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A Brownian dynamics computational study of the interaction of spinach plastocyanin with turnip cytochrome f: the importance of plastocyanin conformational changes

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Abstract

Brownian Dynamics (BD) computer simulations were used to study electrostatic interactions between turnip cytochrome f (cyt f) and spinach plastocyanin (PC). Three different spinach PC structures were studied: The X-ray crystal structure of Xue and coworkers [(1998) Protein Sci 7:2099–2105] and the NMR structure of Musiani et al. [(2005) J Biol Chem 280:18833–18841] and Ubbink and co-workers [(1998) Structure 6:323–335]. Significant differences exist in the backbone conformation between the PC taken from Ubbink and coworkers and the other two PC structures particularly the regions surrounding G10, E59–E60, and D51. Complexes formed in BD simulations using the PC of Ubbink and colleagues had a smaller Cu–Fe distance than the other two. These results suggest that different PC conformations may exist in solution with different capabilities of forming electron-transfer-active docks. All three types of complexes show electrostatic contacts between D42, E43, and D44 on PC and K187 on cyt f as well as between E59 on PC and K58 on cyt f. However, the PC of Ubbink and coworkers reveals additional contacts between D51 and cyt f as a result of the difference in backbone configuration. A second minor complex component was observed for the PC of Ubbink and co-workers and Xue and co-workers which had contacts between K187 on cyt f and E59 and E60 on PC rather than between K187 on cyt f and D42-D44 on PC as observed for the major components. This second type of complex may represent an earlier complex which rearranges to form a final complex capable of electron transfer.

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Abbreviations

BD:

Brownian dynamics

cyt f :

Cytochrome f

PC:

Plastocyanin

RMS:

Root mean square

References

  • Allen JF (2004) Cytochrome b6f structure for signaling and vectorial metabolism. Trends Plant Sci 9:130–137

    Article  PubMed  CAS  Google Scholar 

  • Anderson GP, Sanderson DG, Lee CH, Durell S, Anderson LB, Gross EL (1987) The effect of ethylene diamine chemical modification of plastocyanin on the rate of cytochrome f oxidation and P-7001 reduction. Biochim Biophys Acta 894:386–398

    Article  PubMed  CAS  Google Scholar 

  • Arcangeli C, Bizzari AR, Cannistraro S (2001) Concerted motions in copper plastocyanin and azurin: An essential dynamics study. Biophys Chem 90:45–56

    Article  PubMed  CAS  Google Scholar 

  • Barkiest A (2000) Protein structure and interaction studied by NMR: Spinach plastocyanin and E. coli transhydrogenas. Dissertation, Göteborg University, Sweden

  • Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov LN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242

    Article  PubMed  CAS  Google Scholar 

  • Carrell CJ, Schlarb BG, Bendall DS, Howe CJ, Cramer WA, Smith JL (1999) Structure of the soluble domain of cytochrome f from the cyanobacterium Phormidium laminosum. Biochemistry 38:9590–9599

    Article  PubMed  CAS  Google Scholar 

  • Chi YIL, Huang LS, Zhang Z, Fernandez-Velasco JG, Berry EA (2000) X-ray structure of a truncated form of cytochrome f from Chlamydomonas reinhardtii. Biochemistry 39:7689–7701

    Article  PubMed  CAS  Google Scholar 

  • Ciocchetti A, Bizzarri AR, Cannistraro S (1997) Long-term molecular dynamics simulation of copper plastocyanin in water. Biophys Chem 69:185–198

    Article  PubMed  CAS  Google Scholar 

  • Crowley PB, Ubbink M (2003) Close encounters of the transient kind: protein interactions in the photosynthetic redox chain investigated by NMR spectroscopy. Acc Chem Res 36:723–730

    Article  PubMed  CAS  Google Scholar 

  • Crowley PB, Hunter DM, Sato K, McFarlane W, Dennison K (2004) The parsley plastocyanin-turnip cytochrome f complex: a structurally distorted but kinetically functional acidic patch. Biochem J 378:45–51

    Article  PubMed  CAS  Google Scholar 

  • De Rienzo F, Gabdoulline RR, Menziani MC, De Benedetti PG, Wade RC (2001) Electrostatic analysis and Brownian dynamics simulation of the association of plastocyanin and cytochrome f. Biophys J 81:3090–3104

    PubMed  Google Scholar 

  • Durell SR, Labanowski JK, Gross EL. (1990) Modeling of the electrostatic potential field of plastocyanin. Arch Biochem Biophys 277:241–254

