Common themes and problems of bioenergetics and voltage-gated proton channels

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1458, Issue 1, 2000, Pages 104-119

  Decoursey, Thomas E ^a   Cherny, Vladimir V ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Hydrogen ion; pH regulation; Proton; Proton channel; Proton permeability; Proton transport

Indexed keywords

HEAVY METAL; ION CHANNEL; VOLTAGE GATED CHANNEL FORMING PROTEIN;

BIOENERGY; CELL MEMBRANE; CHANNEL GATING; HYDROGEN BOND; MEMBRANE PERMEABILITY; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTON TRANSPORT; REVIEW;

CELL MEMBRANE; ELECTROCHEMISTRY; ENERGY METABOLISM; HYDROGEN-ION CONCENTRATION; ION CHANNELS; METALS, HEAVY; MODELS, THEORETICAL; PATCH-CLAMP TECHNIQUES; PROTEIN CONFORMATION; PROTEINS; PROTON-MOTIVE FORCE; PROTONS;

EID: 0034640202     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0005-2728(00)00062-1     Document Type: Review

References (123)

1. T.E. DeCoursey, V.V. Cherny, An electrophysiological comparison of voltage-gated proton channels, other ion channels, and other proton channels, Israel J. Chem., in press.
2. Thomas R.C., Meech R.W. Hydrogen ion currents and intracellular pH in depolarized voltage-clamped snail neurones. Nature. 299:1982;826-828.
3. Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:1952;500-544.
4. Hodgkin A.L., Huxley A.F. The components of membrane conductance in the giant axon of Loligo. J. Physiol. 116:1952;473-496.
5. DeCoursey T.E., Cherny V.V. Voltage-activated hydrogen ion currents. J. Membr. Biol. 141:1994;203-223.
6. W. Nernst, Zur Kinetik der in Lösung befindlichen Körper. Theorie der Diffusion, Z. Phys. Chem. 2 (1888) 613-637.
7. Barish M.E., Baud C. A voltage-gated hydrogen ion current in the oocyte membrane of the axolotl, Ambystoma. J. Physiol. 352:1984;243-263.
8. Bernheim L., Krause R.M., Baroffio A., Hamann M., Kaelin A., Bader C.-R. A voltage-dependent proton current in cultured human skeletal muscle myotubes. J. Physiol. 470:1993;313-333.
9. Demaurex N., Grinstein S., Jaconi M., Schlegel W., Lew D.P., Krause K.-H. Proton currents in human granulocytes: regulation by membrane potential and intracellular pH. J. Physiol. 466:1993;329-344.
10. Kapus A., Romanek R., Qu A.Y., Rotstein O.D., Grinstein S. A pH-sensitive and voltage-dependent proton conductance in the plasma membrane of macrophages. J. Gen. Physiol. 102:1993;729-760.
11. + antiport detected through hydrogen ion currents in rat alveolar epithelial cells and human neutrophils. J. Gen. Physiol. 103:1994;755-785.
12. Kuno M., Kawawaki J., Nakamura F. A highly temperature-sensitive proton conductance in mouse bone marrow-derived mast cells. J. Gen. Physiol. 109:1997;731-740.
13. DeCoursey T.E., Cherny V.V. Deuterium isotope effects on permeation and gating of proton channels in rat alveolar epithelium. J. Gen. Physiol. 109:1997;415-434.
14. Cherny V.V., Markin V.S., DeCoursey T.E. The voltage-activated hydrogen ion conductance in rat alveolar epithelial cells is determined by the pH gradient. J. Gen. Physiol. 105:1995;861-896.
15. DeCoursey T.E. Four varieties of voltage-gated proton channels. Frontiers Biosci. 3:1998;d477-d482.
16. DeCoursey T.E., Cherny V.V. Potential, pH, and arachidonate gate hydrogen ion currents in human neutrophils. Biophys. J. 65:1993;1590-1598.
17. Gordienko D.V., Tare M., Parveen S., Fenech C.J., Robinson C., Bolton T.B. Voltage-activated proton current in eosinophils from human blood. J. Physiol. 496:1996;299-316.
18. Schrenzel J., Lew D.P., Krause K.-H. Proton currents in human eosinophils. Am. J. Physiol. 271:1996;C1861-C1871.
