Accelerated exchange of a buried water molecule in selectively disulfide-reduced bovine pancreatic trypsin inhibitor

Biochemistry

Volumn 43, Issue 38, 2004, Pages 12020-12027

  Denisov, Vladimir P ^a   Peters, Jörg ^b   Hörlein, Hans Dietrich ^b   Halle, Bertil ^a  

^a LUND UNIVERSITY   (Sweden)

^b BAYER PHARMA AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DATA REDUCTION; PROTEINS; TEMPERATURE; WATER;

BOVINE PANCREATIC TRYPSIN INHIBITORS (BPTI); CLEAVAGE; EXCHANGE RATES; MAGNETIC RELAXATION DISPERSION (MRD);

MAGNETIC RELAXATION;

AMIDE; APROTININ; CYSTEINE; SERINE; WATER;

ANALYTIC METHOD; ARTICLE; DISULFIDE BOND; MAGNETIC RELAXATION DISPERSION; METHYLATION; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; REDUCTION; ROOM TEMPERATURE;

ANIMALS; APROTININ; CATTLE; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MUTATION; OXIDATION-REDUCTION; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE; THERMODYNAMICS; WATER;

BOVINAE;

EID: 4644298947     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0492049     Document Type: Article

References (52)

1. Schellman, J. A. (1955) The stability of hydrogen-bonded peptide structures in aqueous solution,. C. R. Trav. Lab. Carlsberg, Ser. Chim. 29, 230-259.
2. Goldenberg, D. P. (1992) Native and non-native intermediates in the BPTI folding pathway, Trends Biochem. Sci. 17, 257-261.
3. Creighton, T. E. (1997) Protein folding coupled to disulphide bond formation, Biol. Chem. 378, 731-744.
4. Wlodawer, A., Walter, J., Huber, R., and Sjölin, L. (1984) Structure of bovine pancreatic trypsin inhibitor. Results of joint neutron and X-ray refinement of crystal form 11, J. Mol. Biol. 180, 301-329.
5. Vincent, J.-P., and Lazdunski, M. (1972) Trypsin-pancreatic trypsin inhibitor association. Dynamics of the interaction and role of disulfide bridges, Biochemistry 11, 2967-2977.
6. Hanson, W. M., Beeser, S. A., Oas, T. G., and Goldenberg, D. P. (2003) Identification of a residue critical for maintaining the functional conformation of BPTI, J. Mol. Biol. 333, 425-441.
7. Deisenhofer, J., and Steigemann, W. (1975) Crystallographic refinement of the structure of bovine pancreatic trypsin inhibitor at 1.5 Å resolution, Acta Crystallogr. B 31, 238-250.
8. Wlodawer, A., Deisenhofer, J., and Huber, R. (1987) Comparison of two highly refined structures of bovine pancreatic trypsin inhibitor, J. Mol. Biol. 193, 145-156.
9. Parkin, S., Rupp, B., and Hope, H. (1996) Structure of bovine pancreatic trypsin inhibitor at 125 K: Definition of carboxyl-terminal residues Glu57 and Ala58, Acta Crystallogr. D 52, 18-29.
10. Otting, G., and Wüthrich, K. (1989) Studies of protein hydration in aqueous solution by direct NMR observation of individual protein-bound water molecules, J. Am. Chem. Soc. 111, 1871-1875.
11. Denisov, V. P., and Halle, B. (1995) Protein hydration dynamics in aqueous solution: A comparison of bovine pancreatic trypsin inhibitor and ubiquitin by oxygen-17 spin relaxation dispersion, J. Mol. Biol. 245, 682-697.
12. Denisov, V. P., Halle, B., Peters, J., and Hörlein, H. D. (1995) Residence times of the buried water molecules in bovine pancreatic trypsin inhibitor and its G36S mutant, Biochemistry 34, 9046-9051.
13. Denisov, V. P., Peters, J., Hörlein, H. D., and Halle, B. (1996) Using buried water molecules to explore the energy landscape of proteins, Nat. Struct. Biol. 3, 505-509.
14. Kress, L. F., and Laskowski, M. (1967) The basic trypsin inhibitor of bovine pancreas, VII. Reduction with borohydride of disulfide bond linking half-cystine residues 14 and 38, J. Biol. Chem. 242, 4925-4929.
