Carbon-13 NMR method for the detection of correlated hydrogen exchange at adjacent backbone peptide amides and its application to hydrogen exchange in five antiparallel β strands within the hydrophobic core of Streptomyces subtilisin inhibitor (SSI)

Biochemistry

Volumn 44, Issue 35, 2005, Pages 11811-11820

  Uchida, Kenichi ^a,c   Markley, John L ^b   Kainosho, Masatsune ^a,d  

^a TOKYO METROPOLITAN UNIVERSITY   (Japan)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c TEIKYO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE AMIDES; STREPTOMYCES SUBTILISIN INHIBITOR (SSI);

HYDROGEN; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE; PROTONS;

CARBON;

AMIDE; CARBON 13; DEUTERIUM; PEPTIDE; PROTEIN; PROTON; WATER;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; HYDROGEN BOND; ISOTOPE LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STABILITY; PROTEIN STRUCTURE; SPECTROMETER; STREPTOMYCES;

BACTERIAL PROTEINS; CARBON ISOTOPES; DEUTERIUM EXCHANGE MEASUREMENT; HYDROGEN-ION CONCENTRATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; SUBTILISINS;

STREPTOMYCES;

EID: 24344466934     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050467s     Document Type: Article

References (45)

1. Karplus, M., and McCammon, J. A. (1981) The internal dynamics of globular proteins, CRC Crit. Rev. Biochem. 9, 293-349.
2. Linderstrom-Lang, K. (1955) Deuterium exchange between peptides and water, Chem. Soc. Spec. Publ. 2, 1-20.
3. Woodward, C., Simon, I., and Tuchsen, E. (1982) Hydrogen exchange and the dynamic structure of proteins, Mol. Cell. Biochem. 48, 135-160.
4. Englander, S. W., and Kallenbach, N. R. (1984) Hydrogen exchange and structural dynamics of proteins and nucleic acids, Q. Rev. Biophys. 16, 521-655.
5. Englander, S. W., and Mayne, L. (1992) Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR, Annu. Rev. Biophys. Biomol. Struct. 21, 243-265.
6. Baldwin, R. L. (1993) Pulsed H/D-exchange studies of folding intermediates, Curr. Opin. Struct. Biol. 3, 84-91.
7. Bai, Y., Sosnick, T. R., Mayne, L., and Englander, S. W. (1995) Protein folding intermediates: Native-state hydrogen exchange, Science 269, 192-197.
8. Krishna, M. M. G., Hoang, L., Lin, Y., and Englander, S. W. (2004) Hydrogen exchange methods to study protein folding, Methods 34, 51-64.
9. Mayne, L., Paterson, Y., Cerasoli, D., and Englander, S. W. (1992) Effect of antibody binding on protein motions studied by hydrogen-exchange labeling and two-dimensional NMR, Biochemistry 31, 10678-10685.
10. Zahn, R., Spitzfaden, C., Ottger, M., Wüthrich, K., and Pluckthun, A. (1994) Destabilisation of the complete protein secondary structure on binding to the chaperone GroEL, Nature 368, 261-265.
11. Reid, C. W., Brewer, D., and Clarke, A. J. (2004) Substrate binding affinity of Pseudomonas aeruginosa membrane-bound lytic transglycosylase B by hydrogen-deuterium exchange MALDI MS, Biochemistry 43, 11275-11282.
12. Loftus, D., Gbenle, G. O., Kim, P. S., and Baldwin, R. L. (1986) Effects of denaturants on amide proton exchange rates: A test for structure in protein fragments and folding intermediates, Biochemistry 25, 1428-1436.
13. Englander, J. J., Calhoun, D. B., and Englander, S. W. (1979) Measurement and calibration of peptide group hydrogen-deuterium exchange by ultraviolet spectrophotometry, Ann. Biochem. 92, 517-524.
14. Harmen H. J., de Jong, H., H., Goormaghtigh, E., and Ruysschaert, J.-M. (1985) Tertiary stability of native and methionine-80 modified cytochrome c detected by proton-deuterium exchange using online Fourier transform infrared spectroscopy, Biochemistry 34, 172-179.
15. Wagner, G., and Wüthrich, K. (1979) Structural interpretation of the amide proton exchange in the basic pancreatic trypsin inhibitor and related proteins, J. Mol. Biol. 134, 75-94.
16. Wagner, G., and Wüthrich, K. (1982) Amide protein exchange and surface conformation of the basic pancreatic trypsin inhibitor in solution. Studies with two-dimensional nuclear magnetic resonance, J. Mol. Biol. 160, 343-361.
17. Kossiakoff, A. A. (1982) Protein dynamics investigated by the neutron diffraction-hydrogen exchange technique, Nature 296, 713-721.
18. Pederson, T. G., Sigurskjold, B. W., Anderson, K. V., Kjaer, M., Poulsen, F. M., Dobson, C. M., and Redfield, C. (1991) A nuclear magnetic resonance study of the hydrogen-exchange behaviour of lysozyme in crystals and solution, J. Mol. Biol. 218, 414-426.
19. Lumry, R., and Rosenberg, A. (1975) The mobile defect hypothesis of protein function, Coll. Int. C.N.R.S. L'Eau. Syst. Biol. 246, 55-63.
20. Richards, F. M. (1979) Packing defects, cavities, volume fluctuations, and access to the interior of proteins, Carsberg Res. Commun. 44, 47-63.
