Cardiolipin binding in bacterial respiratory complexes: Structural and functional implications

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 10, 2012, Pages 1937-1949

  Arias Cartin, Rodrigo ^a   Grimaldi, Stéphane ^b,c   Arnoux, Pascal ^d,e   Guigliarelli, Bruno ^b,c   Magalon, Axel ^f  

^a YALE UNIVERSITY   (United States)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d IRFM   (France)

^e University of Aix Marseille   (France)

^f AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Aerobic and anaerobic respiration; Bacteria; Cardiolipin; Formate dehydrogenase; Nitrate reductase; Respiratory complex

Indexed keywords

CARDIOLIPIN; FORMATE DEHYDROGENASE; FORMATE DEHYDROGENASE N; NITRATE REDUCTASE; QUINONE DERIVATIVE; SUCCINATE DEHYDROGENASE; UNCLASSIFIED DRUG;

ANAEROBIC METABOLISM; BINDING KINETICS; CHEMICAL STRUCTURE; COMPLEX FORMATION; CONFERENCE PAPER; ESCHERICHIA COLI; MEMBRANE; MEMBRANE STRUCTURE; MICROBIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE;

BACTERIA; BACTERIAL PROTEINS; CARDIOLIPINS; CRYSTALLOGRAPHY, X-RAY; ELECTRON-TRANSFERRING FLAVOPROTEINS; MEMBRANE PROTEINS;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 84864694828     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.04.005     Document Type: Conference Paper

References (242)

1. R. Phillips, T. Ursell, P. Wiggins, and P. Sens Emerging roles for lipids in shaping membrane-protein function Nature 459 2009 379 385
2. A.G. Lee How lipids affect the activities of integral membrane proteins Biochim. Biophys. Acta 1666 2004 62 87
3. I. Vorobyov, L. Li, and T.W. Allen Assessing atomistic and coarse-grained force fields for protein-lipid interactions: the formidable challenge of an ionizable side chain in a membrane J. Phys. Chem. B 112 2008 9588 9602
4. Y. Sonoda, S. Newstead, N.J. Hu, Y. Alguel, E. Nji, K. Beis, S. Yashiro, C. Lee, J. Leung, A.D. Cameron, B. Byrne, S. Iwata, and D. Drew Benchmarking membrane protein detergent stability for improving throughput of high-resolution X-ray structures Structure 19 2011 17 25
5. R.M. Bill, P.J. Henderson, S. Iwata, E.R. Kunji, H. Michel, R. Neutze, S. Newstead, B. Poolman, C.G. Tate, and H. Vogel Overcoming barriers to membrane protein structure determination Nat. Biotechnol. 29 2011 335 340
6. P.J. Judge, and A. Watts Recent contributions from solid-state NMR to the understanding of membrane protein structure and function Curr. Opin. Chem. Biol. 15 2011 690 695
7. P. Raman, V. Cherezov, and M. Caffrey The Membrane Protein Data Bank Cell. Mol. Life Sci. 63 2006 36 51
8. C. Hunte, and S. Richers Lipids and membrane protein structures Curr. Opin. Struct. Biol. 18 2008 406 411
9. A.M. Ernst, F.X. Contreras, B. Brugger, and F. Wieland Determinants of specificity at the protein-lipid interface in membranes FEBS Lett. 584 2010 1713 1720
10. F.X. Contreras, A.M. Ernst, F. Wieland, and B. Brugger Specificity of intramembrane protein-lipid interactions Cold Spring Harb. Perspect. Biol. 3 2011
11. M. Bogdanov, E. Mileykovskaya, and W. Dowhan Lipids in the assembly of membrane proteins and organization of protein supercomplexes: implications for lipid-linked disorders Subcell. Biochem. 49 2008 197 239
12. H. Palsdottir, and C. Hunte Lipids in membrane protein structures Biochim. Biophys. Acta 1666 2004 2 18
13. A. van Dalen, and B. de Kruijff The role of lipids in membrane insertion and translocation of bacterial proteins Biochim. Biophys. Acta 1694 2004 97 109
14. N. Mizusawa, and H. Wada The role of lipids in photosystem II Biochim. Biophys. Acta 1817 2012 194 208
15. M. Pangborn Isolation and purification of a serologically active phospholipid from beef heart J. Biol. Chem. 143 1942 247 256
16. M. Schlame, and M. Ren The role of cardiolipin in the structural organization of mitochondrial membranes Biochim. Biophys. Acta 1788 2009 2080 2083
17. E. Mileykovskaya, and W. Dowhan Cardiolipin membrane domains in prokaryotes and eukaryotes Biochim. Biophys. Acta 1788 2009 2084 2091
18. T. Romantsov, Z. Guan, and J.M. Wood Cardiolipin and the osmotic stress responses of bacteria Biochim. Biophys. Acta 1788 2009 2092 2100
19. V.E. Kagan, H.A. Bayir, N.A. Belikova, O. Kapralov, Y.Y. Tyurina, V.A. Tyurin, J. Jiang, D.A. Stoyanovsky, P. Wipf, P.M. Kochanek, J.S. Greenberger, B. Pitt, A.A. Shvedova, and G. Borisenko Cytochrome c/cardiolipin relations in mitochondria: a kiss of death Free Radic. Biol. Med. 46 2009 1439 1453
20. M. Klingenberg Cardiolipin and mitochondrial carriers Biochim. Biophys. Acta 1788 2009 2048 2058
21. G. Paradies, G. Petrosillo, V. Paradies, R.J. Reiter, and F.M. Ruggiero Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease J. Pineal Res. 48 2010 297 310
22. A. Corcelli The cardiolipin analogues of Archaea Biochim. Biophys. Acta 1788 2009 2101 2106
23. I. de Andrade Rosa, M. Einicker-Lamas, R. Roney Bernardo, L.M. Previatto, R. Mohana-Borges, J.A. Morgado-Diaz, and M. Benchimol Cardiolipin in hydrogenosomes: evidence of symbiotic origin Eukaryot. Cell 5 2006 784 787
24. N. Depalo, L. Catucci, A. Mallardi, A. Corcelli, and A. Agostiano Enrichment of cardiolipin content throughout the purification procedure of photosystem II Bioelectrochemistry 63 2004 103 106
25. A. Ventrella, L. Catucci, G. Mascolo, A. Corcelli, and A. Agostiano Isolation and characterization of lipids strictly associated to PSII complexes: focus on cardiolipin structural and functional role Biochim. Biophys. Acta 1768 2007 1620 1627
26. T.H. Haines, and N.A. Dencher Cardiolipin: a proton trap for oxidative phosphorylation FEBS Lett. 528 2002 35 39
27. K.C. Huang, R. Mukhopadhyay, and N.S. Wingreen A curvature-mediated mechanism for localization of lipids to bacterial poles PLoS Comput. Biol. 2 2006 e151
