Abstract
A nonplanar distortion of the heme ofc-type cytochromes is conserved in the proteins isolated from diverse species based upon a comprehensive analysis of available highresolution X-ray crystal structures. This distortion is induced through the cysteine thioether linkages between the porphyrin pyrrole groups and the polypeptide and results in an asymmetric pyrrole distortion. This asymmetry in the heme distortion is also conserved. For other heme proteins which lack these covalent bonds, nearly planar porphyrins are observed. Resonance Raman evidence indicates that nonplanar distortion of porphyrins containing metals, like iron, with large core sizes (≳2.00 Å) is energetically unfavorable and can occur only in the presence of significant environmental perturbations. Further, energy minimization and dynamics calculations on the ferric form of yeast iso-1-cytochromec, starting from the crystallographic coordinates and using a molecular mechanics force field which accurately reproduces nonplanar distortions in metalloporphyrins, suggest that this distortion is indeed maintained by the protein tertiary structure. It is proposed that this protein-linked heme distortion modulates electron transfer function through modification of redox potentials of the porphyrin ring and the protein binding properties ofc-type cytochromes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abola, E. E., Berstein, F. C., Bryant, S. H., Koetzle, T. F., and Weng, J. (1987). InData Commission of the International Union of Crystallography (Allen, F. H., Bergerhoff, G., and Sievers, R., eds.), Bonn/Cambridge/Chester, pp. 107–132.
Alden, R. G., Ondrias, M. R., and Shelnutt, J. A. (1990).J. Am. Chem. Soc. 112, 691–697.
Anderson, K. K., Hobbs, J. D., Luo, L., Stanley, K. D., Quirke, J. M. E., and Shelnutt, J. A. (1993).J. Am. Chem. Soc. 115, 12346–12352.
Barkigia, K. M., Chantranupong, L., Smith, K. M., and Fajer, J. (1988).J. Am. Chem. Soc. 110, 7566–7567.
Berghuis, A. M., and Brayer, G. D. (1992).J. Mol. Biol. 214, 959–976.
Berstein, F. C., Koetzle, T. F., Williams, G. J. B., Meyer, Jr., E. F., Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T., and Tasumi, M. (1977).J. Mol. Biol.,112, 535–545.
Blauer, G., Sreerama, N., and Woody, R. W. (1993).Biochemistry 32, 6674–6679.
Brennan, T. D., Scheidt, W. R., and Shelnutt, J. A. (1988).J. Am. Chem. Soc. 110, 3919–3924.
Bushnell, G. W., Louie, G. V., and Brayer, G. D. (1990).J. Mol. Biol. 214, 585–595
Finzel, B. C., Poulos, T. L., and Kraut, M. (1984).J. Biol. Chem. 259, 13027–13036.
Heibel, G. E., Hildebrandt, P., Ludwig, B., Steinrucke, P., Soulimane, T., and Buse, G. (1993).Biochemistry 32, 11866–10877.
Higuchi, Y., Kusunoki, M., Matsuura, Y., Yasuoka, N., and Kakudo, M. (1984).J. Mol. Biol. 172, 109–139.
Hobbs, J. D., Medforth, C. J., Majumder, S. A., Luo, L., Quirke, J. M. E., and Shelnutt, J. A. (1994).J. Am. Chem. Soc. 116, 3216–3270.
Kadish, K. M., Caemelbecke, E. V., Boulas, P., D'Souza, F., Vogel, E., Kisters, M., Medforth, C. J., and Smith, K. M. (1993).Inorg. Chem. 32, 4177–4178.
Lederer, F., Glatigny, A., Bethge, P. H., and Bellamy, H. D. (1981).J. Mol. Biol. 148, 427–448.
Li, X.-Y., Czernuszewicz, R. S., Kincaid, J. R., Stein, P., and Spiro, T. G. (1990).J. Phys. Chem. 94, 47–61.
Louie, G. V., and Brayer, G. D. (1990).J. Mol. Biol. 214, 527–555.
Luisi, B., Liddington, B., Fermi, G., and Shibayama, N. (1990).J. Mol. Biol. 214, 7–14.
Mathews, F. S., Argos, P., and Levine, M. (1972).Cold Spring Harbor Symp. 36, 387–393.
Matsuura, Y., Takano, T., and Dickerson, R. E. (1982).J. Mol. Biol. 156, 389–409.
Mayo, S. L., Olafson, B. D., and Goddard III, W. A. (1990).J. Phys. Chem. 94, 8897–8909.
Medforth, C. J., Hobbs, J. D., Rodriguez, M. R., Abraham, R. J., Shelnutt, J. A., and Smith, K. M. (1994).Inorg. Chem., submitted.
Moore, G. R., and Pettigrew, G. W. (1990). InCytochromes c: Evolutionary, Structural and Physicochemical Aspects, Springer-Verlag, Berlin.
Ochi, H., Hata, Y., Tanaka, N., Kakudo, M., Sakurai, T., Aihara, S., and Morita, Y. (1983).J. Mol. Biol. 266, 407–418.
Poulos, T. L., Finzel, B. C., and Howard, A. J. (1987).J. Mol. Biol. 195, 687–700.
Rappé, A. K., and Goddard III, W. A. (1991).J. Phys. Chem. 95, 3358–3363.
Salemme, F. R., Freer, S. T., Xuong, Ng, H., Alden, R. A., and Kraut, J. (1973).J. Biol. Chem. 248, 3910–3921.
Shelnutt, J. A., Rousseau, D. L., Dethmers, J. K., and Margoliash, E. (1981).Biochemistry 20, 6485–6496.
Shelnutt, J. A., Straub, K. D., Rentzepis, P. M., Gouterman, M., and Davidson, E. R. (1983).Biochemistry 23, 3946–3954.
Shelnutt, J. A., Medforth, C. J., Berber, M. D., Barkigia, K. M., and Smith, K. M. (1991).J. Am. Chem. Soc. 113, 4077–4087.
Sparks, L. D., Medforth, C. J., Park, M.-S., Chamberlain, J. R., Ondfias, M. R., Senge, M. O., Smith, K. M., and Shelnutt, J. A. (1993).J. Am. Chem. Soc. 115, 581–592.
Sparks, L. D., Medforth, C. J., Smith, K. M., Shelnutt, J. A. (1994).Inorg. Chem. 33, 2297–2302.
Takano, T., and Dickerson, R. E. (1981a).J. Mol. Biol. 153, 79–94.
Takano, T., and Dickerson, R. E. (1981b).J. Mol. Biol. 153, 95–115.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hobbs, J.D., Shelnutt, J.A. Conserved nonplanar heme distortions in cytochromesc. J Protein Chem 14, 19–25 (1995). https://doi.org/10.1007/BF01902840
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF01902840