Prokaryotic assembly factors for the attachment of flavin to complex II

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1827, Issue 5, 2013, Pages 637-647

  McNeil, Matthew B ^a   Fineran, Peter C ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Flavin adenine dinucleotide; Flavoprotein; sdh5; sdhA; sdhE; Succinate dehydrogenase

Indexed keywords

FLAVOPROTEIN; QUERCETIN; SUCCINATE DEHYDROGENASE (UBIQUINONE);

COVALENT BOND; ESCHERICHIA COLI; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; REVIEW;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTEINS; ELECTRON TRANSPORT COMPLEX II; FLAVIN-ADENINE DINUCLEOTIDE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 84875709252     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.09.003     Document Type: Review

References (129)

1. M. Mewies, W.S. McIntire, and N.S. Scrutton Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: The current state of affairs Protein Sci. 7-20 1998 7
2. G. Schwarz, R.R. Mendel, and M.W. Ribbe Molybdenum cofactors, enzymes and pathways Nature 460 2009 839
3. C. Kisker, a.H. Schindelin, and D.C. Rees Molybdenum-cofactor containing enzymes:Structure and Mechanism Annu. Rev. Biochem. 66 1997 233 267
4. J.M. Stevens, T. Ucihda, O. Daltrop, and S.J. Ferguson Covalent cofactor attachment to proteins: cytochrome c biogenesis Biochem. Soc. Trans. 33 2005 792 795 (Pubitemid 41160865)
5. A.C. Rosenzweig, and T.V. O'Halloran Structure and chemistry of the copper chaperone proteins Curr. Opin. Chem. Biol. 4 2000 140 147 (Pubitemid 30189303)
6. J. Smeitink, L. van den Heuvel, and S. DiMauro The genetics and pathology of oxidative phosphorylation Nat. Rev. Genet. 2 2001 342
7. M. Saraste Oxidative Phosphorylation at the fin de siecle Science 283 1999 1488 1493 (Pubitemid 29133351)
8. Y. Hatefi The Mitochondrial Electron Transport and Oxidative Phosphorylation System Annu. Rev. Biochem. 54 1985 1015 1069 (Pubitemid 15073670)
9. G. Cecchini Function and structure of Complex II of the respiratory chain Annu. Rev. Biochem. 72 2003 77 109 (Pubitemid 36930442)
10. L. Hederstedt Complex II Is Complex Too Science 299 2003 671 672
11. L. Hederstedt, and L. Rutberg Succinate dehydrogenase-a comparative review Microbiol. Rev. 45 1981 542 555
12. G. Cecchini, I. Schroder, R.P. Gunsalus, and E. Maklashina Succinate dehydrogenase and fumarate reducatse from Escherichia coli Biochim. Biophys. Acta 1553 2002 140 157 (Pubitemid 34137066)
13. V. Yankovskaya, R. Horsefield, S. Tarnroth, C. Luna-Chavez, H. Miyoshi, C. Lager, B. Byrne, G. Cecchini, and S. Iwata Architecture of Succinate Dehydrogenase and Reactive Oxygen Species Generation Science 299 2003 700 704 (Pubitemid 36159483)
14. D. Wood, M.G. Darlison, R.J. Wilde, and J.R. Guest Nucleotide sequence encoding the flavoprotein and hydrophobic subunits of the succinate dehydrogenase of Escherichia coli Biochem. J. 222 1984 519 534
15. C.R.D. Lancaster, A. Krager, M. Auer, and H. Michel Structure of fumarate reductase from Wolinella succinogenes at 2.2A resolution Nature 402 1999 377 385 (Pubitemid 129544818)
16. 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 (Pubitemid 29309437)
17. E. Maklashina, D.A. Berthold, and G. Cecchini Anaerobic Expression of Escherichia coli Succinate Dehydrogenase: Functional Replacement of Fumarate Reductase in the Respiratory Chain during Anaerobic Growth J. Bacteriol. 180 1998 5989 5996 (Pubitemid 28514218)