28. R.N. Lewis, and R.N. McElhaney The physicochemical properties of cardiolipin bilayers and cardiolipin-containing lipid membranes Biochim. Biophys. Acta 1788 2009 2069 2079
29. M. Fry, and D.E. Green Cardiolipin requirement by cytochrome oxidase and the catalytic role of phospholipid Biochem. Biophys. Res. Commun. 93 1980 1238 1246
30. M. Hayer-Hartl, H. Schagger, G. von Jagow, and K. Beyer Interactions of phospholipids with the mitochondrial cytochrome-c reductase studied by spin-label ESR and NMR spectroscopy Eur. J. Biochem. 209 1992 423 430
31. V.M. Poore, and C.I. Ragan A spin label study of the lipid boundary layer of mitochondrial NADH-ubiquinone oxidoreductase Biochim. Biophys. Acta 693 1982 105 112
32. N.C. Robinson, J. Zborowski, and L.H. Talbert Cardiolipin-depleted bovine heart cytochrome c oxidase: binding stoichiometry and affinity for cardiolipin derivatives Biochemistry 29 1990 8962 8969
33. N.C. Robinson Functional binding of cardiolipin to cytochrome c oxidase J. Bioenerg. Biomembr. 25 1993 153 163
34. E. Sedlak, and N.C. Robinson Phospholipase A(2) digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure Biochemistry 38 1999 14966 14972
35. C.A. Yu, and L. Yu Structural role of phospholipids in ubiquinol-cytochrome c reductase Biochemistry 19 1980 5715 5720
36. H. Schagger, T. Hagen, B. Roth, U. Brandt, T.A. Link, and G. von Jagow Phospholipid specificity of bovine heart bc1 complex Eur. J. Biochem. 190 1990 123 130
37. B. Gomez Jr., and N.C. Robinson Phospholipase digestion of bound cardiolipin reversibly inactivates bovine cytochrome bc1 Biochemistry 38 1999 9031 9038
38. K. Beyer, and B. Nuscher Specific cardiolipin binding interferes with labeling of sulfhydryl residues in the adenosine diphosphate/adenosine triphosphate carrier protein from beef heart mitochondria Biochemistry 35 1996 15784 15790
39. K.S. Eble, W.B. Coleman, R.R. Hantgan, and C.C. Cunningham Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy J. Biol. Chem. 265 1990 19434 19440
40. K.E. McAuley, P.K. Fyfe, J.P. Ridge, N.W. Isaacs, R.J. Cogdell, and M.R. Jones Structural details of an interaction between cardiolipin and an integral membrane protein Proc. Natl. Acad. Sci. U. S. A. 96 1999 14706 14711
41. A. Camara-Artigas, D. Brune, and J.P. Allen Interactions between lipids and bacterial reaction centers determined by protein crystallography Proc. Natl. Acad. Sci. U. S. A. 99 2002 11055 11060
42. C. Lange, J.H. Nett, B.L. Trumpower, and C. Hunte Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure EMBO J. 20 2001 6591 6600
43. H. Palsdottir, C.G. Lojero, B.L. Trumpower, and C. Hunte Structure of the yeast cytochrome bc1 complex with a hydroxyquinone anion Qo site inhibitor bound J. Biol. Chem. 278 2003 31303 31311
44. L. Qin, C. Hiser, A. Mulichak, R.M. Garavito, and S. Ferguson-Miller Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 103 2006 16117 16122
45. K. Shinzawa-Itoh, H. Aoyama, K. Muramoto, H. Terada, T. Kurauchi, Y. Tadehara, A. Yamasaki, T. Sugimura, S. Kurono, K. Tsujimoto, T. Mizushima, E. Yamashita, T. Tsukihara, and S. Yoshikawa Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase EMBO J. 26 2007 1713 1725
46. K. Beyer, and M. Klingenberg ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by 31P nuclear magnetic resonance Biochemistry 24 1985 3821 3826
47. E. Pebay-Peyroula, C. Dahout-Gonzalez, R. Kahn, V. Trezeguet, G.J. Lauquin, and G. Brandolin Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Nature 426 2003 39 44
48. H. Nury, C. Dahout-Gonzalez, V. Trezeguet, G. Lauquin, G. Brandolin, and E. Pebay-Peyroula Structural basis for lipid-mediated interactions between mitochondrial ADP/ATP carrier monomers FEBS Lett. 579 2005 6031 6036
49. M. Zhou, N. Morgner, N.P. Barrera, A. Politis, S.C. Isaacson, D. Matak-Vinkovic, T. Murata, R.A. Bernal, D. Stock, and C.V. Robinson Mass spectrometry of intact V-type ATPases reveals bound lipids and the effects of nucleotide binding Science 334 2011 380 385
50. V. Yankovskaya, R. Horsefield, S. Tornroth, C. Luna-Chavez, H. Miyoshi, C. Leger, B. Byrne, G. Cecchini, and S. Iwata Architecture of succinate dehydrogenase and reactive oxygen species generation Science 299 2003 700 704
51. R. Horsefield, V. Yankovskaya, G. Sexton, W. Whittingham, K. Shiomi, S. Omura, B. Byrne, G. Cecchini, and S. Iwata Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase): a mechanism of electron transfer and proton conduction during ubiquinone reduction J. Biol. Chem. 281 2006 7309 7316
52. M. Jormakka, S. Tornroth, B. Byrne, and S. Iwata Molecular basis of proton motive force generation: structure of formate dehydrogenase-N Science 295 2002 1863 1868
53. R. Arias-Cartin, S. Grimaldi, J. Pommier, P. Lanciano, C. Schaefer, P. Arnoux, G. Giordano, B. Guigliarelli, and A. Magalon Cardiolipin-based respiratory complex activation in bacteria Proc. Natl. Acad. Sci. U. S. A. 108 2011 7781 7786
54. P.K. Fyfe, and M.R. Jones Lipids in and around photosynthetic reaction centres Biochem. Soc. Trans. 33 2005 924 930
55. M.R. Jones Lipids in photosynthetic reaction centres: structural roles and functional holes Prog. Lipid Res. 46 2007 56 87
56. M.C. Wakeham, R.B. Sessions, M.R. Jones, and P.K. Fyfe Is there a conserved interaction between cardiolipin and the type II bacterial reaction center? Biophys. J. 80 2001 1395 1405
57. L. Qin, M.A. Sharpe, R.M. Garavito, and S. Ferguson-Miller Conserved lipid-binding sites in membrane proteins: a focus on cytochrome c oxidase Curr. Opin. Struct. Biol. 17 2007 444 450
58. S.S. Hasan, E. Yamashita, C.M. Ryan, J.P. Whitelegge, and W.A. Cramer Conservation of lipid functions in cytochrome bc complexes J. Mol. Biol. 414 2011 145 162