    Article  PubMed  CAS  Google Scholar 

  • Ejdeback M, Bergkvist A, Karlsson BG, Ubbink M (2000) Side-chain interactions in the plastocyanin-cytochrome f complex. Biochemistry 39:5022–5027

    Article  PubMed  CAS  Google Scholar 

  • Ermak DL, McCammon JA (1978) Brownian dynamics with hydrodynamic interactions. J Phys Chem 69:1352–1360

    Article  CAS  Google Scholar 

  • Freeman HC (1981). Electron transfer in “blue” copper proteins. Coord Chem 21:29–52

    Google Scholar 

  • Gabdoulline RR, Wade RC (1998) Brownian dynamics simulation of protein-protein diffusional encounter. Methods 14:329–341

    Article  PubMed  CAS  Google Scholar 

  • Gong XS, Wen JQ, Fisher NE, Young S, Howe CJ, Bendall DS, Gray JC (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

    Article  PubMed  CAS  Google Scholar 

  • Gray J (1992) Cytochrome f: structure, function and biosynthesis. Photosynth Res 34:359–374

    Article  CAS  Google Scholar 

  • Gross EL (1996) Plastocyanin: structure, location, diffusion, electron transfer mechanisms. In: Ort D, Yocum C (eds) Oxygenic photosynthesis: the light reactions. Advances in Photosynthesis, vol 4. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp 413–429

    Google Scholar 

  • Gross EL (2004) A Brownian dynamics study of the interaction of Phormidium laminosum plastocyanin with Phormidium laminosum cytochrome f. Biophys J 87:2043–2059

    Article  PubMed  CAS  Google Scholar 

  • Gross EL, Pearson Jr DC (2003) Brownian dynamics simulations of the interaction of Chlamydomonas cytochrome f with plastocyanin and cytochrome c6. Biophys J 85:2055–2068

    PubMed  CAS  Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723

    Article  PubMed  CAS  Google Scholar 

  • Haddadian EJ, Gross EL (2005) Brownian dynamics study of cytochrome f interactions with cytochrome c6 and plastocyanin in Chlamydomonas reinhardtii: plastocyanin and cytochrome c6 mutants. Biophys J 88:2823–2839

    Article  CAS  Google Scholar 

  • Haddadian EJ, Gross EL (2006) A Brownian dynamics study of the effects of cytochrome f structure and deletion of its small domain in interactions with cytochrome c6 and plastocyanin in Chlamydomonas reinhardtii. Biophys J 90:566–577

    Article  PubMed  CAS  Google Scholar 

  • Harvey SC (1989) Treatment of electrostatic effects in macromolecular modeling. Proteins 5:78–92

    Article  PubMed  CAS  Google Scholar 

  • Hope AB (2000) Electron transfers amongst cytochrome f, plastocyanin and photosystemI: kinetics and mechanisms. Biochim Biophys Acta 1456:5–26

    Article  PubMed  CAS  Google Scholar 

  • Kannt A, Young S, Bendall DS (1996) The role of acidic residues of plastocyanin in its interaction with cytochrome f. Biochim Biophys Acta 1277:115–126

    Article  CAS  Google Scholar 

  • Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1013

    Article  PubMed  CAS  Google Scholar 

  • Lange C, Cornvik T, Diaz-Moreno I, Ubbink M (2005) The transient complex of poplar plastocyanin with cytochrome f: effects of ionic strength and pH. Biochim Biophys Acta 1707:179–188

    Article  PubMed  CAS  Google Scholar 

  • Lee BH, Hibino T, Takabe T, Weisbeek PJ, Takabe T (1995) Site-directed mutagenetic study on the role of negative patches on silene plastocyanin in the interactions with cytochrome f and photosystem I. J Biochem (Tokyo) 117:1209–1217

    CAS  Google Scholar 

  • Martinez SE, Huang D, Szczepaniak A, Cramer WA, Smith JL (1994) Crystal structure of the chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 2:95–105

    Article  PubMed  CAS  Google Scholar 

  • Martinez SE, Huang D, Ponomarev M, Cramer WA, Smith JL (1996) The heme redox center of chloroplast cytochrome f is linked to a buried five-water chain. Protein Sci 5:1081–1092

    Article  PubMed  CAS  Google Scholar 

  • Matthew JB (1985) Electrostatic effects in proteins. Annu Rev Biophys Biophys Chem 14:387–417

    Article  PubMed  CAS  Google Scholar 

  • McCammon JA, Harvey SC (1987) Dynamics of proteins and nucleic acids. Cambridge University Press, Cambridge

    Google Scholar 

  • Morand LZ, Frame MK, Colvert KK, Johnson DA, Krogmann DW, Davis D (1989) Plastocyanin cytochrome f interaction. Biochemistry 28:8039–8047