15. Creighton, T. E. (1975) Interactions between cysteine residues as probes of protein conformation: The disulphide bond between Cys14 and Cys38 of the pancreatic trypsin inhibitor, J. Mol. Biol. 96, 767-776.
16. Kress, L. F., Wilson, K. A., and Laskowski, M. (1968) The basic trypsin inhibitor of bovine pancreas, VIII. Changes in activity following substitution of reduced half-cystine residues 14 and 38 with sulfhydryl reagents, J. Biol. Chem. 243, 1758-1762.
17. Vincent, J.-P., Chicheportiche, R., and Lazdunski, M. (1971) The conformational properties of the basic pancreatic trypsin inhibitor, Eur. J. Biochem. 23, 401-411.
18. 1H NMR in two chemically modified analogues of the basic pancreatic trypsin inhibitor, Eur. J. Biochem. 145, 431-436.
19. Schwartz, H., Hinz, H.-J., Mehlich, A., Tschesche, H., and Wenzel, H. R. (1987) Stability studies on derivatives of the bovine pancreatic trypsin inhibitor. Biochemistry 26, 3544-3551.
20. Hagihara, Y., Shiraki, K., Nakamura, T., Uegaki, K., Takagi, M., Imanaka, T., and Yumoto, N. (2002) Screening for stable mutants with amino acid pairs substituted for the disulfide bond between residues 14 and 38 of bovine pancreatic trypsin inhibitor (BPTI). J. Biol. Chem. 277, 51043-51048.
21. Marks, C. B., Naderi, H., Kosen, P. A., Kuntz, I. D., and Anderson, S. (1987) Mutants of bovine pancreatic trypsin inhibitor lacking cysteines 14 and 38 can fold properly. Science 235, 1370-1373.
22. Hurle, M. R., Marks, C. B., Kosen, P. A., Anderson, S., and Kuntz, I. D. (1990) Denaturant-dependent folding of bovine pancreatic trypsin inhibitor mutants with two intact disulfide bonds, Biochemistry 29, 4410-4419.
23. 1H NMR assignments and three-dimensional structure of Alal4/Ala38 bovine pancreatic trypsin inhibitor based on two-dimensional NMR and distance geometry, in Conformations and Forces in Protein Folding (Nall, B. T., and Dill, K. A., Eds.) pp 86-114, American Asssociation for the Advancement of Science, Washington, DC.
24. Ma, L.-C., and Anderson, S. (1997) Correlation between disulfide reduction and conformational unfolding in bovine pancreatic trypsin inhibitor, Biochemistry 36, 3728-3736.
25. Goldenberg, D. P. (1988) Kinetic analysis of the folding and unfolding of a mutant form of bovine pancreatic trypsin inhibitor lacking the cysteine-14 and -38 thiols, Biochemistry 27, 2481-2489.
26. Berndt, K. D., Beunink, J., Schröder, W., and Wüthrich, K. (1993) Designed replacement of an internal hydration water molecule in BPTI: Structural and functional implications of a glycine-to-serine mutation, Biochemistry 32, 4564-4570.
27. Denisov, V. P., Venu, K., Peters, J., Hörlein, H. D., and Halle, B. (1997) Orientational disorder and entropy of water in protein cavities, J. Phys. Chem. B 101, 9380-9389.
28. Barany, G., Gross, C., Ferrer, M., Barbar, E., Pan, H., and Woodward, C. (1996) Optimized methods for chemical synthesis of bovine pancreatic trypsin inhibitor analogues, in Techniques in Protein Chemistiy (Marshalk, D., Ed.) Vol. VII, pp 503-514, Academic Press, San Diego.
29. Beeser, S. A., Oas, T. G., and Goldenberg, D. P. (1998) Determinants of backbone dynamics in native BPTI: Cooperative influence of the 14-38 disulfide and the Tyr35 side-chain, J. Mol. Biol. 284, 1581-1596.
30. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1983) Reassessment of Ellman reagent, Methods Enzymol. 91, 49-60.
31. Denisov, V. P., and Halle, B. (1995) Hydrogen exchange and protein hydration: The deuteron spin relaxation dispersions of bovine pancreatic trypsin inhibitor and ubiquitin, J. Mol. Biol. 245, 698-709.