59. C. Hunte Specific protein-lipid interactions in membrane proteins Biochem. Soc. Trans. 33 2005 938 942
60. P. Mitchell Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism Nature 191 1961 144 148
61. T. Wenz, R. Hielscher, P. Hellwig, H. Schagger, S. Richers, and C. Hunte Role of phospholipids in respiratory cytochrome bc(1) complex catalysis and supercomplex formation Biochim. Biophys. Acta 1787 2009 609 616
62. A.R. Klingen, H. Palsdottir, C. Hunte, and G.M. Ullmann Redox-linked protonation state changes in cytochrome bc1 identified by Poisson-Boltzmann electrostatics calculations Biochim. Biophys. Acta 1767 2007 204 221
63. R. Hielscher, T. Wenz, C. Hunte, and P. Hellwig Monitoring the redox and protonation dependent contributions of cardiolipin in electrochemically induced FTIR difference spectra of the cytochrome bc(1) complex from yeast Biochim. Biophys. Acta 1787 2009 617 625
64. S.C. Chang, P.N. Heacock, E. Mileykovskaya, D.R. Voelker, and W. Dowhan Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae J. Biol. Chem. 273 1998 14933 14941
65. F. Jiang, M.T. Ryan, M. Schlame, M. Zhao, Z. Gu, M. Klingenberg, N. Pfanner, and M.L. Greenberg Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function J. Biol. Chem. 275 2000 22387 22394
66. M. Zhang, E. Mileykovskaya, and W. Dowhan Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane J. Biol. Chem. 277 2002 43553 43556
67. K. Pfeiffer, V. Gohil, R.A. Stuart, C. Hunte, U. Brandt, M.L. Greenberg, and H. Schagger Cardiolipin stabilizes respiratory chain supercomplexes J. Biol. Chem. 278 2003 52873 52880
68. E. Mileykovskaya, M. Zhang, and W. Dowhan Cardiolipin in energy transducing membranes Biochemistry (Mosc.) 70 2005 154 158
69. M. Zhang, E. Mileykovskaya, and W. Dowhan Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria J. Biol. Chem. 280 2005 29403 29408
70. Y. Xu, A. Malhotra, M. Ren, and M. Schlame The enzymatic function of tafazzin J. Biol. Chem. 281 2006 39217 39224
71. M. McKenzie, M. Lazarou, D.R. Thorburn, and M.T. Ryan Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients J. Mol. Biol. 361 2006 462 469
72. D. Acehan, A. Malhotra, Y. Xu, M. Ren, D.L. Stokes, and M. Schlame Cardiolipin affects the supramolecular organization of ATP synthase in mitochondria Biophys. J. 100 2011 2184 2192
73. P. Vreken, F. Valianpour, L.G. Nijtmans, L.A. Grivell, B. Plecko, R.J. Wanders, and P.G. Barth Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome Biochem. Biophys. Res. Commun. 279 2000 378 382
74. A.J. Chicco, and G.C. Sparagna Role of cardiolipin alterations in mitochondrial dysfunction and disease Am. J. Physiol. Cell Physiol. 292 2007 C33 C44
75. A.S. Joshi, J. Zhou, V.M. Gohil, S. Chen, and M.L. Greenberg Cellular functions of cardiolipin in yeast Biochim. Biophys. Acta 1793 2009 212 218
76. R.A. van Gestel, P.J. Rijken, S. Surinova, M. O'Flaherty, A.J. Heck, J.A. Killian, A.I. de Kroon, and M. Slijper The influence of the acyl chain composition of cardiolipin on the stability of mitochondrial complexes; an unexpected effect of cardiolipin in alpha-ketoglutarate dehydrogenase and prohibitin complexes J. Proteomics 73 2010 806 814
77. A. Corcelli, M. Colella, G. Mascolo, F.P. Fanizzi, and M. Kates A novel glycolipid and phospholipid in the purple membrane Biochemistry 39 2000 3318 3326
78. V.M. Lattanzio, A. Corcelli, G. Mascolo, and A. Oren Presence of two novel cardiolipins in the halophilic archaeal community in the crystallizer brines from the salterns of Margherita di Savoia (Italy) and Eilat (Israel) Extremophiles 6 2002 437 444
79. T.H. Chiu, H. Morimoto, and J.J. Baker Biosynthesis and characterization of phosphatidylglycerophosphoglycerol, a possible intermediate in lipoteichoic acid biosynthesis in Streptococcus sanguis Biochim. Biophys. Acta 1166 1993 222 228
80. W. Fischer The polar lipids of group B Streptococci. I. Glucosylated diphosphatidylglycerol, a novel glycopholipid Biochim. Biophys. Acta 487 1977 74 88
81. W. Fischer, and D. Arneth-Seifert d-Alanylcardiolipin, a major component of the unique lipid pattern of Vagococcus fluvialis J. Bacteriol. 180 1998 2950 2957
82. T. Gutberlet, U. Dietrich, H. Bradaczek, G. Pohlentz, K. Leopold, and W. Fischer Cardiolipin, alpha-d-glucopyranosyl, and l-lysylcardiolipin from gram-positive bacteria: FAB MS, monofilm and X-ray powder diffraction studies Biochim. Biophys. Acta 1463 2000 307 322
83. N.C. Johnston, and H. Goldfine Isolation and characterization of new phosphatidylglycerol acetals of plasmalogens. A family of ether lipids in clostridia Eur. J. Biochem. 223 1994 957 963
84. N.C. Johnston, H. Goldfine, and W. Fischer Novel polar lipid composition of Clostridium innocuum as the basis for an assessment of its taxonomic status Microbiology 140 Pt 1 1994 105 111
85. W. Fischer, and K. Leopold Polar lipids of four Listeria species containing l-lysylcardiolipin, a novel lipid structure, and other unique phospholipids Int. J. Syst. Bacteriol. 49 Pt 2 1999 653 662
86. J. Peter-Katalinic, and W. Fischer alpha-d-glucopyranosyl-, d-alanyl- and l-lysylcardiolipin from gram-positive bacteria: analysis by fast atom bombardment mass spectrometry J. Lipid Res. 39 1998 2286 2292
87. C. Schaffer, A.I. Beckedorf, A. Scheberl, S. Zayni, J. Peter-Katalinic, and P. Messner Isolation of glucocardiolipins from Geobacillus stearothermophilus NRS 2004/3a J. Bacteriol. 184 2002 6709 6713
88. W. Martin, M. Hoffmeister, C. Rotte, and K. Henze An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle Biol. Chem. 382 2001 1521 1539
89. B.E. Tropp Cardiolipin synthase from Escherichia coli Biochim. Biophys. Acta 1348 1997 192 200
90. J.E. Cronan Jr. Phospholipid alterations during growth of Escherichia coli J. Bacteriol. 95 1968 2054 2061