18. S.O. Mansoorabadi, C.J. Thibodeaux, and H.W. Liu The diverse roles of flavin coenzymes-Nature's most versatile thespians J. Org. Chem. 72 2007 6329 6342 (Pubitemid 47267554)
19. D.E. Edmondson, and P. Newton-Vinson The Covalent FAD of Monoamine Oxidase: Structural and Functional Role and Mechanism of the Flavinylation Reaction Antioxid. Redox Signal. 3 2001 789 806 (Pubitemid 33131270)
20. T. Senda, M. Senda, S. Kimura, and T. Ishida Redox control of protein conformation in flavoproteins Antioxid. Redox Signal. 11 2009 1742 1766
21. A. Bacher, S. Eberhardt, M. Fischer, K. Kis, and G. Richter Biosynthesis of Vitamin B2 (Riboflavin) Annu. Rev. Nutr. 20 2000 153 167
22. M. Fischer, and A. Bacher Biosynthesis of flavocoenzymes Nat. Prod. Rep. 22 2005 324 350 (Pubitemid 40885715)
23. S. Frago, M. Martinez-Julvez, A. Serrano, and M. Medina Structural analysis of FAD synthetase from Corynebacterium ammoniagenes BMC Microbiol. 8 2008 160
24. D.J. Manstein, and E.F. Pai Purification and characterization of FAD synthetase from Brevibacterium ammoniagenes J. Biol. Chem. 261 1986 16169 16173 (Pubitemid 17202877)
25. B. Herguedas, M. Martinez-Julvez, S. Frago, M. Medina, and J.A. Hermoso Crystallization and preliminary X-ray diffraction studies of FAD synthetase from Corynebacterium ammoniagenes Acta Crystallogr. 65 2009 1285 1288
26. S. Grill, S. Busenbender, M. Pfeiffer, U. Kohler, and M. Mack The bifunctional flavokinase/flavin adenine dinucleotide synthetase from Streptomyces davawensis produces inactive flavin cofactors and is not involved in resistance to the antibiotic roseoflavin J. Bacteriol. 190 2008 1546 1553 (Pubitemid 351304008)
27. W. Wang, R. Kim, H. Yokota, and S.H. Kim Crystal structure of flavin binding to FAD synthetase of Thermotoga maritima Proteins 58 2005 246 248 (Pubitemid 39665636)
28. B. Herguedas, M. Martanez-Jalvez, S. Frago, M. Medina, and J.A. Hermoso Oligomeric State in the Crystal Structure of Modular FAD Synthetase Provides Insights into its Sequential Catalysis in Prokaryotes J. Mol. Biol. 400 2010 218 230
29. M.W. Fraaije, and A. Mattevi Flavoenzymes: diverse catalysts with recurrent features Trends Biochem. Sci. 25 2000 126 132 (Pubitemid 30122424)
30. D.P.H.M. Heuts, N.S. Scrutton, W.S. McIntire, and M.W. Fraaije What's in a covalent bond? FEBS J. 276 2009 3405
31. I. Alexeev, A. Sultana, P. Mantsaia, and G. Schneider Aclacinomycin oxidoreductase (AknOx) from the biosynthetic pathway of the antibiotic aclacinomycin is an unusual flavoenzyme with a dual active site Proc. Natl. Acad. Sci. U. S. A. 104 2007 6170 6175 (Pubitemid 47186067)
32. C.H. Huang, A. Winkler, C.L. Chen, W.L. Lai, Y.C. Tsai, P. Macheroux, and S.H. Liaw Functional roles of the 6-S-cysteinyl, 8alpha-N1-histidyl FAD in glucooligosaccharide oxidase from Acremonium strictum J. Biol. Chem. 283 2008 30990 30996
33. A. Winkler, K. Motz, S. Riedl, M. Puhl, P. Macheroux, and K. Gruber Structural and mechanistic studies reveal the functional role of bicovalent flavinylation in berberine bridge enzyme J. Biol. Chem. 284 2009 19993 20001
34. T.M. Bandeiras, C. Salgueiro, A. Kletzin, C.M. Gomes, and M. Teixeira Acidianus ambivalens type-II NADH dehydrogenase: genetic characterisation and identification of the flavin moiety as FMN FEBS Lett. 531 2002 273 277 (Pubitemid 35341207)
