Heme coordination states of unfolded ferrous cytochrome c

Biophysical Journal

Volumn 91, Issue 8, 2006, Pages 3022-3031

  Droghetti, Enrica ^a   Oellerich, Silke ^b,c   Hildebrandt, Peter ^b   Smulevich, Giulietta ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; FERROUS ION; HEME; HISTIDINE; IMIDAZOLE; IRON; METHIONINE; PEROXIDASE;

ABSORPTION; ARTICLE; CONTROLLED STUDY; DENATURATION; ELECTRICITY; HYDROGEN BOND; MICELLE; NONHUMAN; PH; PHOSPHOLIPID VESICLE; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SPECTROSCOPY; TEMPERATURE;

EID: 33749525655     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.079749     Document Type: Article

References (53)

1. Scott, R. A., and A. G. Mauk. 1995. Cytochrome c - A Multidisciplinary Approach. University Science Books, Sausalito, CA.
2. Liu, X., C. N. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptotic program in cell-free extracts: requirement for DATP and cytochrome c. Cell. 86:147-157.
3. Kluck, R. M., L. M. Ellerby, H. M. Ellerby, S. Naiem, M. P. Yaffe, E. Margoliash, D. Bredesen, A. G. Mauk, F. Sherman, and D. D. Newmeyer. 2000. Determinants of cytochrome c pro-apoptotic activity. The role of lysine 72 trimethylation. J. Biol. Chem. 275:16127-16133.
4. Feng, Y., H. Roder, S. W. Englander, A. J. Wand, and D. L. Di Stefano. 1989. Proton resonance assignments of horse ferricytochrome c. Biochemistry. 28:195-203.
5. 1H NMR spectrum of horse ferricytochrome c. Biophys. J. 57:15-22.
6. Bushnell, G. W., G. V. Louie, and G. D. Brayer. 1990. High resolution three-dimensional structure of horse heart cytochrome c. J. Mol. Biol. 214:585-595.
7. Englander, S. W. 2000. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29:213-238.
8. Freire, E. 1995. Thermodynamics of partly folded intermediates in proteins. Annu. Rev. Biophys. Biomol. Struct. 24:141-165.
9. Takahashi, S., S.-R. Yeh, T. K. Das, C.-K. Chan, D. S. Gottfried, and D. L. Rousseau. 1997. Folding of cytochrome c initiated by submillisecond mixing. Nat. Struct. Biol. 4:44-50.
10. Yeh, S.-R., S. Takahashi, B. Fan, and D. L. Rousseau. 1997. Ligand exchange during cytochrome c folding. Nat. Struct. Biol. 4:51-56.
11. Yeh, S.-R., and D. L. Rousseau. 1998. Folding intermediates in cytochrome c. Nat. Struct. Biol. 5:222-228.
12. Russell, B. S., and K. L. Bren. 2002. Denaturant dependence of equilibrium unfolding intermediates and denatured state structure of horse ferricytochrome c. J. Biol. Inorg. Chem. 7:909-916.
13. Oellerich, S., H. Wackerbarth, and P. Hildebrandt. 2002. Spectroscopic characterization of nonnative conformational states of cytochrome c. J. Phys. Chem. Part B. 106:6566-6580.
14. 1H NMR structural characterization of the cytochrome c modifications in a micellar environment. Biochemistry. 42:15342-15351.
15. Yeh, S.-R., S.-W. Han, and D. L. Rousseau. 1998. Cytochrome c folding and unfolding: a biphasic mechanism. Acc. Chem. Res. 31:727-736.
16. Tezcan, F. A., J. R. Winkler, and H. B. Gray. 1998. Effects of ligation and folding on reduction potentials of heme proteins. J. Am. Chem. Soc. 120:13383-13388.
17. Bhuyan, A. K., and R. Kumar. 2002. Kinetic barriers to the folding of horse cytochrome c in the reduced state. Biochemistry. 41:12821-12834.
18. Nishida, S., T. Nada, and M. Terazima. 2005. Hydrogen-bonding dynamics during protein folding of reduced cytochrome c: temperature and denaturant concentration dependence. Biophys. J. 89:2004-2010.
