Electrostatic strain and concerted motions in the transient complex between plastocyanin and cytochrome f from the cyanobacterium Phormidium laminosum

Bioelectrochemistry

Volumn 77, Issue 1, 2009, Pages 43-52

  Díaz Moreno, Irene ^a   Muñoz López, Francisco J ^a   Frutos Beltrán, Estrella ^a   De la Rosa, Miguel A ^a   Díaz Quintana, Antonio ^a  

^a Universidad de Sevilla CSIC   (Spain)

Author keywords

Cytochrome f; Domain motions; Molecular dynamics; Plastocyanin; Transient protein complexes

Indexed keywords

COMPLEX CONFORMATION; CYANOBACTERIUM; CYTOCHROME F; DOMAIN MOTIONS; ELECTRON TRANSFER; ELECTRON TRANSPORT; ELECTROSTATIC INTERACTIONS; METAL SITES; MOLECULAR DYNAMICS SIMULATIONS; PHORMIDIUM; PLASTOCYANIN; PLASTOCYANINS; TRANSIENT COMPLEXES;

BIOLOGY; CONFORMATIONS; DYNAMICS; ELECTRON TRANSITIONS; ELECTROSTATICS; MOLECULAR DYNAMICS;

PRINCIPAL COMPONENT ANALYSIS;

CYTOCHROME F; METAL; PLASTOCYANIN;

ARTICLE; CONFORMATION; CYANOBACTERIUM; ELECTRICITY; ELECTRON TRANSPORT; MOLECULAR DYNAMICS; NONHUMAN; PHORMIDIUM LAMINOSUM; PRINCIPAL COMPONENT ANALYSIS; PROTEIN INTERACTION; SIMULATION;

CYTOCHROMES F; MOLECULAR DYNAMICS SIMULATION; MOVEMENT; OSCILLATORIA; PLASTOCYANIN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; TIME FACTORS;

PHORMIDIUM LAMINOSUM;

EID: 70349462943     PISSN: 15675394     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bioelechem.2009.06.003     Document Type: Article

References (61)

