Brownian dynamics study of cytochrome f interactions with cytochrome c 6 and plastocyanin in Chlamydomonas reinhardtii plastocyanin, and cytochrome c6 mutants

Biophysical Journal

Volumn 88, Issue 3, 2005, Pages 2323-2339

  Haddadian, Esmael J ^a   Gross, Elizabeth L ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CYTOCHROME C6; CYTOCHROME F; HEME; MUTANT PROTEIN; PLASTOCYANIN; RECOMBINANT PROTEIN;

ALGA; ARTICLE; BROWNIAN DYNAMICS; CALCULATION; CHLAMYDOMONAS REINHARDTII; ELECTRON TRANSPORT; EXPERIMENT; HYDROPHOBIC INTERACTION; MODEL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUTATION; PROTEIN PROTEIN INTERACTION; SIMULATION; VAN DER WAALS INTERACTION; AMINO ACID SUBSTITUTION; ANIMAL; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DIFFUSION; ELECTRICITY; GENETICS; KINETICS; METABOLISM; PROTEIN BINDING; SITE DIRECTED MUTAGENESIS;

ALGAE; CHLAMYDOMONAS REINHARDTII;

AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CHLAMYDOMONAS REINHARDTII; COMPUTER SIMULATION; CYTOCHROMES C6; CYTOCHROMES F; DIFFUSION; ELECTROSTATICS; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PLASTOCYANIN; PROTEIN BINDING; RECOMBINANT PROTEINS;

EID: 21244491250     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.053561     Document Type: Article

References (60)

