Proton translocation by bacteriorhodopsin and heme-copper oxidases

Current Opinion in Structural Biology

Volumn 8, Issue 4, 1998, Pages 480-488

  Wikström, Mårten ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; CYTOCHROME C OXIDASE; MEMBRANE PROTEIN; OXIDOREDUCTASE; POTASSIUM CHANNEL; PROTON PUMP;

CONTROLLED STUDY; ENZYME SUBUNIT; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; REVIEW; X RAY CRYSTALLOGRAPHY;

EID: 0032143387     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(98)80127-9     Document Type: Article

References (68)

1. Mitchell P. Chemiosmotic Coupling in Oxidative and Photosynthetic Phosphorylation. 1966;Glynn Research Ltd. Bodmin. UK.
2. Lancaster CRD, Michel H. The coupling of light-induced electron transfer and proton uptake as derived from crystal structures of reaction centres from Rhodopseudomonas viridis modified at the binding site of the secondary quinone, QB. Structure. 5:1997;1339-1359.
3. Grigorieff N., Ceska TA, Downing KH, Baldwin JM, Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol. 259:1996;393-421.
4. Kimura Y, Vassylyev DG, Miyazawa A, Kidera A, Matsushima M, Mitsuoka K, Murata K, Hirai T, Fujiyoshi Y. Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. of outstanding interest Nature. 389:1997;206-211 This electron crystallogrpahic structure of bacteriorhodopsin has the highest resolution thus far and appears to distinguish between protonated and ionized acidic sidechains.
5. Pebay-Peyroula E, Rumme G, Rosenousch JP, Landau EM. X-ray structure of bacteriorhodopsin at 2.5 Å from microcrystals grown in lipid cubic phases. of outstanding interest Nature. 277:1997;1676-1681 The first high-resolution X-ray structure of bacteriorhodopsin.
6. Iwata S, Ostermeier C, Ludwig B, Michel H. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 376:1995;660-669.
7. Tsukihara T., Aoyama H, Yamashita E, Torrizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å Science. 269:1995;1069-1074.
8. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H., Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å Science. 272:1996;1136-1144.
9. B) histidine ligand and a tyrosine and discusses the properties of proton transfer pathways.
10. Gohlke U, Warne T, Saraste M. Projection structure of the cytochrome bo ubiquinol oxidase from Escherichia coli at 6 Å resolution. EMBO J. 16:1997;1181-1188.
11. Babcock GT, Wikström M. Oxygen activation and the conservation of energy in cell respiration. Nature. 356:1992;301-309.
12. Ferguson-Miller S, Babcock GT. Heme/copper oxidases. Chem. Rev. 96:1996;2889-2907.
13. Ostermeie C, Iwata S, Michel H. Cytochrome c oxidase. Curr Opin Struct Biol. 6:1996;460-466.
14. Lanyi JK. Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim Biophys Acta. 1183:1993;241-261.
15. Lanyi JK. Bacteriorhodopsin as a model for proton pumps. Nature. 375:1995;461-463.
16. Lanyi JK. Mechanism of ion transport across membranes. Bacteriorhodopsin as a prototype for proton pumps. of special interest J. Biol Chem. 272:1997;31209-31212 An excelent short review on the state of the art bacteriorhodopsin structure and function.
17. Nagle JF, Mille M, Morowitz HJ. Theory of hydrogen bonded chains in bioenergetics. J Chem Phys. 72:1980;3959-3971.
18. Agmon N. The Grotthuss mechanism. Chem Phys Lett. 244:1995;456-462.
19. + translocation along then single-file water chain in the gramicidin A channel. Biophys J. 71:1996;19-39.
20. Shaltiel S, Cox S, Taylor SS. Conserved water molecules contribute to the extensive network of interactions at the active site of protein kinase A. Proc Natl Acad Sci USA. 95:1998;484-491.
21. Oprea TI, Hummer G, Garcia AE. Identification of a functional water channel in cytochrome P450 enzymes. Proc Natl Acad Sci USA. 94:1997;2133-2138.