1. Prudêncio M., and Ubbink M. Transient complexes of redox proteins: structural and dynamic details from NMR studies. J. Mol. Recogn. 17 (2004) 524-539
2. Hervás M., Navarro J.A., and De la Rosa M.A. Electron transfer between membrane complexes and soluble proteins in photosynthesis. Acc. Chem. Res. 36 (2003) 798-805
3. Hope A.B. Electron transfers amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms. Biochim. Biophys. Acta 1456 (2000) 5-26
4. Volkov A.N., Worrall J.A.R., Holtzmann E., and Ubbink M. From the cover: solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc. Natl. Acad. Sci. USA 103 (2006) 18945-18950
5. Crowley P.B., and Ubbink M. Close encounters of the transient kind: protein interactions in the photosynthetic redox chain investigated by NMR spectroscopy. Acc. Chem. Res. 36 (2003) 723-730
6. Gray J.C. Cytochrome f: structure, function and biosynthesis. Photosynth. Res. 34 (1992) 359-374
7. Albarrán C., Navarro J.A., De la Rosa M.A., and Hervás M. The specificity in the interaction between cytochrome f and plastocyanin from the cyanobacterium Nostoc sp. PCC 7119 is mainly determined by the copper protein. Biochemistry 46 (2007) 997-1003
8. Díaz-Moreno I., Díaz-Quintana A., De la Rosa M.A., and Ubbink M. Structure of the complex between plastocyanin and cytochrome f from the cyanobacterium Nostoc sp. PCC 7119 as determined by paramagnetic NMR: the balance between electrostatic and hydrophobic interactions within the transient complex determines the relative orientation of the two proteins. J. Biol. Chem. 280 (2005) 18908-18915
9. Díaz-Moreno I., Díaz-Quintana A., De la Rosa M.A., Crowley P.B., and Ubbink M. Different modes of interaction in cyanobacterial complexes of plastocyanin and cytochrome f. Biochemistry 44 (2005) 3176-3183
10. Martínez S.E., Huang D., Szczepaniak A., Cramer W.A., and Smith J.L. Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 2 (1994) 95-105
11. Gong X.-S., Wen J.Q., Fisher N.E., Young S., Howe C.J., Bendall D.S., and 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. 267 (2000) 3461-3468
12. Illerhaus J., Altschmied L., Reichert J., Zak E., Herrmann R.G., and Haehnel W. Dynamic interaction of plastocyanin with the cytochrome bf complex. J. Biol. Chem. 275 (2000) 17590-17595
13. Kannt A., Young S., and Bendall D.S. The role of acidic residues of plastocyanin in its interaction with cytochrome f. Biochim. Biophys. Acta 1277 (1996) 115-126
14. Schlarb-Ridley B.G., Bendall D.S., and Howe C.J. Role of electrostatics in the interaction between cytochrome f and plastocyanin of the cyanobacterium Phormidium laminosum. Biochemistry 41 (2002) 3279-3285
15. Schlarb-Ridley B.G., Bendall D.S., and Howe C.J. Relation between interface properties and kinetics of electron transfer in the interaction of cytochrome f and plastocyanin from plants and the cyanobacterium Phormidium laminosum. Biochemistry 42 (2003) 4057-4063
16. Albarrán C., Navarro J.A., Molina-Heredia F.P., Murdoch P.d.S., De la Rosa M.A., and Hervás M. Laser flash-induced kinetic analysis of cytochrome f oxidation by wild-type and mutant plastocyanin from the cyanobacterium Nostoc sp. PCC 7119. Biochemistry 44 (2005) 11601-11607
17. Ullmann G.M., Knapp E.W., and Kostic N.M. Computational simulation and analysis of dynamic association between plastocyanin and cytochrome f. Consequences for the electron-transfer reaction. J. Am. Chem. Soc. 119 (1997) 42-52
18. Hulsker R., Baranova M.V., Bullerjahn G.S., and Ubbink M. Dynamics in the transient complex of plastocyanin-cytochrome f from Prochlorothrix hollandica. J. Am. Chem. Soc. 130 (2008) 1985-1991
19. Musiani F., Dikiy A., Semenov A.Y., and Ciurli S. Structure of the intermolecular complex between plastocyanin and cytochrome f from spinach. J. Biol. Chem. 280 (2005) 18833-18841
20. De Rienzo F., Gabdoulline R.R., Menziani M.C., De Benedetti P.G., and Wade R.C. Electrostatic analysis and Brownian dynamics simulation of the association of plastocyanin and cytochrome f. Biophys. J. 81 (2001) 3090-3104
21. De Rienzo F., Grant G.H., and Menziani M.C. Theoretical descriptors for the quantitative rationalisation of plastocyanin mutant functional properties. J. Comput.-Aided Mol. Des. 16 (2002) 501-509
22. 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 (2007) 411-422
23. Gross E.L. A Brownian dynamics study of the interaction of Phormidium laminosum plastocyanin with Phormidium laminosum cytochrome f. Biophys. J. 87 (2004) 2043-2059
24. 6. Biophys. J. 85 (2003) 2055-2068
25. Gross E.L., and Rosenberg I. A Brownian dynamics study of the interaction of Phormidium cytochrome f with various cyanobacterial plastocyanins. Biophys. J. 90 (2006) 366-380
26. 6 mutants. Biophys. J. 88 (2005) 2323-2339
27. 6 and plastocyanin in Chlamydomonas reinhardtii. Biophys. J. 90 (2006) 566-577
28. 6: the effects of the Rieske FeS protein on the interactions. Biophys. J. 91 (2006) 2589-2600
29. Crowley P.B., Otting G., Schlarb-Ridley B.G., Canters G.W., and Ubbink M. Hydrophobic interactions in a cyanobacterial plastocyanin-cytochrome f complex. J. Am. Chem. Soc. 123 (2001) 10444-10453
30. Ubbink M., Ejdeback M., Karlsson B.G., and Bendall D.S. The structure of the complex of plastocyanin and cytochrome f, determined by paramagnetic NMR and restrained rigid-body molecular dynamics. Structure 15 (1998) 323-335
