Characterization of alkaline transitions in ferricytochrome C using carbon-deuterium infrared probes

Biochemistry

Volumn 47, Issue 51, 2008, Pages 13470-13480

  Weinkam, Patrick ^a,b   Zimmermann, Jörg ^a   Sagle, Laura B ^a   Matsuda, Shigeo ^a   Dawson, Philip E ^a   Wolynes, Peter G ^b   Romesberg, Floyd E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE CONDITIONS; ALKALINE TRANSITIONS; EQUILIBRIUM CONDITIONS; HIGH RESOLUTIONS; INFRARED PROBES; IR ABSORPTIONS; IRON REDUCTIONS; NATIVE SPECIES; NATIVE TOPOLOGIES; PROTEIN FUNCTIONS; STRUCTURAL TRANSITIONS; TERTIARY STRUCTURES;

AMINES; AMINO ACIDS; CHROMOPHORES; DEUTERIUM; PROTEIN FOLDING;

DEPROTONATION;

ALKALI METAL; AMINO ACID; CARBON; CYTOCHROME C; DEUTERIUM; HYDROXIDE; IRON; LYSINE;

ARTICLE; CHROMATOPHORE; CONTROLLED STUDY; INFRARED RADIATION; MECHANICAL PROBE; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON TRANSPORT; SIMULATION;

CARBON; CYTOCHROMES C; DEUTERIUM; HYDROGEN-ION CONCENTRATION; MOLECULAR CONFORMATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SPECTROPHOTOMETRY, INFRARED; SPECTROPHOTOMETRY, ULTRAVIOLET; THERMODYNAMICS;

EID: 58149171911     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801223n     Document Type: Article

References (57)