91. C.L. Randle, P.W. Albro, and J.C. Dittmer The phosphoglyceride composition of Gram-negative bacteria and the changes in composition during growth Biochim. Biophys. Acta 187 1969 214 220
92. S.A. Short, and D.C. White Metabolism of phosphatidylglycerol, lysylphosphatidylglycerol, and cardiolipin of Staphylococcus aureus J. Bacteriol. 108 1971 219 226
93. I. Shibuya Metabolic regulations and biological functions of phospholipids in Escherichia coli Prog. Lipid Res. 31 1992 245 299
94. S. Hiraoka, H. Matsuzaki, and I. Shibuya Active increase in cardiolipin synthesis in the stationary growth phase and its physiological significance in Escherichia coli FEBS Lett. 336 1993 221 224
95. H.U. Koch, R. Haas, and W. Fischer The role of lipoteichoic acid biosynthesis in membrane lipid metabolism of growing Staphylococcus aureus Eur. J. Biochem. 138 1984 357 363
96. Y. Kanemasa, T. Yoshioka, and H. Hayashi Alteration of the phospholipid composition of Staphylococcus aureus cultured in medium containing NaCl Biochim. Biophys. Acta 280 1972 444 450
97. J.T. McGarrity, and J.B. Armstrong The effect of salt on phospholipid fatty acid composition in Escherichia coli K-12 Biochim. Biophys. Acta 398 1975 258 264
98. K.J. Miller Effects of monovalent and divalent salts on the phospholipid and fatty acid compositions of a halotolerant Planococcus sp. Appl. Environ. Microbiol. 52 1986 580 582
99. L. Catucci, N. Depalo, V.M. Lattanzio, A. Agostiano, and A. Corcelli Neosynthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress Biochemistry 43 2004 15066 15072
100. C.S. Lopez, H. Heras, S.M. Ruzal, C. Sanchez-Rivas, and E.A. Rivas Variations of the envelope composition of Bacillus subtilis during growth in hyperosmotic medium Curr. Microbiol. 36 1998 55 61
101. C.S. Lopez, A.F. Alice, H. Heras, E.A. Rivas, and C. Sanchez-Rivas Role of anionic phospholipids in the adaptation of Bacillus subtilis to high salinity Microbiology 152 2006 605 616
102. G.L. Card, and J.K. Trautman Role of anionic lipid in bacterial membranes Biochim. Biophys. Acta 1047 1990 77 82
103. J.H. Weiner, B.D. Lemire, M.L. Elmes, R.D. Bradley, and D.G. Scraba Overproduction of fumarate reductase in Escherichia coli induces a novel intracellular lipid-protein organelle J. Bacteriol. 158 1984 590 596
104. M.L. Elmes, D.G. Scraba, and J.H. Weiner Isolation and characterization of the tubular organelles induced by fumarate reductase overproduction in Escherichia coli J. Gen. Microbiol. 132 1986 1429 1439
105. F. Kawai, H. Hara, H. Takamatsu, K. Watabe, and K. Matsumoto Cardiolipin enrichment in spore membranes and its involvement in germination of Bacillus subtilis Marburg Genes Genet. Syst. 81 2006 69 76
106. C. Miyazaki, M. Kuroda, A. Ohta, and I. Shibuya Genetic manipulation of membrane phospholipid composition in Escherichia coli: pgsA mutants defective in phosphatidylglycerol synthesis Proc. Natl. Acad. Sci. U. S. A. 82 1985 7530 7534
107. Y. Asai, Y. Katayose, C. Hikita, A. Ohta, and I. Shibuya Suppression of the lethal effect of acidic-phospholipid deficiency by defective formation of the major outer membrane lipoprotein in Escherichia coli J. Bacteriol. 171 1989 6867 6869
108. S. Kikuchi, I. Shibuya, and K. Matsumoto Viability of an Escherichia coli pgsA null mutant lacking detectable phosphatidylglycerol and cardiolipin J. Bacteriol. 182 2000 371 376
109. K. Matsumoto Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids Mol. Microbiol. 39 2001 1427 1433
110. M. Suzuki, H. Hara, and K. Matsumoto Envelope disorder of Escherichia coli cells lacking phosphatidylglycerol J. Bacteriol. 184 2002 5418 5425
111. E. Mileykovskaya, A.C. Ryan, X. Mo, C.C. Lin, K.I. Khalaf, W. Dowhan, and T.A. Garrett Phosphatidic acid and N-acylphosphatidylethanolamine form membrane domains in Escherichia coli mutant lacking cardiolipin and phosphatidylglycerol J. Biol. Chem. 284 2009 2990 3000
112. S. Nishijima, Y. Asami, N. Uetake, S. Yamagoe, A. Ohta, and I. Shibuya Disruption of the Escherichia coli cls gene responsible for cardiolipin synthesis J. Bacteriol. 170 1988 775 780
113. D. Guo, and B.E. Tropp A second Escherichia coli protein with CL synthase activity Biochim. Biophys. Acta 1483 2000 263 274
114. A.M. Michaelis, and Z. Gitai Dynamic polar sequestration of excess MurG may regulate enzymatic function J. Bacteriol. 192 2010 4597 4605
115. Z. Gitai The new bacterial cell biology: moving parts and subcellular architecture Cell 120 2005 577 586
116. D.Z. Rudner, and R. Losick Protein subcellular localization in bacteria Cold Spring Harb. Perspect. Biol. 2 2010 a000307
117. D.M. Engelman Membranes are more mosaic than fluid Nature 438 2005 578 580
118. K. Matsumoto, J. Kusaka, A. Nishibori, and H. Hara Lipid domains in bacterial membranes Mol. Microbiol. 61 2006 1110 1117
119. A. Maftah, J.M. Petit, M.H. Ratinaud, and R. Julien 10-N nonyl-acridine orange: a fluorescent probe which stains mitochondria independently of their energetic state Biochem. Biophys. Res. Commun. 164 1989 185 190
120. J.M. Petit, A. Maftah, M.H. Ratinaud, and R. Julien 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria Eur. J. Biochem. 209 1992 267 273
121. E. Mileykovskaya, and W. Dowhan Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange J. Bacteriol. 182 2000 1172 1175
122. F. Kawai, M. Shoda, R. Harashima, Y. Sadaie, H. Hara, and K. Matsumoto Cardiolipin domains in Bacillus subtilis marburg membranes J. Bacteriol. 186 2004 1475 1483
123. P. Bernal, J. Munoz-Rojas, A. Hurtado, J.L. Ramos, and A. Segura A Pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality Environ. Microbiol. 9 2007 1135 1145
124. C.M. Koppelman, T. Den Blaauwen, M.C. Duursma, R.M. Heeren, and N. Nanninga Escherichia coli minicell membranes are enriched in cardiolipin J. Bacteriol. 183 2001 6144 6147
