Electron transfer and energy transduction in the terminal part of the respiratory chain - Lessons from bacterial model systems

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 6, 2009, Pages 626-634

  Richter, Oliver Matthias H ^a   Ludwig, Bernd ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Cofactor insertion; Complex III; Cytochrome c oxidase; Paracoccus denitrificans; Proton pumping; Thermus thermophilus

Indexed keywords

BACTERIAL ENZYME; CYTOCHROME C; CYTOCHROME C OXIDASE; OXYGEN; PROTON; UBIQUINOL CYTOCHROME C REDUCTASE;

BIOGENESIS; BIOLOGICAL MODEL; ELECTRON TRANSPORT; ENERGY TRANSFER; MEMBRANE; MITOCHONDRION; NONHUMAN; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL; PROKARYOTE; PROTEIN INTERACTION; RESPIRATORY CHAIN; REVIEW; THERMUS;

BACTERIAL PROTEINS; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; ENERGY METABOLISM; ENERGY TRANSFER; MODELS, BIOLOGICAL; MODELS, MOLECULAR; OXIDATION-REDUCTION; PARACOCCUS DENITRIFICANS; PROTONS; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); PARACOCCUS DENITRIFICANS; PROKARYOTA; THERMUS THERMOPHILUS;

EID: 66349104071     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.02.020     Document Type: Review

References (124)

1. Belevich I., and Verkhovsky M.I. Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid. Redox Signal. 10 (2008) 1-29
2. Hosler J.P., Ferguson-Miller S., and Mills D.A. Energy transduction: proton transfer through the respiratory complexes. Annu. Rev. Biochem. 75 (2006) 165-187
3. Richter O.-M.H., and Ludwig B. Cytochrome c oxidase - structure, function, and physiology of a redox-driven molecular machine. Rev. Physiol. Biochem. Pharmacol. 147 (2003) 47-74
4. Ludwig B., Bender E., Arnold S., Hüttemann M., Lee I., and Kadenbach B. Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chem. Bio. Chem. 2 (2001) 392-403
5. Iwata S., Ostermeier C., Ludwig B., and Michel H. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376 (1995) 660-669
6. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and Yoshikawa S. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 269 (1995) 1069-1074
7. Yoshikawa S., Shinzawa-Itoh K., Nakashima R., Yaono R., Yamashita E., Inoue N., Yao M., Fei M.J., Libeu C.P., Mizushima T., Yamaguchi H., Tomizaki T., and Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280 (1998) 1723-1729
8. Ostermeier C., Harrenga A., Ermler U., and Michel H. Structure at 2.7 Å resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody Fv fragment. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10547-10553
9. Baker S.C., Ferguson S.J., Ludwig B., Page M.D., Richter O.-M.H., and van Spanning R.J.M. Molecular genetics of the genus Paracoccus - metabolically versatile bacteria with bioenergetic flexibility. Microbiol. Mol. Biol. Rev. 62 (1998) 1046-1078
10. 3) from Paracoccus denitrificans. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 196-200
11. 3 has a third subunit. Eur. J. Biochem. 172 (1988) 543-546
12. 3 from Paracoccus denitrificans and the 13-subunit beef heart enzyme. Biophys. J. 60 (1991) 415-423
13. Witt H., and Ludwig B. Isolation, analysis, and deletion of the gene coding for subunit IV of cytochrome c oxidase in Paracoccus denitrificans. J. Biol. Chem. 272 (1997) 5514-5517
14. Nicoletti F., Witt H., Ludwig B., Brunori M., and Malatesta F. Paracoccus denitrificans cytochrome c oxidase: a kinetic study on the two- and four-subunit complexes. Biochim. Biophys. Acta 1365 (1998) 393-403
