Solution NMR of supramolecular complexes: Providing new insights into function

Nature Methods

Volumn 4, Issue 9, 2007, Pages 697-703

  Sprangers, Remco ^a   Velyvis, Algirdas ^a   Kay, Lewis E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 13; DEUTERIUM; ISOLEUCINE; LEUCINE; NITROGEN 15; PROTEASOME; PROTON; VALINE;

ARTICLE; ISOTOPE LABELING; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PROBE; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; SIGNAL DETECTION;

ASPARTATE CARBAMOYLTRANSFERASE; ENDOPEPTIDASE CLP; ISOTOPE LABELING; LIGANDS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS;

EID: 34548304719     PISSN: 15487091     EISSN: 15491676     Source Type: Journal    
DOI: 10.1038/nmeth1080     Document Type: Article

References (48)

1. Wüthrich, K. NMR of Proteins and Nucleic Acids (John Wiley & Sons, New York, 1986).
2. Bax, A. Weak alignment offers new NMR opportunities to study protein structure and dynamics. Protein Sci. 12, 1-16 (2003).
3. Wider, G. & Wüthrich, K. NMR spectroscopy of large molecules and multimolecular assemblies in solution. Curr. Opin. Struct. Biol. 9, 594-601 (1999).
4. Bax, A. Multidimensional nuclear magnetic resonance methods for protein studies. Curr. Opin. Struct. Biol. 4, 738-744 (1994).
5. 15N multidimensional NMR to study the structure and dynamics of proteins. Annu. Rev. Biophys. Biomol. Struct. 27, 357-406 (1998).
6. Farmer, B.T. & Venters, R.A. in Biological Magnetic Resonance (eds. Krishna, N.R. & Berliner, L.J.) 75-120 (Kluwer/Plenum, New York, 1998).
7. 2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 94, 12366-12371 (1997).
8. Fiaux, J., Bertelsen, E.B., Horwich, A.L. & Wüthrich, K. NMR analysis of a 900K GroEL-GroES complex. Nature 418, 207-221 (2002).
9. Tjandra, N. & Bax, A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278, 1111-1114 (1997).
10. Tolman, J.R., Flanagan, J.M., Kennedy, M.A. & Prestegard, J.H. Nuclear magnetic dipole interactions in field-oriented proteins: Information for structure determination in solution. Proc. Natl. Acad. Sci. USA 92, 9279-9283 (1995).
11. Tugarinov, V., Choy, W.Y., Orekhov, V.Y. & Kay, L.E. Solution NMR-derived global fold of a monomeric 82-kDa enzyme. Proc. Natl. Acad. Sci. USA 102, 622-627 (2005).
12. Palmer, A.G., Williams, J. & McDermott, A. Nuclear magnetic resonance studies of biopolymer dynamics. J. Phys. Chem. 100, 13293-13310 (1996).
13. Mittermaier, A. & Kay, L.E. New tools provide new insights in NMR studies of protein dynamics. Science 312, 224-228 (2006).
14. Goto, N.K. & Kay, L.E. New developments in isotope labeling strategies for protein solution NMR spectroscopy. Curr. Opin. Struct. Biol. 10, 585-592 (2000).
15. Clore, G.M. & Gronenborn, A.M. Structures of larger proteins in solution: Three-and four-dimensional heteronuclear NMR spectroscopy. Science 252, 1390-1399 (1991).
16. LeMaster, D.M. & Richards, F.M. NMR sequential assignment of Escherichia coli thioredoxin utilizing random fractional deuteration. Biochemistry 27, 142-150 (1988).
17. 15N-enriched proteins. Applications to triple resonance 4D J-connectivity of sequential amides. J. Am. Chem. Soc. 115, 4369-4370 (1993).
18. Tugarinov, V. & Kay, L.E. An isotope labeling strategy for methyl TROSY spectroscopy. J. Biomol. NMR 28, 165-172 (2004).
19. Janin, J., Miller, S. & Chothia, C. Surface, subunit interfaces and interior of oligomeric proteins. J. Mol. Biol. 204, 155-164 (1988).
20. Dalvit, C. & Stockman, B.J. NMR screening techniques in drug discovery and drug design. Prog. Nucl. Magn. Reson. Spectrosc. 41, 187-231 (2002).
21. Gardner, K.H., Rosen, M.K. & Kay, L.E. Global folds of highly deuterated, methyl protonated proteins by multidimensional NMR. Biochemistry 36, 1389-1401 (1997).
22. Zheng, D. et al. Automated protein fold determination using a minimal NMR constraint strategy. Protein Sci. 12, 1232-1246 (2003).