35. Y.S. Li, J.Y. Ho, C.C. Huang, S.Y. Lyu, C.Y. Lee, Y.T. Huang, C.J. Wu, H.C. Chan, C.J. Huang, N.S. Hsu, M.D. Tsai, and T.L. Li A unique flavin mononucleotide-linked primary alcohol oxidase for glycopeptide A40926 maturation J. Am. Chem. Soc. 129 2007 13384 13385
36. A. Willie, D.E. Edmondson, and M.S. Jorns Sarcosine oxidase contains a novel covalently bound FMN Biochemistry 35 1996 5292 5299 (Pubitemid 26129470)
37. M. Hayashi, Y. Nakayama, M. Yasui, M. Maeda, K. Furuishi, and T. Unemoto FMN is covalently attached to a threonine residue in the NqrB and NqrC subunits of Na+-translocating NADH-quinone reductase from Vibrio alginolyticus FEBS Lett. 488 2001 5 8 (Pubitemid 32332796)
38. D.J. Steenkamp, W. McIntire, and W.C. Kenney Structure of the covalently bound coenzyme of trimethylamine dehydrogenase. Evidence for a 6-substituted flavin J. Biol. Chem. 253 1978 2818 2824 (Pubitemid 8326490)
39. C.-C. Yang, L.C. Packman, and N.S. Scrutton The Primary Structure of Hyphomicrobium X Dimethylamine Dehydrogenase Eur. J. Biochem. 232 1995 264 271
40. M. Ilbert, V. Mejean, M.-T. Giudici-Orticoni, J.-P. Samama, and C. Iobbi-Nivol Involvement of a Mate Chaperone (TorD) in the Maturation Pathway of Molybdoenzyme TorA J. Biol. Chem. 278 2003 28787 28792 (Pubitemid 36935788)
41. M.B. McNeil, P.C. Fineran, unpublished data.
42. A.C. Rosenzweig Metallochaperones: Bind and Deliver Chem. Biol. 9 2002 673 677 (Pubitemid 34653061)
43. D.L. Huffman, and T.V. O'Halloran Function, structure, and mechanism of intracellular copper trafficking proteins Annu. Rev. Biochem. 70 2001 677 701 (Pubitemid 32662222)
44. F. Blasco, J.-P. Dos Santos, A. Magalon, C. Frixon, B. Guigliarelli, C.-L. Santini, and G. Giordano NarJ is a specific chaperone required for molybdenum cofactor assembly in nitrate reductase A of Escherichia coli Mol. Microbiol. 28 1998 435 447 (Pubitemid 28218391)
45. F. Hussain, and P. Wittung-Stafshede Impact of cofactor on stability of bacterial (CopZ) and human (Atox1) copper chaperones Biochim. Biophys. Acta (BBA) - Protein Proteomics 1774 2007 1316 1322 (Pubitemid 47484295)
46. M. Blokesch, and A. Böck Maturation of [NiFe]-hydrogenases in Escherichia coli: The HypC Cycle J. Mol. Biol. 324 2002 287 296 (Pubitemid 35379028)
47. H. Schulz, H. Hennecke, and L. Thöny-Meyer Prototype of a Heme Chaperone Essential for Cytochrome c Maturation Science 281 1998 1197 1200 (Pubitemid 28406296)
48. E. Reid, D.J. Eaves, and J.A. Cole The CcmE protein from Escherichia coli is a haem-binding protein FEMS Microbiol. Lett. 166 1998 369 375 (Pubitemid 128384184)
49. H.-X. Hao, O. Khalimonchuk, M. Schraders, N. Dephoure, J.-P. Bayley, H. Kunst, P. Devilee, C.W.R.J. Cremers, J.D. Schiffman, B.G. Bentz, S.P. Gygi, D.R. Winge, H. Kremer, and J. Rutter SDH5, a Gene Required for Flavination of Succinate Dehydrogenase, Is Mutated in Paraganglioma Science 325 2009 1139 1142
50. F. Pierrel, M.L. Bestwick, P.A. Cobine, O. Khalimonchuk, J.A. Cricco, and D.R. Winge Coa1 links the Mss51 post-translational function to Cox1 cofactor insertion in cytochrome c oxidase assembly EMBO J. 26 2007 4335 4346 (Pubitemid 47587663)
51. M. Ilbert, V. Mejean, and C. Iobbi-Nivol Functional and structural analysis of members of the TorD family, a large chaperone family dedicated to molybdoproteins Microbiology 150 2004 935 943 (Pubitemid 38519314)