1. + reduction. Biochim. Biophys. Acta. 894:386-398.
2. 1H-NMR chemical shift analysis. Protein Sci. 10:2623-2626.
3. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, L. N. Shindyalov, and P. E. Bourne. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242.
4. Chi, Y. I., L. S. Huang, Z. Zhang, J. G. Fernandez-Velasco, and E. A. Berry. 2000. X-ray structure of a truncated form of cytochrome f from Chlamydomonas reinhardtii. Biochemistry. 39:7689-7701.
5. Crowley, P. B., and M. Ubbink. 2003. Close encounters of the transient kind: protein interactions in the photosynthetic redox chain investigated by NMR spectroscopy. Acc. Chem. Res. 36:723-730.
6. Cui, M., J. Shen, J. M. Briggs, W. Fu, J. Wu, Y. Zhang, X. Luo, Z. Chi, R. Ji, H. Jiang, and K. Chen. 2002. Brownian dynamics simulations of the recognition of the scorpion toxin P05 with small-conductance calcium-activated potassium channels. J. Mol. Biol. 318:417-428.
7. De Rienzo, F., R. R. Gabdoulline, M. C. Menziani, P. G. De Benedetti, and R. C. Wade. 2001. Electrostatic analysis and Brownian dynamics simulation of the association of plastocyanin and cytochrome f. Biophys. J. 81:3090-3104.
8. Durell, S. R., J. K. Labanowski, and E. L. Gross. 1990. Modeling the electrostatic potential field of plastocyanin. Arch. Biochem. Biophys. 277: 241-254.
9. Ejdeback, M., A. Bergkvist, B. G. Karlsson, and M. Ubbink. 2000. Side-chain interactions in the plastocyanin-cytochrome f complex. Biochemistry. 39:5022-5027.
10. Elcock, A. H., R. R. Gabdoulline, R. C. Wade, and J. A. McCammon. 1999. Computer simulation of protein-protein kinetics: acetylcholinesterase- fasciculin. J. Mol. Biol. 291:149-162.
11. Ermark, D. L., and J. C. McCammon. 1978. Brownian dynamics with hydrodynamic interactions. J. Phys. Chem. 69:1352-1360.
12. Gabdoulline, R. R., and J. C. Wade. 2001. Protein-protein associations: investigation of factors influencing association rates by Brownian dynamics simulations. J. Mol. Biol. 9:1139-1155.
13. Gabdoulline, R. R., and R. C. Wade. 1996. Effective charges for macromolecules in solvent. J. Phys. Chem. 100:3868-3878.
14. Gong, X. S., J. Q. Wen, N. E. Fisher, S. Young, C. J. Howe, D. S. Bendall, and J. C. Gray. 2000. The role of individual lysine residues in the basic patch on turnip cytochrome f for the electrostatic interactions with plastocyanin in vitro. Eur. J. Biochem. 267:3461-3468.
15. Gross, E. L. 1996. Plastocyanin: structure, location, diffusion, and electron transfer mechanisms. In Oxygenic Photosynthesis: the Light Reactions. D. On and C. Yocum, editors. Kluwer Academic Publishers. Dordrecht, The Netherlands. 413-429.
16. Gross, E. L. 2004. A Brownian dynamics study of the interaction of Phormidium laminosum plastocyanin with Phormidium laminosum cytochrome f. Biophys. J. 87:2043-2059.
17. 6. Biophys. J. 85:2055-2068.
18. 6 and plastocyanin in Arabidopsis. Nature. 417:567-571.
19. Harvey, S. C. 1989. Treatment of electrostatic effects in macromolecular modeling. Proteins. 5:78-92.
20. Hope, A. B. 2000. Electron transfers amongst cytochrome f, plastocyanin and photosystem 1: kinetics and mechanisms. Biochim. Biophys. Acta. 1456:5-26.
21. Kannt, A., S. Young, and D. S. Bendall. 1996. The role of acidic residues of plastocyanin in its interaction with cytochrome f. Biochim. Biophys. Acta. 1277:115-126.
22. 6 at 1.9 Å resolution: evidence for functional oligomerization. J. Mol. Biol. 250:627-647.
23. Kerfeld, C. A., and D. W. Krogmann. 1998. Photosynthetic cytochromes c in cyanobacteria, algae, and plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:397-425.
24. 6f complex of oxygenic photosynthesis: tuning the cavity. Science. 302:1009-1014.
25. Lee, B. H., T. Hibino, T. Takabe, P. J. Weisbeek, and T. Takabe. 1995. Site-directed mutagenetic study on the role of negative patches on silène plastocyanin in the interactions with cytochrome f and photosystem I. J. Biochem. (Tokyo). 117:1209-1217.
26. Martinez, S. E., D. Huang, M. Ponomarev, W. A. Cramer, and J. L. Smith. 1996. The heme redox center of chloroplast cytochrome f is linked to a buried five-water chain. Protein Sci. 5:1081-1092.
27. Martinez, S. E., D. Huang, A. Szczepaniak, W. A. Cramer, and J. L. Smith. 1994. Crystal structure of the chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure. 2:95-105.
28. Matthew, J. B. 1985. Electrostatic effects in proteins. Annu. Rev. Biophys. Chem. 14:387-417.
29. McCammon, J. A., and S. C. Harvey. 1987. Dynamics of Proteins and Nucleic Acids. Cambridge University Press, Cambridge, UK.
30. Merchant, S., and L. Bogorad. 1986. Regulation by copper of the expression of plastocyanin and cytochrome c552 in Chlamydomonas reinhardtii. Mol. Cell. Biol. 6:462-469.
31. Meyer, T. E., Z. G. Zhao, M. A. Cusanovich, and G. Tollin. 1993. Transient kinetics of electron transfer from a variety of c-type cytochromes to plastocyanin. Biochemistry. 32:4552-4559.