    Article  PubMed  CAS  Google Scholar 

  • Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL (1992) Nature of biological electron transfer. Nature 355:796–802

    Article  PubMed  CAS  Google Scholar 

  • Moser CC, Page CC, Farid R, Dutton PL (1995) Biological electron transfer. J Bioenerg Biomembr 27:263–274

    Article  PubMed  CAS  Google Scholar 

  • Musiani F, Dikyi A, Semenov AY, Ciurli S (2005) Structure of the intermolecular complex between plastocycanin and cytochrome f from spinach. J Biol Chem 280:18833–18841

    Article  PubMed  CAS  Google Scholar 

  • Nicholls A, Honig B (1991) A rapid finite-difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation. J Comp Chem 12:435–445

    Article  CAS  Google Scholar 

  • Northrup SH (1996) Theoretical simulation of protein-protein interactions. In: Scott RA, Mauk AG (eds) Cytochrome c: a multidiciplinary approach. University Science Publishers, Sausalito, CA, pp 543–570

    Google Scholar 

  • Northrup SH (1999) Macrodox v.2.3.1: software for the prediction of macromolecular interaction. Tennessee Technological University, Cookeville, TN

    Google Scholar 

  • Northrup SH, Boles JO, Reynolds JCL (1987). Electrostatic effects in the Brownian dynamics of association and orientation of heme proteins. J Phys Chem 91:5991–5998

    Article  CAS  Google Scholar 

  • Northrup SH, Boles JO, Reynolds JC (1988) Brownian dynamics of cytochrome c and cytochrome c peroxidase association. Science 241:67–70

    Article  PubMed  CAS  Google Scholar 

  • Northrup SH, Thomasson KA, Miller CM, Barker PD, Eltis LD, Guillemette JG, Inglis SC, Mauk AG (1993) Effect of charged amino acid mutations on the bimolecular kinetics of reduction of yeast iso-1-ferricytochrome c by bovine ferrocytochrome b5. Biochemistry 32:6613–6623

    Article  PubMed  CAS  Google Scholar 

  • Pearson DC Jr, Gross EL (1998) Brownian dynamics study of the interaction between plastocyanin and cytochrome f. Biophys J 75:2698–2711

    Article  PubMed  CAS  Google Scholar 

  • Redinbo MR, Yeates TO, Merchant S (1994) Plastocyanin: structural and functional analysis. J Bioenerg Biomembr 26:49–66

    Article  PubMed  CAS  Google Scholar 

  • Sigfridsson K (1998) Plastocyanin, an electron-transfer protein. Photosynth Res 57:1–28

    Article  CAS  Google Scholar 

  • Soriano GM, Ponomarev MV, Tae GS, Cramer WA (1996) Effect of the interdomain basic region of cytochrome f on its redox reactions in vivo. Biochemistry 35:14590–14598

    Article  PubMed  CAS  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical heme in the cytochrome b(6)f complex. Nature 426:413–418

    Article  PubMed  CAS  Google Scholar 

  • Sykes AG (1991) Plastocyanin and the blue copper proteins. Struct Bond 75:175–224

    CAS  Google Scholar 

  • Ubbink M (2004) Complexes of photosynthetic redox proteins studied by NMR. Photosynth Res 81:277–287

    Article  PubMed  CAS  Google Scholar 

  • Ubbink M, Ejdebäck M, Karlsson BG, Bendall DS (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

    Article  PubMed  CAS  Google Scholar 

  • Warwicker J, Watson HC (1982) Calculation of the electric potential in the active site cleft due to alpha-helix dipoles. J Mol Biol 157:671–679

    Article  PubMed  CAS  Google Scholar 

  • Xue Y, Okvist M, Hansson O, Young S (1998) Crystal structure of spinach plastocyanin at 1.7 Å resolution. Protein Sci 7:2099–2105

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author wishes to thank the Dept. of Biochemistry at OSU for its support and Mr. Bryan Hill for his careful reading of the manuscript.

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  1. Department of Biochemistry, The Ohio State University, 484 W. 12th. Ave, Columbus, OH, 43235, USA

    Elizabeth L. Gross

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  1. Elizabeth L. Gross
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Correspondence to Elizabeth L. Gross.

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Professor Elizabeth L. Gross, Professor Emeritus of Biochemistry, The Ohio State University, passed away on June 27, 2007.

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Gross, E.L. A Brownian dynamics computational study of the interaction of spinach plastocyanin with turnip cytochrome f: the importance of plastocyanin conformational changes. Photosynth Res 94, 411–422 (2007). https://doi.org/10.1007/s11120-007-9192-y

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