1. McLachlan, A. D. (1982) Rapid comparison of protein structures. Acta Crystallogr. A38, 871-873.
2. Weinkam, P., Zong, C., and Wolynes, P. G. (2005) A funneled energy landscape for cytochrome c directly predicts the sequential folding route inferred from hydrogen exchange experiments. Proc. Natl. Acad. Sci. U.S.A. 102, 12401-12406.
3. Scott, R. A., and Mauk, A. G. (1996) , pp 611-634, University Science Books, Sausalito, CA.
4. Jones, C. M., Henry, E. R., Hu, Y., Chan, C., Luck, S. D., Bhuyan, A., Roder, H., Hofrichter, J., and Eaton, W. A. (1993) Fast events in protein folding initiated by nanosecond laser photolysis. Proc. Natl. Acad. Sci. U.S.A. 90, 11860-11864.
5. Theorell, H., and Akesson, A. J. (1941) Studies on cytochrome c. II. The optical properties of pure cytochrome c and some of its derivatives. J. Am. Chem. Soc. 63, 1812-1818.
6. Moore, G. R., and Pettigrew, G. W. (1990) Cytochromes c. Evolutionary, Structural and Physiochemical Aspects, Springer-Verlag, Berlin.
7. Dopner, S., Hildebrandt, P., Rosell, F. I., and Mauk, A. G. (1998) Alkaline conformational transitions of ferricytochrome c studied by resonance Raman spectroscopy. J. Am. Chem. Soc. 120, 11246-11255.
8. Gray, H. B., and Winkler, J. R. (1996) Electron transfer in proteins. Annu. Rev. Biochem. 65, 537-561.
9. Blouin, C., Guillemette, J. G., and Wallace, C. J. (2001) Resolving the individual components of a pH-induced conformational change. Biophys. J. 81, 2331-2338.
10. Eaton, W. A., and Hochstrasser, R. M. (1967) Electronic spectrum of single crystals of ferricytochrome-c. J. Chem. Phys. 46, 2533-2539.
11. Smith, D. W., and Williams, R. J. P. (1970) The spectra of ferric haems and haemoproteins. Struct. Bonding (Berlin) 7, 1-45.
12. Hoang, L., Maity, H., Krishna, M. M., Lin, Y., and Englander, S. W. (2003) Folding units govern the cytochrome c alkaline transition. J. Mol. Biol. 331, 37-43.
13. Rosell, F. I., Ferrer, J. C., and Mauk, A. G. (1998) Protein-linked protein conformational switching: definition of the alkaline conformational transition of yeast iso-1-ferricytochrome c. J. Am. Chem. Soc. 120, 11234-11245.
14. Tonge, P., Moore, G. R., and Wharton, C. W. (1989) Fourier-transform infra-red studies of the alkaline isomerization of mitochondrial cytochrome c and the ionization of carboxylic acids. Biochem. J. 258, 599-605.
15. Filosa, A., Ismail, A. A., and English, A. M. (1999) FTIR-monitored thermal titration reveals different mechanisms for the alkaline isomerization of tuna compared to horse and bovine cytochromes c. J. Biol. Inorg. Chem. 4, 717-726.
16. Filosa, A., Wang, Y., Ismail, A. A., and English, A. M. (2001) Two-dimensional infrared correlation spectroscopy as a probe of sequential events in the thermal unfolding of cytochromes c. Biochemistry 40, 8256-8263.
17. Hong, X. L., and Dixon, D. W. (1989) NMR study of the alkaline isomerization of ferricytochrome c. FEBS Lett. 246, 105-108.
18. Ferrer, J. C., Guillemette, J. G., Bogumil, R., Inglis, S. C., Smith, M., and Mauk, A. G. (1993) Identification of Lys79 as an iron ligand in one form of alkaline yeast iso-1-ferricytochrome-c. J. Am. Chem. Soc. 115, 7507-7508.
19. Assfalg, M., Bertini, I., Dolfi, A., Turano, P., Mauk, A. G., Rosell, F. I., and Gray, H. B. (2003) Structural model for an alkaline form of ferricytochrome c. J. Am. Chem. Soc. 125, 2913-2922.
20. Silkstone, G. G., Cooper, C. E., Svistunenko, D., and Wilson, M. T. (2005) EPR and optical spectroscopic studies of Met80X mutants of yeast ferricytochrome c: models for intermediates in the alkaline transition. J. Am. Chem. Soc. 127, 92-99.
21. Perroud, T. D., Bokoch, M. P., and Zare, R. N. (2005) Cytochrome c conformations resolved by the photon counting histogram: Watching the alkaline transition with single-molecule sensitivity. Proc. Natl. Acad. Sci. U.S.A. 102, 17570-17575.
22. Maity, H., Rumbley, J. N., and Englander, S. W. (2006) Functional role of a protein foldon - An omega-loop foldon controls the alkaline transition in ferricytochrome c. Proteins 63, 349-355.
23. Pollock, W. B., Rosell, F. I., Twitchett, M. B., Dumont, M. E., and Mauk, A. G. (1998) Bacterial expression of a mitochondrial cytochrome c. Trimethylation of lys72 in yeast iso-1-cytochrome c and the alkaline conformational transition. Biochemistry 37, 6124-6131.
24. Pettigrew, G. W., Aviram, I., and Schejter, A. (1976) The role of the lysines in the alkaline heme-linked ionization of ferric cytochrome c. Biochem. Biophys. Res. Commun. 68, 807-813.
25. Uno, T., Nishimura, Y., and Masamichi, T. (1984) Time-resolved resonance Raman study of alkaline isomerization of ferricytochrome c. Biochemistry 23, 6802-6808.
26. Hasumi, H. (1980) Kinetic studies on isomerization of ferricytochrome c in alkaline and acid pH ranges by the circular dichroism stopped-flow method. Biochim. Biophys. Acta 626, 265-276.
27. Kihara, H., Saigo, S., Nakatani, H., Hiromi, K., Ikeda-Saito, M., and Iizuka, T. (1976) Kinetic study of isomerization of ferricytochrome c at alkaline pH. Biochim. Biophys. Acta 430, 225-243.
28. Chin, J. K., Jimenez, R., and Romesberg, F. E. (2002) Protein dynamics and cytochrome c: Correlations between ligand vibrations and redox activity. J. Am. Chem. Soc. 124, 1846-1847.
