The local electric field within phospholipid membranes modulates the charge transfer reactions in reaction centres

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 8, 2009, Pages 1039-1049

  Pilotelle Bunner, Anne ^a   Beaunier, Patricia ^b   Tandori, Julia ^a   Maroti, Peter ^c   Clarke, Ronald J ^d   Sebban, Pierre ^a  

^a UNIVERSITÉ PARIS SUD   (France)

^b UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^c UNIVERSITY OF SZEGED   (Hungary)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Biological membrane; Cholesterol; Dipole potential; Electron transfer; Proton transfer; Reaction centre protein

Indexed keywords

6 OXOCHOLESTANOL; 7 OXOCHOLESTEROL; CHOLESTEROL DERIVATIVE; PHLORETIN; PHOSPHOLIPID; QUINONE DERIVATIVE;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRIC FIELD; ELECTRON TRANSPORT; EQUILIBRIUM CONSTANT; MODULATION TRANSFER FUNCTION; NONHUMAN; PH; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROTEOLIPOSOME; PROTON TRANSPORT; REACTION ANALYSIS; ROOM TEMPERATURE; TRANSPORT KINETICS;

ANTHRAQUINONES; CELL MEMBRANE; CHOLESTEROL; ELECTROMAGNETIC FIELDS; ELECTRON TRANSPORT; HYDROGEN-ION CONCENTRATION; KETOCHOLESTEROLS; KINETICS; LIPOSOMES; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; PHLORETIN; PHOSPHATIDYLCHOLINES; PHOSPHOLIPIDS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RHODOBACTER SPHAEROIDES; TEMPERATURE; THERMODYNAMICS;

RHODOBACTER SPHAEROIDES;

EID: 67649394349     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.03.011     Document Type: Article

References (67)

