Characterizing the use of perdeuteration in NMR studies of large proteins: 13C, 15N and 1H assignments of human carbonic anhydrase II

Journal of Molecular Biology

Volumn 264, Issue 5, 1996, Pages 1101-1116

  Venters, Ronald A ^a   Farmer II, Bennett T ^b   Fierke, Carol A ^c   Spicer, Leonard D ^a,c  

^a DUKE UNIVERSITY   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Carbonic anhydrase; Isotope shifts; NMR assignments; Perdeuteration; Secondary structure

Indexed keywords

CARBONATE DEHYDRATASE II; DEUTERIUM; NITROGEN 15;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; ENZYME STRUCTURE; HUMAN; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

EID: 0030596171     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0699     Document Type: Article

References (73)

1. 1H NMR assignments and secondary structure in solution of Escherichia coli trp repressor. Biochemistry, 29, 6332-6341.
2. Barlow, P. N., Steinkasserer, A., Norman, D. G., Kieffer, B., Wiles, A. P., Sim, R. B. & Campbell, I. D. (1993). Solution structure of a pair of complement modules by nuclear magnetic resonance. J. Mol. Biol. 232, 268-284.
3. Bax, A. & Grzesiek, S. (1993). Methodological advances in protein NMR. Acc. Chem. Res. 26, 131-138.
4. Bax, A. & Ikura, M. (1991). An efficient 3D NMR technique for correlating the proton and nitrogen-15 backbone amide resonance with the α-carbon of the preceding residue in uniformly nitrogen-15/carbon-13 enriched proteins. J. Biomol. NMR, 1, 99-104.
5. 15N NMR: comparisons with X-ray data for the Fab. Proteins: Struct. Funct. Genet. 15, 290-311.
6. Davis, J. H., Bradley, E. K., Miljanich, G. P., Nadasdi, L., Ramachandran, J. & Basus, V. J. (1993). Solution structure of ω-conotoxin GVIA using 2-D NMR spectroscopy and relaxation matrix analysis. Biochemistry, 32, 7396-7405.
7. Dayie, K. T. & Wagner, G. (1995). Carbonyl-carbon relaxation rates reveal a dynamic heterogeneity of the polypeptide backbone in villin 14T. J. Magn. Reson. ser. B, 109, 105-108.
8. Dodgson, S. J. (1991). The carbonic anhydrases: Overview of their importance in cellular physiology and in molecular genetics. In The Carbonic Anhydrase: Cellular Physiology and Molecular Genetics (Dodgson, S. J., Tashian, R. E., Gros, G. & Carter, N. D., eds), pp. 3-14, Plenum Press, New York.
9. 13C resonances in perdeuterated proteins. J. Am. Chem. Soc. 117, 4187-4188.
10. 15N resonances in perdeuterated proteins. J. Biomol. NMR, 7, 59-71.
11. + binding site on the MurB enzyme by NMR. Nat. Struct. Biol. In the press.
12. 15N backbone assignments of the 269-residue serine protease PB92 from Bacillus alcalophilus. J. Biomol. NMR, 4, 123-128.
13. β resonances. J. Biomol. NMR, 4, 703-726.
14. 15N-enriched proteins. J. Biomol. NMR, 3, 185-204.
15. Grzesiek, S. & Bax, A. (1994). Deuterium, relaxation, and protein NMR; presented at the XVIth International Conference on Magnetic Resonance in Biological Systems; Veldhoven, The Netherlands, 1994.
16. 15N-enriched proteins. Application to triple resonance 4D J connectivity of sequential amides. J. Am. Chem. Soc. 115, 4369-4370.
17. 14N NMR study of glycine. J. Am. Chem. Soc. 103, 2534-2539.
18. Hakansson, K., Carlsson, M., Svensson, L. A. & Liljas, A. (1992). Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes. J. Mol. Biol. 227, 1192-1204.
19. Hansen, P. E. (1988). Isotope effects in nuclear shielding. Prog. NMR Spectrosc. 20, 207-255.
20. 15N spectra of larger proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry, 29, 4659-4667.
21. Johnson, M. L. (1983). Evaluation and propagation of confidence intervals in nonlinear, asymmetrical variance spaces. Biophys. J. 44, 101-106.
22. Jönsson, P. G. & Kvich, A. (1972). Precision neuron diffraction structure determination of protein and nucleic acid components. III. The crystal and molecular structure of the amino acid α-glycine. Acta Crystallogr. sect. B, 28, 1827-1833.
