Quantitative NMR studies of high molecular weight proteins: Application to domain orientation and ligand binding in the 723 residue enzyme malate synthase G

Journal of Molecular Biology

Volumn 327, Issue 5, 2003, Pages 1121-1133

  Tugarinov, Vitali ^a   Kay, Lewis E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Dipolar couplings; Ligand binding; Malate synthase G; Multi dimensional NMR; Protein domains

Indexed keywords

ACETIC ACID DERIVATIVE; ACETYL COENZYME A; CARBONYL DERIVATIVE; GLYOXYLIC ACID; MALATE SYNTHASE; MALATE SYNTHASE G; MONOMER; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CATALYSIS; CITRIC ACID CYCLE; CONTROLLED STUDY; ESCHERICHIA COLI; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; X RAY ANALYSIS;

ESCHERICHIA COLI;

EID: 0037432547     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00238-9     Document Type: Article

References (56)

1. I. Molina, M.T. Pellicer, J. Badia, J. Aguilar and L. Baldoma, Molecular characterization of Escherichia coli malate synthase G. Differentiation with the malate synthase A isoenzyme. Eur. J. Biochem. 224 (1994), pp. 541-548.
2. J.W. Comforth, J.W. Redmond, H. Eggerer, W. Buckel and C. Gutschow, Asymmetric methyl groups, and the mechanism ofmalate synthase. Nature 221 (1969), pp. 1212-1213.
3. J. Luthy, J. Retey and D. Arigoni, Preparation and detection of chiral methyl groups. Nature 221 (1969), pp. 1213-1215.
4. B.R. Howard, J.A. Endrizzi and S.J. Remington, Crystal structure of Escherichia coli malate synthase G complexed with magnesium and glyoxylate at 2.0 Å resolution: mechanistic implications. Biochemistry 39 (2000), pp. 3156-3168.
5. G. Schmid, H. Durchschlag, G. Biedermann, H. Eggerer and R. Jaenicke, Molecular structure ofmalate synthase and structural changes upon ligand binding to the enzyme. Biochem. Biophys. Res. Commun. 58 (1974), pp. 419-426.
6. S. Beeckmans, A.S. Khan, L. Kanarek and E. Van Driessche, Ligand binding to maize (Zea mays) malate synthase: a structural study. Biochem. J. 303 (1994), pp. 413-421.
7. P. Zipper and H. Durchschlag, Small-angle X-ray studies on malate synthase from baker's yeast. Biochem. Biophys. Res. Commun. 75 (1977), pp. 394-400.
8. T.M. Larsen, L.T. Laughlin, H.M. Holden, I. Rayment and G.H. Reed, Structure of rabbit muscle pyruvate kinase complexed with Mtr2+, K+, and pyruvate. Biochemistry 33 (1994), pp. 6301-6309.
9. T.M. Larsen, L.T. Laughlin, H.M. Holden, I. Rayment and G.H. Reed, Ligand-induced domain movement in pymvate kinase: structure of the enzyme from rabbit muscle with Mg2+, K+, and -phospholactate at 2.7 Å resolution. Arch. Biochem. Biophys. 345 (1997), pp. 199-206.
10. S.J. Remington, G. Wiegand and R. Huber, Crystallographic refinement and atomic models of two different forms of citrate synthase at 2.7 and 1.7 Å resolution, J. Mol. Biol. 158 (1982), pp. 111-152.
11. V. Tugarinov, R. Muhandiram, A. Ayed and L.E. Kay, Four-dimensional NMR spectroscopy of a 723-residue protein: chemical shift assignments and secondary structure ofmalate synthase G. J. Am. Chem. Soc. 124 (2002), pp. 10025-10035.
12. N. Tjandra and A. Bax, Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278 (1997), pp. 1111-1114.
13. M.R. Hansen, L. Mueller and A. Pardi, Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nature Struct. Biol. 5 (1998), pp. 1065-1074.
14. G.M. Clore, M.R. Starich and A.M. Gronenborn, 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 (1998), pp. 10571-10572.
