Proton Transfer Dynamics at the Membrane/Water Interface: Dependence on the Fixed and Mobile pH Buffers, on the Size and Form of Membrane Particles, and on the Interfacial Potential Barrier

Biophysical Journal

Volumn 86, Issue 2, 2004, Pages 665-680

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

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b FRUMKIN INSTITUTE OF PHYSICAL CHEMISTRY AND ELECTROCHEMISTRY   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; HYDROGEN; HYDROXIDE; WATER;

ARTICLE; DYNAMICS; ELECTRICITY; MEMBRANE; PARTICLE SIZE; PH; PROTON TRANSPORT; REACTION ANALYSIS; SURFACE PROPERTY;

EID: 1142274318     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74146-6     Document Type: Article

References (75)

1. 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.
2. Arata, H., I. Takenaka, and M. Nishimura. 1987. Flash-induced proton release in Rhodopseudomonas sphaeroides spaeroplasts. J. Biochem. 101:261-265.
3. Baur, J. E., and R. M. Wightman. 1991. Diffusion-coefficients determined with microelectrodes. J. Electroanal. Chem. 305:73-81.
4. Bell, R. P. 1973. The Proton in Chemistry. Chapman & Hall, London, UK.
5. Berry, R. S., S. A. Rice, and J. Ross. 1980. Physical Chemistry. Wiley, New York.
6. Blom, J. G., R. A. Trompert, and J. G. Verwer. 1996. Algorithm 758: VLUGR2: a vectorizable adaptive-grid solver for PDEs in 2D. Acm Transactions on Mathematical Software. 22:302-328.
7. Blom, J. G., and P. A. Zegeling. 1994. A moving-grid interface for systems of one-dimensional time-dependent partial differential equations. ACM Trans. Math. Soft. 20:194-214.
8. Bockris, J. O., and A. K. N. Reddy. 1977. Modern Electrochemistry. Plenum Press, New York.
9. Brandsburg-Zabary, S., O. Fried, Y. Marantz, E. Nachliel, and M. Gutman. 2000. Biophysical aspects of intra-protein proton transfer. Biochim. Biophys. Acta. 1458:120-134.
10. Checover, S., E. Nachliel, N. A. Dencher, and M. Gutman. 1997. Mechanism of proton entry into the cytoplasmic section of the proton-conducting channel of bacteriorhodopsin. Biochemistry. 36:13919-13928.
11. Cheng, J.-X., S. Pautot, D. A. Weitz, and S. Xie. 2003. Ordering of water molecules between phospholipid bilayers visualized by coherent anti-Stokes Raman scattering microscopy. Proc. Natl. Acad. Sci. USA. 100:9826-9830.
12. Cherepanov, D. A., B. A. Feniouk, W. Junge, and A. Y. Mulkidjanian. 2003. Low dielectric permittivity of water at the membrane interface: effect on the energy coupling mechanism in biological membranes. Biophys. J. 2:1307-1316.
13. Clement, N. R., and J. M. Gould. 1981. Pyranine (8-hydroxy-1,3, 6-pyrenetrisulfonate) as a probe of internal aqueous hydrogen ion concentration in phospholipid vesicles. Biochemistry. 20:1534-1538.
14. Cramer, W. A., and D. B. Knaff. 1991. Energy Transduction in Biological Membranes: A Textbook of Bioenergetics. Springer, New York.
15. Culbertson, C. T., S. C. Jacobson, and J. M. Ramsey. 2002. Diffusion coefficient measurements in microfluidic devices. Talanta. 56:365-373.
16. Dioumaev, A. K., H. T. Richter, L. S. Brown, M. Tanio, S. Tuzi, H. Saito, Y. Kimura, R. Needleman, and J. K. Lanyi. 1998. Existence of a proton transfer chain in bacteriorhodopsin: participation of Glu-194 in the release of protons to the extracellular surface. Biochemistry. 37:2496-2506.
17. + release and uptake, and electric events in bacteriorhodopsin. FEBS Lett. 178:331-336.
18. Drachev, L. A., A. D. Kaulen, and A. Y. Komrakov. 1992. Interrelations of M-intermediates in bacteriorhodopsin photocycle. FEBS Lett. 313:248-250.
19. Elferink, M. G., I. Friedberg, K. J. Hellingwerf, and W. N. Konings. 1983. The role of the proton-motive force and electron flow in light-driven solute transport in Rhodopseudomonas sphaeroides. Eur. J. Biochem. 129:583-587.
20. Essen, L., R. Siegert, W. D. Lehmann, and D. Oesterhelt. 1998. Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex. Proc. Natl. Acad. Sci. USA. 95:11673-11678.
21. Ferguson, S. J. 1985. Fully delocalised chemiosmotic of localised proton flow pathways in energy coupling? A scrutiny of experimental evidence. Biochim. Biophys. Acta. 811:47-95.