125. D. Lopez, and R. Kolter Functional microdomains in bacterial membranes Genes Dev. 24 2010 1893 1902
126. K.C. Huang, and K.S. Ramamurthi Macromolecules that prefer their membranes curvy Mol. Microbiol. 76 2010 822 832
127. R. Mukhopadhyay, K.C. Huang, and N.S. Wingreen Lipid localization in bacterial cells through curvature-mediated microphase separation Biophys. J. 95 2008 1034 1049
128. K. Muchova, A.J. Wilkinson, and I. Barak Changes of lipid domains in Bacillus subtilis cells with disrupted cell wall peptidoglycan FEMS Microbiol. Lett. 325 2011 92 98
129. T. Romantsov, A.R. Battle, J.L. Hendel, B. Martinac, and J.M. Wood Protein localization in Escherichia coli cells: comparison of the cytoplasmic membrane proteins ProP, LacY, ProW, AqpZ, MscS, and MscL J. Bacteriol. 192 2010 912 924
130. E. Mileykovskaya, and W. Dowhan Role of membrane lipids in bacterial division-site selection Curr. Opin. Microbiol. 8 2005 135 142
131. T.H. Szeto, S.L. Rowland, L.I. Rothfield, and G.F. King Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts Proc. Natl. Acad. Sci. U. S. A. 99 2002 15693 15698
132. E. Mileykovskaya, I. Fishov, X. Fu, B.D. Corbin, W. Margolin, and W. Dowhan Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo J. Biol. Chem. 278 2003 22193 22198
133. H. Strahl, and L.W. Hamoen Membrane potential is important for bacterial cell division Proc. Natl. Acad. Sci. U. S. A. 107 2010 12281 12286
134. T. Romantsov, S. Helbig, D.E. Culham, C. Gill, L. Stalker, and J.M. Wood Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli Mol. Microbiol. 64 2007 1455 1465
135. T. Romantsov, L. Stalker, D.E. Culham, and J.M. Wood Cardiolipin controls the osmotic stress response and the subcellular location of transporter ProP in Escherichia coli J. Biol. Chem. 283 2008 12314 12323
136. L.D. Renner, and D.B. Weibel Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes Proc. Natl. Acad. Sci. U. S. A. 108 2011 6264 6269
137. W. Dowhan, and M. Bogdanov Lipid-dependent membrane protein topogenesis Annu. Rev. Biochem. 78 2009 515 540
138. R. Lill, W. Dowhan, and W. Wickner The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins Cell 60 1990 271 280
139. J.P. Hendrick, and W. Wickner SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane J. Biol. Chem. 266 1991 24596 24600
140. D.J. du Plessis, N. Nouwen, and A.J. Driessen The Sec translocase Biochim. Biophys. Acta 1808 2011 851 865
141. V.A. Gold, A. Robson, H. Bao, T. Romantsov, F. Duong, and I. Collinson The action of cardiolipin on the bacterial translocon Proc. Natl. Acad. Sci. U. S. A. 107 2010 10044 10049
142. N.I. Mikhaleva, C.L. Santini, G. Giordano, M.A. Nesmeyanova, and L.F. Wu Requirement for phospholipids of the translocation of the trimethylamine N-oxide reductase through the Tat pathway in Escherichia coli FEBS Lett. 463 1999 331 335
143. E. Erez, G. Stjepanovic, A.M. Zelazny, B. Brugger, I. Sinning, and E. Bibi Genetic evidence for functional interaction of the Escherichia coli signal recognition particle receptor with acidic lipids in vivo J. Biol. Chem. 285 2010 40508 40514
144. V.Q. Lam, D. Akopian, M. Rome, D. Henningsen, and S.O. Shan Lipid activation of the signal recognition particle receptor provides spatial coordination of protein targeting J. Cell Biol. 190 2010 623 635
145. G.F. Dancey, and B.M. Shapiro Specific phospholipid requirement for activity of the purified respiratory chain NADH dehydrogenase of Escherichia coli Biochim. Biophys. Acta 487 1977 368 377
146. J.W. Thomson, and B.M. Shapiro The respiratory chain NADH dehydrogenase of Escherichia coli. Isolation of an NADH:quinone oxidoreductase from membranes and comparison with the membrane-bound NADH:dichlorophenolindophenol oxidoreductase J. Biol. Chem. 256 1981 3077 3084
147. Y. Tanaka, Y. Anraku, and M. Futai Escherichia coli membrane d-lactate dehydrogenase. Isolation of the enzyme in aggregated from and its activation by Triton X-100 and phospholipids J. Biochem. 80 1976 821 830
148. M. Esfahani, B.B. Rudkin, C.J. Cutler, and P.E. Waldron Lipid-protein interactions in membranes: interaction of phospholipids with respiratory enzymes of Escherichia coli membrane J. Biol. Chem. 252 1977 3194 3198
149. T.L. Reddy, and M.M. Weber Solubilization, purification, and characterization of succinate dehydrogenase from membranes of Mycobacterium phlei J. Bacteriol. 167 1986 1 6
150. K. Kita, K. Konishi, and Y. Anraku Terminal oxidases of Escherichia coli aerobic respiratory chain. I. Purification and properties of cytochrome b562-o complex from cells in the early exponential phase of aerobic growth J. Biol. Chem. 259 1984 3368 3374
151. B.L. Berg, and V. Stewart Structural genes for nitrate-inducible formate dehydrogenase in Escherichia coli K-12 Genetics 125 1990 691 702
152. F. Blasco, B. Guigliarelli, A. Magalon, M. Asso, G. Giordano, and R.A. Rothery The coordination and function of the redox centres of the membrane-bound nitrate reductases Cell. Mol. Life Sci. 58 2001 179 193
153. M.G. Bertero, R.A. Rothery, M. Palak, C. Hou, D. Lim, F. Blasco, J.H. Weiner, and N.C. Strynadka Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A Nat. Struct. Biol. 10 2003 681 687
154. R.A. Rothery, F. Blasco, A. Magalon, and J.H. Weiner The diheme cytochrome b subunit (Narl) of Escherichia coli nitrate reductase A (NarGHI): structure, function, and interaction with quinols J. Mol. Microbiol. Biotechnol. 3 2001 273 283
155. B. Guigliarelli, M. Asso, C. More, V. Augier, F. Blasco, J. Pommier, G. Giordano, and P. Bertrand EPR and redox characterization of iron-sulfur centers in nitrate reductases A and Z from Escherichia coli. Evidence for a high-potential and a low-potential class and their relevance in the electron-transfer mechanism Eur. J. Biochem. 207 1992 61 68