15. M. Ottiger and A. Bax, Bicelle-based liquid crystals for NMR-measurement of dipolar couplings at acidic and basic pH values. J. Biomol. NMR 13 (1999), pp. 187-191.
16. M. Ruckert and G. Otting, Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments, J. Am. Chem. Soc. 122 (2000), pp. 7793-7797.
17. M. Ottiger, F. Delaglio and A. Bax, Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131 (1998), pp. 373-378.
18. 2H-labeled proteins. J. Biomol. NMR 14 (1999), pp. 333-343.
19. G. Kontaxis, G.M. Clore and A. Bax, Evaluation of cross-correlation effects and measurement of one-bond couplings in proteins with short transverse relaxation times. J. Magn. Reson. 143 (2000), pp. 184-196.
20. 2H)-labeled proteins. J. Biomol. NMR 17 (2000), pp. 43-54.
21. M.W. Fischer, J.A. Losonczi, J.L. Weaver and J.H. Prestegard, Domain orientation and dynamics in multidomain proteins from residual dipolar couplings. Biochemistry 38 (1999), pp. 9013-9022.
22. N.R. Skrynnikov, N.K. Goto, D. Yang, W.Y. Choy, J.R. Tolman, G.A. Mueller and L.E. Kay, Orienting domains in proteins using dipolar couplings measured by liquid-state NMR: differences in solution and crystal forms ofmaltodextrin binding protein loaded with -cyclodextrin. J. Mol. Biol. 295 (2000), pp. 1265-1273.
23. J. Evenas, V. Tugarinov, N.R. Skrynnikov, N.K. Goto, R. Muhandiram and L.E. Kay, Ligand-induced structural changes to maltodextrin-binding protein as studied by solution NMR spectroscopy, J. Mol. Biol. 309 (2001), pp. 961-974.
24. 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 (1997), pp. 12366-12371.
25. E.W. Bastiaan, C. MacLean, P.C.M. van Zijl and A.A. Bothner-By, High resolution NMR of liquids and gases: effects of magnetic-field-induced molecular alignment. Annu. Rep. NMR Spectrosc. 9 (1987), pp. 3635-3677.
26. J.R. Tolman, J.M. Flanagan, M.A. Kennedy and J.H. Prestegard, Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc. Natl Acad. Sci. 92 (1995), pp. 9279-9283.
27. 15N enriched human ubiquitin resulting from relaxation interference and residual dipolar coupling, d. Am. Chem. Soc. 118 (1996), pp. 6264-6272.
28. 15N chemical shifts in a protein-DNA complex resulting from magnetic ordering in solution, J. Am. Chem. Soc. 119 (1997), pp. 9825-9830.
29. G. Cornilescu, J. Marquardt, M. Ottiger and A. Bax, Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase, J. Am. Chem. Soc. 120 (1998), pp. 6836-6837.
30. 15N chemical shifts in dilute bicelle, solution, J. Am. Chem. Soc. 121 (1999), pp. 7441-7442.
31. W.Y. Choy, M. Tollinger, G.A. Mueller and L.E. Kay, Direct structure refinement of high molecular weight proteins against residual dipolar couplings and carbonyl chemical shift changes upon alignment: an application to maltose binding protein, J. Biomol. NMR 21 (2001), pp. 31-40.
32. R.S. Lipsitz and N. Tjandra, Carbonyl CSA restraints from solution NMR for protein structure refinement, J. Am. Chem. Soc. 123 (2001), pp. 11065-11066.
33. 31P chemical shift anisotropy as an aid in determining nucleic acid structure in liquid crystals. J. Am. Chem. Soc. 123 (2001), pp. 3617-3618.
34. 14N electric field gradient tensor orientations with respect to the molecular frame in a polypeptide, J. Am. Chem. Soc. 114 (1992), pp. 5312-5321.
35. 1HN-detected triple resonance TROSY-based experiments, J. Biomol. NMR 13 (1999), pp. 3-10.