22. Ferguson, S. J. 1995. Chemiosmotic coupling. Protons fast and slow. Curr. Biol. 5:25-27.
23. Ferguson, S. J. 2000. Proton transfer: it's a stringent process. Curr. Biol. 10:R627-R630.
24. Fernandez, C., and M. J. Politi. 1997. Effects of probe-amphiphile interaction on pyranine proton transfer reactions in lecithin vesicles. Journal of Photochemistry and Photobiology A-Chemistry. 104:165-172.
25. Georgievskii, Y., E. S. Medvedev, and A. A. Stuchebrukhov. 2002. Proton transport via the membrane surface. Biophys. J. 82:2833-2846.
26. B of the reaction center in chromatophores of Rhodobacter sphaeroides: retarded conveyance by neutral water. Proc. Natl. Acad. Sci. USA. 96:13159-13164.
27. Grzesiek, S., and N. A. Dencher. 1986. Time-course and stoichiometry of light-induced proton release and uptake during the photocycle of bacteriorhodopsin. FEBS Lett. 208:337-342.
28. Guffanti, A. A., and T. A. Krulwich. 1984. Bioenergetic problems of alkalophilic bacteria. Biochem. Soc. Trans. 12:411-412.
29. 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.
30. Gutman, M. 1986. Application of the laser-induced proton pulse for measuring the protonation rate constants of specific sites on proteins and membranes. Methods Enzymol. 127:522-38.
31. Gutman, M., A. B. Kotlyar, N. Borovok, and E. Nachliel. 1993. Reaction of bulk protons with a mitochondrial inner membrane preparation: time-resolved measurements and their analysis. Biochemistry. 32:2942-2946.
32. Gutman, M., and E. Nachliel. 1995. The dynamics of proton exchange between bulk and surface groups. Biochim. Biophys. Acta. 1231:123-138.
33. Gutman, M., Y. Tsfadia, A. Masad, and E. Nachliel. 1992. Quantitation of physical-chemical properties of the aqueous phase inside the phoE ionic channel. Biochim. Biophys. Acta. 1109:141-148.
34. Haumann, M., and W. Junge. 1994a. Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production. Biochemistry. 33:864-872.
35. Haumann, M., and W. Junge. 1994b. The rates of proton uptake and electron transfer at the reducing side of photosystem II in thylakoids. FEBS Lett. 347:45-50.
36. Hänggi, P., P. Talkner, and M. Borkovec. 1990. Reaction-rate theory: fifty years after Kramers. Rev. Mod. Phys. 62:251-341.
37. Heberle, J. 1991. Zeitauflösende Untersuchung der Protonentranslokationsschritte von Bakteriorhodopsin mittels chemisch-gekoppelter pH-Indikatoren. Freien Universität, Berlin.
38. Heberle. J. 2000. Proton transfer reactions across bacteriorhodopsin and along the membrane. Biochim. Biophys. Acta. 1458:135-147.
39. Heberle, J., and N. A. Dencher. 1992. Surface-bound optical probes monitor protein translocation and surface potential changes during the bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. USA. 89:5996-6000.
40. 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.
41. Hong, Y. Q., and W. Junge. 1983. Localized or delocalized protons in photophosphorylation? On the accessibility of the thylakoid lumen for ions and buffers. Biochim. Biophys. Acta. 722:197-208.
42. Israelachvili, J. N. 1992. Intermolecular and Surface Forces. Academic Press, London, UK.
43. Israelachvili, J. N., and R. M. Pashley. 1983. Molecular layering of water at surfaces and origin of repulsive hydration forces. Nature. 306:249-250.
44. 1 complex following single turnover flash exitation of intact cells of Rhodobacter capsulatus. Biochim. Biophys. Acta. 975:34-43.
45. Jones, M. R., and J. B. Jackson. 1990. Proton efflux from right-side-out membrane vesicles of Rhodobacter sphaeroides after short flashes. Biochim. Biophys. Acta. 1019:51-58.
46. Junge, W. 1987. Complete tracking of transient proton flow through active chloroplast ATP synthase. Proc. Natl. Acad. Sci. USA. 84:7084-7088.
47. Junge, W., A. McGeer, and W. Ausländer, 1978. Calibration of flash induced pH changes inside thylakoids and kinetic resolution of proton ejection and consumption. In Frontiers of Biological Energetics, Vol. 1. P. L. Dutton, J. S. Leigh, J. S. Scarpa, editors. Academic Press, New York. 275-283.