22. Ernst JA, Clubb RT, Zhou H-X, Gronenborn AM, Clore GM. Demonstration of positionally disordered water within a protein hydrophobic cavity by NMR. Science. 267:1995;1813-1817.
23. Eigen M. Protonenübertragung: Zeure-Base-Katalyse und Enzymatische Hydrolyse. Teil I: Elementarvorgänge. Angew Chem Int Ed. 75:1963;489-508.
24. Humphrey W, Logunov I, Schulten K, Sheves M. Molecular dynamics study of bacteriorhodopsin and artificial pigments. Biochemistry. 33:1994;3668-3678.
25. Roux B, Nina M, Pomès R, Smith JC. Thermodynamic stability of water molecules in the bacteriorhodopsin proton channel: a molecular dynamics free energy perturbation study. Biophys J. 71:1996;670-681.
26. Heberle J, Dencher NA. Proton transfer in the light-harvesting protein bacteriorhodopsin: an investigation with optical pH-indicators. Bountis T. Proton Transfer in Hydrogen-Bonded Systems. 1992;187-197 Plenum Press, New York.
27. Le Coultre J, Gerwert K. Kinetic isotope effects reveal an ice-like and a liquid-phase-type intramolecular proton transfer in bacteriorhodopsin. FEBS Lett. 398:1996;333-336.
28. Heberle J, Dencher NA. Surface-bound optical probes monitor proton translocation and surface potential changes during the bacteriorhodopsinphotocycle. Proc Natl Acad Sci USA. 89:1992;5996-6000.
29. + conduction along hydrogen-bonded chains of water molecules. Biophys J. 1998;. in press.
30. Hatanaka M, Kandori H, Maeda A. Localization and orientation of functional water molecules in bacteriorhodopsin as revealed by polarized Fourier transform infrared spectroscopy. of special interest Biophys J. 73:1997;1001-1006 An interesting study into the orientation of Asp85 and a water molecule in its vicinity and their respective changes during the photocycle.
31. Korstantinov AA, Siletsky S, Mitchell D, Kaulen A, Gennis RB. The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. of outstanding interest Proc Natl Acad Sci USA. 94:1997;9085-9090 Mutations in the K-pathway are shown to have no effect on the charge translocation that is coupled to the oxidative half of the catalytic cycle.
32. Ädelroth P, Gennis RB, Brzezinski P. Role of the pathway through K(I-362) in proton transfer in cytochrome c oxidase from R. sphaeroides. of outstanding interest Biochemistry. 37:1998;2470-2476 Mutations in the K-pathway are shown to have no effect on the chemistry and proton uptake of the oxidative half of the catalytic cycle.
33. B.
34. Riistama S, Hummer G, Puustinen A, Dyer BR, Woodruff WH, Wikström M. Bouhd water in the proton translocation mechanism of the haem-copper oxidases. of outstanding interest FEBS Lett. 414:1997;275-280 Statistical and mechanical computation places bound water molecules in cytochrome c oxidase. Sidechain isomerization of Glu242, as part of proton transfer, is proposed on the basis of mutagenesis experiments in which the sidechain is tethered to a lysine or an arginine.
35. Hofacker I, Schulten K. Oxygen and proton pathways in cytochrome c oxidase. of outstanding interest Proteins. 30:1998;100-107 This paper shows computational analysis of the positioning of bound water molecules and oxygen dynamics in cytochrome c oxidase. Isomerization of the sidechains of Glu242 and Lys319 in proton transfer is proposed.
36. Mills DA, Ferguson-Miller S. Proton uptake and release in cytochrome c oxidase: separate pathways in time and space? of special interest Biochim Biophys Acta. 1365:1998;46-52 A timely minireview of the properties of proton transfer pathways in heme-copper oxidases.
37. Brzezinski P, Ädelroth P. Pathways of proton transfer in cytochrome c oxidase. J Bioenerg Biomembr. 30:1998;99-107.