31. Hart S.E., Schlarb-Ridley B.G., Delon C., Bendall D.S., and Howe C.J. Role of charges on cytochrome f from the cyanobacterium Phormidium laminosum in its interaction with plastocyanin. Biochemistry 42 (2003) 4829-4836
32. Díaz-Moreno I., Díaz-Quintana A., Díaz-Moreno S., Subías G., and De la Rosa M.A. Transient binding of plastocyanin to its physiological redox partners modifies the copper site geometry. FEBS Lett. 580 (2006) 6187-6194
33. Bond C.S., Bendall D.S., Freeman H.C., Guss J.M., Howe C.J., Wagner M.J., and Wilce M.C.J. The structure of plastocyanin from the cyanobacterium Phormidium laminosum. Acta Crystallogr., Sect D: Biol. Crystallogr. 55 (1999) 414-421
34. Carrell C.J., Schlarb B.G., Bendall D.S., Howe C.J., Cramer W.A., and Smith J.L. Structure of the soluble domain of cytochrome f from the cyanobacterium Phormidium laminosum. Biochemistry 38 (1999) 9590-9599
35. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N., and Bourne P.E. The protein data bank. Nucleic Acids Res. 28 (2000) 235-242
36. Case D.A., Darden T.A., Cheatham T.E., Simmerling C.L., Wang J., Duke R.E., Luo R., Merz K.M., Wang B., Pearlman D.A., Crowley M., Brozell S., Tsui V., Gohlke H., Mongan J., Hornak V., Cui G., Beroza P., Schafmeister C., Caldwell J.W., Ross W.S., and Kollman P.A. AMBER 8 (2004), University of California, San Francisco
37. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz K.M., Ferguson D.M., Spellmeyer D.C., Fox T., Caldwell J.W., and Kollman P.A. A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J. Am. Chem. Soc. 117 (1995) 5179-5197
38. Comba P., and Remenyi R. A new molecular mechanics force field for the oxidized form of blue copper proteins. J. Comput. Chem. 23 (2002) 697-705
39. Banci L., Bertini I., Ciurli S., Dikiy A., Dittmer J., Rosato A., Sciara G., and Thompsett A.R. NMR solution structure, backbone mobility, and homology modeling of c type cytochromes from gram-positive bacteria. ChemBioChem 3 (2002) 299-310
40. Díaz-Moreno I., Díaz-Moreno S., Subías G., De la Rosa M.A., and Díaz-Quintana A. The atypical iron-coordination geometry of cytochrome f remains unchanged upon binding to plastocyanin, as inferred by XAS. Photosynth. Res. 90 (2006) 23-28
41. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., and Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983) 926-935
42. Berendsen H.J.C., Postma J.P.M., Vangunsteren W.F., Dinola A., and Haak J.R. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 81 (1984) 3684-3690
43. Ryckaert J.P., Ciccotti G., and Berendsen H.J.C. Numerical-integration of Cartesian equations of motion of a system with constraints - molecular-dynamics of N-alkanes. J. Comput. Physics 23 (1977) 327-341
44. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graphics 14 (1996) 33-38
45. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
46. Bertini I., and Luchinat C. NMR of paramagnetic substances. Coord. Chem. Rev. 150 (1996) 1-300
47. Bertini I., Turano P., and Vila A.J. Nuclear-magnetic-resonance of paramagnetic metalloproteins. Chem. Rev. 93 (1993) 2833-2932
48. Worrall J.A.R., Kolczak U., Canters G.W., and Ubbink M. Interaction of yeast iso-1-cytochrome c with cytochrome c peroxidase investigated by [N-15, H-1] heteronuclear NMR spectroscopy. Biochemistry 40 (2001) 7069-7076
49. Berendsen H.J.C., van der Spoel D., and Vandrunen R. Gromacs - a message-passing parallel molecular-dynamics implementation. Comput. Phys. Commun. 91 (1995) 43-56
50. van der Spoel D., Lindahl E., Hess B., Groenhof G., Mark A.E., and Berendsen H.J.C. GROMACS: fast, flexible, and free. J. Comput. Chem. 26 (2005) 1701-1718
51. D. van der Spoel, E. Lindhal, B. Hess, A.R. van Buuren, E. Apol, P.J. Meulenhoff, D.P. Tieleman, A.L.T.M. Sijbers, K.A. Feenstra, R. van Drunen, H.J.C. Berendsen, Gromacs user manual 2004.
52. Lindahl E., Hess B., and van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7 (2001) 306-317
53. Hayward S., and Berendsen H.J.C. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins: Struct. Funct. Bioinform. 30 (1998) 144-154
54. Nicholls A., and Honig B. A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation. J. Comput. Chem. 12 (1991) 435-445
55. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
56. Sheinerman F.B., and Honig B. On the role of electrostatic interactions in the design of protein-protein interfaces. J. Mol. Biol. 318 (2002) 161-177
57. Lange C., Cornvik T., Díaz-Moreno I., and Ubbink M. The transient complex of poplar plastocyanin with cytochrome f: effects of ionic strength and pH. Biochim. Biophys. Acta 1707 (2005) 179-188
58. Hess B. Similarities between principal components of protein dynamics and random diffusion. J. Mol. Graphics Model. 18 (2000) 203
59. Amadei A., Ceruso M.A., and Nola A.D. On the convergence of the conformational coordinates basis set obtained by the essential dynamics analysis of proteins' molecular dynamics simulations. Proteins: Struct. Funct. Genet. 36 (1999) 419-424
60. de Groot B.L., van Aalten D.M.F., Amadei A., and Berendsen H.J.C. The consistency of large concerted motions in proteins in molecular dynamics simulations. Biophys. J. 71 (1996) 1707-1713
61. Hess B. Similarities between principal components of protein dynamics and random diffusion. Phys. Rev. E 62 (2000) 8438-8448