156. B. Guigliarelli, A. Magalon, M. Asso, P. Bertrand, C. Frixon, G. Giordano, and F. Blasco Complete coordination of the four Fe-S centers of the beta subunit from Escherichia coli nitrate reductase. Physiological, biochemical, and EPR characterization of site-directed mutants lacking the highest or lowest potential [4Fe-4S] clusters Biochemistry 35 1996 4828 4836
157. R.A. Rothery, M.G. Bertero, R. Cammack, M. Palak, F. Blasco, N.C. Strynadka, and J.H. Weiner The catalytic subunit of Escherichia coli nitrate reductase A contains a novel [4Fe-4S] cluster with a high-spin ground state Biochemistry 43 2004 5324 5333
158. M. Jormakka, D. Richardson, B. Byrne, and S. Iwata Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes Structure (Camb) 12 2004 95 104
159. P. Lanciano, A. Savoyant, S. Grimaldi, A. Magalon, B. Guigliarelli, and P. Bertrand New method for the spin quantitation of [4Fe-4S](+) clusters with S = (3) / (2). Application to the FS0 center of the NarGHI nitrate reductase from Escherichia coli J. Phys. Chem. B 111 2007 13632 13637
160. S. Grimaldi, P. Lanciano, P. Bertrand, F. Blasco, and B. Guigliarelli Evidence for an EPR-detectable semiquinone intermediate stabilized in the membrane-bound subunit NarI of nitrate reductase A (NarGHI) from Escherichia coli Biochemistry 44 2005 1300 1308
161. P. Lanciano, A. Magalon, P. Bertrand, B. Guigliarelli, and S. Grimaldi High-stability semiquinone intermediate in nitrate reductase A (NarGHI) from Escherichia coli is located in a quinol oxidation site close to heme bD Biochemistry 46 2007 5323 5329
162. R. Arias-Cartin, S. Lyubenova, P. Ceccaldi, T. Prisner, A. Magalon, B. Guigliarelli, and S. Grimaldi HYSCORE evidence that endogenous mena- and ubisemiquinone bind at the same Q site (Q(D)) of Escherichia coli nitrate reductase A J. Am. Chem. Soc. 132 2010 5942 5943
163. S. Grimaldi, R. Arias-Cartin, P. Lanciano, S. Lyubenova, B. Endeward, T.F. Prisner, A. Magalon, and B. Guigliarelli Direct evidence for nitrogen ligation to the high stability semiquinone intermediate in Escherichia coli nitrate reductase A J. Biol. Chem. 285 2010 179 187
164. S. Grimaldi, R. Arias-Cartin, P. Lanciano, S. Lyubenova, R. Szenes, B. Endeward, T.F. Prisner, B. Guigliarelli, and A. Magalon Determination of the proton environment of high stability menasemiquinone intermediate in Escherichia coli nitrate reductase A by pulsed EPR J. Biol. Chem. 287 2012 4662 4670
165. C. More, V. Belle, M. Asso, A. Fournel, G. Roger, B. Guigliarelli, and P. Bertrand EPR spectroscopy: a powerful technique for the structural and functional investigation of metalloproteins Biospectroscopy 5 1999 S3 S18
166. E.A. Berry, and F.A. Walker Bis-histidine-coordinated hemes in four-helix bundles: how the geometry of the bundle controls the axial imidazole plane orientations in transmembrane cytochromes of mitochondrial complexes II and III and related proteins J. Biol. Inorg. Chem. 13 2008 481 498
167. P. Lanciano, A. Vergnes, S. Grimaldi, B. Guigliarelli, and A. Magalon Biogenesis of a respiratory complex is orchestrated by a single accessory protein J. Biol. Chem. 282 2007 17468 17474
168. A. Magalon, and R. Mendel Biosynthesis and insertion of the molybdenum
169. A. Magalon, J. Fedor, A. Walburger, and J.H. Weiner Molybdenum enzymes in bacteria and their maturation Coord. Chem. Rev. 255 2011 1159 1178
170. S. Heber, and B.E. Tropp Genetic regulation of cardiolipin synthase in Escherichia coli Biochim. Biophys. Acta 1129 1991 1 12
171. L. Rinyu, E.W. Martin, E. Takahashi, P. Maroti, and C.A. Wraight Modulation of the free energy of the primary quinone acceptor (QA) in reaction centers from Rhodobacter sphaeroides: contributions from the protein and protein-lipid(cardiolipin) interactions Biochim. Biophys. Acta 1655 2004 93 101
172. L. Nagy, F. Milano, M. Dorogi, A. Agostiano, G. Laczko, K. Szebenyi, G. Varo, M. Trotta, and P. Maroti Protein/lipid interaction in the bacterial photosynthetic reaction center: phosphatidylcholine and phosphatidylglycerol modify the free energy levels of the quinones Biochemistry 43 2004 12913 12923
173. M. Giustini, F. Castelli, I. Husu, M. Giomini, A. Mallardi, and G. Palazzo Influence of cardiolipin on the functionality of the Q(a) site of the photosynthetic bacterial reaction center J. Phys. Chem. B 109 2005 21187 21196
174. R.A. Rothery, G.J. Workun, and J.H. Weiner The prokaryotic complex iron-sulfur molybdoenzyme family Biochim. Biophys. Acta 1778 2008 1897 1929
175. B. Schoepp-Cothenet, R. van Lis, P. Philippot, A. Magalon, M.J. Russell, and W. Nitschke The ineluctable requirement for the trans-iron elements molybdenum and/or tungsten in the origin of life Sci. Rep. 2 2012 263
176. N.R. Stanley, F. Sargent, G. Buchanan, J. Shi, V. Stewart, T. Palmer, and B.C. Berks Behaviour of topological marker proteins targeted to the Tat protein transport pathway Mol. Microbiol. 43 2002 1005 1021
177. F. Sargent, B.C. Berks, and T. Palmer Assembly of membrane-bound respiratory complexes by the Tat protein-transport system Arch. Microbiol. 178 2002 77 84
178. S. Aibara, M. Kato, M. Ishinaga, and M. Kito Changes in positional distribution of fatty acids in the phospholipids of Escherichia coli after shift-down in temperature Biochim. Biophys. Acta 270 1972 301 306
179. M. Kito, S. Aibara, M. Kato, and T. Hata Differences in fatty acid composition among phosphatidylethanolamine, phosphatidylglycerol and cardiolipin of Escherichia coli Biochim. Biophys. Acta 260 1972 475 478
180. C.R. Lancaster Succinate:quinone oxidoreductases: an overview Biochim. Biophys. Acta 1553 2002 1 6
