Journal of Biomolecular NMR

, Volume 34, Issue 2, pp 101–115 | Cite as

A Thorough Dynamic Interpretation of Residual Dipolar Couplings in Ubiquitin

  • Nils A. Lakomek
  • Teresa Carlomagno
  • Stefan Becker
  • Christian Griesinger
  • Jens Meiler
Article

Abstract

The presence of slow motions with large amplitudes, as detected by measurements based on residual dipolar couplings [Peti, W., Meiler, J., Brueschweiler, R. and Griesinger, C. (2002) J. Am. Chem. Soc., 124, 5822–5833], has stirred up much discussion in recent years. Based on ubiquitin NH residual dipolar couplings (rdcs) measured in 31 different alignment conditions, a model-free analysis of structure and dynamics [Meiler, J., Peti, W., Prompers, J., Griesinger, C. and Brueschweiler, R. (2001) J. Am. Chem. Soc., 123, 6098–6107] is presented. Starting from this broad experimental basis, rdc-based order parameters with so far unattained accuracy were determined. These rdc-based order parameters underpin the presence of new modes of motion slower than the inverse overall tumbling correlation time. Amplitudes and anisotropies of the motion were derived. The effect of structural noise on the results was proven to be negligible.

Keywords

dynamical averaging model free approach nuclear magnetic resonance (NMR) residual dipolar couplings (rdcs) ubiquitin 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