32. Morand, L. Z., M. K. Frame, K. K. Colvert, D. A. Johnson, D. W. Krogmann, and D. J. Davis. 1989. Plastocyanin cytochrome f interaction. Biochemistry. 28:8039-8047.
33. Moser, C. C., J. M. Keske, K. Warncke, R. S. Farid, and P. L. Dutton. 1992. Nature of biological electron transfer. Nature. 355:796-802.
34. Moser, C. C., C. C. Page, R. Farid, and P. L. Dutton. 1995. Biological electron transfer. J. Bioenerg. Biomembr. 27:263-274.
35. Nelson, N., D. C. Pearson, Jr., and E. L. Gross. 1999. The interaction of plastocyanin with cytochrome f: A Brownian dynamics study, in Photosynthesis: Mechanisms and Effects, Vol. 3. G. Garab, editor. Kluwer Academic Publishers, Dordrecht, The Netherlands. 1493-1498.
36. Nicholls, A., and B. Honig. 1991. A rapid finite-difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation. J. Comput. Chem. 12:435-445.
37. Niwa, S., H. Ishikawa, and S. Nikai. 1980. Electron transfer reactions between cytochrome f and plastocyanin from Brassica komatsuna. J. Biochem. (Tokyo). 88:1177-1183.
38. Northrup, S. H. 1996. Theoretical simulation of protein-protein interactions. In Cytochrome c: A Multidisciplinary Approach. R. A. Scott and A. G. Mauk, editors. University Science Publishers, Sausalito, CA. 543-570.
39. Northrup, S. H. 1999. MacroDox v.2.3.1: Software for the Prediction of Macromolecular Interaction. Tennessee Technological University, Cookeville, TN. http://pirn.chem.tntech.edu/macrodox.html
40. Northrup, S. H., J. O. Boles, and J. C. Reynolds. 1987a. Electrostatic effects in the Brownian dynamics of association and orientation of heme proteins. J. Phys. Chem. 91:5991-5998.
41. Northrup, S. H., J. O. Boles, and J. C. Reynolds. 1988. Brownian dynamics of cytochrome c and cytochrome c peroxidase association. Science. 241: 67-70.
42. Northrup, S. H., J. A. Luton, J. O. Boles, and J. C. Reynolds. 1987b. Brownian dynamics simulation of protein association. J. Comput. Aided Mol. Des. 1:291-311.
43. 5. Biochemistry. 32: 6613-6623.
44. Pearson, D. C., Jr. 2000. Brownian dynamics study of the interaction between cytochrome/and mobile electron transfer proteins. PhD thesis. The Ohio State University, Columbus, OH.
45. Pearson, D. C., Jr., and E. L. Gross. 1998. Brownian dynamics study of the interaction between plastocyanin and cytochrome f. Biophys. J. 75:2698-2711.
46. Pearson, D. C., Jr., E. L. Gross, and E. S. David. 1996. The electrostatic properties of cytochrome f: implications for docking with plastocyanin. Biophys. J. 71:64-76.
47. Qin, L., and N. M. Kostic. 1993. Importance of protein rearrangement in the electron-transfer reaction between the physiological partners cytochrome f and plastocyanin. Biochemistry. 32:6073-6080.
48. Redinbo, M. R., D. Cascio, M. K. Choukair, D. Rice, S. Merchant, and T. O. Yeates. 1993. The 1.5-Å crystal structure of plastocyanin from the green alga Chlamydomonas reinhardtii. Biochemistry. 32:10560-10567.
49. Sigfridsson, K. 1998. Plastocyanin, an electron-transfer protein. Pholosynth. Res. 57:1-28.
50. Soriano, G. M., M. V. Pomamarev, R. A. Piskorowski, and W. A. Cramer. 1998. Identification of the basic residues of cytochrome/responsible for electrostatic docking interactions with plastocyanin in vitro: relevance to the electron transfer reaction in vivo. Biochemistry. 37:15120-15128.
51. Soriano, G. M., M. V. Ponomarev, G. S. Tae, and W. A. Cramer. 1996. Effect of the interdomain basic region of cytochrome f on its redox reactions in vivo. Biochemistry. 35:14590-14598.
52. 6f complex. Nature. 426:413-418.
53. Takabe, T., H. Ishikawa, S. Niwa, and Y. Tanaka. 1984. Electron transfer reactions of chemically modified plastocyanin with P700 and cytochrome f. Importance of local charges. J. Biochem. (Tokyo). 96:385-393.
54. Takabe, T., K. Takenaka, H. Kawamura, and Y. Beppu. 1986. Charges on proteins and distances of electron of electron transfer in metalloprotein redox reactions. J. Biochem. (Tokyo). 99:833-840.
55. Takenaka, K., and T. Takabe. 1984. Importance of local positive charges on cytochrome f for electron transfer to plastocyanin and potassium ferricyanide. J. Biochem. (Tokyo). 96:1813-1821.
56. Ubbink, M., M. Ejdeback, B. G. Karlsson, and D. S. Bendall. 1998. The structure of the complex of plastocyanin and cytochrome f, determined by paramagnetic NMR and restrained rigid-body molecular dynamics. Structure. 6:323-335.
57. 6 may be isofunctional with tyrosine 83 in plastocyanin. Biochemistry. 36:16187-16196.
58. Ullmann, G. M., E. W. Knapp, and N. M. Kostic. 1997b. Computational simulation and analysis of dynamic association between plastocyanin and cytochrome f. Consequences for the electron-transfer reaction. J. Am. Chem. Soc. 119:42-52.
59. Warwicker, J., and H. C. Watson. 1982. Calculation of the electric potential in the active site cleft due to alpha-helix dipoles. J. Mol. Biol. 157:671-679.
60. Zhou, J., J. G. Fernandez-Velasco, and R. Malkin. 1996. N-terminal mutants of chloroplast cytochrome f: Effect on redox reactions and growth in Chlamydomonas reinhardtii. J. Biol. Chem. 271:6225-6232.