181. K. Kita, C.R. Vibat, S. Meinhardt, J.R. Guest, and R.B. Gennis One-step purification from Escherichia coli of complex II (succinate: ubiquinone oxidoreductase) associated with succinate-reducible cytochrome b556 J. Biol. Chem. 264 1989 2672 2677
182. C. Hagerhall, and L. Hederstedt A structural model for the membrane-integral domain of succinate: quinone oxidoreductases FEBS Lett. 389 1996 25 31
183. L. Hederstedt Respiration without O2 Science 284 1999 1941 1942
184. C.R. Lancaster, A. Kroger, M. Auer, and H. Michel Structure of fumarate reductase from Wolinella succinogenes at 2.2 A resolution Nature 402 1999 377 385
185. C.R. Lancaster Wolinella succinogenes quinol:fumarate reductase and its comparison to E. coli succinate:quinone reductase FEBS Lett. 555 2003 21 28
186. G. Cecchini, E. Maklashina, V. Yankovskaya, T.M. Iverson, and S. Iwata Variation in proton donor/acceptor pathways in succinate:quinone oxidoreductases FEBS Lett. 545 2003 31 38
187. J. Ruprecht, V. Yankovskaya, E. Maklashina, S. Iwata, and G. Cecchini Structure of Escherichia coli succinate:quinone oxidoreductase with an occupied and empty quinone-binding site J. Biol. Chem. 284 2009 29836 29846
188. J. Ruprecht, S. Iwata, R.A. Rothery, J.H. Weiner, E. Maklashina, and G. Cecchini Perturbation of the quinone-binding site of complex II alters the electronic properties of the proximal [3Fe-4S] iron-sulfur cluster J. Biol. Chem. 286 2011 12756 12765
189. Q.M. Tran, R.A. Rothery, E. Maklashina, G. Cecchini, and J.H. Weiner Escherichia coli succinate dehydrogenase variant lacking the heme b Proc. Natl. Acad. Sci. U. S. A. 104 2007 18007 18012
190. K.S. Oyedotun, P.F. Yau, and B.D. Lemire Identification of the heme axial ligands in the cytochrome b562 of the Saccharomyces cerevisiae succinate dehydrogenase J. Biol. Chem. 279 2004 9432 9439
191. K.S. Oyedotun, C.S. Sit, and B.D. Lemire The Saccharomyces cerevisiae succinate dehydrogenase does not require heme for ubiquinone reduction Biochim. Biophys. Acta 1767 2007 1436 1445
192. H. Eubel, J. Heinemeyer, S. Sunderhaus, and H.P. Braun Respiratory chain supercomplexes in plant mitochondria Plant Physiol. Biochem. 42 2004 937 942
193. J. Vonck, and E. Schafer Supramolecular organization of protein complexes in the mitochondrial inner membrane Biochim. Biophys. Acta 1793 2009 117 124
194. R.A. Stuart Supercomplex organization of the oxidative phosphorylation enzymes in yeast mitochondria J. Bioenerg. Biomembr. 40 2008 411 417
195. N.V. Dudkina, R. Kouril, K. Peters, H.P. Braun, and E.J. Boekema Structure and function of mitochondrial supercomplexes Biochim. Biophys. Acta 1797 2010 664 670
196. G. Lenaz, and M.L. Genova Kinetics of integrated electron transfer in the mitochondrial respiratory chain: random collisions vs. solid state electron channeling Am. J. Physiol. Cell Physiol. 292 2007 C1221 C1239
197. M.L. Genova, C. Bianchi, and G. Lenaz Structural organization of the mitochondrial respiratory chain Ital. J. Biochem. 52 2003 58 61
198. C. Bianchi, M.L. Genova, G. Parenti Castelli, and G. Lenaz The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis J. Biol. Chem. 279 2004 36562 36569
199. M.I. Garcia Fernandez, D. Ceccarelli, and U. Muscatello Use of the fluorescent dye 10-N-nonyl acridine orange in quantitative and location assays of cardiolipin: a study on different experimental models Anal. Biochem. 328 2004 174 180
200. K. Brandner, D.U. Mick, A.E. Frazier, R.D. Taylor, C. Meisinger, and P. Rehling Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth Syndrome Mol. Biol. Cell 16 2005 5202 5214
201. S.M. Claypool, Y. Oktay, P. Boontheung, J.A. Loo, and C.M. Koehler Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane J. Cell Biol. 182 2008 937 950
202. H. Schagger Respiratory chain supercomplexes of mitochondria and bacteria Biochim. Biophys. Acta 1555 2002 154 159
203. G. Petrosillo, F.M. Ruggiero, N. Di Venosa, and G. Paradies Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin FASEB J. 17 2003 714 716
204. G. Paradies, G. Petrosillo, M. Pistolese, N. Di Venosa, A. Federici, and F.M. Ruggiero Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin Circ. Res. 94 2004 53 59
205. M.L. Genova, A. Baracca, A. Biondi, G. Casalena, M. Faccioli, A.I. Falasca, G. Formiggini, G. Sgarbi, G. Solaini, and G. Lenaz Is supercomplex organization of the respiratory chain required for optimal electron transfer activity? Biochim. Biophys. Acta 1777 2008 740 746
206. G. Unden, and J. Bongaerts Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors Biochim. Biophys. Acta 1320 1997 217 234
207. V.B. Borisov, R. Murali, M.L. Verkhovskaya, D.A. Bloch, H. Han, R.B. Gennis, and M.I. Verkhovsky Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode Proc. Natl. Acad. Sci. U. S. A. 108 2011 17320 17324
208. W.J. Ingledew, and R.K. Poole The respiratory chains of Escherichia coli Microbiol. Rev. 48 1984 222 271
209. T. Iwasaki, K. Matsuura, and T. Oshima Resolution of the aerobic respiratory system of the thermoacidophilic archaeon, Sulfolobus sp. strain 7. I. The archaeal terminal oxidase supercomplex is a functional fusion of respiratory complexes III and IV with no c-type cytochromes J. Biol. Chem. 270 1995 30881 30892
210. M. Lubben, S. Arnaud, J. Castresana, A. Warne, S.P. Albracht, and M. Saraste A second terminal oxidase in Sulfolobus acidocaldarius Eur. J. Biochem. 224 1994 151 159
211. E.A. Berry, and B.L. Trumpower Isolation of ubiquinol oxidase from Paracoccus denitrificans and resolution into cytochrome bc1 and cytochrome c-aa3 complexes J. Biol. Chem. 260 1985 2458 2467
212. A. Stroh, O. Anderka, K. Pfeiffer, T. Yagi, M. Finel, B. Ludwig, and H. Schagger 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