15. Hellwig P., Ostermeier C., Michel H., Ludwig B., and Mäntele W. Electrochemically induced FT-IR difference spectra of the two- and four-subunit cytochrome c oxidase from P. denitrificans reveal the same conformational changes upon electron and proton transfer. Biochim. Biophys. Acta 1409 (1998) 107-112
16. Rich R.P. Towards an understanding of the chemistry of oxygen reduction and proton translocation in the iron-copper respiratory oxidases. Aust. J. Plant Physiol. 22 (1995) 479-486
17. 1 in the electron transport network of Paracoccus denitrificans: redundant or subtly different in function?. J. Bacteriol. 183 (2001) 7017-7026
18. 552 from Paracoccus denitrificans in the oxidized and reduced states. J. Mol. Biol. 295 (2000) 667-678
19. 552 in the reduced state. Eur. J. Biochem. 267 (2000) 4205-4212
20. 552 in both redox states. Biochemistry 40 (2001) 12312-12320
21. 552 acting as electron donor to the Paracoccus denitrificans cytochrome c oxidase. Biochim. Biophys. Acta 1411 (1999) 114-120
22. 552, and its truncated and site-directed mutants. Biochemistry 41 (2002) 10629-10634
23. Margoliash E., and Bosshard H.R. Guided by electrostatics, a textbook protein comes of age. Trends Biochem. Sci. 8 (1983) 3316-3320
24. McLendon G., and Hake R. Interprotein electron transfer. Chem. Rev. 92 (1992) 481-490
25. Capaldi R.A., Darley-Usmar V., Fuller S., and Millett F. Structural and functional features of the interaction of cytochrome c with complex III and cytochrome c oxidase. FEBS L. 138 (1982) 1-7
26. A redox site in cytochrome c oxidase into a mononuclear copper center. Biochemistry 36 (1997) 3232-3236
27. A mutant of cytochrome c oxidase from Paracoccus denitrificans. Conclusive evidence on the initial electron entry metal center. FEBS-L. 434 (1998) 322-324
28. Witt H., Zickermann V., and Ludwig B. Site-directed mutagenesis of cytochrome c oxidase reveals two acidic residues involved in the binding of cytochrome c. Biochim. Biophys. Acta 1230 (1995) 74-76
29. Witt H., Malatesta F., Nicoletti F., Brunori M., and Ludwig B. Cytochrome c binding site on cytochrome oxidase in Paracoccus denitrificans. Eur. J. Biochem. 251 (1998) 367-373
30. Witt H., Malatesta F., Nicoletti F., Brunori M., and Ludwig B. Tryptophan 121 of subunit II is the electron entry site to cytochrome c oxidase in Paracoccus denitrificans - involvement of a hydrophobic patch in the docking reaction. J. Biol. Chem. 273 (1998) 5132-5136
31. 3 oxidase: electron entry and kinetic phases of the reaction. Eur. J. Biochem. 269 (2002) 2980-2988
32. Wienk H., Maneg O., Lücke C., Pristovsek P., Löhr F., Ludwig B., and Rüterjans H. Interaction of cytochrome c with cytochrome c oxidase: an NMR study on two soluble fragments derived from Paracoccus denitrificans. Biochemistry 42 (2003) 6005-6012
33. Lyubenova S., Siddiqui K., Penning de Vries M., Ludwig B., and Prisner T.F. Protein-protein interactions studied by EPR relaxation measurements: cytochrome c and cytochrome c oxidase. J.Phys.Chem.B 111 (2007) 3839-3846
34. Fee J.A., Kuila D., Mather M.W., and Yoshida T. Respiratory proteins from extremely thermophilic, aerobic bacteria. Biochim. Biophys. Acta 853 (1986) 153-185
35. Than M.E., Hof P., Huber R., Bourenkov G.P., Bartunik H.D., Buse G., and Soulimane T. Thermus thermophilus cytochrome-c552: a new highly thermostable cytochrome-c structure obtained by MAD phasing. Biochemistry 38 (1999) 1057-1065
36. 3-type cytochrome c oxidase at 1.6 Å resolution. Nature Struct. Biol. 6 (1999) 509-516
37. 3-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19 (2000) 1766-1776