19. V.V. Cherny, W. Zhou, L.L. Thomas, T.E. DeCoursey, Proton currents in human basophils, Biophys. J. 76 (1999) A349 (abstract).
20. Nordström T., Rotstein O.D., Romanek R., Asotra S., Heersche J.N.M., Manolson M.F., Brisseau G.F., Grinstein S. Regulation of cytoplasmic pH in osteoclasts: contribution of proton pumps and a proton-selective conductance. J. Biol. Chem. 270:1995;2203-2212.
21. Eder C., Fischer H.-G., Hadding U., Heinemann U. Properties of voltage-gated currents of microglia developed using macrophage colony-stimulating factor. Pflügers Archiv. 430:1995;526-533.
22. Byerly L., Suen Y. Characterization of proton currents in neurones of the snail, Lymnaea stagnalis. J. Physiol. 413:1989;75-89.
23. T.E. DeCoursey, S. Grinstein, Ion channels and carriers in leukocytes, in: J.I. Gallin, R. Snyderman (Eds.), Inflammation: Basic Principles and Clinical Correlates, 3rd edn., Lippincott, Williams and Wilkins, Philadelphia, PA, 1999, pp. 639-659.
24. + channel. Biochem. J. 246:1987;325-329.
25. Schrenzel J., Serrander L., Bánfi B., Nüsse O., Fouyouzi R., Lew D.P., Demaurex N., Krause K.-H. Electron currents generated by the human phagocyte NADPH oxidase. Nature. 392:1998;734-737.
26. + conducting channel. Biochem. J. 251:1988;563-567.
27. Henderson L.M., Chappell J.B., Jones O.T.G. Superoxide generation by the electrogenic NADPH oxidase of human neutrophils is limited by the movement of a compensating charge. Biochem. J. 255:1988;285-290.
28. Demaurex N., Downey G.P., Waddell T.K., Grinstein S. Intracellular pH regulation during spreading of human neutrophils. J. Cell Biol. 133:1996;1391-1402.
29. Byerly L., Meech R., Moody W. Rapidly activating hydrogen ion currents in perfused neurones of the snail, Lymnaea stagnalis. J. Physiol. 351:1984;199-216.
30. Meech R.W., Thomas R.C. Voltage-dependent intracellular pH in Helix aspersa neurones. J. Physiol. 390:1987;433-452.
31. Schwiening C.J., Kennedy H.J., Thomas R.C. Calcium-hydrogen exchange by the plasma membrane Ca-ATPase of voltage-clamped snail neurons. Proc. R. Soc. Lond. Ser. B. 253:1993;285-289.
32. + conductance in Rana esculenta oocytes. Cell. Signal. 8:1996;375-379.
33. DeCoursey T.E. Hydrogen ion currents in rat alveolar epithelial cells. Biophys. J. 60:1991;1243-1253.
34. 2 elimination by the lung? Am. J. Physiol. Cell Physiol. 278 (2000) C1-C10.
35. R.A. Robinson, R.H. Stokes, Electrolyte Solutions, Butterworths, London, 1959, 571 pp.
36. 3O· ion. J. Chem. Phys. 24:1956;834-850.
37. deGrotthuss C.J.T. Sur la décomposition de l'eau et des corps qu'elle tient en dissolution à l'aide de l'électricité galvanique. Ann. Chimie. LVIII:1806;54-74.
38. Danneel H. Notiz über Ionengeschwindigkeiten. Zeitschrift für Elektrochemie und angewandte physikalische Chemie. 11:1905;249-252.
39. Bernal J.D., Fowler R.H. A theory of water and ionic solution, with particular reference to hydrogen and hydroxyl ions. J. Chem. Phys. 1:1933;515-548.
40. Eigen M., De Maeyer L. Self-dissociation and protonic charge transport in water and ice. Proc. R. Soc. Lond. Ser. A. 247:1958;505-533.
41. Huggins M.L. The role of hydrogen bonds in conduction by hydrogen and hydroxyl ions. J. Am. Chem. Soc. 53:1931;3190-3191.
42. Agmon N. Hydrogen bonds, water rotation and proton mobility. J. Chem. Phys. 93:1996;1714-1736.
43. G. Zundel, Proton polarizability of hydrogen bonds and proton transfer processes, their role in electrochemistry and biology, Institut für Physikalische Chemie der Universität München, 1997, 250 pp.
44. Nagle J.F., Morowitz H.J. Molecular mechanisms for proton transport in membranes. Proc. Natl. Acad. Sci. USA. 75:1978;298-302.
45. Scheiner S. Proton transfers in hydrogen-bonded systems: cationic oligomers of water. J. Am. Chem. Soc. 103:1981;315-320.