supp.pdf (858 kb)
Supplementary material

References

  1. Akke, M., Palmer, A.G. 1996J. Am. Chem. Soc.118911912CrossRefGoogle Scholar
  2. Barrientos, L.G., Dolan, C., Gronenborn, A.M. 2000J. Biomol. NMR16329337CrossRefGoogle Scholar
  3. Beal, R., Deveraux, Q., Xia, G., Rechsteiner, M., Pickart, C. 1996Proc. Natl. Acad. Sci. U.S.A93861866CrossRefADSGoogle Scholar
  4. Bernado, P., Blackledge, M. 2004aJ. Am. Chem. Soc.12649074920Google Scholar
  5. Bernado, P., Blackledge, M. 2004bJ. Am. Chem. Soc.12677607761Google Scholar
  6. Bertoncini, C.W., Jung, Y.S., Fernandez, C.O., Hoyer, W., Griesinger, C., Jovin, T.M., Zweckstetter, M. 2005Proc. Natl. Acad. Sci. U.S.A10214301435CrossRefADSGoogle Scholar
  7. Bremi, T., Brueschweiler, R. 1997J. Am. Chem. Soc.11966726673Google Scholar
  8. Bremi, T., Brueschweiler, R., Ernst, R.R. 1997J. Am. Chem. Soc.11942724284Google Scholar
  9. Briggman, K.B., Tolman, J.R. 2003J. Am. Chem. Soc.1251016410165CrossRefGoogle Scholar
  10. Brutscher, B., Brueschweiler, R., Ernst, R.R. 1997Biochemistry361304313053CrossRefGoogle Scholar
  11. Burch, T.J., Haas, A.L. 1994Biochemistry3373007308CrossRefGoogle Scholar
  12. Chang, S.-L., Tjandra, N. 2005J. Magn. Res.1744353CrossRefADSGoogle Scholar
  13. Chou, J.J., Gaemers, S., Howder, B., Louis, J.M., Bax, A. 2001J. Biomol. NMR21377382Google Scholar
  14. Clore, G.M., Schwieters, C.D. 2004J. Am. Chem. Soc.12629232938CrossRefGoogle Scholar
  15. Cornilescu, G., Marquardt, J.L., Ottiger, M., Bax, A. 1998J. Am. Chem. Soc.12068366837CrossRefGoogle Scholar
  16. Alba, E., Baber, J.L., Tjandra, N. 1999J. Am. Chem. Soc.12142824283Google Scholar
  17. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., Bax, A. 1995J. Biomol. NMR6277293CrossRefGoogle Scholar
  18. Dittmer, J., Bodenhausen, G. 2004J. Am. Chem. Soc.12613141315CrossRefGoogle Scholar
  19. Fushman, D., Cowburn, D. 1998J. Am. Chem. Soc.12071097110Google Scholar
  20. Haas, A.L., Siepmann, T.J. 1997FASEB J.1112571268Google Scholar
  21. Johnson, E.C., Lazar, G.A., Desjarlais, J.R., Handel, T.M. 1999Structure Fold Des.7967976Google Scholar
  22. Kay, L.E., Torchia, D.A., Bax, A. 1989Biochemistry2889728979Google Scholar
  23. Kitahara, R., Yokoyama, S., Akasaka, K. 2005J. Mol. Biol.347277285CrossRefGoogle Scholar
  24. Koenig, B.W., Hu, J.-S., Ottiger, M., Bose, S., Hendler, R.W., Bax, A. 1999J. Am. Chem. Soc.12113851386CrossRefGoogle Scholar
  25. Kopple, K.D., Bhandary, K.K., Kartha, G., Wang, Y.S., Parameswaran, K.N. 1986J. Am. Chem. Soc.10846374642CrossRefGoogle Scholar
  26. Lakomek, N.A., Farés, C., Becker, S., Carlomagno, T., Meiler, J., Griesinger, C. 2005Angew. Chem. Int. Ed.4477767778CrossRefGoogle Scholar
  27. Lienin, S.F., Bremi, T., Brutscher, B., Brueschweiler, R., Ernst, R.R. 1998J. Am. Chem. Soc.12098709879CrossRefGoogle Scholar
  28. Lindorff-Larsen, K., Best, R.B., Depristo, M.A., Dobson, C.M., Vendruscolo, M. 2005Nature433128132CrossRefADSGoogle Scholar
  29. Lipari, G., Szabo, A. 1982aJ. Am. Chem. Soc.10445464559Google Scholar
  30. Lipari, G., Szabo, A. 1982bJ. Am. Chem. Soc.10445594570Google Scholar
  31. Losonczi, J.A., Prestegard, J.H. 1998J. Biomol. NMR12447451CrossRefGoogle Scholar
  32. Massi, F., Grey, M.J., Palmer, A.G. 2005Protein Sci.14735742CrossRefGoogle Scholar
  33. Meiler, J., Peti, W., Griesinger, C. 2000J. Biomol. NMR17283294CrossRefGoogle Scholar
  34. Meiler, J., Peti, W., Prompers, J., Griesinger, C., Brueschweiler, R. 2001J. Am. Chem. Soc.12360986107CrossRefGoogle Scholar
  35. Meiler, J., Peti, W., Griesinger, C. 2003J. Am. Chem. Soc.12580728073CrossRefGoogle Scholar
  36. Mills, J.L., Szyperski, T. 2002J. Biomol. NMR236367CrossRefGoogle Scholar
  37. Miura, T., Klaus, W., Gsell, B., Miyamoto, C., Senn, H. 1999J. Mol. Biol.290213228CrossRefGoogle Scholar
  38. Nederveen, A.J., Bonvin, A.M.J.J. 2005J. Chem. Theory Comput.1363374CrossRefGoogle Scholar
  39. Ottiger, M., Delaglio, F., Bax, A. 1998J. Magn. Res.131373378CrossRefGoogle Scholar
  40. Palmer, A.G.,3rd 2004Chem. Rev.10436233640CrossRefGoogle Scholar
  41. Peti, W., Meiler, J., Brueschweiler, R., Griesinger, C. 2002J. Am. Chem. Soc.12458225833CrossRefGoogle Scholar
  42. Ramage, R., Green, J., Muir, T.W., Ogunjobi, O.M., Love, S., Shaw, K. 1994Biochem. J.299151158Google Scholar
  43. Ruckert, M., Otting, G. 2000J. Am. Chem. Soc.12277937797CrossRefGoogle Scholar
  44. Sass, H.J., Musco, G., Stahl, S.J., Wingfield, P.T., Grzesiek, S. 2000J. Biomol. NMR18303309CrossRefGoogle Scholar
  45. Schneider, D.M., Dellwo, M.J., Wand, A.J. 1992Biochemistry3136453652Google Scholar
  46. Sivaraman, T., Arrington, C.B., Robertson, A.D. 2001Nat. Struct. Biol.8331333CrossRefGoogle Scholar
  47. Tjandra, N., Feller, S.E., Pastor, R.W., Bax, A. 1995J. Am. Chem. Soc.1171256212566Google Scholar
  48. Tolman, J.R. 2001Curr. Opin. Struct. Biol.11532539CrossRefGoogle Scholar
  49. Tolman, J.R. 2002J. Am. Chem. Soc.1241202012030CrossRefGoogle Scholar
  50. Tolman, J.R., Flanagan, J.M., Kennedy, M.A., Prestegard, J.H. 1995Proc. Natl. Acad. Sci. U.S.A9292799283ADSGoogle Scholar
  51. Tolman, J.R., Prestegard, J.H. 1996aJ. Magn. Reson. B112245252Google Scholar
  52. Tolman, J.R., Prestegard, J.H. 1996bJ. Magn. Reson. B112269274Google Scholar
  53. Tolman, J.R., Flanagan, J.M., Kennedy, M.A., Prestegard, J.H. 1997Nat. Struct. Biol.4292297CrossRefGoogle Scholar
  54. Tolman, J.R., Al-Hashimi, H.M., Kay, L.E., Prestegard, J.H. 2001J. Am. Chem. Soc.12314161424CrossRefGoogle Scholar
  55. Tycko, R., Blanco, F.J., Ishii, Y. 2000J. Am. Chem. Soc.12293409341CrossRefGoogle Scholar
  56. Vijay Kumar, S., Bugg, C.E., Cook, W.J. 1987J. Mol. Biol.194531544Google Scholar
  57. Wilkinson, K.D., Laleli-Sahin, E., Urbauer, J., Larsen, C.N., Shih, G.H., Haas, A.L., Walsh, S.T., Wand, A.J. 1999J. Mol. Biol.29110671077Google Scholar
  58. Wist, J., Frueh, D., Tolman, J.R., Bodenhausen, G. 2004J. Biomol. NMR28263272CrossRefGoogle Scholar
  59. Zweckstetter, M., Bax, A. 2001J. Biomol. NMR20365377CrossRefGoogle Scholar
  60. Zweckstetter, M., Bax, A. 2002J. Biomol. NMR23127137CrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Nils A. Lakomek
    • 1
  • Teresa Carlomagno
    • 1
  • Stefan Becker
    • 1
  • Christian Griesinger
    • 1
  • Jens Meiler
    • 2
  1. 1.NMR based structural biologyMax Planck Institute for Biophysical ChemistryGoettingenGermany
  2. 2.Center of Structural Biology, Department of ChemistryVanderbilt UniversityNashvilleUSA

Personalised recommendations