Low dielectric permittivity of water at the membrane interface: Effect on the energy coupling mechanism in biological membranes

Biophysical Journal

Volumn 85, Issue 2, 2003, Pages 1307-1316

  Cherepanov, Dmitry A ^a,b   Feniouk, Boris A ^a,c   Junge, Wolfgang ^a   Mulkidjanian, Armen Y ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

MONOVALENT ANION; MONOVALENT CATION; PROTON; PROTON PUMP; UNCLASSIFIED DRUG; WATER;

ALKALIPHILIC BACTERIUM; ARTICLE; BACTERIAL MEMBRANE; BACTERIUM IDENTIFICATION; BIOLOGICAL MODEL; CALCULATION; CHLOROPLAST; CONCENTRATION RESPONSE; DIELECTRIC CONSTANT; ELECTRICITY; ELECTROCHEMICAL ANALYSIS; ENERGY; ENERGY COUPLING MECHANISM; ENTROPY; MATHEMATICAL ANALYSIS; MEMBRANE MODEL; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; MESOPHILIC BACTERIUM; MITOCHONDRIAL MEMBRANE; NONHUMAN; PH MEASUREMENT; PHASE TRANSITION; PHOSPHATE TRANSPORT; PROBLEM SOLVING; PROTON MOTIVE FORCE; SMOLUCHOWSKI EQUATION; STEADY STATE; SURFACE PROPERTY; SYNTHESIS; WATER TRANSPORT;

BACTERIA (MICROORGANISMS); SOUSA;

EID: 0041843662     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74565-2     Document Type: Article

References (67)