213. N. Sone, M. Sekimachi, and E. Kutoh Identification and properties of a quinol oxidase super-complex composed of a bc1 complex and cytochrome oxidase in the thermophilic bacterium PS3 J. Biol. Chem. 262 1987 15386 15391
214. T. Tanaka, M. Inoue, J. Sakamoto, and N. Sone Intra- and inter-complex cross-linking of subunits in the quinol oxidase super-complex from thermophilic Bacillus PS3 J. Biochem. 119 1996 482 486
215. A. Niebisch, and M. Bott Purification of a cytochrome bc-aa3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum. Identification of a fourth subunity of cytochrome aa3 oxidase and mutational analysis of diheme cytochrome c1 J. Biol. Chem. 278 2003 4339 4346
216. C. Castelle, M. Guiral, G. Malarte, F. Ledgham, G. Leroy, M. Brugna, and M.T. Giudici-Orticoni A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans J. Biol. Chem. 283 2008 25803 25811
217. P.M. Sousa, S.T. Silva, B.L. Hood, N. Charro, J.N. Carita, F. Vaz, D. Penque, T.P. Conrads, and A.M. Melo Supramolecular organizations in the aerobic respiratory chain of Escherichia coli Biochimie 93 2011 418 425
218. L. Prunetti, P. Infossi, M. Brugna, C. Ebel, M.T. Giudici-Orticoni, and M. Guiral New functional sulfide oxidase-oxygen reductase supercomplex in the membrane of the hyperthermophilic bacterium Aquifex aeolicus J. Biol. Chem. 285 2010 41815 41826
219. Y. Gao, B. Meyer, L. Sokolova, K. Zwicker, M. Karas, B. Brutschy, G. Peng, and H. Michel Heme-copper terminal oxidase using both cytochrome c and ubiquinol as electron donors Proc. Natl. Acad. Sci. U. S. A. 109 2012 3275 3280
220. A.S. Johnson, S. van Horck, and P.J. Lewis Dynamic localization of membrane proteins in Bacillus subtilis Microbiology 150 2004 2815 2824
221. T. Lenn, M.C. Leake, and C.W. Mullineaux Clustering and dynamics of cytochrome bd-I complexes in the Escherichia coli plasma membrane in vivo Mol. Microbiol. 70 2008 1397 1407
222. T. Lenn, M.C. Leake, and C.W. Mullineaux Are Escherichia coli OXPHOS complexes concentrated in specialized zones within the plasma membrane? Biochem. Soc. Trans. 36 2008 1032 1036
223. E. Schafer, N.A. Dencher, J. Vonck, and D.N. Parcej Three-dimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria Biochemistry 46 2007 12579 12585
224. H.G. Enoch, and R.L. Lester The purification and properties of formate dehydrogenase and nitrate reductase from Escherichia coli J. Biol. Chem. 250 1975 6693 6705
225. M. Jormakka, S. Tornroth, J. Abramson, B. Byrne, and S. Iwata Purification and crystallization of the respiratory complex formate dehydrogenase-N from Escherichia coli Acta Crystallogr. D Biol. Crystallogr. 58 2002 160 162
226. L. Loschi, S.J. Brokx, T.L. Hills, G. Zhang, M.G. Bertero, A.L. Lovering, J.H. Weiner, and N.C. Strynadka Structural and biochemical identification of a novel bacterial oxidoreductase J. Biol. Chem. 279 2004 50391 50400
227. G. Unden Differential roles for menaquinone and demethylmenaquinone in anaerobic electron transport of E. coli and their fnr-independent expression Arch. Microbiol. 150 1988 499 503
228. A.I. Shestopalov, A.V. Bogachev, R.A. Murtazina, M.B. Viryasov, and V.P. Skulachev Aeration-dependent changes in composition of the quinone pool in Escherichia coli. Evidence of post-transcriptional regulation of the quinone biosynthesis FEBS Lett. 404 1997 272 274
229. M. Bekker, G. Kramer, A.F. Hartog, M.J. Wagner, C.G. de Koster, K.J. Hellingwerf, and M.J. de Mattos Changes in the redox state and composition of the quinone pool of Escherichia coli during aerobic batch-culture growth Microbiology 153 2007 1974 1980
230. K. Mobius, R. Arias-Cartin, D. Breckau, A.L. Hannig, K. Riedmann, R. Biedendieck, S. Schroder, D. Becher, A. Magalon, J. Moser, M. Jahn, and D. Jahn Heme biosynthesis is coupled to electron transport chains for energy generation Proc. Natl. Acad. Sci. U. S. A. 107 2010 10436 10441
231. T.M. Iverson, C. Luna-Chavez, G. Cecchini, and D.C. Rees Structure of the Escherichia coli fumarate reductase respiratory complex Science 284 1999 1961 1966
232. M.L. Rodrigues, T.F. Oliveira, I.A. Pereira, and M. Archer X-ray structure of the membrane-bound cytochrome c quinol dehydrogenase NrfH reveals novel haem coordination EMBO J. 25 2006 5951 5960
233. M. Marcia, U. Ermler, G. Peng, and H. Michel The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration Proc. Natl. Acad. Sci. U. S. A. 106 2009 9625 9630
234. J.I. Yeh, U. Chinte, and S. Du Structure of glycerol-3-phosphate dehydrogenase, an essential monotopic membrane enzyme involved in respiration and metabolism Proc. Natl. Acad. Sci. U. S. A. 105 2008 3280 3285
235. M. Jormakka, K. Yokoyama, T. Yano, M. Tamakoshi, S. Akimoto, T. Shimamura, P. Curmi, and S. Iwata Molecular mechanism of energy conservation in polysulfide respiration Nat. Struct. Mol. Biol. 15 2008 730 737
236. R.G. Efremov, R. Baradaran, and L.A. Sazanov The architecture of respiratory complex I Nature 465 2010 441 445
237. R.K. Hite, Z. Li, and T. Walz Principles of membrane protein interactions with annular lipids deduced from aquaporin-0 2D crystals EMBO J. 29 2010 1652 1658
238. G. Wisedchaisri, S.L. Reichow, and T. Gonen Advances in structural and functional analysis of membrane proteins by electron crystallography Structure 19 2011 1381 1393
239. R. Harkewicz, and E.A. Dennis Applications of mass spectrometry to lipids and membranes Annu. Rev. Biochem. 80 2011 301 325
240. L.M. Loura, and M. Prieto FRET in membrane biophysics: an overview Front. Physiol. 2 2011 82
241. A.W. Smith Lipid-protein interactions in biological membranes: a dynamic perspective Biochim. Biophys. Acta 1818 2012 172 177
242. M. Sud, E. Fahy, D. Cotter, A. Brown, E.A. Dennis, C.K. Glass, A.H. Merrill Jr., R.C. Murphy, C.R. Raetz, D.W. Russell, and S. Subramaniam LMSD: LIPID MAPS structure database Nucleic Acids Res. 35 2007 D527 D532