19. Varhac, R., and M. Antalík. 2004. Determination of the pK for the acid-induced denaturation of ferrocytochrome c. Biochemistry. 43:3564-3569.
20. Chen, E., R. A. Goldbeck, and D. S. Kliger. 2003. Earliest events in protein folding: submicrosecond secondary structure formation in reduced cytochrome c. J. Phys. Chem. A. 107:8149-8155.
21. Wang, W., X. Ye, A. A. Demidov, F. Rosca, T. Sjodin, W. Cao, M. Sheeran, and P. M. Champion. 2000. Femtosecond multicolor pump-probe spectroscopy of ferrous cytochrome c. J. Phys. Chem. B. 104:10789-10801.
22. Cianetti, S., M. Négrerie, M. H. Vos, J.-L. Martin, and S. G. Kruglik. 2004. Photodissociation of heme distal methionine in ferrous cytochrome c revealed by subpicosecond time-resolved resonance Raman spectroscopy. J. Am. Chem. Soc. 126:13932-13933.
23. Bhuyan, A. K., and J. B. Udgaonkar. 2001. Folding of horse cytochrome c in the reduced state. J. Mol. Biol. 312:1135-1160.
24. Varhac, R., M. Antalík, and M. Bánó. 2004. Effect of temperature and guanidine hydrochloride on ferrocytochrome c at neutral pH. J. Biol. Inorg. Chem. 9:12-22.
25. Hagen, S., R. F. Latypov, D. A. Olgikh, and H. Oder. 2002. Rapid intrachain binding of histidine-26 and histidine-33 to heme in unfolded ferrocytochrome c. Biochemistry. 41:1372-1380.
26. Telford, J. R., F. A. Tezcan, H. B. Gray, and J. R. Winkler. 1999. Role of ligand substitution in ferrocytochrome c folding. Biochemistry. 38:1944-1949.
27. Yoshimura, T. A. 1988. Change in the heme stereochemistry of cytochrome upon addition of sodium dodecyl sulfate. Electron paramagnetic resonance and electronic absorption spectral study. Arch. Biochem. Biophys. 264:450-461.
28. Hildebrandt, P., and M. Stockburger. 1989. Cytochrome c at charged interfaces. 1. Conformational and redox equilibria at the electrode/electrolyte interface probed by surface-enhanced resonance Raman spectroscopy. Biochemistry. 28:6710-6721.
29. Wang, J.-S., and H. E. Van Wart. 1989. Resonance Raman characterization of the heme c group in N-acetyl microperoxidase-8: a thermal intermediate spin-high spin state mixture. J. Phys. Chem. 93:7925-7931.
30. Döpner, S., P. Hildebrandt, A. G. Mauk, H. Lenk, and W. Stempfle. 1996. Analysis of vibrational spectra of multicomponent systems. Application to pH-dependent resonance Raman spectra of ferricytochrome c. Spectrochimica Acta A. 52:573-584.
31. Margoliash, E., and N. Frohwirt. 1959. Spectrum of horse-heart cytochrome c. Biochem. J. 71:570-572.
32. Andrew, C. R., E. L. Green, D. M. Lawson, and R. R. Eady. 2001. Resonance Raman studies of cytochrome c′ support the binding of NO and CO to opposite sides of the heme: implications for ligand discrimination in heme-based sensor. Biochemistry. 40:4115-4122.
33. Othman, S., A. Le Lirzin, and A. Desbois. 1993. A heme c-peptide model system for the resonance Raman study of c-type cytochromes: characterization of the solvent-dependence of peptide-histidine-heme interactions. Biochemistry. 32:9781-9791.
34. Marques, H. M., and C. B. Perry. 1999. Hemepeptide models for hemoproteins: the behavior of N-acetylmicroperoxidase-11 in aqueous solution. J. Inorg. Biochem. 75:281-291.
35. IINAcMP8). J. Inorg. Biochem. 98:1471-1482.
36. Spiro, T. G., and X.-Y. Li. 1988. Resonance Raman Spectroscopy of Metalloporphyrins, Vol. 3. T. G. Spiro, editor. John Wiley & Sons, New York.