52. A. Vergnes, K. Gouffi-Belhabich, F. Blasco, G.r. Giordano, and A. Magalon Involvement of the Molybdenum Cofactor Biosynthetic Machinery in the Maturation of the Escherichia coli Nitrate Reductase A J. Biol. Chem. 279 2004 41398 41403 (Pubitemid 39313580)
53. S. Leimkühler, and W. Klipp Role of XDHC in Molybdenum Cofactor Insertion into Xanthine Dehydrogenase of Rhodobacter capsulatus J. Bacteriol. 181 1999 2745 2751 (Pubitemid 29211088)
54. A. Hassan-Abdallah, R.C. Bruckner, G. Zhao, and M.S. Jorns Biosynthesis of Covalently Bound Flavin: Isolation and in Vitro Flavinylation of the Monomeric Sarcosine Oxidase Apoprotein Biochemistry 44 2005 6452 6462 (Pubitemid 40593796)
55. P. Trickey, M.A. Wagner, M.S. Jorns, and F.S. Mathews Monomeric sarcosine oxidase: structure of a covalently flavinylated amine oxidizing enzyme Structure 7 1999 331 345 (Pubitemid 29159692)
56. M.A. Wagner, P. Khanna, and M.S. Jorns Structure of the flavocoenzyme of two homologous amine oxidases: monomeric sarcosine oxidase and N-methyltryptophan oxidase Biochemistry 38 1999 5588 5595
57. N. Tahallah, R.H.H. van den Heuvel, W.A.M. van den Berg, C.S. Maier, W.J.H. van Berkel, and A.J.R. Heck Cofactor-dependent Assembly of the Flavoenzyme Vanillyl-alcohol Oxidase J. Biol. Chem. 277 2002 36425 36432
58. J. Jianfeng, H. Mazon, R.H.H. van den Heuvel, A.J. Heck, D.B. Janssen, and M.W. Fraaije Covalent flavinylation of vanillyl-alcohol oxidase is an autocatalytic process FEBS J. 275 2008 5191 5200
59. R. Brandsch, and V. Bichler Autoflavinylation of apo6-hydroxy-D-nicotine oxidase J. Biol. Chem. 266 1991 19056 19062 (Pubitemid 21908192)
60. J.W.A. Koetter, and G.E. Schulz Crystal Structure of 6-Hydroxy-d-nicotine Oxidase from Arthrobacter nicotinovorans J. Mol. Biol. 352 2005 418 428 (Pubitemid 41207792)
61. J. Kim, J.H. Fuller, V. Kuusk, L. Cunane, Z.-w. Chen, F.S. Mathews, and W.S. McIntire The Cytochrome Subunit Is Necessary for Covalent FAD Attachment to the Flavoprotein Subunit of p-Cresol Methylhydroxylase J. Biol. Chem. 270 1995 31202 31209 (Pubitemid 26018399)
62. L.M. Cunane, Z.W. Chen, W.S. McIntire, and F.S. Mathews p-Cresol methylhydroxylase: alteration of the structure of the flavoprotein subunit upon its binding to the cytochrome subunit Biochemistry 44 2005 2963 2973 (Pubitemid 40293671)
63. O. Dym, and D. Eisenberg Sequence-structure analysis of FAD-containing proteins Protein Sci. 10 2001 1712 1728 (Pubitemid 32848768)
64. C. Walsh Flavin coenzymes: at the crossroads of biological redox chemistry Acc. Chem. Res. 13 1980 148 155
65. E.B. Kearney, and T.P. Singer On the prosthetic group of succinic dehydrogenase Biochim. Biophys. Acta 17 1955 596 597
66. T.P. Singer, E.B. Kearney, and V. Massey Observations on the flavin moiety of succinic dehydrogenase Arch. Biochem. Biophys. 60 1956 255 257
67. T.P. Singer, E.B. Kearney, and N. Zastrow Isolation and properties of succinic dehydrogenase Biochim. Biophys. Acta 17 1955 154 155
68. W.H. Walker, and T.P. Singer Identification of the Covalently Bound Flavin of Succinate Dehydrogenase as 8α-(Histidyl) Flavin Adenine Dinucleotide J. Biol. Chem. 245 1970 4224 4225
69. J. Salach, W.H. Walker, T.P. Singer, A. Ehrenberg, P. Hemmerich, S. Ghisla, and U. Hartmann Studies on succinate dehydrogenase. Site of attachment of the covalently-bound flavin to the peptide chain Eur. J. Biochem. 26 1972 267 278