23. 13C NMR spectroscopy. Application to the leucine residues of staphylococal nuclease. Biochemistry 31, 5253-5263 (1992).
24. 2H NMR relaxation studies of the 723-residue enzyme malate synthase G reveal a dynamic binding interface. Biochemistry 44, 15970-15977 (2005).
25. 2H-labeled proteins. J. Biomol. NMR 13, 369-374 (1999).
26. Lowe, J. et al. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268, 533-539 (1995).
27. McCaldon, P. & Argos, P. Oligopeptide biases in protein sequences and their use in predicting protein coding regions in nucleotide sequences. Proteins 4, 99-122 (1988).
28. Ernst, R.R., Bodenhausen, G. & Wokaun, A. Principles of Nuclear Magnetic Resonance in One and Two Dimensions (Oxford University Press, Oxford, UK, 1987).
29. 13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J. Am. Chem. Soc. 125, 10420-10428 (2003).
30. Sprangers, R., Gribun, A., Hwang, P.M., Houry, W.A. & Kay, L.E. Quantitative NMR spectroscopy of supramolecular complexes: Dynamic side pores in ClpP are important for product release. Proc. Natl. Acad. Sci. USA 102, 16678-16683 (2005).
31. Sprangers, R. & Kay, L.E. Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445, 618-622 (2007).
32. Kainosho, M. et al. Optimal isotope labelling for NMR protein structure determinations. Nature 440, 52-57 (2006).
33. Velyvis, A., Yang, Y.R., Schachman, H.K. & Kay, L.E. A solution NMR study showing that active site ligands and nucleotides directly perturb the allosteric equilibrium in aspartate transcarbamoylase. Proc. Natl. Acad. Sci. USA (2007).
34. Schachman, H.K. Can a simple model account for the allosteric transition of aspartate transcarbamoylase? J. Biol. Chem. 263, 18583-18586 (1988).
35. Wang, J., Harting, J.A. & Flanagan, J.M. The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell 91, 447-456 (1997).
36. Ortega, J., Singh, S.K., Ishikawa, T., Maurizi, M.R. & Steven, A.C. Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. Mol. Cell 6, 1515-1521 (2000).
37. Choi, K.H. & Licht, S. Control of peptide product sizes by the energy-dependent protease ClpAP. Biochemistry 44, 13921-13931 (2005).
38. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. J. Biomol. NMR 4, 727-734 (1994).
39. Montelione, G.T. & Wagner, G. 2D chemical-exchange NMR-spectroscopy by proton detected heteronuclear correlation. J. Am. Chem. Soc. 111, 3096-3098 (1989).
40. Palmer, A.G., III, Grey, M.J. & Wang, C. Solution NMR spin relaxation methods for characterizing chemical exchange in high-molecular-weight systems. Methods Enzymol. 394, 430-465 (2005).
41. Korzhnev, D.M., Kloiber, K., Kanelis, V., Tugarinov, V. & Kay, L.E. Probing slow dynamics in high molecular weight proteins by methyl-TROSY NMR spectroscopy: Application to a 723-residue enzyme. J. Am. Chem. Soc. 126, 3964-3973 (2004).
42. Gribun, A. et al. The ClpP double ring tetradecameric protease exhibits plastic ring-ring interactions, and the N termini of its subunits form flexible loops that are essential for ClpXP and ClpAP complex formation. J. Biol. Chem. 280, 16185-16196 (2005).
43. Goldberg, A.L., Gaczynska, M., Grant, E., Michalek, M. & Rock, K.L. Functions of the proteasome in antigen presentation. Cold Spring Harb. Symp. Quant. Biol. 60, 479-490 (1995).
44. Pickart, C.M. & Cohen, R.E. Proteasomes and their kin: Proteases in the machine age. Nat. Rev. Mol. Cell Biol. 5, 177-187 (2004).
45. Goldberg, A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895-899 (2003).
46. Tugarinov, V., Sprangers, R. & Kay, L.E. Probing side-chain dynamics in the proteasome by relaxation violated coherence transfer NMR spectroscopy. J. Am. Chem. Soc. 129, 1743-1750 (2007).
47. Gavin, A.C. et al. Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636 (2006).
48. Whitby, F.G. et al. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408, 115-120 (2000).