38. 3 oxidase from Thermus thermophilus: effect of temperature. Biochemistry 38 (1999) 1057-1065
39. - 1 with a combined electrochemical and FT-IR spectroscopic setup. Biopolymers 74 (2004) 73-76
40. A site of Thermus thermophilus. Biophys. J. 93 (2007) 2845-2851
41. A fragments with their substrates. J. Biol. Chem. 278 (2003) 46734-46740
42. Maneg O., Malatesta F., Ludwig B., and Drosou V. Interaction of cytochrome c with cytochrome oxidase: two different docking scenarios. Biochim. Biophys. Acta 1655 (2004) 274-281
43. 3 oxidase - a combined NMR and computational approach. J. Biol. Chem. 281 (2006) 14503-14513
44. 3. J. Biol. Chem. 268 (1993) 5395-5408
45. 3 oxidase in Thermus thermophilus. IUBMB Life 59 (2007) 563-569
46. Stroh A., Anderka O., Pfeiffer K., Yagi T., Finel M., Ludwig B., and Schägger H. Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J. Biol. Chem. 279 (2004) 5000-5007
47. Wikström M.K.F. Proton pump coupled to cytochrome c oxidase in mitochondria. Nature 266 (1977) 271-273
48. Pereira M.M., Sousa F.L., Veríssimo A.F., and Teixeira M. Looking for the minimum common denominator in haem-copper oxygen reductases: towards a unified catalytic mechanism. Biochim. Biophys. Acta 1777 (2008) 929-934
49. 3 contributions and assignment of vibrational modes. Biochemistry 38 (1999) 1685-1694
50. Verkhovsky M.I., Morgan J.E., and Wikström M. Control of electron delivery to the oxygen reduction site of cytochrome c oxidase: a role for protons. Biochemistry 34 (1995) 7483-7491
51. Belevich I., Bloch D.A., Belevich N., Wikström M., and Verkhovsky M.I. Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 2685-2690
52. Kaila V.R.I., Verkhovsky M.I., Hummer G., and Wikström M. Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 6255-6259
53. Schmidt B., McCracken J., and Ferguson-Miller S. A discrete water exit pathway in the membrane protein cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15539-15542
54. 3 propionate, Asp399 and the binuclear center of cytochrome c oxidase from Paracoccus denitrificans. Biochim. Biophys. Acta 1777 (2008) 220-226
55. Kannt A., Pfitzner U., Ruitenberg M., Hellwig P., Ludwig B., Mäntele W., Fendler K., and Michel H. Mutation of Arg-54 strongly influences heme composition and rate and directionality of electron transfer in Paracoccus denitrificans cytochrome c oxidase. J. Biol. Chem. 274 (1999) 37974-37981
56. Jasaitis A., Backgren C., Morgan J.E., Puustinen A., Verkhovsky M.I., and Wikström M. Electron and proton transfer in the arginine-54-methionine mutant of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 40 (2001) 5269-5274
57. Thomas J.W., Puustinen A., Alben J.O., Gennis R.B., and Wikström M. Substitution of asparagine for aspartate-135 in subunit I of the cytochrome bo ubiquinol oxidase of Escherichia coli eliminates proton-pumping activity. Biochemistry 32 (1993) 10923-10928
58. Thomas J.W., Lemieux L.J., Alben J.O., and Gennis R.B. Site-directed mutagenesis of highly conserved residues in helix VIII of subunit I of the cytochrome bo ubiquinol oxidase from Escherichia coli: an amphipathic transmembrane helix that may be important in conveying protons to the binuclear center. Biochemistry 32 (1993) 11173-11180
59. 3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I. J. Bioenerg. Biomembranes 30 (1998) 89-97
60. 3 from Escherichia coli is required for the function of the heme-copper oxidase. Biochemistry 38 (1999) 15150-15156