38. Thomas JW, Puustinen A, Alben JO, Gennis RB, Wikström M. Substitution of asparagine for aspartate-135 in subunit 1 of the cytochrome bo ubiquinol oxidase of Escherichia coli eliminates proton-pumping activity. Biochemistry. 32:1993;10923-10928.
39. 3 ubiquinol oxidase of Escherichia coli: second-site mutations in subunit I that restore proton pumping in the mutant asp 135→asn. Biochemistry. 34:1995;4428-4433.
40. Fetter JR, Qian J, Shapleign J, Thomas JW, Garcia-Horsman JA, Schmidt E, Hosler J, Babcock GT, Gennis RB, Ferguson-Miller S. Possible proton relay pathways in cytochrome c oxidase. Proc Natl Acad Sci USA. 92:1995;1604-1608.
41. Mitchell R, Rich PR. Proton uptake by cytochrome c oxidase on reduction and on ligand binding. Biochim Biophys Acta. 1186:1994;19-26.
42. Wikström M, Morgan JE, Hummer G, Woodruff WH, Verkhovsky MI. Oxygen reduction and proton translocation by the haem-copper oxidases. Papa S, Guerrieri F, Tager JM. Frontiers of Cellular Bioenergetics. 1998;Plenum Press, New York. in press.
43. Wikström M, Morgan JE, Verkhovsky MI. On the mechanism of proton translocation by respiratory enzyme. J Bioenerg Biomembr. 30:1998;139-145.
44. 3 is onvolved in proton translocation. of outstanding interest Proc Natl Acad Sci USA. 94:1997;10128-10131 The authors provide a description of a method to reconstitute quinol oxidase into proteoliposomes. First direct evidence is shown for the involvement of Glu242 (numbering of mitochondrial enzyme) in proton translocation.
45. B ligand and Glu242.
46. Hellwig P, Rost B, Kaiser U, Ostermeier C, Michel H, Mäntele W. Carboxyl group protonation upon reduction of the Paracoccus denitrificans cytochrome c oxidase: direct evidence by FTIR spectroscopy. FEBS Lett. 385:1996;53-57.
47. Lübben M, Gerwert K. Redox difference spectroscopy using caged electrons reveals contributions of carboxyl groups to the catalytic mechanism of haem-copper oxidases. FEBS Lett. 397:1996;303-307.
48. Hellwig P, Behr J, Ostermeier C, Richter O-MH, Pfitzner U, Odenwald A, Ludwig B, Michel H, Mäntele W. Involvement of glutamic acid 278 in the redox reaction of the cytochrome c oxidase from Paracoccus denitrificans investigated by FT-IR spectroscopy. of outstanding interest Biochemistry. 1998; Redox potential titrations reveal the carboxyl IR stretch of Glu242 (bovine mitochondrial numbering) and its changes with the redox state of the enzyme.
49. Kannt A, Lancaster CRD, Michel H. The coupling of electron transfer and proton translocation: electrostatic calculations on Paracoccus denitrificans cytochrome c oxidase. of outstanding interest Biophys J. 74:1998;708-721 The first, thorough calculation of the key electrostatic interactions in the cytochrome c oxidase structure and how these may be influenced by the catalytic chemistry.
50. Pomès R, Hummer G, Wikström M. Structure and dynamics of a proton shuttle in cytochrome c oxidase. of special interest Biochim Biophys Acta. 1365:1998;255-260 Molecular dynamics calculations show that the isomerization of Glu242 between the input and output conformers is both thermodynamically and kinetically feasible.
51. Qian J, Shi W, Pressler M, Hogansson C, Mills D, Babcock GT, Ferguson-Miller S. Aspartate-407 in Rhodobacter sphaeroides cytochrome c oxidase is not required for proton pumping or manganese binding. Biochemistry. 36:1997;2539-2543.
52. Riesle J, Oesterhelt D, Dencher NA, Heberle J. D38 is an essential part of the proton translocation pathway in bacteriorhodopsin. Biochemistry. 35:1996;6635-6643.
53. Checover S, Nachliel E, Dencher NA, Gutman M. Mechanism of proton entry into the cytoplasmic section of the proton-conducting channel of bacteriorhodopsin. Biochemistry. 36:1997;13919-13928.