1. Adams, J. 1993. MUDPACK-2: multigrid software for elliptic partial differential equations on uniform grids with any resolution. Appl. Math. Comp. 53:235-249.
2. Alexiev, U., R. Mollaaghababa, P. Scherrer, H. G. Khorana, and M. P. Heyn. 1995. Rapid long-range proton diffusion along the surface of the purple membrane and delayed proton transfer into the bulk. Proc. Natl. Acad. Sci. USA. 92:372-376.
3. Andersen, O. S. 1983. Ion movement through gramicidin A channels. Studies on the diffusion-controlled association step. Biophys. J. 41:147-165.
4. Antonenko, Y. N., O. N. Kovbasnjuk, and L. S. Yaguzhinsky. 1993. Evidence in favor of the existence of a kinetic barrier for proton transfer from a surface of bilayer phospholipid membrane to bulk water. Biochim. Biophys. Acta. 1150:45-50.
5. Arata, H., I. Takenaka, and M. Nishimura. 1987. Flash-induced proton release in Rhodopseudomonas sphaeroides spaeroplasts. J. Biochem. 101:261-265.
6. Benjamin, I. 1993. Mechanism and dynamics of ion transfer across a liquid-liquid interface. Science. 261:1558-1560.
7. Bockris, J. O., and A. K. N. Reddy. 1977. Modem Electrochemistry. Plenum Press, New York.
8. Bopp, P. A., A. A. Kornyshev, and G. Sutmann. 1998. Frequency and wave-vector dependent dielectric function of water: collective modes and relaxation spectra. J. Chem. Phys. 109:1939-1959.
9. Boyer, P. D. 2002. A research journey with ATP synthase. J. Biol. Chem. 277:39045-39061.
10. Cotton, N. P., S. A. White, S. J. Peake, S. McSweeney, and J. B. Jackson. 2001. The crystal structure of an asymmetric complex of the two nucleotide binding components of proton-translocating transhydrogenase. Structure. 9:165-176.
11. Cramer, W. A., and D. B. Knaff. 1991. Energy Transduction in Biological Membranes: A Textbook of Bioenergetics. Springer, New York.
12. Cukierman, S. 2000. Proton mobilities in water and in different stereoisomers of covalently linked gramicidin A channels. Biophys. J. 78:1825-1834.
13. Decker, E. R., and D. G. Levitt. 1988. Use of weak acids to determine the bulk diffusion limitation of H+ ion conductance through the gramicidin channel. Biophys. J. 53:25-32.
14. + release and uptake, and electric events in bacteriorhodopsin. FEBS Lett. 178:331-336.
15. Dutzler, R., E. B. Campbell, M. Cadene, B. T. Chait, and R. MacKinnon. 2002. X-ray structure of a CIC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature. 415:287-294.
16. 1-ATP synthase each. Biophys. J. 82:1115-1122.
17. Ferguson, S. J. 1985. Fully delocalised chemiosmotic or localised proton flow pathways in energy coupling? A scrutiny of experimental evidence. Biochim. Biophys. Acta. 811:47-95.
18. Georgievskii, Y., E. S. Medvedev, and A. A. Stuchebrukhov. 2002. Proton transport via the membrane surface. Biophys. J. 82:2833-2846.
19. Gopta, O. A., D. A. Cherepanov, W. Junge, and A. Y. Mulkidjanian. 1999. Proton transfer from the bulk to the bound ubiquinone QB of the reaction center in chromatophores of Rhodobacter sphaeroides: retarded conveyance by neutral water. Proc. Natl. Acad. Sci. USA. 96:13159-13164.
20. Guffanti, A. A., and T. A. Krulwich. 1984. Bioenergetic problems of alkalophilic bacteria. Biochem. Soc. Trans. 12:411-412.
21. Guffanti, A. A., M. Mann, T. L. Sherman, and T. A. Krulwich. 1984. Patterns of electrochemical proton gradient formation by membrane vesicles from an obligately acidophilic bacterium. J. Bacteriol. 159:448-452.
22. Harold, F. M. 1986. The Vital Force: A Study of Bioenergetics. W.H. Freeman and Company, New York.
23. Haumann, M., and W. Junge. 1994. The rates of proton uptake and electron transfer at the reducing side of Photosystem II in thylakoids. FEBS Lett. 347:45-50.
24. Heberle, J. 1991. Zeitauflbsende Untersuchung der Protonentranslokationsschritte von bakteriorhodopsin mittels chemisch-gekoppelter pH-Indikatoren. Freien Universität Berlin.
25. Heberle, J., and N. A. Dencher. 1992a. Surface-bound optical probes monitor protein translocation and surface potential changes during the bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. USA. 89:5996-6000.
26. Heberle, J., and N. A. Dencher. 1992b. The surface of the purple membrane: a transient pool for protons. In Structures and Functions of Retinal Proteins. J. L. Rigaud, editor. John Libbey Eurotext Ltd. 221-224.
27. Heberle, J., J. Riesle, G. Thiedemann, D. Oesterhelt, and N. A. Dencher. 1994. Proton migration along the membrane surface and retarded surface to bulk transfer. Nature. 370:379-382.
28. Heinz, W. F., and J. H. Hoh. 1999. Relative surface charge density mapping with the atomic force microscope. Biophys. J. 76:528-538.
29. Ishino, T., H. Hieda, K. Tanaka, and N. Gemma. 1994. Measurements of electrostatic double-layer forces due to charged functional groups on Langmuir-Blodgett films with an atomic force microscope. Jpn. J. Appl. Phys. 33:4718-4722.
30. Israelachvili, J. N. 1992. Intermolecular and Surface Forces. Academic Press, London.
31. 1 complex following single turnover flash excitation of intact cells of Rhodobacter capsulatus. Biochim. Biophys. Acta. 975:34-43.
32. Junge, W., and S. McLaughlin. 1987. The role of fixed and mobile buffers in the kinetics of proton movement. Biochim. Biophys. Acta. 890:1-5.
33. 1-ATPase. FEBS Lett. 504:152-160.
34. Junge, W., and A. Polle. 1986. Theory of proton flow along appressed thylakoid membranes under both non-stationary and stationary conditions. Biochim. Biophys. Acta. 848:265-273.
