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. 2001 Dec;81(6):3090–3104. doi: 10.1016/S0006-3495(01)75947-4

Electrostatic analysis and Brownian dynamics simulation of the association of plastocyanin and cytochrome f.

F De Rienzo 1, R R Gabdoulline 1, M C Menziani 1, P G De Benedetti 1, R C Wade 1
PMCID: PMC1301771  PMID: 11720977

Abstract

The oxidation of cytochrome f by the soluble cupredoxin plastocyanin is a central reaction in the photosynthetic electron transfer chain of all oxygenic organisms. Here, two different computational approaches are used to gain new insights into the role of molecular recognition and protein-protein association processes in this redox reaction. First, a comparative analysis of the computed molecular electrostatic potentials of seven single and multiple point mutants of spinach plastocyanin (D42N, E43K, E43N, E43Q/D44N, E59K/E60Q, E59K/E60Q/E43N, Q88E) and the wt protein was carried out. The experimentally determined relative rates (k(2)) for the set of plastocyanin mutants are found to correlate well (r(2) = 0.90 - 0.97) with the computed measure of the similarity of the plastocyanin electrostatic potentials. Second, the effects on the plastocyanin/cytochrome f association rate of these mutations in the plastocyanin "eastern site" were evaluated by simulating the association of the wild type and mutant plastocyanins with cytochrome f by Brownian dynamics. Good agreement between the computed and experimental relative rates (k(2)) (r(2) = 0.89 - 0.92) was achieved for the plastocyanin mutants. The results obtained by applying both computational techniques provide support for the fundamental role of the acidic residues at the plastocyanin eastern site in the association with cytochrome f and in the overall electron-transfer process.