54. Karpefors M, Ädelroth P, Aagaard A, Sigurdson H, Svensson Ek M, Brzezinski P. Electron-proton interactions in terminal oxidases. Biochim Biophys Acta. 1365:1998;159-169.
55. Dioumaev AK, Richter H-T, Brown LS, Tanio M, Tuzi S, Saitô H, Kimura Y, Needleman R, Lanyi JK. Existence of a proton transfer chain in bacteriorhodopsin: participation of glu-194 in the release of protons to the extracellular surface. Biochemistry. 37:1998;2496-2506.
56. Rammelsberg R, Huhn G, Lübben M, Gerwert K. Bacteriorhodopsin's intramolecular proton release pathway consists of a hydrogen-bonded network. of outstanding interest Biochemistry. 1998; Fourier transform IR data reveal that decreases of IR absorption continuum bands accompany the L→M and M→N transitions in bacteriorhodopsin.
57. Oliveberg M, Hallén S, Nilsson T. Uptake and release of protons during the reaction between cytochrome c oxidase and molecular oxygen a flow-flash investigation. Biochemistry. 30:1991;438-440.
58. Verkhovsky MI, Morgan JE, Verkhovskaya ML, Wikström M. Translocation of electrical charge during a single turnover of cytochrome c oxidase. of outstanding interest Biochim Biophys Acta. 1318:1997;6-10 Time-resolved electrometric measurments reveal that equal charge translocation is associated with the P→F and F→O steps in the reaction between reduced cytochrome c oxidase and oxygen.
59. Wikström M. Identification of the electron transfers in cytochrome oxidase that are coupled to proton-pumping. Nature. 338:1989;776-778.
60. 2 transition.
61. Subramaniam S, Faruqi, Oesterhelt D, Henderson R. Electron diffraction studies of light-induced conformational changes in the leu-93 → ala bacteriorhodopsin mutant. of special interest Proc. Natl Acad Sci USA. 94:1997;1767-1772 A description of the conformational changes in bacteriorhodopsin studied by electron diffraction.
62. Rink T, Riesle J, Oesterheld D, Gerwert K, Steinhoff H-J. Spin-labelling studies of the conformational changes in the vicinity of D36, D38, T46 and E161 of bacteriorhodopsin during the photocycle. Biophys J. 73:1997;983-993.
63. Sass HJ, Gessenich R, Koch MHU, Oesterhelt D, Dencher NA, Büldt G, Rapp G. Evidence for charge controlled conformational changes in the photocycle of bacteriorhodopsin. Biophys J. 1998;. in press.
64. 2 transition. Biophys J. 73:1997;2071-2080.
65. Haupts U, Tittor J, Bamberg E, Oesterhelt D. General concept for ion translocation by halobacterial retinal proteins: the isomerization/switch/transfer (IST) model. of outstanding interest Biochemistry. 36:1997;2-7 The authors describe a model for proton translocation in bacteriorhodopsin (bR) that emphasizes the kinetic independence of proton (ion) transfer from and to the Schiff base and discusses the switching of the Schiff-base accessibility for protons between input and output channels. The behavior of several retinal proteins and bR mutants is summarized.
66. Le Coutre J, Tittor J, Oesterhelt D, Gerwert K. Experimental evidence for hydrogen-bonded network proton transfer in bacteriorhodopsin shown by Fourier-transform infrared spectroscopy using azide as catalyst. Proc Natl Acad Sci USA. 92:1995;4962-4966.
67. Zundel G. Proton polarizability and proton transfer processes in hydrogen bonds and cation polarizabilities of other cation bonds - their importance to understand molecular processes in electrochemistry and biology. Trends Phys Chem. 3:1992;129-156.
68. 2. of outstanding interest Biophys J. 74:1998;403-412 Bacteriorhodposin was expressed in the plasma membrane of oocytes and the voltage dependence of the pump current was studied in detail. A parallel, nontransporting reaction cycle was identified at high negative potentials, indicating control of the pump by the electric field.