61. Brändén M., Tomson F., Gennis R.B., and Brzezinski P. The entry point of the K-proton-transfer pathway in cytochrome c oxidase. Biochemistry 41 (2002) 10794-10798
62. Richter O.-M.H., Dürr K.L., Kannt A., Ludwig B., Scandurra F.M., Giuffrè A., Sarti P., and Hellwig P. Probing the access of protons to the K pathway in the Paracoccus denitrificans cytochrome c oxidase. FEBS J. 272 (2005) 404-412
63. Pfitzner U., Hoffmeier K., Harrenga A., Kannt A., Michel H., Bamberg E., Richter O.-M.H., and Ludwig B. Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39 (2000) 6756-6762
64. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272 (1996) 1136-1144
65. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., and Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15304-15309
66. Salje J., Ludwig B., and Richter O.-M.H. Is a third proton-conducting pathway operative in bacterial cytochrome c oxidase?. Biochem. Soc. Trans. 33 (2005) 829-831
67. Lee H.M., Das T.K., Rousseau D.L., Mills D., Ferguson-Miller S., and Gennis R.B. Mutations in the putative H-channel in the cytochrome c oxidase from Rhodobacter sphaeroides show that this channel is not important for proton conduction but reveal modulation of the properties of heme a. Biochemistry 39 (2000) 2989-2996
68. Konstantinov A.A., Siletsky S., Mitchell D., Kaulen A., and Gennis R.B. 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. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 9085-9090
69. Ruitenberg M., Kannt A., Bamberg E., Ludwig B., Michel H., and Fendler K. Single-electron reduction of the oxidized state is coupled to proton uptake via the K pathway in Paracoccus denitrificans cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4632-4636
70. Verkhovsky M.I., Belevich N., Morgan J.E., and Wikström M. Proton linkage of cytochrome a oxidoreduction in carbon monoxide-treated cytochrome c oxidase. Biochim. Biophys. Acta 1412 (1999) 184-189
71. Ruitenberg M., Kannt A., Bamberg E., Fendler K., and Michel H. Reduction of cytochrome c oxidase by a second electron leads to proton translocation. Nature 417 (2002) 99-102
72. Forte E., Scandurra F.M., Richter O.-M.H., D'Itri E., Sarti P., Brunori M., Ludwig B., and Giuffrè A. Proton uptake upon anaerobic reduction of the Paracoccus denitrificans cytochrome c oxidase: a kinetic investigation of the K354M and D124N mutants. Biochemistry 43 (2004) 2957-2963
73. Hellwig P., Behr J., Ostermeier C., Richter O.-M.H., Pfitzner U., Odenwald A., Ludwig B., Michel H., and Mäntele W. Involvement of glutamic acid 278 in the redox reaction of the cytochrome c oxidase from Paracoccus denitrificans investigated by FTIR spectroscopy. Biochemistry 37 (1998) 7390-7399
74. Rost B., Behr J., Hellwig P., Richter O.-M.H., Ludwig B., Michel H., and Mäntele W. Time-resolved FT-IR studies on the CO adduct of Paracoccus denitrificans cytochrome c oxidase: comparison of the fully reduced and the mixed valence form. Biochemistry 38 (1999) 7565-7571
75. Riistama S., Hummer G., Puustinen A., Dyer R.B., Woodruff W.H., and Wikström M. Bound water in the proton translocation mechanism of the haem-copper oxidases. FEBS L. 414 (1997) 275-280
76. Wikström M., Verkhovsky M.I., and Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1604 (2003) 61-65
77. Popović D.M., and Stuchebrukhov A.A. Proton pumping mechanism and catalytic cycle of cytochrome c oxidase: coulomb pump model with kinetic gating. FEBS L. 566 (2004) 126-130