35. Kell, D. B. 1979. On the functional proton current pathway of electron transport phosphorylation, An electrodynamic view. Biochim. Biophys. Acta. 549:55-99.
36. Kell, D. B. 1986. Localized protonic coupling: overview and critical evaluation of techniques. Methods Enzymol. 127:538-557.
37. Kornyshev, A. A. 1985. Nonlocal electrostatics of solvation. In The Chemical Physics of Solvation. R.R. Dogonadze, E. Kalman, A.A. Kornyshev, and J. Ulstrup, editors. Elsevier, Amsterdam. 77-118.
38. Kornyshev, A. A., A. M. Kuznetsov, and M. Urbakh. 2002. Coupled ion-interface dynamics and ion transfer across the interface of two immiscible liquids. J. Chem. Phys. 117:6766-6779.
39. Kramer, D. M., C. A. Sacksteder, and J. A. Cruz. 1999. How acidic is the lumen? Photosynth. Res. 60:151-163.
40. + gradients on the internal mitochondrial membrane. FEBS Lett. 440:223-225.
41. Krulwich, T. A., M. Ito, R. Gilmour, M. G. Sturr, A. A. Guffanti, and D. B. Hicks. 1996. Energetic problems of extremely alkaliphilic aerobes. Biochim. Biophys. Acta. 1275:21-26.
42. Lancaster, C. R., A. Kroger, M. Auer, and H. Michel. 1999. Structure of fumarate reductase from Wolinella succinogenes at 2.2 Å resolution. Nature. 402:377-385.
43. Leikin, S., V. A. Parsegian, D. C. Rau, and R. P. Rand. 1993. Hydration forces. Annu. Rev. Phys. Chem. 44:369-395.
44. Marcus, R. A. 2000. On the theory of ion transfer rates across the interface of two immiscible liquids, J. Chem. Phys. 113:1618-1629.
45. Margulis, L. 1993. Symbiosis in Cell Evolution. Freeman, New York.
46. - state of bacterial photosynthetic reaction centers: rate limitation within the protein. Biophys. J. 73:367-381.
47. Matsuura, K., K. Masamoto, S. Itoh, and M. Nishimura. 1979. Effect of surface potential on the intramembrane electrical field measured with carotenoid spectral shift in chromatophores from Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta. 547:91-102.
48. Michel, H., and D. Oesterhelt. 1980. Electrochemical proton gradient across the cell membrane of Halobacterium halobium: comparison of the light-induced increase with the increase of intracellular adenosine triphosphate under steady-state illumination. Biochemistry. 19:4615-4619.
49. Mitchell, P. 1961. Coupling of photophosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature. 191:144-148.
50. Mitchell, P. 1966. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Physiol. Rev. 41:445-502.
51. Mulkidjanian, A. Y., and W. Junge. 1994. Calibration and time resolution of lumenal pH-transients in chromatophores of Rhodobacter capsulatus following a single turnover flash of light: proton release by the cytochrome bcl-complex is strongly electrogenic. FEBS Lett. 353:189-193.
52. Mdller, D. J., and A. Engel. 1997. The height of biomolecules measured with the atomic force microscope depends on electrostatic interactions. Biophys. J. 73:1633-1644.
53. Nachliel, E., and M. Gutman. 1996. Quantitative evaluation of the dynamics of proton transfer from photoactivated bacteriorhodopsin to the bulk. FEBS Lett. 393:221-225.
54. Pashley, R. M. 1981. DLVO and hydration forces between mica surfaces in Li, Na, K and Cs electrolyte solutions: a correlation of double-layer and hydration forces with surface cation exchange properties. J. Colloid Interface Sci. 83:531-546.
55. Ramos, S., and H. R. Kaback. 1977a. The electrochemical proton gradient in Escherichia coli membrane vesicles. Biochemistry. 16:848-854.
56. Ramos, S., and H. R. Kaback. 1977b. The relationship between the electrochemical proton gradient and active transport in Escherichia coli membrane vesicles. Biochemistry. 16:854-859.
57. Rau, D. C., and V. A. Parsegian. 1992. Direct measurement of the intermolecular forces between counterion-condensed DNA double helices. Evidence for long range attractive hydration forces. Biophys. J. 61:246-259.
58. Samec, Z., Y. I. Kharkats, and Y. Y. Gurevich. 1986. Stochastic approach to the ion transfer kinetics across the interface between two immiscible electrolyte solutions. Comparison with the experimental data. J. Electroanal. Chem. 204:257-266.
59. Sassaki, R. M., R. A. Douglas, M. U. Kleinke, and O. Teschke. 1996. Structure imaging by atomic force microscopy and transmission electron microscopy of different light emitting species of porous silicon. J. Vac. Sci. Technol. B. 14:2432-2437.
60. Schabert, F. A., and A. Engel. 1994. Reproducible acquisition of Escherichia coli porin surface topographs by atomic force microscopy. Biophys. J. 67:2394-2403.
61. Schweighofer, K. J., and I. Benjamin. 1995. Transfer of small ions across the water/1,2-dichloroethane interface. J. Chem. Phys. 99:9974-9985.
62. 2+ signals: essential information for decisions in cell division. FASEB J. 13(Suppl 2):S209-S215.
63. Teschke, O., G. Ceotto, and E. F. de Souza. 2001. Interfacial water dielectric-permittivity-profile measurements using atomic force microscopy. Phys. Rev. E. 64:011605.
64. +/ATP coupling ratio of the ATP synthase from thiol-modulated chloroplasts and two cyanobacterial strains is four. FEBS Lett. 379:309-313.
65. Wandlowski, T., V. Marecek, K. Holub, and Z. Samec. 1989. Ion transfer across liquid-liquid phase boundaries: Electrochemical kinetics by Faradic impedance. J. Phys. Chem. 93:8204-8212.
66. Williams, R. J. P. 1978. The multifarious couplings of energy transduction. Biochim. Biophys. Acta. 505:1-44.
67. Zhang, J., and P. R. Unwin. 2002. Proton diffusion at phospholipid assemblies. J. Am. Chem. Soc. 124:2379-2383.