1. - and the associated processes in Rhodobacter sphaeroides R-26 reaction centers. Biochemistry 37 (1998) 2818-2829
2. Okamura M.Y., Paddock M.L., Graige M.S., and Feher G. Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta 1458 (2000) 148-163
3. Tiede D.M., Vazquez J., Cordova J., and Marone P.A. Time-resolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center. Biochemistry 35 (1996) 10763-10775
4. B electron transfer. Biochemistry 37 (1998) 8278-8281
5. (B) electron transfer reaction in bacterial photosynthetic reaction centers: pH dependence of the conformational gating step. Biochemistry 41 (2002) 2694-2701
6. Wraight C.A. Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides. Front Biosci. 9 (2004) 309-337
7. Takahashi E., and Wraight C.A. Proton and electron transfer in the acceptor quinone complex of Rhodobacter sphaeroides reaction centers: characterization of site-directed mutants of the two ionizable residues, GluL212 and AspL213, in the QB binding site. Biochemistry 31 (1992) 855-866
8. Tandori J., Sebban P., Michel H., and Baciou L. In Rb. sphaeroides reaction centers, mutation of proline l209 to aromatic residues in the vicinity of a water channel alters the dynamic coupling between electron and proton transfer processes. Biochemistry 40 (1999) 13179-13187
9. Maroti P., and Wraight C.A. Flash-induced H+ binding by bacterial photosynthetic reaction centers: influences of the redox states of the acceptor quinones and primary donor. Biochim. Biophys. Acta 934 (1988) 329-347
10. -. Biochim. Biophys. Acta 934 (1988) 348-368
11. Tandori J., Baciou L., Alexov E., Maroti P., Schiffer M., Hanson D.K., and Sebban P. Revealing the involvement of extended hydrogen bond networks in the cooperative function between distant sites in bacterial reaction centers. J. Biol. Chem. 276 (2001) 45513-45515
12. Tandori J., Maroti P., Alexov E., Sebban P., and Baciou L. Key role of proline L209 in connecting the distant quinone pockets in the reaction center of Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6702-6706
13. 2+ on bacterial reaction center mutants: proton-transfer uses interdependent pathways. Biochemistry 41 (2002) 9132-9138
14. Adelroth P., Paddock M.L., Tehrani A., Beatty J.T., Feher G., and Okamura M.Y. Identification of the proton pathway in bacterial reaction centers: decrease of proton transfer rate by mutation of surface histidines at H126 and H128 and chemical rescue by imidazole identifies the initial proton donors. Biochemistry 40 (2001) 14538-14546
15. Paddock M.L., Feher G., and Okamura M.Y. Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett. 555 (2003) 45-50
16. Cheap H., Tandori J., Derrien V., Benoit M., de Oliveira P., Koepke J., Lavergne J., Maroti P., and Sebban P. Evidence for delocalized anticooperative flash induced proton binding as revealed by mutants at the M266His iron ligand in bacterial reaction centers. Biochemistry 46 (2007) 4510-4521
17. Koepke J., Krammer E.M., Klingen A.R., Sebban P., Ullmann G.M., and Fritzsch G. pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states. J. Mol. Biol. 371 (2007) 396-409
18. E.M. Krammer, M.S. Till, P. Sebban, G.M. Ullmann, Proton transfer pathways in photosynthetic reaction centers analyzed by profile hidden Markov models and network calculations, J. Mol. Biol. (in press) (2009).
19. A charge recombination kinetics in the reaction centers from Rhodobacter sphaeroides, reconstituted with anthraquinones. Biochim. Biophys. Acta 936 (1988) 124-132
20. Baciou L., and Sebban P. Heterogeneity of the quinone electron acceptor system in bacterial reaction centers. Photochem. Photobiol. 62 (1995) 271-278
21. A-recombination kinetics in reaction centers from Rps. viridis. The effects of pH and temperature. Biochim. Biophys. Acta 974 (1989) 54-65
22. A-state in reaction centers from Rhodopseudomonas viridis. Biochim. Biophys. Acta 893 (1987) 409-425
23. Baciou L., Gulik-Krzywicki T., and Sebban P. Involvement of the protein-protein interactions in the thermodynamics of the electron-transfer process in the reaction centers from Rhodopseudomonas viridis. Biochemistry 30 (1991) 1298-1302
24. Sebban P., Parot P., Baciou L., Mathis P., and Vermeglio A. Low temperature and lipid rigidity effects on the charge recombination process in bacterial reaction centers. Biochim. Biophys. Acta 1057 (1991) 109-114
25. Rokitskaya T.I., Antonenko Y.N., and Kotova E.A. Effect of the dipole potential of a bilayer lipid membrane on gramicidin channel dissociation kinetics. Biophys. J. 73 (1997) 850-854
26. Starkov A.A., Bloch D.A., Chernyak B.V., Dedukhova V.I., Mansurova S.E., Severina, Simonyan R.A., Vygodina T.V., and Skulachev V.P. 6-Ketocholestanol is a recoupler for mitochondria, chromatophores and cytochrome oxidase proteoliposomes. Biochim. Biophys. Acta 1318 (1997) 159-172
27. Antonenko Y.N., Rokitskaya T.I., and Kotova E.A. Effect of dipole modifiers on the kinetics of sensitized photoinactivation of gramicidin channels in bilayer lipid membranes. Membr. Cell Biol. 13 (1999) 111-120
28. Bala S., Kombrabail M.H., and Prabhananda B.S. Effect of phloretin on ionophore mediated electroneutral transmembrane translocations of H(+), K(+) and Na(+) in phospholipid vesicles. Biochim. Biophys. Acta 1510 (2001) 258-269
29. Becucci L., Moncelli M.R., and Guidelli R. Thallous ion movements through gramicidin channels incorporated in lipid monolayers supported by mercury. Biophys. J. 82 (2002) 852-864
30. Rokitskaya T.I., Kotova E.A., and Antonenko Y.N. Membrane dipole potential modulates proton conductance through gramicidin channel: movement of negative ionic defects inside the channel. Biophys. J. 82 (2002) 865-873
31. Cladera J., and O'Shea P. Intramembrane molecular dipoles affect the membrane insertion and folding of a model amphiphilic peptide. Biophys. J. 74 (1998) 2434-2442
32. Alakoskela J.M., Soderlund T., Holopainen J.M., and Kinnunen P.K. Dipole potential and head-group spacing are determinants for the membrane partitioning of pregnanolone. Mol. Pharmacol. 66 (2004) 161-168