23. Kallan, J., Spitzfaden, C., Zurini, M. G., Wider, G., Widmer, H., Wüthrich, K. & Walkinshaw, M. D. (1991). Structure of human cyclophilin and its binding site for cyclosporin A determined by X-ray crystallography and NMR spectroscopy. Nature, 353, 276-279.
24. Kay, L. E., Ikura, M., Tschudin, R. & Bax, A. (1990). Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. J. Magn. Reson. 89, 496-514.
25. Kay, L. E., Keifer, P. & Saarinen, T. (1992a). Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665.
26. 2 values in proteins. J. Magn. Reson. 97, 359-375.
27. 2O samples of proteins. J. Magn. Reson. ser. B, 101, 333-337.
28. Khalifah, R. G., Strader, D. J., Bryant, S. H. & Gibson, S. M. (1977). Carbon-13 nuclear magnetic resonance probe of active-site ionizations in human carbonic anhydrase B. Biochemistry, 16, 2241-2247.
29. Kiefer, L. L., Patrerno, S. A. & Fierke, C. A. (1995). Hydrogen bond network in the metal binding site of carbonic anhydrase enhances zinc affinity and catalytic efficiency. J. Am. Chem. Soc. 117, 6831-6837.
30. Krebs, J. F., Fierke, C. A., Ippolito, J. A. & Christianson, D. W. (1993). Structural and functional importance of a conserved hydrogen bond network in human carbonic anhydrase II. J. Biol. Chem. 268, 27458-27466.
31. Lefèvre, J.-F., Dayie, K. T., Peng, J. W. & Wagner, G. (1996). Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry, 35, 2674-2686.
32. 15N Overhauser effects. J. Magn. Reson. ser. B, 105, 45-51.
33. Majerski, Z., Zuanic, M. & Metelko, B. (1985). Deuterium isotope effects on carbon-13 chemical shifts of protoadamantane. Evidence for geometrical dependence of 3D and 4D effects. J. Am. Chem. Soc. 107, 1721-1726.
34. Markus, M. A., Dayie, K. T., Matsudairat, P. & Wagner, G. (1994). Effect of deuteration on the amide proton relaxation rates in proteins. Heteronuclear NMR experiments on Villin 4T. J. Magn. Reson. ser. B, 105, 192-195.
35. Markus, M. A., Dayie, K. T., Matsudaira, P. & Wagner, G. (1996). Local mobility within Villin 14T probed via heteronuclear relaxation measurements and a reduced spectral density mapping. Biochemistry, 35, 1722-1732.
36. 15N NMR assignments and global folding pattern. Biochemistry, 32, 13818-13829.
37. blk kinase. Biochemistry, 35, 6201-6211.
38. 15N-labeled protein: potential in structure determination of large proteins by NMR. J. Am. Chem. Soc. 118, 6800-6801.
39. Montelione, G. T., Lyons, B. A., Emerson, S. D. & Tashiro, M. J. (1992). An efficient triple resonance experiment using carbon-13 isotropic mixing for determining sequence-specific resonance assignments of isotopically-enriched proteins. J. Am. Chem. Soc. 114, 10974-10975.
40. Muhandiram, D. R. & Kay, L. E. (1994). Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson. ser. B, 103, 203-216.
41. Nair, S. K., Calderone, T. L., Christianson, D. W. & Fierke, C. A. (1991). Altering the mouth of a hydrophobic pocket. Structure and kinetics of human carbonic anhydrase II mutants at residue val-121. J. Biol. Chem. 266, 17320-17325.
42. 13C NMR spectra of carbons bonded to nitrogen in a sample spinning at the magic angle. J. Chem. Phys. 74, 5393-5397.
43. Nietlispach, D., Clowes, R. T., Broadhurst, R. W., Ito, Y., Keeler, J., Kelly, M., Ashurst, J., Oschkinat, H., Domaille, P. J. & Laue, E. D. (1996). An approach to the structure determination of larger proteins using triple resonance NMR experiments in conjunction with random fractional deuteration. J. Am. Chem. Soc. 118, 407-415.
44. 1H NMR studies of deuterated ribonuclease HI selectively labeled with protonated amino acids. J. Biomol. NMR, 2, 137-147.
45. Olejniczak, E. T., Xu, R. T., Petros, A. M. & Fesik, S. W. (1992). Optimized constant-time 4D HNCAHA and HN(CO)CAHA experiments. Applications to the backbone assignments of the FKBP/ascomycin complex. J. Magn. Reson. 100, 444-450.
46. Pachter, R., Arrowsmith, C. H. & Jardetzky, O. (1992). The effect of selective deuteration on magnetization transfer in larger proteins. J. Biomol. NMR, 2, 183-194.