32. Halle, B., Denisov, V. P., and Venu, K. (1999) Multinuclear relaxation dispersion studies of protein hydration, in Modern Techniques in Protein NMR (Berliner, L. J., and Krishna, N. R., Eds.) pp 419-484, Plenum, New York.
33. Modig, K., Liepinsh, E., Otting, G., and Halle, B. (2004) Dynamics of protein and peptide hydration, J. Am. Chem. Soc. 126, 102-114.
34. Gottschalk, M., Venu, K., and Halle, B. (2003) Protein self-association in solution: The bovine pancreatic trypsin inhibitor decamer, Biophys. J. 84, 3941-3958.
35. Hamiaux, C., Prangé, T., Riès-Kautt, M., Ducruix, A., Lafont, S., Astier, J. P., and Veesler, S. (1999) The decameric structure of bovine pancreatic trypsin inhibitor (BPTI) crystallized from thiocyanate at 2.7 Å resolution, Acta Crystallogr. D 55, 103-113.
36. Kosen, P. A., Creighton, T. E., and Blout, E. R. (1981) Circulardichroism spectroscopy of bovine pancreatic trypsin-inhibitor and 5 altered conformational states. Relationship of conformation and the refolding pathway of the trypsin-inhibitor, Biochemistry 20, 5744-5754.
37. Wagner, G., Tschesche, H., and Wüthrich, K. (1979) The influence of localized chemical modifications of the basic pancreatic trypsin inhibitor on static and dynamic aspects of the molecular conformation in solution, Eur. J. Biochem. 95, 239-248.
38. Brunner, H., Holz, M., and Jering, H. (1974) Raman studies on native, reduced, and modified basic pancreatic trypsin inhibitor, Eur. J. Biochem. 50, 129-133.
39. 1H nuclear magnetic resonance of the basic pancreatic trypsin inhibitor after reduction of the disulfide bond between Cys-14 and Cys-38, Eur. J. Biochem. 95, 249-253.
40. Yoshioki, S., Abe, H., Noguti, T., Go, N., and Nagayama, K. (1983) Conformational change of a globular protein elucidated at atomic resolution, J. Mol. Biol. 170, 1031-1036.
41. Halle, B. (2004) Protein hydration dynamics in solution: a critical survey, Philos. Trans. R. Soc. London, Ser. B 359, 1207-1224.
42. Beeser, S. A., Goldenberg, D. P., and Oas, T. G. (1997) Enhanced protein flexibility caused by a destabilizing amino acid replacement in BPTI, J. Mol. Biol. 269, 154-164.
43. Barbar, E., Hare, M., Daragan, V., Barany, G., and Woodward, C. (1998) Dynamics of the conformational ensemble of partially folded bovine pancreatic trypsin inhibitor, Biochemistry 37, 7822-7833.
44. 1H NMR of two chemically modified analogs of the basic pancreatic trypsin inhibitor, Eur. J. Biochem. 145, 423-430.
45. Schulman, B. A., and Kim, P. S. (1994) Hydrogen exchange in BPTI variants that do not share a common disulfide bond, Protein Sci. 3, 2226-2232.
46. Halle, B. (2002) Flexibility and packing in proteins, Proc. Natl. Acad. Sci. U.S.A. 99, 1274-1279.
47. 15N spin relaxation times, J. Biomol. NMR 3, 151-164.
48. Otting, G., Liepinsh, E., and Wüthrich, K. (1993) Disulfide bond isomerization in BPTI and BPTI(G36S): An NMR study of correlated mobility in proteins. Biochemistry 32, 3571-3582.
49. Grey, M. J., Wang, C., and Palmer, A. G. (2003) Disulfide bond isomerization in basic pancreatic trypsin inhibitor: Multisite chemical exchange quantified by CPMG relaxation dispersion and chemical shift modeling, J. Am. Chem. Soc. 125, 14324-14335.
50. 2H and temperature, Biochemistry 24, 7396-7407.
51. Kim, K.-S., Fuchs, J. A., and Woodward, C. K. (1993) Hydrogen exchange identifies native-state motional domains important in protein folding, Biochemistry 32, 9600-9608.
52. Tüchsen, E., Hayes, J. M., Ramaprasad, S., Copie, V., and Woodward, C. (1987) Solvent exchange of buried water and hydrogen exchange of peptide NH groups hydrogen bonded to buried waters in bovine pancreatic trypsin inhibitor. Biochemistry 26, 5163-5172.