33. Cladera J., Martin I., Ruysschaert J.M., and O'Shea P. Characterization of the sequence of interactions of the fusion domain of the simian immunodeficiency virus with membranes. Role of the membrane dipole potential. J. Biol. Chem. 274 (1999) 29951-29959
34. Buzon V., and Cladera J. Effect of cholesterol on the interaction of the HIV GP41 fusion peptide with model membranes. Importance of the Membrane Dipole Potential. Biochemistry 45 (2006) 15768-15775
35. Starke-Peterkovic T., Turner N., Vitha M.F., Waller M.P., Hibbs D.E., and Clarke R.J. Cholesterol effect on the dipole potential of lipid membranes. Biophys. J. 90 (2006) 4060-4070
36. Le Goff G., Vitha M.F., and Clarke R.J. Orientational polarisability of lipid membrane surfaces. Biochim. Biophys. Acta 1768 (2007) 562-570
37. Cladera J., O'Shea P., Hadgraft J., and Valenta C. Influence of molecular dipoles on human skin permeability: use of 6-ketocholestanol to enhance the transdermal delivery of bacitracin. J. Pharm. Sci. 92 (2003) 1018-1027
38. (+)-ATPase. Biochim. Biophys. Acta 1235 (1995) 183-196
39. R.J. Clarke, DJ. Kane, Optical detection of membrane dipole potential: avoidance of fluidity and dye-induced effects, Biochim. Biophys. Acta 1323 (2) (1997), 223-239.
40. +-ATPase molecular activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 (2005) R663-670
41. Szabo G. Dual mechanism for the action of cholesterol on membrane permeability. Nature 252 (1974) 47-49
42. McIntosh T.J., Magid A.D., and Simon S.A. Cholesterol modifies the short-range repulsive interactions between phosphatidylcholine membranes. Biochemistry 28 (1989) 17-25
43. Nabedryk E., Breton J., Sebban P., and Baciou L. Quinone (Q(B)) binding site and protein stuctural changes in photosynthetic reaction center mutants at Pro-L209 revealed by vibrational spectroscopy. Biochemistry 42 (2003) 5819-5827
44. Okamura M.Y., Isaacson R.A., and Feher G. Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides. Proc. Natl. Acad. Sci. U. S. A. 72 (1975) 3491-3495
45. Sebban P. Activation free energy of P+QA-absorption decay in reaction centers from Rb. sphaeroides reconstituted with different anthraquinones. FEBS Lett. 233 (1988) 331-334
46. Miksovska J., Valerio-Lepiniec M., Schiffer M., Hanson D.K., and Sebban P. In bacterial reaction centers, a key residue suppresses mutational blockage of two different proton transfer steps. Biochemistry 37 (1998) 2077-2083
47. Remy A., and Gerwert K. Coupling of light-induced electron transfer to proton uptake in photosynthesis. Nat. Struct. Biol. 10 (2003) 637-644
48. Taly A., Baciou L., and Sebban P. The DMPC lipid phase transition influences differently the first and the second electron transfer reactions in bacterial reaction centers. FEBS Lett. 532 (2002) 91-96
49. Shinkarev V.P., and Wraight C.A. The interaction of quinone and detergent with reaction centers of purple bacteria. I. Slow quinone exchange between reaction center micelles and pure detergent micelles. Biophys. J. 72 (1997) 2304-2319
50. Kuglstatter A., Miksovska J., Sebban P., and Fritzsch G. Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides reconstituted with anthraquinone as primary quinone Q(A). FEBS Lett. 472 (2000) 114-116
51. Gunner M.R., Tiede D.M., Prince R.C., and Dutton P.L. Quinones as prosthetic groups in membrane electron-transfer proteins 1: Systematic replacement of the primary ubiquinone of photochemical reaction centers with other quinones. In: Trumpower B.L. (Ed). Functions of Quinones in Energy Conserving Systems (1982), Academic Press, New York 265-269
52. Woodbury N.W., Parson W.W., Gunner M.R., Prince R.C., and Dutton P.L. Radical-pair energetics and decay mechanisms in reaction centers containing anthraquinones, naphthoquinones or benzoquinones in place of ubiquinone. Biochim. Biophys. Acta 851 (1986) 6-22
53. Sebban P., and Barbet J.C. Intermediate states between P* and Pf in bacterial reaction centers, as detected by the fluorescence kinetics. FEBS Lett. 165 (1984) 107-110
54. Woodbury N.W., and Parson W.W. Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 767 (1984) 345-361
55. Prince R.C. Hopanoids: the world's most abundant biomolecules?. Trends Biochem. Sci. 12 (1987) 455-456
56. B-. in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 11679-11684
57. B in photosynthetic reaction centers. Biochemistry 39 (2000) 5940-5952
58. (B) reduction. Biophys. J. 84 (3) (2003), 2090-2098.
59. Alexov E.G., and Gunner M.R. Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties. Biophys. J. 72 (1997) 2075-2093
60. B in bacterial photosynthetic reaction centers. Biochemistry 38 (1999) 8253-8270
61. Gunner M.R., and Alexov E. A pragmatic approach to structure based calculation of coupled proton and electron transfer in proteins. Biochim. Biophys. Acta 1458 (2000) 63-87
62. Rabenstein B., Ullmann G.M., and Knapp E.W. Energetics of electron-transfer and protonation reactions of the quinones in the photosynthetic reaction center of Rhodopseudomonas viridis. Biochemistry 37 (1998) 2488-2495
63. Rabenstein B., Ullmann G.M., and Knapp E.W. Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes. Biochemistry 39 (2000) 10487-10496
64. B-charge recombinations in Rhodopseudomonas viridis chromatophores and in reaction centers reconstituted in phosphatidylcholine liposomes. Existence of two conformational states of the reaction centers and effects of pH and o-phenanthroline. Biochemistry 29 (1990) 2966-2976
65. Palazzo G., Mallardi A., Giustini M., Berti D., and Venturoli G. Cumulant analysis of charge recombination kinetics in bacterial reaction centers reconstituted into lipid vesicles. Biophys. J. 79 (2000) 1171-1179
66. Sham Y.Y., Muegge I., and Warshel A. The effect of protein relaxation on charge-charge interactions and dielectric constants of proteins. Biophys. J. 74 (1998) 1744-1753
67. Stowell M.H., McPhillips T.M., Rees D.C., Soltis S.M., Abresch E., and Feher G. Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. Science 276 (1997) 812-816