37. Stein, P., and T. G. Spiro. 1980. Hydrogen-bond and deprotonation effects on the resonance Raman iron-imidazole mode in deoxyhemoglobin models: implication for hemoglobin cooperativity. J. Am. Chem. Soc. 102:7795-7797.
38. Hori, H., and T. Kitagawa. 1980. Iron-ligand stretching band in the resonance Raman spectra of ferrous iron porphyrin derivatives. Importance as a probe for quaternary structure of hemoglobin. J. Am. Chem. Soc. 102:3608-3613.
39. Hu, S., I. K. Morris, J. P. Singh, K. M. Smith, and T. G. Spiro. 1993. Complete assignment of cytochrome c resonance Raman spectra via enzymatic reconstitution with isotopically labeled hemes. J. Am. Chem. Soc. 115:12446-12458.
40. Santoni, E., S. Scatragli, F. Sinibaldi, L. Fiorucci, R. Santucci, and G. Smulevich. 2004. A model for the misfolded bis-His intermediate of cytochrome c: the 1-56 N-fragment. J. Inorg. Biochem. 98:1067-1077.
41. Othman, S., P. Richard, A. Vermeglio, and A. Desbois. 1996. Evidence for a proximal histidine-protein interaction in the structure of cytochromes c′ in solution: a resonance Raman study. Biochemistry. 35:9224-9234.
42. Smulevich, G., A. Feis, and B. D. Howes. 2005. Fifteen years of Raman spectroscopy of engineered heme containing peroxidases: what have we learned? Acc. Chem. Res. 38:433-440.
43. Berghuis, A. M., and G. D. Brayer. 1992. Oxidation state-dependent conformational changes in cytochrome c. J. Mol. Biol. 223:959-976.
44. Samuni, U., Y. Ouellet, M. Guertin, J. M. Friedman, and S. R. Yeh. 2004. The absence of proximal strain in the truncated hemoglobins from mycobacterium tuberculosis. J. Am. Chem. Soc. 126:2682-2683.
45. Muga, A., H. H. Mantsch, and W. K. Surewicz. 1991. Membrane binding induces destabilization of cytochrome c structure. Biochemistry. 30:7219-7224.
46. Heimburg, T., and D. Marsh. 1993. Investigation of secondary and tertiary structural changes of cytochrome c in complexes with anionic lipids using amide hydrogen exchange measurements: an FTIR study. Biophys. J. 65:2408-2417.
47. Murgida, D. H., and P. Hildebrandt. 2004. Electron transfer processes of cytochrome c at interfaces. New insights by surface-enhanced resonance Raman spectroscopy. Acc. Chem. Res. 37:854-861.
48. Murgida, D. H., and P. Hildebrandt. 2005. Redox and redox-coupled processes of heme proteins and enzymes at electrochemical interfaces. Phys. Chem. Chem. Phys. 7:3773-3784.
49. Neumann, E. 1986. Chemical electric field effects in biological macromolecules. Prog. Biophys. Mol. Biol. 47:197-231.
50. Murgida, D. H., and P. Hildebrandt. 2001. Heterogeneous electron transfer of cytochrome c on coated silver electrodes. Electric field effects on structure and redox potential. J. Phys. Chem. B. 105:1578-1586.
51. Rivas, L., D. H. Murgida, and P. Hildebrandt. 2002. Conformational and redox equilibria and dynamics of cytochrome c immobilized on electrodes via hydrophobic interactions. J. Phys. Chem. B. 106:4823-4830.
52. Oellerich, S., H. Wackerbarth, and P. Hildebrandt. 2003. Conformational equilibria and dynamics of cytochrome c induced by binding of sodium dodecyl sulfate monomers and micelles. Eur. Biophys. J. 32:599-613.
53. Oellerich, S., S. Lecomte, M. Paternostre, T. Heimburg, and P. Hildebrandt. 2004. Peripheral and integral binding of cytochrome c to phospholipids vesicles. J. Phys. Chem. B. 108:3871-3878.