Measuring 13Cβ chemical shifts of invisible excited states in proteins by relaxation dispersion NMR spectroscopy

Journal of Biomolecular NMR

Volumn 44, Issue 3, 2009, Pages 139-155

  Lundström, Patrik ^a   Lin, Hong ^b   Kay, Lewis E ^c  

^a LINKÖPING UNIVERSITY   (Sweden)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

13C Chemical shifts; Chemical exchange; CPMG; Excited protein states; Selective labeling

Indexed keywords

GLUCOSE; SUCCINATE DEHYDROGENASE; CARBON; ESCHERICHIA COLI PROTEIN;

ACCURACY; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBON SOURCE; CONTROLLED STUDY; DISPERSION; ENZYME CONFORMATION; ESCHERICHIA COLI; INTERMETHOD COMPARISON; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; BIOLOGICAL MODEL; CHEMISTRY; CITRIC ACID CYCLE; ENZYMOLOGY; GENETICS; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY;

CARBON ISOTOPES; CITRIC ACID CYCLE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL;

EID: 67649392285     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-009-9321-3     Document Type: Article

References (80)

1. Boehr DD, McElheny D, Dyson HJ, Wright PE (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313:1638-1642
2. Bystrov VF (1976) Spin-spin coupling and the conformational states of peptide systems. Prog Nucl Mag Res Spectrosc 10:41-82
3. Carr HY, Purcell EM (1954) Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 94:630-638
4. Castellani F, van Rossum B, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420:98-102
5. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289-302
6. Cronan JE, LaPorte DC (1996) Tricarboxylic cycle and glyoxylate bypass. In: Neidhardt FC, Curtiss R (eds) Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington D.C., pp 206-216
7. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645
8. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe - a multidimensional spectral processing system based on unix pipes. J Biomol NMR 6:277-293
9. Drubin DG, Mulholland J, Zhu ZM, Botstein D (1990) Homology of a yeast actin-binding protein to signal transduction proteins and myosin-I. Nature 343:288-290
10. Eisenmesser EZ, Bosco DA, Akke M, Kern D (2002) Enzyme dynamics during catalysis. Science 295:1520-1523
11. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE, Kern D (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438:117-121
12. Farmer BT, Venters RA (1999) NMR of perdeuterated larger proteins. In: Krishna NR, Berliner LJ (eds) Biological magnetic resonance, vol 16. Kluwer Academic/Plenum Publishers, New York, pp 75-120
13. Freeman R (1999) Spin choreography - basic steps in high resolution NMR. Oxford University Press, Oxford, p 123
14. 15N multidimensional NMR to study the structure and dynamics of proteins. Annu Rev Biophys Biomol Struct 27:357-406
15. Geen H, Freeman R (1991) Band-selective radiofrequency pulses. J Magn Reson 93:93-141
16. 2H- labeled proteins. J Biomol NMR 13:369-374
17. Gronostajski RM, Sadowski PD (1985) The Flp protein of the 2-micron plasmid of yeast - intermolecular and intramolecular reactions. J Biol Chem 260:2328-2335
18. Gross JD, Gelev VM, Wagner G (2003) A sensitive and robust method for obtaining intermolecular NOEs between side chains in large protein complexes. J Biomol NMR 25:235-242
19. 15N-enriched proteins - application to triple-resonance 4D J-connectivity of sequential amides. J Am Chem Soc 115:4369-4370
20. Hahn EL, Maxwell DE (1952) Spin echo measurements of nuclear spin coupling in molecules. Phys Rev 88:1070-1084
21. 13C α dipolar couplings of invisible protein states by spin-state selective relaxation dispersion NMR spectroscopy. J Am Chem Soc 130:8397-8405
22. Hansen DF, Vallurupalli P, Lundström P, Neudecker P, Kay LE (2008b) Probing chemical shifts of invisible states of proteins with relaxation dispersion NMR spectroscopy: How well can we do? J Am Chem Soc 130:2667-2675
23. Haynes J, Garcia B, Stollar EJ, Rath A, Andrews BJ, Davidson AR (2007) The biologically relevant targets and binding affinity requirements for the function of the yeast actin-binding protein 1 Src-homology 3 domain vary with genetic context. Genetics 176:193-208
24. 13C NMR spin relaxation. J Am Chem Soc 122:11610-11619