29. Chin, J. K., Jimenez, R., and Romesberg, F. E. (2001) Direct observation of protein vibrations by selective incorporation of spectroscopically observable carbon-deuterium bonds in cytochrome c. J. Am. Chem. Soc. 123, 2426-2427.
30. Sagle, L. B., Zimmermann, J., Dawson, P. E., and Romesberg, F. (2006) Direct and high resolution characterization of cytochrome c equilibrium folding. J. Am. Chem. Soc. 128, 14232-14233.
31. Sagle, L. B., Zimmermann, J., Matsuda, S., Dawson, P. E., and Romesberg, F. E. (2006) Redox-coupled dynamics and folding in cytochrome c. J. Am. Chem. Soc. 128, 7909-7915.
32. Thielges, M. C., Case, D. A., and Romesberg, F. E. (2008) Carbon-deuterium bonds as probes of dihydrofolate reductase. J. Am. Chem. Soc. (Web release date: April 16, 2008).
33. Onuchic, J. N., Wolynes, P. G., Luthey-Schulten, Z., and Socci, N. D. (1995) Toward an outline of the topography of a realistic protein-folding funnel. Proc. Natl. Acad. Sci. U.S.A. 92, 3626-3630.
34. Ueda, Y., Taketomi, H., and Go, N. (1978) Studies on protein folding, unfolding, and fluctuations by computer simulation. II. A. Three-dimensional lattice model of lysozyme. Biopolymers 17, 1531-1548.
35. Alm, E., and Baker, D. (1999) Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures. Proc. Natl. Acad. Sci. U.S.A. 96, 11305-11310.
36. Clementi, C., Jennings, P. A., and Onuchic, J. N. (2000) How native-state topology affects the folding of dihydrofolate reductase and interleukin-1β. Proc. Natl. Acad. Sci. U.S.A. 97, 5871-5876.
37. Koga, N., and Takeda, S. (2001) Roles of native topology and chain-length scaling in protein folding: a simulation study with a Go-like model. J. Mol. Biol. 313, 171-180.
38. Levy, Y., Cho, S., Shen, T., Onuchic, J. N., and Wolynes, P. G. (2005) Symmetry and frustration in protein energy landscapes: a near degeneracy resolves the Rop dimer-folding mystery. Proc. Natl. Acad. Sci. U.S.A. 102, 2373-2378.
39. Wallace, C. J., and Clark-Lewis, I. (1992) Functional role of heme ligation in cytochrome c. Effects of replacement of methionine 80 with natural and non-natural residues by semisynthesis. J. Biol. Chem. 267, 3852-3861.
40. Yang, A., and Honig, B. (1993) On the pH dependence of protein stability. J. Mol. Biol. 231, 459-474.
41. Aune, K. C., and Tanford, C. (1969) Thermodynamics of the denaturation of lysozyme by guanidine hydrochloride. I. Depdendence on pH at 25 degrees. Biochemistry 8, 4579-4585.
42. Friedrichs, M. S., and Wolynes, P. G. (1989) Toward protein tertiary structure recognition by means of associative memory Hamiltonians. Science 246, 371-373.
43. Banci, L., Bertini, I., Gray, H. B., Luchinat, C., Reddig, T., Rosato, A., and Turano, P. (1997) Solution structure of oxidized horse heart cytochrome c. Biochemistry 36, 9867-9877.
44. Eastwood, M., and Wolynes, P. G. (2001) Role of explicitly cooperative interactions in protein folding funnels: a simulation study. J. Chem. Phys. 114, 4702-4716.
45. Morishima, I., Ogawa, S., Yonezawa, T., and Iizuka, T. (1977) Nuclear magnetic resonance studies in hemoproteins. IX. pH dependent features of horse heart ferric cytochrome c. Biochim. Biophys. Acta 495, 287-298.
46. Maity, H., Maity, M., and Englander, S. W. (2004) How cytochrome c folds, and why: submolecular foldon units and their stepwise sequential stabilization. J. Mol. Biol. 343, 223-233.
47. Rosell, F. I., Harris, T. R., Hildebrand, D. P., Dopner, S., Hildebrandt, P., and Mauk, A. G. (2000) Characterization of an alkaline transition intermediate stabilized in the Phe82Trp variant of yeast iso-1-cytochrome c. Biochemistry 39, 9047-9054.
48. Shen, T., Zong, C., Hamelberg, D., McCammon, J. A., and Wolynes, P. G. (2005) The folding energy landscape and phosphorylation: modeling the conformational switch of the NFAT regulatory domain. FASEB J. 19, 1389-1395.
49. Kyte, J. (1995) Structure in Protein Chemistry, Garland Science, New York.
50. Schaller, W., and Robertson, A. D. (1995) pH, ionic strength, and temperature dependences of ionization equilibria for the carboxyl groups in turkey ovomucoid third domain. Biochemistry 34, 4714-4723.
51. Castro, C., Jamin, M., Yokoyama, W., and Wade, R. (1986) Ligation and reduction of iron(III) porphyrines by amines. A model for cytochrome P-450 monoamine oxidase. J. Am. Chem. Soc. 108, 4179-4187.
52. Marques, H., Munro, O., Munro, T., deWet, M., and Vashi, P. (1999) Coordination of N-donor ligands by the monomeric ferric porphyrin N-acetylmicroperoxidase-8. Inorg. Chem. 38, 2312-2319.
53. Li, Y., Imaeda, K., and Inokuchi, H. (1994) pH and temperature effect on the absorption spectra of Pseudomonas aeruginosa cytochrome c-551 solution. J. Phys. Chem. 98, 4726-4728.
54. Ångström, J., Moore, G. R., and Williams, R. J. P. (1982) The magnetic susceptibility of ferricytochrome c. Biochim. Biophys. Acta 703, 87-94.
55. Gadsby, P. M., Peterson, J., Foote, N., Greenwood, C., and Thomson, A. J. (1987) Identification of the ligand-exchange process in the alkaline transition of horse heart cytochrome c. Biochem. J. 246, 43-54.
56. Luntz, T. L., Schejter, A., Garber, E. A., and Margoliash, E. (1989) Structural significance of an internal water molecule studied by site-directed mutagenesis of tyrosine-67 in rat cytochrome c. Proc. Natl. Acad. Sci. U.S.A. 86, 3524-3528.
57. Oellerich, S., Wackbarth, H., and Hildebrandt, P. (2002) Spectroscopic characterization of nonnative conformational states of cytochrome c. J. Phys. Chem. B 106, 6566-6580.