70. K.M. Robinson, and B.D. Lemire Covalent Attachment of FAD to the Yeast Succinate Dehydrogenase Flavoprotein Requires Import into Mitochondria, Presequence Removal, and Folding J. Biol. Chem. 271 1996 4055 4060 (Pubitemid 26070499)
71. C.J. Alteri, S.N. Smith, and H.L.T. Mobley Fitness of Escherichia coli during Urinary Tract Infection Requires Gluconeogenesis and the TCA Cycle PLoS Pathog. 5 2009 e1000448
72. M. Tchawa Yimga, M.P. Leatham, J.H. Allen, D.C. Laux, T. Conway, and P.S. Cohen Role of Gluconeogenesis and the Tricarboxylic Acid Cycle in the Virulence of Salmonella enterica Serovar Typhimurium in BALB/c Mice Infect. Immun. 74 2006 1130 1140 (Pubitemid 43185551)
73. R. Mercado-Lubo, E.J. Gauger, M.P. Leatham, T. Conway, and P.S. Cohen A Salmonella enterica Serovar Typhimurium Succinate Dehydrogenase/Fumarate Reductase Double Mutant Is Avirulent and Immunogenic in BALB/c Mice Infect. Immun. 76 2008 1128 1134 (Pubitemid 351428073)
74. S.D. Bowden, V.K. Ramachandran, G.M. Knudsen, J.C.D. Hinton, and A.R. Thompson An incomplete TCA cycle increases survival of Salmonella Typhimurium during infection of resting and activated murine macrophages PLoS One 5 2010 e13871
75. L. Hederstedt Succinate dehydrogenase mutants of Bacillus subtilis lacking covalently bound flavin in the flavoprotein subunit Eur. J. Biochem. 132 1983 589 593
76. R. Brandsch, and V. Bichler Covalent cofactor binding to flavoenzymes requires specific effectors Eur. J. Biochem. 182 1989 125 128 (Pubitemid 19145490)
77. K.M. Robinson, and B.D. Lemire A Requirement for Matrix Processing Peptidase but Not for Mitochondrial Chaperonin in the Covalent Attachment of FAD to the Yeast Succinate Dehydrogenase Flavoprotein J. Biol. Chem. 271 1996 4061 4067 (Pubitemid 26074147)
78. T. Gristwood, P. Fineran, L. Everson, N. Williamson, and G. Salmond The PhoBR two-component system regulates antibiotic biosynthesis in Serratia in response to phosphate BMC Microbiol. 9 2009 112
79. N.R. Williamson, P.C. Fineran, W. Ogawa, L.R. Woodley, and G.P. Salmond Integrated regulation involving quorum sensing, a two-component system, a GGDEF/EAL domain protein and a post-transcriptional regulator controls swarming and RhlA-dependent surfactant biosynthesis in Serratia Environ. Microbiol. 10 2008 1202 1217 (Pubitemid 351499238)
80. P.C. Fineran, H. Slater, L. Everson, K. Hughes, and G.P. Salmond Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production Mol. Microbiol. 56 2005 1495 1517 (Pubitemid 40780646)
81. H. Slater, M. Crow, L. Everson, and G.P. Salmond Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways Mol. Microbiol. 47 2003 303 320 (Pubitemid 36121023)
82. P.C. Fineran, N.R. Williamson, K.S. Lilley, and G.P. Salmond Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX J. Bacteriol. 189 2007 7653 7662 (Pubitemid 350035075)
83. T. Gristwood, P.C. Fineran, L. Everson, and G.P. Salmond PigZ, a TetR/AcrR family repressor, modulates secondary metabolism via the expression of a putative four-component resistance-nodulation-cell-division efflux pump, ZrpADBC, in Serratia sp. ATCC 39006 Mol. Microbiol. 69 2008 418 435 (Pubitemid 351988015)