46. Finkelstein A., Andersen O.S. The gramicidin A channel: a review of its permeability characteristics with special reference to the single-file aspect of transport. J. Membr. Biol. 59:1981;155-171.
47. B. Hille, Ionic selectivity of Na and K channels of nerve membranes, in: G. Eisenman. (Ed.), Membranes: A Series of Advances, Dekker, New York, 1975, pp. 255-323.
48. Nagle J.F., Mille M., Morowitz H.J. Theory of hydrogen bonded chains in bioenergetics. J. Chem. Phys. 72:1980;3959-3971.
49. Nagle J.F., Tristram-Nagle S. Hydrogen bonded chain mechanisms for proton conduction and proton pumping. J. Membr. Biol. 74:1983;1-14.
50. Chen M.-S., Onsager L., Bonner J., Nagle J. Hopping of ions in ice. J. Chem. Phys. 60:1974;405-419.
51. + conduction along hydrogen-bonded chains of water molecules. Biophys. J. 75:1998;33-40.
52. Drukker K., de Leeuw S.W., Hammes-Schiffer S. Proton transport along water chains in an electric field. J. Chem. Phys. 108:1998;6799-6808.
53. Cowin J.P., Tsekouras A.A., Iedema M.J., Wu K., Ellison G.B. Immobility of protons in ice from 30 to 190 K. Nature. 398:1999;405-407.
54. 1 ATPases? Biophys. J. 60:1991;101-109.
55. 0: its time-averaged single-channel conductance as a function of pH, temperature, isotopic and ionic medium composition. J. Membr. Biol. 108:1989;263-271.
56. 2O. J. Am. Chem. Soc. 55:1933;3504-3506.
57. J.E. Crooks, Proton transfer to and from atoms other than carbon, in: C.H. Bamford, C.F.H. Tipper (Eds.), Chemical Kinetics, Vol. 8, Proton Transfer, Elsevier, New York, 1977, pp. 248-250.
58. Scheiner S., Nagle J.F. Ab initio molecular orbital estimates of charge partitioning between Bjerrum and ionic defects in ice. J. Phys. Chem. 87:1983;4267-4272.
59. + translocation along the single-file water chain in the gramicidin A channel. Biophys. J. 71:1996;19-39.
60. Cukierman S., Quigley E.P., Crumrine D.S. Proton conduction in gramicidin A and in its dioxolane-linked dimer in different lipid bilayers. Biophys. J. 73:1997;2489-2502.
61. Nagle J.F. Theory of passive proton conductance in lipid bilayers. J. Bioenerg. Biomembr. 19:1987;413-426.
62. Phillips L.R., Cole C.D., Hendershot R.J., Cotten M., Cross T.A., Busath D.D. In gramicidin hydrogen transport the rate limiting water reorientation must be initiated at the channel exit. Biophys. J. 76:1999;A25.
63. Myers V.B., Haydon D.A. Ion transfer across lipid membranes in the presence of gramicidin A: the ion selectivity. Biochim. Biophys. Acta. 274:1972;313-322.
64. Levitt D.G., Elias S.R., Hautman J.M. Number of water molecules coupled to the transport of sodium, potassium and hydrogen ions via gramicidin, nonactin or valinomycin. Biochim. Biophys. Acta. 512:1978;436-451.
65. Chiu S.-W., Subramaniam S., Jakobsson E., McCammon J.A. Water and polypeptide conformations in the gramicidin channel: a molecular dynamics study. Biophys. J. 56:1989;253-261.
66. Mackay D.H.J., Berens P.H., Wilson K.R., Hagler A.T. Structure and dynamics of ion transport through gramicidin A. Biophys. J. 46:1984;229-248.
67. Elber R., Chen D.P., Rojewska D., Eisenberg R. Sodium in gramicidin: an example of a permion. Biophys. J. 68:1995;906-924.
68. Jordan P.C. Ion-water and ion-polypeptide correlations in a gramicidin-like channel: a molecular dynamics study. Biophys. J. 58:1990;1133-1156.
69. Duca K.A., Jordan P.C. Ion-water and water-water interactions in a gramicidinlike channel: effects due to group polarizability and backbone flexibility. Biophys. Chem. 65:1997;123-141.
70. Hladky S.B., Haydon D.A. Ion transfer across lipid membranes in the presence of gramicidin A: I. studies of the unit conductance channel. Biochim. Biophys. Acta. 274:1972;294-312.