36. M. Salzmann, K. Pervushin, G. Wider, H. Senn and K. Wtithrich, TROSY in tripleresonance experiments: new perspectives for sequential NMR assignment of large proteins. Proc. Natl Acad. Sci. USA 95 (1998), pp. 13585-13590.
37. F.A.A. Mulder, D. Schipper, R. Bott and R. Boelens, Altered flexibility in the substrate-binding site of related natve and engineered high-alkaline Bacillus subtilisins. J. Mol. Biol. 292 (1999), pp. 111-123.
38. T.L. Hwang, P.C. van Zijl and S. Mori, Accurate quantitation ofwater-amide proton exchange rates using the phase-modulated CLEAN chemical EXchange (CLEANEXPM) approach with a Fast-HSQC (FHSQC) detection scheme. J. Biomol. NMR 11 (1998), pp. 221-226.
39. A.G. Palmer, C.D. Kroenke and J.P. Loria, NMR methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 339 (2001), pp. 204-238.
40. J. Sandstrom. Dynamic NMR Spectroscopy, Academic Press, New York (1982).
41. M. Hensmann, G.W. Booker, G. Panayotou, J. Boyd, J. Linacre, M. Waterfield and I.D. Campbell, Phosphopeptide binding to the N-terminal SH2 domain of the p85 alpha subunit of PI 3′-kinase: a heteronuclear NMR study. Protein Sci. 3 (1994), pp. 1020-1030.
42. U.L. Günther and B. Schaffhausen, NMRKIN: simulating lineshapes from twodimensional spectra of proteins upon ligand binding. J. Biomol. NMR 22 (2002), pp. 201-209.
43. A. Fersht. Enzyme Structure and Mechanism (2nd edit. ed.), Freeman, Co, New York (1985).
44. V.A. Feher, E.P. Baldwin and F.W. Dahlquist, Access of ligands to cavities within the core of a protein is rapid. Nature Struct. Biol. 3 (1996), pp. 516-521.
45. J.H. Prestegard, New techniques in structural NMR - anisotropic interactions. Nature Struct. Biol. NMR supplement 5 (1998), pp. 517-522.
46. M. Zweckstetter and A. Bax, Characterization of molecular alignment in aqueous suspensions of Pfl bacteriophage. J. Biomol. NMR 20 (2001), pp. 365-377.
47. D.S. Garrett, R. Powers, A.M. Gronenborn and G.M. Clore, A common sense approach to peak picking in two-, three-, and four-dimensional spectra using at@omatic computer analysis of contour diagrams. J. Magn. Reson. 95 (1991), pp. 214-220.
48. D. Yang and L.E. Kay, Improved lineshape and sensitivity in the HNCO-family of triple-resonance experiments. J. Biomol. NMR 14 (1999), pp. 273-276.
49. D. Yang and L.E. Kay, TROSY triple resonance four-dimensional NMR spectroscopy of a 46 ns tumbling protein. J. Am. Chem. Soc. 121 (1999), pp. 2571-2575.
50. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer and A. Bax, NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995), pp. 277-293.
51. B.A. Johnson and R.A. Blevins, NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994), pp. 603-614.
52. 15N NMR relaxation. Biochemistry 33 (1994), pp. 5984-6003.
53. P.E. Johnson, P. Tomme, M.D. Joshi and L.P. Mclntosh, Interaction of soluble cellooligosaccharides with the N-terminal cellulose-binding domain of Cellulomonas fimi CenC 2. NMR and ultraviolet absorption spectroscopy. Biochemistry 35 (1996), pp. 13895-13906.
54. G.S. Huang and T.G. Oas, Submillisecond folding ofmonomefic repressor. Proc. Natl Acad. Sci. USA 92 (1995), pp. 6878-6882.
55. R.E. Burton, R.S. Busby and T.G. Oas, ALASKA: a mathematica package for twostate kinetic analysis of protein folding reactions. J. Biomol. NMR 11 (1998), pp. 355359.
56. R. Koradi, M. Billeter and K. Wüthrich, MOLMOL: a program for display and analysis ofmacromolecular structures. J. Mol. Graph. 14 (1996), pp. 51-55.