78. Dürr K., Koepke J., Hellwig P., Müller H., Angerer H., Peng G., Olkhova E., Richter O.-M.H., Ludwig B., and Michel H. A D-pathway mutation decouples the Paracoccus denitrificans cytochrome c oxidase by altering the side-chain orientation of a distant conserved glutamate. J. Mol. Biol. 384 (2008) 865-877
79. Namslauer A., Pawate A.S., Gennis R.B., and Brzezinski P. Redox-coupled proton translocation in biological systems: proton shuttling in cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15543-15547
80. Olkhova E., Helms V., and Michel H. Titration behavior of residues at the entrance of the D-pathway of cytochrome c oxidase from Paracoccus denitrificans investigated by continuum electrostatic calculations. Biophys. J. 89 (2005) 2324-2331
81. 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
82. Wiertz F.G.M., Richter O.-M.H., Cherepanov A.V., MacMillan F., Ludwig B., and de Vries S. An oxo-ferryl tryptophan radical catalytic intermediate in cytochrome c and quinol oxidases trapped by microsecond freeze-hyperquenching (MHQ). FEBS L. 575 (2004) 127-130
83. Buse G., Soulimane T., Dewor M., Meyer H.E., and Blüggel M. Evidence for a copper coordinated histidine-tyrosine crosslink in the active site of cytochrome oxidase. Prot. Sci. 8 (1999) 985-990
84. Pinakoulaki E., Pfitzner U., Ludwig B., and Varotsis C. The role of the cross-link His-Tyr in the functional properties of the binuclear center in cytochrome c oxidase. J. Biol. Chem. 277 (2002) 13563-13568
85. 2 reaction. J. Biol. Chem. 278 (2003) 18761-18766
86. Hellwig P., Pfitzner U., Behr J., Rost B., Pesavento R.P., Donk W.V., Gennis R.B., Michel H., Ludwig B., and Mäntele W. Vibrational modes of tyrosines in cytochrome c oxidase from Paracoccus denitrificans: FTIR and electrochemical studies on Tyr-D4-labeled and on Tyr280His and Tyr35Phe mutant enzymes. Biochemistry 41 (2002) 9116-9125
87. Gorbikova E.A., Belevich I., Wikström M., and Verkhovsky M.I. The proton donor for O-O bond scissionby cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 10733-10737
88. Gorbikova E.A., Wikström M., and Verkhovsky M.I. The protonation state of the cross-linked tyrosine during the catalytic cycle of cytochrome c Oxidase. J. Biol. Chem. 283 (2008) 34907-34912
89. Budiman K., Kannt A., Lyubenova S., Richter O.-M.H., Ludwig B., Michel H., and MacMillan F. Tyrosine 167: the origin of the radical species observed in the reaction of cytochrome c oxidase with hydrogen peroxide in Paracoccus denitrificans. Biochemistry 43 (2004) 11709-11716
90. Wiertz F.G.M., Richter O.-M.H., Ludwig B., and de Vries S. Kinetic resolution of a tryptophan-radical intermediate in the reaction cycle of Paracoccus denitrificans cytochrome c oxidase. J. Biol. Chem. 282 (2007) 31580-31591
91. MacMillan F., Budiman K., Angerer H., and Michel H. The role of tryptophan 272 in the Paracoccus denitrificans cytochrome c oxidase. FEBS L. 580 (2006) 1345-1349
92. Barrientos A., Gouget K., Horn D., Soto I.C., and Fontanesi F. Suppression mechanisms of COX assembly defects in yeast and human: insights into the COX assembly process. Biochim. Biophys. Acta 1793 (2009) 97-107
93. Cobine P.A., Pierrel F., and Winge D.R. Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim. Biophys. Acta 1763 (2006) 759-772
94. Herrmann J.M., and Funes S. Biogenesis of cytochrome oxidase-Sophisticated assembly lines in the mitochondrial inner membrane. Gene 354 (2005) 43-52
95. Greiner P., Hannappel A., Werner C., and Ludwig B. Biogenesis of cytochrome c oxidase - bacterial approaches to study cofactor insertion into subunit I. Biochim. Biophys. Acta 1777 (2008) 904-911