71. Neher E., Sandblom J., Eisenman G. Ionic selectivity, saturation, and block in gramicidin A channels. II. Saturation behavior of single channel conductances and evidence for the existence of multiple binding sites in the channel. J. Membr. Biol. 40:1978;97-116.
72. Woolley G.A., Zunic V., Karanicolas J., Jaikaran A.S.I., Starostin A.V. Voltage-dependent behavior of a 'ball-and-chain' gramicidin channel. Biophys. J. 73:1997;2465-2475.
73. Dunker A.K., Marvin D.A. A model for membrane transport through α-helical protein pores. J. Theor. Biol. 72:1978;9-16.
74. 2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc. Natl. Acad. Sci. USA. 94:1997;11301-11306.
75. DeCoursey T.E., Cherny V.V. Voltage-activated proton currents in membrane patches of rat alveolar epithelial cells. J. Physiol. 489:1995;299-307.
76. DeCoursey T.E., Cherny V.V. Voltage-activated proton currents in human THP-1 monocytes. J. Membr. Biol. 152:1996;131-140.
77. 2+ and other divalent cations. J. Gen. Physiol. 114:1999;819-838.
78. + currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J. Gen. Physiol. 112:1998;503-522.
79. Nagle J.F., Dilley R.A. Models of localized energy coupling. J. Bioenerg. Biomembr. 18:1986;55-64.
80. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 191:1961;144-148.
81. Mitchell P. A commentary on alternative hypotheses of protonic coupling in the membrane systems catalysing oxidative and photosynthetic phosphorylation. FEBS Lett. 78:1977;1-20.
82. Kell D.B. On the functional proton current pathway of electron transport phosphorylation: an electrodic view. Biochim. Biophys. Acta. 549:1979;55-99.
83. Williams R.J.P. The history and the hypotheses concerning ATP-formation by energised protons. FEBS Lett. 85:1978;9-19.
84. Kasianowicz J., Benz R., McLaughlin S. How do protons cross the membrane-solution interface? Kinetic studies on bilayer membranes exposed to the protonophore S-13 (5-chloro-3-tert-butyl-2′-chloro-4′nitrosalicylanilide). J. Membr. Biol. 95:1987;73-89.
85. Eigen M. Proton transfer, acid-base catalysis, and enzymatic hydrolysis. Part I: elementary processes. Angewandte Chemie, International Edition. 3:1964;1-19.
86. Silverman D.N., Vincent S.H. Proton transfer in the catalytic mechanism of carbonic anhydrase. CRC Crit. Rev. Biochem. 14:1983;207-235.
87. Jonsson B.-H., Steiner H., Lindskog S. Participation of buffer in the catalytic mechanism of carbonic anhydrase. FEBS Lett. 64:1976;310-314.
88. A- state of bacterial photosynthetic reaction centers: rate limitation within the protein. Biophys. J. 73:1997;367-381.
89. Läuger P. Diffusion-limited ion flow through pores. Biochim. Biophys. Acta. 455:1976;493-509.
90. B. Hille, Ionic Channels of Excitable Membranes, 2nd edn., Sinauer Associates, Sunderland, MA, 1992, 607 pp.
91. Jordan P.C. How pore mouth charge distributions alter the permeability of transmembrane ionic channels. Biophys. J. 51:1987;297-311.
92. Prats M., Tocanne J.F., Teissie J. Lateral proton conduction at a lipid/water interface. Effect of lipid nature and ionic content of the aqueous phase. Eur. J. Biochem. 162:1987;379-385.
93. Sacks V., Marantz Y., Aagaard A., Checover S., Nachliel E., Gutman M. The dynamic feature of the proton collecting antenna of a protein surface. Biochim. Biophys. Acta. 1365:1998;232-240.
94. + ion conductance through the gramicidin channel. Biophys. J. 53:1988;25-32.
95. P. Läuger, Electrogenic Ion Pumps, Sinauer Associates, Sunderland, MA, 1991, 313 pp.
96. Lukacs G.L., Kapus A., Nanda A., Romanek R., Grinstein S. Proton conductance of the plasma membrane: properties, regulation, and functional role. Am. J. Physiol. 265:1993;C3-C14.