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Selected References

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  1. Adman E. T. Copper protein structures. Adv Protein Chem. 1991;42:145–197. doi: 10.1016/s0065-3233(08)60536-7. [DOI] [PubMed] [Google Scholar]
  2. Blomberg N., Gabdoulline R. R., Nilges M., Wade R. C. Classification of protein sequences by homology modeling and quantitative analysis of electrostatic similarity. Proteins. 1999 Nov 15;37(3):379–387. doi: 10.1002/(sici)1097-0134(19991115)37:3<379::aid-prot6>3.0.co;2-k. [DOI] [PubMed] [Google Scholar]
  3. Carrell C. J., Schlarb B. G., Bendall D. S., Howe C. J., Cramer W. A., Smith J. L. Structure of the soluble domain of cytochrome f from the cyanobacterium Phormidium laminosum. Biochemistry. 1999 Jul 27;38(30):9590–9599. doi: 10.1021/bi9903190. [DOI] [PubMed] [Google Scholar]
  4. Ciocchetti A., Bizzarri A. R., Cannistraro S. Long-term molecular dynamics simulation of copper plastocyanin in water. Biophys Chem. 1997 Dec 1;69(2-3):185–198. doi: 10.1016/s0301-4622(97)00089-6. [DOI] [PubMed] [Google Scholar]
  5. De Rienzo F., Gabdoulline R. R., Menziani M. C., Wade R. C. Blue copper proteins: a comparative analysis of their molecular interaction properties. Protein Sci. 2000 Aug;9(8):1439–1454. doi: 10.1110/ps.9.8.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ejdebäck M., Bergkvist A., Karlsson B. G., Ubbink M. Side-chain interactions in the plastocyanin-cytochrome f complex. Biochemistry. 2000 May 2;39(17):5022–5027. doi: 10.1021/bi992757c. [DOI] [PubMed] [Google Scholar]
  7. Elcock A. H., Gabdoulline R. R., Wade R. C., McCammon J. A. Computer simulation of protein-protein association kinetics: acetylcholinesterase-fasciculin. J Mol Biol. 1999 Aug 6;291(1):149–162. doi: 10.1006/jmbi.1999.2919. [DOI] [PubMed] [Google Scholar]
  8. Gabdoulline R. R., Wade R. C. Brownian dynamics simulation of protein-protein diffusional encounter. Methods. 1998 Mar;14(3):329–341. doi: 10.1006/meth.1998.0588. [DOI] [PubMed] [Google Scholar]
  9. Gabdoulline R. R., Wade R. C. On the protein-protein diffusional encounter complex. J Mol Recognit. 1999 Jul-Aug;12(4):226–234. doi: 10.1002/(SICI)1099-1352(199907/08)12:4<226::AID-JMR462>3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  10. Gabdoulline R. R., Wade R. C. Protein-protein association: investigation of factors influencing association rates by brownian dynamics simulations. J Mol Biol. 2001 Mar 9;306(5):1139–1155. doi: 10.1006/jmbi.2000.4404. [DOI] [PubMed] [Google Scholar]
  11. Gabdoulline R. R., Wade R. C. Simulation of the diffusional association of barnase and barstar. Biophys J. 1997 May;72(5):1917–1929. doi: 10.1016/S0006-3495(97)78838-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gong X. S., Wen J. Q., Fisher N. E., Young S., Howe C. J., Bendall D. S., Gray J. C. The role of individual lysine residues in the basic patch on turnip cytochrome f for electrostatic interactions with plastocyanin in vitro. Eur J Biochem. 2000 Jun;267(12):3461–3468. doi: 10.1046/j.1432-1327.2000.01366.x. [DOI] [PubMed] [Google Scholar]
  13. Gong X. S., Wen J. Q., Gray J. C. The role of amino-acid residues in the hydrophobic patch surrounding the haem group of cytochrome f in the interaction with plastocyanin. Eur J Biochem. 2000 Mar;267(6):1732–1742. doi: 10.1046/j.1432-1327.2000.01168.x. [DOI] [PubMed] [Google Scholar]
  14. Gross E. L., Curtiss A., Durell S. R., White D. Chemical modification of spinach plastocyanin using 4-chloro-3,5-dinitrobenzoic acid: characterization of four singly-modified forms. Biochim Biophys Acta. 1990 Mar 15;1016(1):107–114. doi: 10.1016/0005-2728(90)90012-s. [DOI] [PubMed] [Google Scholar]
  15. Hibino T., Lee B. H., Yajima T., Odani A., Yamauchi O., Takabe T. Kinetic and cross-linking studies on the interactions of negative patch mutant plastocyanin from Silene pratensis with photosystem I complexes from cyanobacteria, green algae, and plants. J Biochem. 1996 Sep;120(3):556–563. doi: 10.1093/oxfordjournals.jbchem.a021450. [DOI] [PubMed] [Google Scholar]