96. U. Pfitzner, PhD thesis, Frankfurt (2000).
97. B and magnesium centers of cytochrome c oxidase. J. Biol. Chem. 275 (2000) 619-623
98. Carr H.S., George G.N., and Winge D.R. Yeast Cox11, a protein essential for cytochrome c oxidase assembly, is a Cu(I)-binding protein. J. Biol. Chem. 277 (2002) 31237-31242
99. Schwarz D., Dötsch V., and Bernhard F. Production of membrane proteins using cell-free expression systems. Proteomics 8 (2008) 3933-3946
100. Khalimonchuk O., and Ostermann K. and G. Rödel. Evidence for the association of yeast mitochondrial ribosomes with Cox11p, a protein required for the Cu(B) site formation of cytochrome c oxidase. Curr. Genet. 47 (2005) 223-233
101. Pecina P., Houštková H., Hansíková H., Zeman J., and Houštěk J. Genetic Defects of Cytochrome c Oxidase Assembly. Physiol. Res. 53 (2004) S213-S223
102. Bratton M., Mills D., Castleden C.K., Hosler J., and Meunier B. Disease-related mutations in cytochrome c oxidase studied in yeast and bacterial models. Eur. J. Biochem. 270 (2003) 1222-1230
103. Poyau A., Buchet K., and Godinot C. Sequence conservation from human to prokaryotes of Surf1, a protein involved in cytochrome c oxidase assembly, deficient in Leigh syndrome. FEBS L. 462 (1999) 416-420
104. Agostino1 A., Invernizzi F., Tiveron C., Fagiolari G., Prelle A., Lamantea E., Giavazzi A., Battaglia G., Tatangelo L., Tiranti V., and Zeviani M. Constitutive knockout of Surf1 is associated with high embryonic lethality, mitochondrial disease and cytochrome c oxidase deficiency in mice. Hum. Mol. Genet. 12 (2003) 399-413
105. Smith D., Gray J., Mitchell L., Antholine W.E., and Hosler J.P. Assembly of cytochrome-c oxidase in the absence of assembly protein surf1p leads to loss of the active site heme. J. Biol. Chem. 280 (2005) 17652-17656
106. Mick D.U., Wagner K., van der Laan M., Frazier A.E., Perschil I., Pawlas M., Meyer H.E., Warscheid B., and Rehling P. Shy1 couples Cox1 translational regulation to cytochrome c oxidase assembly. EMBO J. 26 (2007) 4347-4358
107. Bundschuh F.A., Hoffmeier K., and Ludwig B. Two variants of the assembly factor Surf1 target specific terminal oxidases in Paracoccus denitrificans. Biochim. Biophys.Acta 1777 (2008) 1336-1343
108. H. Biochim. Biophys. Acta 1777 (2008) 1038-1043
109. 1 complex. FEBS L. 545 (2003) 39-46
110. Berry E.A., Guergova-Kuras M., Huang L.-s., and Crofts A.R. Structure and function of cytochrome bc complexes. Annu. Rev. Biochem. 69 (2000) 1005-1075
111. 1 complex of Paracoccus denitrificans. Eur. J. Biochem. 255 (1998) 100-106
112. 1 complex. Biochemistry 40 (2001) 15396-15402
113. 1 complex from Paracoccus denitrificans: evidence for protonation reactions coupled with quinone binding. Biochemistry 42 (2003) 12391-12399
114. Bachmann J., Bauer B., Zwicker K., Ludwig B., and Anderka O. The Rieske protein from Paracoccus denitrificans is integrated into the cytoplasmic membrane by the twin-arginine translocase. FEBS-J. 273 (2006) 4817-4830
115. 1 complex implies communication between center P sites as part of the mechanism of anti-cooperative quinol oxidation. J. Biol. Chem. 282 (2007) 22289-22297
116. 1 complex from Paracoccus denitrificans. FEBS-J. 275 (2008) 4773-4785
117. 1 complex from Paracoccus denitrificans in solutions of dodecyl maltoside. Progr. Colloid Polym. Sci. 119 (2002) 77-83
118. Morgner N., Kleinschroth T., Barth H.-D., Ludwig B., and Brutschy B. A novel approach to analyze membrane proteins by laser mass spectrometry: from protein subunits to the integral complex. J. Am. Soc. Mass Spectrom. 8 (2007) 1429-1438
119. 1 complex and its substrate cytochrome c. Biochem. Soc. Trans. 36 (2008) 981-985
120. 3 complexes. J. Biol. Chem. 260 (1985) 2458-2467
121. 1 and its physiological redox partners. Biochim. Biophys. Acta 1777 (2008) 250-259
122. 552 interaction by mutagenesis and fast kinetics. Biochemistry 47 (2008) 12974-12984
123. 1 complex complements the respiratory chain of Thermus thermophilus. Biochim. Biophys. Acta 1708 (2005) 262-274
124. Mooser D., Maneg O., MacMillan F., Malatesta F., Soulimane T., and Ludwig B. The menaquinol-oxidizing cytochrome bc complex from Thermus thermophilus: protein domains and subunits. Biochim. Biophys. Acta 1757 (2006) 1084-1094