The unfolding of oxidized c-type cytochromes: The instructive case of Bacillus pasteurii

Journal of Molecular Biology

Volumn 321, Issue 4, 2002, Pages 693-701

  Bartalesi, Ilaria ^a   Bertini, Ivano ^a   Ghosh, Kaushik ^a   Rosato, Antonio ^a   Turano, Paola ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Cytochrome c; Gram positive; Iron coordination; NMR spectroscopy; Protein unfolding

Indexed keywords

AMIDE; CYTOCHROME C; HEME DERIVATIVE; LIGAND; PROTON;

ALPHA HELIX; ARTICLE; BACILLUS; CARBOXY TERMINAL SEQUENCE; CORRELATION ANALYSIS; COVALENT BOND; ENZYME METABOLISM; HYDROGEN BOND; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SPECTROSCOPY; SPOROSARCINA PASTEURII; STRUCTURE ANALYSIS;

POSIBACTERIA; SPOROSARCINA PASTEURII;

EID: 0036968299     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00678-2     Document Type: Article

References (38)

1. Scott, R. A. & Mauk, A. G. (1996). Cytochrome c. A Multidisciplinary Approach, University Science Books, Sausalito, CA.
2. Hong, X. & Dixon, D. W. (1989). NMR study of the alkaline isomerization of ferricytochrome c. FEBS Letters, 246, 105-108.
3. Pearce, L. L., Gärtner, A. L., Smith, M. & Mauk, A. G. (1989). Mutation induced perturbation of the cyto-chrome c alkaline transition. Biochemistry, 28, 3152-3156.
4. Taler, G., Schejter, A., Navon, G., Vig, I. & Margoliash, E. (1995). The nature of the thermal equilibrium affecting the iron coordination of ferric cytochrome c. Biochemistry, 34, 14209-14212.
5. 553 reduction potential by structural and solution parameters. J. Biol. Inorg. Chem. 3, 371-382.
6. Wiley, W. R. & Stokes, J. L. (1963). Effect of pH and ammonium ions on the permeability of Bacillus pasteurii. J. Bacteriol. 86, 1152-1156.
7. Larson, A. D. & Kallio, R. E. (1954). Purification and properties of bacterial urease. J. Bacteriol. 68, 67-73.
8. Bornside, G. H. & Kallio, R. E. (1956). Urea-hydrolyzing bacilli. I. A physiological approach to identification. J. Bacteriol. 71, 627-634.
9. Wiley, W. R. & Stokes, J. L. (1962). Requirement of an alkaline pH and ammonia for substrate oxidation by Bacillus pasteurii. J. Bacteriol. 84, 730-734.
10. 553 at 0.97 Å resolution. Biochemistry, 39, 13115-13126.
11. Banci, L., Bertini, I., Ciurli, S., Dikiy, A., Dittmer, J., Rosato, A. et al. (2002). NMR solution structure, backbone mobility and homology modeling of c-type cytochromes from Gram-positive bacteria. ChemBioChem. 3, 299-310.
12. Cavanagh, J., Fairbrother, W. J., Palmer, A. G. III & Skelton, N. J. (1996). Protein NMR Spectroscopy. Principles and Practice, Academic Press, San Diego, CA.
13. Moore, G. R. & Pettigrew, G. W. (1990). Cytochromes c; Evolutionary, Structural and Physicochemical Aspects, Springer, Berlin.
14. Myers, J. K., Pace, C. N. & Scholtz, J. M. (1995). Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148.
15. Santoro, M. M. & Bolen, D. W. (1988). Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethane-sulfonyl alpha-chymotrypsin using different denaturants. Biochemistry, 27, 8063-8068.
16. Pace, C. N. (1986). Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131, 266-280.
17. Jeener, J., Meier, B. H., Bachmann, P. & Ernst, R. R. (1979). Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553.
18. Thanabal, V., de Ropp, J. S. & La Mar, G. N. (1987). (1)H NMR study of the electronic and molecular structure of the heme cavity in horseradish peroxi-dase. Complete heme resonance assignments based on saturation transfer and nuclear Overhauser effects. J. Am. Chem. Soc. 109, 265-272.
19. Inubushi, T. & Becker, E. D. (1983). Efficient detection of paramagnetically shifted NMR resonances by optimizing the WEFT pulse sequence. J. Magn. Reson. 51, 128-133.
20. Hammack, B., Godbole, S. & Bowler, B. E. (1998). Cytochrome c folding traps are not due solely to histidine-heme ligation: direct demonstration of a role for N-terminal amino group-heme ligation. J. Mol. Biol. 275, 719-724.
21. Bertini, I., Cowan, J. A., Luchinat, C., Natarajan, K. & Piccioli, M. (1997). Characterization of a partially unfolded high potential iron protein relevant to the folding pathway and cluster stability. Biochemistry, 36, 9332-9339.
22. Sivaraman, T., Arrington, C. B. & Robertson, A. D. (2001). Kinetics of unfolding and folding from amide hydrogen exchange in native ubiquitin. Nature Struct. Biol. 8, 331-333.
23. Louro, R. O., de Waal, E. C., Ubbink, M. & Turner, D. L. (2002). Replacement of the methionine axial ligand in cytochrome c(550) by a lysine: effects on the hame electronic structure. FEBS Letters, 510, 185-188.
24. 3 and at high temperature. Eur. J. Inorg. Chem. 1, 583-591.
25. Yeh, S. R. & Rousseau, D. L. (1999). Ligand exchange during unfolding of cytochrome c. J. Biol. Chem. 274, 17853-17859.
26. Bai, Y. W., Sosnick, T. R., Mayne, L. & Englander, S. W. (1995). Protein folding intermediates: native-state hydrogen exchange. Science, 269, 192-197.
27. Russell, B. S., Melenkivitz, R. & Bren, K. L. (2000). NMR investigation of ferricytochrome c unfolding: detection of an equilibrium unfolding intermediate and residual structure in the denatured state. Proc. Natl Acad. Sci. USA, 97, 8312-8317.
28. 15N relaxation measurements for oxidized and reduced iso-1-cytochrome c. Biochemistry, 38, 4480-4492.
29. 1ρ investigation of the oxidized and reduced species. Eur. J. Biochem. 268, 4468-4476.
30. Rosell, F. I., Ferrer, J. C. & Mauk, A. G. (1998). Proton-linked protein conformational switching: definition of the alkaline conformational transition of yeast iso-1-ferricytochrome c. J. Am. Chem. Soc. 120, 11234-11245.
31. Wilson, M. T. & Greenwood, C. (1996). The alkaline transition in ferricytochrome c. In Cytochrome c. A multidisciplinary Approach (Scott, R. A. & Mauk, A. G., eds), pp. 611-634, University Science Books, Sausalito, CA.
32. Pelletier, H. & Kraut, J. (1992). Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c. Science, 258, 1748-1755.
33. Lange, C. & Hunte, C. (2002). From the cover: crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome c. Proc. Natl Acad. Sci. USA, 99, 2800-2805.
34. Bodenhausen, G. & Ruben, D. J. (1980). Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters, 69, 185-188.
35. Peng, J. W. & Wagner, G. (1992). Mapping of spectral density function using heteronuclear NMR relaxation measurements. J. Magn. Reson. 98, 308-332.
36. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry, 28, 8972-8979.
37. 2O in protein NMR. Application to sensitivity enhancement and NOE measurements. J. Am. Chem. Soc. 115, 12593-12594.
38. Koradi, R., Billeter, M. & Wüthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structure. J. Mol. Graph. 14, 51-55.