methods Enzymol. 339: 204-238.
36. Schneider, D.M., Dellwo, M.J., and Wand, A.J. 1992. Fast internal main-chain dynamics of human ubiquitin. Biochemistry 31: 3645-3652.
37. 15N NMR relaxation. J. Am. Chem. Soc. 117: 12562-12566.
38. 15N chemical shift anisotropy from quantitative measurement of relaxation interference effects. J. Am. Chem. Soc. 118: 6986-6991.
39. Tolman, J.R., Al-Hashimi, H.M., Kay, L.E., and Prestegard, J.H. 2001. Structural and dynamic analysis of residual dipolar coupling data for proteins. J. Am. Chem. Soc. 123: 1416-1424.
40. Wang, C., and Palmer, A.G. 2002. Differential multiple quantum relaxation caused by chemical exchange outside the fast exchange limit. J. Biomol. NMR 24: 263-268.
41. 15N-labeled proteins. Magn. Reson. Chem. 41: 866-876.
42. Wang, C., Grey, M.J., and Palmer, A.G. 2001a. CPMG sequences with enhanced sensitivity to chemical exchange. J. Biomol. NMR 21: 361-366.
43. Wang, L.C., Pang, Y.X., Holder, T., Brender, J.R., Kurochkin, A.V., and Zuiderweg, E.R.P. 2001b. Functional dynamics in the active site of the ribonuclease binase. Proc. Natl. Acad. Sci. 98: 7684-7689.
44. Wilkinson, K.D., Laleli-Sahin, E., Urbauer, J., Larsen, C.N., Shih, G.H., Haas, A.L., Walsh, S.T.R., and Wand, A.J. 1999. The binding site for UCH-L3 on ubiquitin: Mutagenesis and NMR studies on the complex between ubiquitin and UCH-L3. J. Mol. Biol. 291: 1067-1077.
45. Wishart, D.S. and Case, D.A. 2001. Use of chemical shifts in macromolecular structure determination. Methods Enzymol. 338: 3-34.
46. Wist, J., Frueh, D., Tolman, J.R., and Bodenhausen, G. 2004. Triple quantum decoherence under multiple refocusing: Slow correlated chemical shift modulations of C′ and N nuclei in proteins. J. Biomol. NMR 28: 263-272.
47. 13C′ chemical shifts in proteins using a density functional database. J. Biomol. NMR 21: 321-333.
48. 13C′ chemical shifts in peptide using density functional theory. Biopolymers 65: 408-423.
49. Zhang, Y.-P. 1995. "Protein and peptide structure and interactions studied by hydrogen exhange and NMR". Ph.D. thesis, University of Pennsylvania, Philadelphia, PA.
50. Zhang, H., Neal, S., and Wishart, D.S. 2003. RefDB: A database of uniformly referenced protein chemical shifts. J. Biomol. NMR 25: 173-195.