21. Englander, S. W., and Mauel, C. (1972) Hydrogen exchange studies of respiratory proteins. II. Detection of discrete, ligand-induced changes in hemoglobin, J. Biol. Chem. 247, 2387-2394.
22. Englander, S. W., Calhoun, D. B., Englander, J. J., Kallenbach, N. R., Leim, R. H., Malin, E. L., Mandal, C., and Rogero, J. R. (1980) Individual breathing reactions measured in hemoglobin by hydrogen exchange methods, Biophys. J. 32, 577-589.
23. Roder, H., Wagner, G., and Wüthrich, K. (1985) Individual amide proton exchange rates in thermally unfolded basic pancreatic trypsin inhibitor, Biochemistry 24, 7396-7407.
24. Akasaka, K., Inoue, T., Hatano, H., and Woodword, C. K. (1985) Hydrogen exchange kinetics of core peptide protons in Streptomyces subtilisin inhibitor, Biochemistry 24, 2973-2979.
25. Kawata, Y., Goto, Y., Hamaguchi, K. Hayashi, F., Kobayashi, Y., and Kyogoku, Y. (1988) Hydrogen-exchange kinetics of the indole NH proton of the buried tryptophan in the constant fragment of the immunoglobulin light chain, Biochemistry 27, 346-350.
26. Wagner, G. (1980) A novel application of nuclear Overhauser enhancement (NOE) in proteins: Analysis of correlated events in the exchange of internal labile protons, Biochim. Biophys. Rev. Commun. 97, 614-620.
27. Miranker, A., Robinson, C. V., Radford, S. E., Aplin, R. T., and Dobson, C. M. (1993) Detection of transient protein folding populations by mass spectrometry, Science 262, 896-900.
28. Zhang, Z., Post, C. B., and Smith, D. L. (1996) Amide hydrogen exchange determined by mass spectrometry: Application to rabbit muscle aldolase, Biochemistry 35, 779-791.
29. Kainosho, M., and Tsuji, T. (1982) Assignment of the three methionyl carbonyl carbon resonances in Streptomyces subtilisin inhibitor by a carbon-13 and nitrogen-15 double-labeling technique. A new strategy for structural studies of proteins in solution, Biochemistry 21, 6273-6279.
30. Kainosho, M., Nagao, H., and Tsuji, T. (1987) Local structural features around the C-terminal segment of Streptomyces subtilisin inhibitor studied by carbonyl carbon nuclear magnetic resonances three phenylalanyl residues, Biochemistry 26, 1068-1075.
31. 13C NMR resonances of cysteinyl residues, J. Biomol. NMR 1, 49-64.
32. Markley, J. L., and Kainosho, M. (1993) Stable isotope labeling and resonance assignments in larger proteins, in NMR of Macromolecules (Roberts, G. C. K., Ed.) pp 101-152, Oxford University Press, New York.
33. Hansen, P. E. (1983) Isotope effects on nuclear shielding, Annu. Rep. NMR Spectrosc. 15, 105-234.
34. Akasaka, K., Fujii, S., Hayashi, F., Rokushika, S., and Hatano, H. (1982) A novel technique for the detection of dissociation-association equilibrium in a highly associable macromolecular system, Biochem. Ind. 5, 637-642.
35. Hiromi, K., Akasaka, K., Mitsui, Y., Tonomura, B., and Murao, S. (1985) Protein Protease Inhibition-The Case of Streptomyces Subtilisin Inhibitor (SSI), Elsevier. Amsterdam, The Netherlands.
36. Nakanishi, M., and Tsuboi, M. (1976) Structure and fluctuation of a Streptomyces subtilisin inhibitor, Biochim. Biochim. Acta 434, 365-376.
37. Marquardt, D. W. (1963) An algorithm for least squares estimation of nonlinear parameters, J. Soc. Ind. Appl. Math. 11, 431-441.
38. Goto, Y., and Hamaguchi, K. (1979) The role of the intrachain disulfide bond in the conformation and stability of the constant fragment of the immunoglobulin light chain, J. Biochem. 86, 1433-1441.
39. Mitsui, Y., Satow, Y., Watanabe, Y., and Iitaka, Y. (1979) Crystal structure of a bacterial protein proteinase inhibitor (Streptomyces subtilisin inhibitor) at 2.6 Å resolution, J. Mol. Biol. 131, 697-724.
40. Havdt, A., and Nielsen, S. O. (1966) Hydrogen exchange in proteins, Adv. Protein Chem. 21, 287-386.
41. Molday, R. S., Englander, S. W., and Kallen, R. G. (1972) Primary structure effects on peptide group hydrogen exchange, Biochemistry 11, 150-158.
42. Bai, Y., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary structure effects on peptide group hydrogen exchange, Proteins 17, 75-86.
43. Komiyama, T., Miwa, M., Yatabe, T., and Ikeda, H. (1984) A circular dichroism study on thermal denaturation of a dimeric globular protein, Streptomyces subtilisin inhibitor, J. Biochem. 95, 1569-1575.
44. Akasaka, K. (1984) Molecular strategy for the active conformation of Streptomyces subtilsin inhibitor, Biomed. Res. 25 (supplement). 177-186.
45. Akasaka, K. Proton magnetic resonance spectra of a new proteinase inhibitor, Streptomyces subtilisin inhibitor (SSI) at 360 MHz. General characteristic and tyrosine titrations, in Proceedings of the European Conference on NMR of Macromolecules (Conti, F., Ed.) pp 475-483, Lerici, Rome, Italy.