25. Igumenova TI, Brath U, Akke M, Palmer AG (2007) Characterization of chemical exchange using residual dipolar coupling. J Am Chem Soc 129:13396-13397
26. Ikura M, Bax A (1992) Isotope-filtered 2D NMR of a protein peptide complex - study of a skeletal-muscle myosin light chain kinase fragment bound to calmodulin. J Am Chem Soc 114:2433-2440
27. Ishima R, Torchia DA (2003) Extending the range of amide proton relaxation dispersion experiments in proteins using a constant-time relaxation-compensated CPMG approach. J Biomol NMR 25:243-248
28. Ishima R, Baber J, Louis JM, Torchia DA (2004) Carbonyl carbon transverse relaxation dispersion measurements and ms-μs timescale motion in a protein hydrogen bond network. J Biomol NMR 29:187-198
29. Kainosho M, Torizawa T, Iwashita Y, Terauchi T, Ono AM, Guntert P (2006) Optimal isotope labelling for NMR protein structure determinations. Nature 440:52-57
30. Kay LE, Torchia DA, Bax A (1989) Backbone dynamics of proteins as studied by 15 N inverse detected heteronuclear NMR-spectroscopy - application to staphylococcal nuclease. Biochemistry 28:8972-8979
31. Kay LE, Clore GM, Bax A, Gronenborn AM (1990a) 4-Dimensional heteronuclear triple-resonance NMR spectroscopy of interleukin-1-beta in solution. Science 249:411-414
32. Kay LE, Ikura M, Tschudin R, Bax A (1990b) 3-Dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. J Magn Reson 89:496-514
33. Korzhnev DM, Salvatella X, Vendruscolo M, Di Nardo AA, Davidson AR, Dobson CM, Kay LE (2004) Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430:586-590
34. Korzhnev DM, Neudecker P, Mittermaier A, Orekhov VY, Kay LE (2005) Multiple-site exchange in proteins studied with a suite of six NMR relaxation dispersion experiments: An application to the folding of a Fyn SH3 domain mutant. J Am Chem Soc 127:15602-15611
35. Lee LK, Rance M, Chazin WJ, Palmer AG (1997) Rotational diffusion anisotropy of proteins from simultaneous analysis of N-15 and C-13(alpha) nuclear spin relaxation. J Biomol NMR 9:287-298
36. LeMaster DM (1990) Deuterium labeling in NMR structural analysis of larger proteins. Q Rev Biophys 23:133-174
37. 13C NMR relaxation analysis. J Am Chem Soc 118:9255-9264
38. Levitt MH (1986) Composite pulses. Prog Nucl Mag Res Spectrosc 18:61-122
39. Li M, Ho PY, Yao SJ, Shimizu K (2006) Effect of sucA or sucC gene knockout on the metabolism in Escherichia coli based on gene expressions, enzyme activities, intracellular metabolite concentrations and metabolic fluxes by C-13-labeling experiments. Biochem Eng J 30:286-296
40. Lila T, Drubin DG (1997) Evidence for physical and functional interactions among two Saccharomyces cerevisiae SH3 domain proteins, an adenylyl cyclase-associated protein and the actin cytoskeleton. Mol Biol Cell 8:367-385
41. Löhr F, Rüterjans H (1998) Detection of nitrogen-nitrogen J-couplings in proteins. J Magn Reson 132:130-137
42. Loria JP, Rance M, Palmer AG (1999) A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J Am Chem Soc 121:2331-2332
43. Lundström P, Teilum K, Carstensen T, Bezsonova I, Wiesner S, Hansen DF, Religa TL, Akke M, Kay LE (2007a) Fractional 13C enrichment of isolated carbons using [1-13C]- or [2-13C]-glucose facilitates the accurate measurement of dynamics at backbone Ca and side-chain methyl positions in proteins. J Biomol NMR 38:199-212
44. 13C-relaxation dispersion experiment with improved sensitivity. J Biomol NMR 38:79-88
45. 13C labeled samples. J Biomol NMR 42:35-47
46. Lundström P, Hansen DF, Vallurupalli P, Kay LE (2009) Accurate measurement of alpha proton chemical shifts of excited protein states by relaxation dispersion NMR spectroscopy. J Am Chem Soc 131:1915-1926
47. Marion D, Ikura M, Tschudin R, Bax A (1989) Rapid recording of 2D NMR-spectra without phase cycling - application to the study of hydrogen-exchange in proteins. J Magn Reson 85:393-399
48. Meiboom S, Gill D (1958) Modified spin-echo method for measuring nuclear relaxation times. Rev Sci Instrum 29:688-691
49. Molenaar D, Van der Rest ME, Petrovic S (1998) Biochemical and genetic characterization of the membrane-associated malate dehydrogenase (acceptor) from Corynebacterium glutamicum. Eur J Biochem 254:395-403