47. Palmer, A. G., III, Cavanagh, J., Wright, P. E. & Rance, M. (1991). Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J. Magn. Reson. 93, 151-170.
48. Palmer, A. G., III, Skelton, N. J., Chazin, W. J., Wright, P. E. & Rance, M. (1992). Suppression of the effects of cross-relaxation between dipolar and anisotropic chemical shift relaxation mechanisms in the measurement of spin-spin relaxation rates. Mol. Phys. 75, 699-711.
49. Peng, J. W. & Wagner, G. (1992a). Mapping of spectral density functions using heteronuclear NMR relaxation measurements. J. Magn. Reson. 98, 308-332.
50. Peng, J. W. & Wagner, G. (1992b). Mapping of the spectral densities of N-H bond motions in eglin c using heteronuclear relaxation experiments. Biochemistry, 31, 8571-8586.
51. 15N NMR backbone assignments and secondary structure of the 269-residue protease subtilisin 309 from Bacillus lentus. J. Biomol. NMR, 4, 257-278.
52. Richards, F. M. & Kundrot, C. E. (1988). Identification of structural motifs from protein coordinate data: secondary structure and first-level supersecondary structure. Proteins: Struct. Funct. Genet. 31, 71-84.
53. Rosenberg, A. H., Lade, B. N., Chui, D. S., Lin, S. W., Dunn, J. J. & Studier, F. W. (1987). Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene, 56, 125-135.
54. Sambrook, S., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edit., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
55. α protons (HN(CA)H) in isotopically enriched proteins. J. Magn. Reson. 100, 406-410.
56. Senn, H. & Klaus, W. (1993). The nuclear magnetic resonance solution structure of flavoridin, an antagonist of the platelet GP IIb-IIIa receptor. J. Mol. Biol. 232, 907-925.
57. 2H-decoupling. J. Am. Chem. Soc. 118, 6570-6579.
58. Silverman, D. N. & Lindskog, S. (1988). The catalytic mechanism of carbonic anhydrase: implications of a rate-limiting protolysis of water. Acc. Chem. Res. 21, 30-36.
59. Sly, W. S. (1991). Carbonic anhydrase II deficiency syndrome: clinical delineation, interpretation, and implications. In The Carbonic Anhydrase: Cellular Physiology and Molecular Genetics (Dodson, S. J., Tashian, R. E., Gros, G. & Carter, N. D., eds), pp. 183-193, Plenum Press, New York.
60. 13C nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. 113, 5490-5492.
61. Stivers, J. T., Abeygunawardana, C., Whitman, C. P. & Mildvan, A. S. (1996). 4-Oxalocrotonate tautomerase, a 41-kDa homohexamer: backbone and side-chain resonance assignments, solution secondary structure, and location of active site residues by heteronuclear NMR spectroscopy. Protein Sci. 5, 729-741.
62. Studier, F. W. & Moffatt, B. A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113-130.
63. 13C isotope labeling of proteins with sodium acetate for NMR studies: application to human carbonic anhydrase II. Biochemistry, 30, 4491-4494.
64. 15N labeling of proteins for NMR studies. J. Biomol. NMR, 5, 339-344.
65. N NOEs to determine protein global folds in perdeuterated proteins. J. Am. Chem. Soc. 117, 9592-9593.
66. Verpoorte, J. A., Mehta, S. & Edsall, J. J. (1967). Esterase activities of human carbonic anhydrases B and C. J. Biol. Chem. 242, 4221-4229.
67. 15N resonance assignments and secondary structure analysis of the HU protein from Bacillus stearothermophilus using two- and three-dimensional double- and triple-resonance heteronuclear magnetic resonance spectroscopy. Biochemistry, 33, 14858-14870.
68. 13C chemical-shift data. J. Biomol. NMR, 4, 171-180.
69. Wittekind, M. & Mueller, L. (1993). HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J. Magn. Reson. ser. B, 101, 201-205.
70. 2H labeled proteins with high sensitivity. J. Am. Chem. Soc. 116, 11655-11666.
71. 2H-labeled proteins: application to a 37-kDa trp repressor-DNA complex. J. Am. Chem. Soc. 116, 6464-6465.
72. α carbons. J. Am. Chem. Soc. 116, 8266-8278.
73. 1H chemical shifts in proteins. J. Am. Chem. Soc. 117, 3556-3564.