97. + fluxes through a channel. J. Physiol. 398:1988;313-327.
98. Mitchell P. Proton translocation mechanisms and energy transduction by adenosine triphosphatases: an answer to criticisms. FEBS Lett. 50:1975;95-97.
99. Mills D.A., Ferguson-Miller S. Proton uptake and release in cytochrome c oxidase: separate pathways in time and space? Biochim. Biophys. Acta. 1365:1998;46-52.
100. Jardetzky O. Simple allosteric model for membrane pumps. Nature. 211:1966;969-970.
101. Lanyi J.K. Bacteriorhodopsin as a model for proton pumps. Nature. 375:1995;461-463.
102. Wikström M., Bogachev A., Finel M., Morgan J.E., Puustinen A., Raitio M., Verkhovskaya M., Verkhovsky M.I. Mechanism of proton translocation by the respiratory oxidases: the histidine cycle. Biochim. Biophys. Acta. 1187:1994;106-111.
103. Stoeckenius W., Lozier R.H., Bogomolni R.A. Bacteriorhodopsin and the purple membrane of halobacteria. Biochim. Biophys. Acta. 505:1979;215-278.
104. Lanyi J.K. Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim. Biophys. Acta. 1183:1993;241-261.
105. 0-ATP synthases: glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 200:1997;217-224.
106. Elston T., Wang H., Oster G. Energy transduction in ATP synthase. Nature. 391:1998;510-513.
107. Rydström J., Hu X., Fjellström O., Meuller J., Zhang J., Johansson C., Bizouarn T. Domains, specific residues and conformational states involved in hydride ion transfer and proton pumping by nicotinamide nucleotide transhydrogenase from Escherichia coli. Biochim. Biophys. Acta. 1365:1998;10-16.
108. Nair S.K., Christianson D.W. Unexpected pH-dependent conformation of His-64, the proton shuttle of carbonic anhydrase II. J. Am. Chem. Soc. 113:1991;9455-9458.
109. Gennis R.B. Multiple proton-conducting pathways in cytochrome oxidase and a proposed role for the active-site tyrosine. Biochim. Biophys. Acta. 1365:1998;241-248.
110. Christianson D.W., Fierke C.A. Carbonic anhydrase: evolution of the zinc binding site by nature and by design. Acc. Chem. Res. 29:1996;331-339.
111. 18O exchange catalyzed by human carbonic anhydrase II. J. Biol. Chem. 256:1981;9466-9470.
112. Owen B.B., Sweeton F.H. The conductance of hydrochloric acid in aqueous solutions from 5 to 65° J. Am. Chem. Soc. 63:1941;2811-2817.
113. S. Cukierman, Flying protons in linked gramicidin monomers, Israel J. Chem., in press .
114. Eisenman G., Enos B., Hägglund J., Sandblom J. Gramicidin as an example of a single-filing ionic channel. Ann. New York Acad. Sci. 329:1980;8-20.
115. Duff K.C., Ashley R.H. The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers. Virology. 190:1992;485-489.
116. + permeation and pH regulation at a mammalian serotonin receptor. J. Neurosci. 17:1997;2257-2266.
117. Meister M., Lowe G., Berg H.C. The proton flux through the bacterial flagellar motor. Cell. 49:1987;643-650.
118. 0 is greater than 10 fS. FEBS Lett. 203:1986;289-294.
119. Schindler H., Nelson N. Proteolipid of adenosinetriphosphatase from yeast mitochondria forms proton-selective channels in planar lipid bilayers. Biochemistry. 21:1982;5787-5794.
120. DeGrado W.F., Lear J.D. Conformationally constrained α-helical peptide models for protein ion channels. Biopolymers. 29:1990;205-213.
121. Fung D.C., Berg H.C. Powering the flagellar motor of Escherichia coli with an external voltage source. Nature. 375:1995;809-812.
122. Blair D.F., Berg H.C. The MotA protein of E. coli is a proton-conducting component of the flagellar motor. Cell. 60:1990;439-449.
123. Stolz B., Berg H.C. Evidence for interactions between MotA and MotB, torque-generating elements of the flagellar motor of Escherichia coli. J. Bacteriol. 173:1991;7033-7037.