  16. Hirota S., Hayamizu K., Okuno T., Kishi M., Iwasaki H., Kondo T., Hibino T., Takabe T., Kohzuma T., Yamauchi O. Spectroscopic and electrochemical studies on structural change of plastocyanin and its tyrosine 83 mutants induced by interaction with lysine peptides. Biochemistry. 2000 May 30;39(21):6357–6364. doi: 10.1021/bi9929812. [DOI] [PubMed] [Google Scholar]
  17. Hooft R. W., Sander C., Vriend G. Positioning hydrogen atoms by optimizing hydrogen-bond networks in protein structures. Proteins. 1996 Dec;26(4):363–376. doi: 10.1002/(SICI)1097-0134(199612)26:4<363::AID-PROT1>3.0.CO;2-D. [DOI] [PubMed] [Google Scholar]
  18. Hope A. B. Electron transfers amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms. Biochim Biophys Acta. 2000 Jan 3;1456(1):5–26. doi: 10.1016/s0005-2728(99)00101-2. [DOI] [PubMed] [Google Scholar]
  19. Illerhaus J., Altschmied L., Reichert J., Zak E., Herrmann R. G., Haehnel W. Dynamic interaction of plastocyanin with the cytochrome bf complex. J Biol Chem. 2000 Jun 9;275(23):17590–17595. doi: 10.1074/jbc.275.23.17590. [DOI] [PubMed] [Google Scholar]
  20. Lee B. H., Hibino T., Takabe T., Weisbeek P. J., Takabe T. Site-directed mutagenetic study on the role of negative patches on silene plastocyanin in the interactions with cytochrome f and photosystem I. J Biochem. 1995 Jun;117(6):1209–1217. doi: 10.1093/oxfordjournals.jbchem.a124846. [DOI] [PubMed] [Google Scholar]
  21. Martinez S. E., Huang D., Szczepaniak A., Cramer W. A., Smith J. L. Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure. 1994 Feb 15;2(2):95–105. doi: 10.1016/s0969-2126(00)00012-5. [DOI] [PubMed] [Google Scholar]
  22. Northrup S. H., Boles J. O., Reynolds J. C. Brownian dynamics of cytochrome c and cytochrome c peroxidase association. Science. 1988 Jul 1;241(4861):67–70. doi: 10.1126/science.2838904. [DOI] [PubMed] [Google Scholar]
  23. Pearson D. C., Jr, Gross E. L. Brownian dynamics study of the interaction between plastocyanin and cytochrome f. Biophys J. 1998 Dec;75(6):2698–2711. doi: 10.1016/S0006-3495(98)77714-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pearson D. C., Jr, Gross E. L., David E. S. Electrostatic properties of cytochrome f: implications for docking with plastocyanin. Biophys J. 1996 Jul;71(1):64–76. doi: 10.1016/S0006-3495(96)79236-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Qin L., Kostić N. M. Importance of protein rearrangement in the electron-transfer reaction between the physiological partners cytochrome f and plastocyanin. Biochemistry. 1993 Jun 15;32(23):6073–6080. doi: 10.1021/bi00074a019. [DOI] [PubMed] [Google Scholar]
  26. Redinbo M. R., Yeates T. O., Merchant S. Plastocyanin: structural and functional analysis. J Bioenerg Biomembr. 1994 Feb;26(1):49–66. doi: 10.1007/BF00763219. [DOI] [PubMed] [Google Scholar]
  27. Roberts V. A., Freeman H. C., Olson A. J., Tainer J. A., Getzoff E. D. Electrostatic orientation of the electron-transfer complex between plastocyanin and cytochrome c. J Biol Chem. 1991 Jul 15;266(20):13431–13441. [PubMed] [Google Scholar]
  28. Soriano G. M., Cramer W. A., Krishtalik L. I. Electrostatic effects on electron-transfer kinetics in the cytochrome f-plastocyanin complex. Biophys J. 1997 Dec;73(6):3265–3276. doi: 10.1016/S0006-3495(97)78351-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ubbink M., Ejdebäck M., Karlsson B. G., Bendall D. S. The structure of the complex of plastocyanin and cytochrome f, determined by paramagnetic NMR and restrained rigid-body molecular dynamics. Structure. 1998 Mar 15;6(3):323–335. doi: 10.1016/s0969-2126(98)00035-5. [DOI] [PubMed] [Google Scholar]
  30. Vriend G. WHAT IF: a molecular modeling and drug design program. J Mol Graph. 1990 Mar;8(1):52-6, 29. doi: 10.1016/0263-7855(90)80070-v. [DOI] [PubMed] [Google Scholar]
  31. Xue Y., Okvist M., Hansson O., Young S. Crystal structure of spinach plastocyanin at 1.7 A resolution. Protein Sci. 1998 Oct;7(10):2099–2105. doi: 10.1002/pro.5560071006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zhou H. X., Briggs J. M., Tara S., McCammon J. A. Correlation between rate of enzyme-substrate diffusional encounter and average Boltzmann factor around active site. Biopolymers. 1998 Apr;45(5):355–360. doi: 10.1002/(SICI)1097-0282(19980415)45:5<355::AID-BIP4>3.0.CO;2-K. [DOI] [PubMed] [Google Scholar]

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