48. 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.
49. 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.
50. Kano, K., and J. H. Fendler. 1978. Pyranine as a sensitive pH probe for liposome interiors and surfaces. pH gradients across phospholipid vesicles. Biochim. Biophys. Acta. 509:289-299.
51. Kell, D. B. 1979. On the functional proton current pathway of electron transport phosphorylation. An electrodic view. Biochim. Biophys. Acta. 549:55-99.
52. Kotlyar, A. B., N. Borovok, S. Kiryati, E. Nachliel, and M. Gutman. 1994. The dynamics of proton transfer at the C side of the mitochondrial membrane: picosecond and microsecond measurements. Biochemistry. 33:873-879.
53. 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.
54. A-state of bacterial photosynthetic reaction centers: rate limitation within the protein. Biophys. J. 73:367-381.
55. 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.
56. Mitchell. P. 1961. Coupling of photophosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature. 191:144-148.
57. 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.
58. 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.
59. Nachliel, E., M. Gutman, S. Kiryati, and N. A. Dencher. 1996. Protonation dynamics of the extracellular and cytoplasmic surface of bacteriorhodopsin in the purple membrane. Proc. Natl. Acad. Sci. USA. 93:10747-10752.
60. Okamura, M. Y., M. L. Paddock, M. S. Graige, and G. Feher. 2000. Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta. 1458:148-163.
61. Packham, N. K., J. A. Berriman, and J. B. Jackson. 1978. The charging capacitance of the chromatophore membrane. FEBS Lett. 89:205-210.
62. Polle, A., and W. Junge. 1989. Proton diffusion along the membrane surface of thylakoids is not enhanced over that in bulk water. Biophys. J. 56:27-31.
63. Porschke, D. 2002. Reaction coupling, acceptor pK, and diffusion control in light induced proton release of bacteriorhodopsin. J. Phys. Chem. B. 106:10233-10241.
64. Schatzler, B., N. A. Dencher, J. Tittor, D. Oesterhelt, S. Yaniv-Checover, E. Nachliel, and M. Gutman. 2003. Subsecond proton-hole propagation in bacteriorhodopsin. Biophys. J. 84:671-686.
65. Scherrer, P., U. Alexiev, T. Marti, H. G. Khorana, and M. P. Heyn. 1994. Covalently bound pH-indicator dyes at selected extracellular or cytoplasmic sites in bacteriorhodopsin. 1. Proton migration along the surface of bacteriorhodopsin micelles and its delayed transfer from surface to bulk. Biochemistry. 33:13684-13692.
66. Sedgwick. E. G., and P. D. Bragg. 1990. pH probes respond to redox changes in cytochrome o. Arch. Biochem. Biophys. 282:372-376.
67. Serowy, S., S. M. Saparov. Y. N. Antonenko, W. Kozlovsky, V. Hagen, and P. Pohl. 2003. Structural proton diffusion along lipid bilayers. Biophys. J. 84:1031-1037.
68. Talkner, P. 1995. Anharmonic barrier corrections for the Kramers rate problem in the spatial diffusion regime. In New Trends in Kramers Reaction Rate Theory. P. Talkner and P. Hänggi, editors. Kluwer Academic Publishers, Dordrecht, Boston. MA and London, UK. 47-68.
69. 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.
70. Varela, L. M., M. Garcia. and V. Mosquera. 2003. Exact mean-field theory of ionic solutions: non-Debye screening. Physics Reports-Review Section of Physics Letters. 382:1-111.
71. Williams, R. J. 2001. The structures of organelles and reticula: localised bioenergetics and metabolism. Chembiochem. 2:637-641.
72. Williams, R. J. 1978. The multifarious couplings of energy transduction. Biochim. Biophys. Acta. 505:1-44.
73. Yam, R., E. Nachliel, S. Kiryati, M. Gutman, and D. Huppert. 1991. Proton transfer dynamics in the nonhomogeneous electric field of a protein. Biophys. J. 59:4-11.
74. Zhang, J., and P. R. Unwin. 2002. Proton diffusion at phospholipid assemblies. J. Am. Chem. Soc. 124:2379-2383.
75. Ziegler, M., and H. S. Penefsky. 1993. The adenine nucleotide translocase modulates oligomycin-induced quenching of pyranine fluorescence in submitochondrial particles. J. Biol. Chem. 268:25320-25328.