50. 15N triple-resonance experiments. J Magn Reson 87:183-188
51. Mulder FAA, Mittermaier A, Hon B, Dahlquist FW, Kay LE (2001a) Studying excited states of proteins by NMR spectroscopy. Nat Struct Biol 8:932-935
52. 15N relaxation dispersion NMR spectroscopy: application to Asn and Gln residues in a cavity mutant of T4 lysozyme. J Am Chem Soc 123:967-975
53. Mulder FAA, Hon B, Mittermaier A, Dahlquist FW, Kay LE (2002) Slow internal dynamics in proteins: Application of NMR relaxation dispersion spectroscopy to methyl groups in a cavity mutant of T4 lysozyme. J Am Chem Soc 124:1443-1451
54. Palmer AG, Kroenke CD, Loria JP (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339:204-238
55. Palmer AG, Grey MJ, Wang CY (2005) Solution NMR spin relaxation methods for characterizing chemical exchange in high-molecular-weight systems. Methods Enzymol 394:430-465
56. Press WH, Flannery BP, Teukolsky SA and Vetterling WT (1988) Numerical recipes in C. University Press, Cambridge
57. Rath A, Davidson AR (2000) The design of a hyperstable mutant of the Abp1p SH3 domain by sequence alignment analysis. Protein Sci 9:2457-2469
58. Sattler M, Schleucher J, Griesinger C (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog Nucl Mag Res Spectrosc 34:93-158
59. Shaka AJ, Barker PB, Freeman R (1985) Computer-optimized decoupling scheme for wideband applications and low-level operation. J Magn Reson 64:547-552
60. Shen Y, Bax A (2007) Protein backbone chemical shifts predicted from searching a database for torsion angle and sequence homology. J Biomol NMR 38:289-302
61. Skrynnikov NR, Dahlquist FW, Kay LE (2002) Reconstructing NMR spectra of "invisible" excited protein states using HSQC and HMQC experiments. J Am Chem Soc 124:12352-12360
62. 13C nuclear magnetic resonance chemical shifts. J Am Chem Soc 113:5490-5492
63. Studier FW, Moffatt BA (1986) Use of bacteriophage-T7 RNA-polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189:113-130
64. Sugase K, Dyson HJ, Wright PE (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447:1021-1025
65. Tollinger M, Skrynnikov NR, Mulder FAA, Forman-Kay JD, Kay LE (2001) Slow dynamics in folded and unfolded states of an SH3 domain. J Am Chem Soc 123:11341-11352
66. Tugarinov V, Kay LE (2004) An isotope labeling strategy for methyl TROSY spectroscopy. J Biomol NMR 28:165-172
67. Vallurupalli P, Kay LE (2006) Complementarity of ensemble and single-molecule measures of protein motion: A relaxation dispersion NMR study of an enzyme complex. Proc Natl Acad Sci USA 103:11910-11915
68. Vallurupalli P, Hansen DF, Stollar E, Meirovitch E, Kay LE (2007) Measurement of bond vector orientations in invisible excited states of proteins. Proc Natl Acad Sci USA 104:18473-18477
69. Vallurupalli P, Hansen DF, Kay LE (2008a) Probing structure in invisible protein states with anisotropic NMR chemical shifts. J Am Chem Soc 130:2734-2735
70. Vallurupalli P, Hansen DF, Kay LE (2008b) Structures of invisible, excited protein states by relaxation dispersion NMR spectroscopy. Proc Natl Acad Sci USA 105:11766-11771
71. 13C α chemical shifts in the 'invisible' excited states of proteins. J Biomol NMR. doi 10.1007/s10858-009-9310-6
72. Voet D, Voet JG (1995) Biochemistry. Wiley, Hoboken
73. 13C-enriched proteins. J Magn Reson B 108:173-175
74. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s (218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523-1526
75. Watt ED, Shimada H, Kovrigin EL, Loria JP (2007) The mechanism of rate-limiting motions in enzyme function. Proc Natl Acad Sci USA 104:11981-11986
76. Wishart DS, Case DA (2002) Use of chemical shifts in macromolecular structure determination. Methods Enzymol 338:3-34
77. 13C chemical-shift data. J Biomol NMR 4:171-180
78. Wolf-Watz M, Thai V, Henzler-Wildman K, Hadjipavlou G, Eisenmesser EZ, Kern D (2004) Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat Struct Mol Biol 11:945-949
79. Zeeb M, Balbach J (2005) NMR spectroscopic characterization of millisecond protein folding by transverse relaxation dispersion measurements. J Am Chem Soc 127:13207-13212
80. 1H] HMQC-NOE-HMQC NMR-spectroscopy - resolving tertiary NOE distance constraints in the spectra of larger proteins. J Am Chem Soc 113:370-372