84. P.C. Fineran, L. Everson, H. Slater, and G.P. Salmond A GntR family transcriptional regulator (PigT) controls gluconate-mediated repression and defines a new, independent pathway for regulation of the tripyrrole antibiotic, prodigiosin, in Serratia Microbiology 151 2005 3833 3845 (Pubitemid 41829965)
85. T. Gristwood, M.B. McNeil, J.S. Clulow, G.P.C. Salmond, and P.C. Fineran PigS and PigP Regulate Prodigiosin Biosynthesis in Serratia via Differential Control of Divergent Operons, Which Include Predicted Transporters of Sulfur-Containing Molecules J. Bacteriol. 193 2011 1076 1085
86. J.P. Ramsay, N.R. Williamson, D.R. Spring, and G.P.C. Salmond A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium Proc. Natl. Acad. Sci. U. S. A. 108 2011 14932 14937
87. M.B. McNeil, J.S. Clulow, N.M. Wilf, G.P.C. Salmond, and P.C. Fineran SdhE Is a Conserved Protein Required for Flavinylation of Succinate Dehydrogenase in Bacteria J. Biol. Chem. 287 2012 18418 18428
88. M.Y. Galperin, and E.V. Koonin 'Conserved hypothetical' proteins: prioritization of targets for experimental study Nucleic Acids Res. 32 2004 5452 5463 (Pubitemid 39545662)
89. M.Y. Galperin, and E.V. Koonin From complete genome sequence to 'complete' understanding? Trends Biotechnol. 28 2010 398
90. L.J. Jensen, M. Kuhn, M. Stark, S. Chaffron, C. Creevey, J. Muller, T. Doerks, P. Julien, A. Roth, M. Simonovic, P. Bork, and C. von Mering STRING 8: a global view on proteins and their functional interactions in 630 organisms Nucleic Acids Res. 37 2009 D412 D416
91. I.T. Creaghan, and J.R. Guest Succinate Dehydrogenase-dependent Nutritional Requirement for Succinate in Mutants of Escherichia coli K12 J. Gen. Microbiol. 107 1978 1 13 (Pubitemid 8379222)
92. J.R. Guest Partial Replacement of Succinate Dehydrogenase Function by Phage- and Plasmid-specified Fumarate Reductase in Escherichia coli J. Gen. Microbiol. 122 1981 171 179 (Pubitemid 11144065)
93. M.E. Spencer, and J.R. Guest Proteins of the Inner Membrane of Escherichia coli: Identification of Succinate Dehydrogenase by Polyacrylamide Gel Electrophoresis with sdh Amber Mutants J. Bacteriol. 117 1974 947 953
94. K.M. Robinson, A. von Kieckebusch-Guck, and B.D. Lemire Isolation and characterization of a Saccharomyces cerevisiae mutant disrupted for the succinate dehydrogenase flavoprotein subunit J. Biol. Chem. 266 1991 21347 21350 (Pubitemid 121000187)
95. V. Bafunno, T.A. Giancaspero, C. Brizio, D. Bufano, S. Passarella, E. Boles, and M. Barile Riboflavin uptake and FAD synthesis in Saccharomyces cerevisiae Mitochondria: Involvement of the Flx1p carrier in FAD export J. Biol. Chem. 279 2004 95 102 (Pubitemid 38044803)
96. J. Koziol Fluorometric analyses of riboflavin and its coenzymes D.B. McCormick, L.D. Wright, Methods in Enzymology 1971 Academic Press 253 285
97. P. Macheroux, B. Kappes, and S.E. Ealick Flavogenomics-a genomic and structural view of flavin-dependent proteins FEBS J. 278 2011 2625 2634
98. K. Lim, V. Doseeva, E. Demirkan, S. Pullalarevu, W. Krajewski, A. Galkin, A. Howard, and O. Herzberg Crystal structure of the YgfY from Escherichia coli, a protein that may be involved in transcriptional regulation Proteins: Structure, Function, and Bioinformatics 58 2005 759 763 (Pubitemid 40176049)
99. G. Liu, D.K. Sukumaran, D. Xu, Y. Chiang, T. Acton, S. Goldsmith-Fischman, B. Hoing, G.T. Montelione, and T. Szyperski NMR structure of the hypothetical protein NMA1147 from Neisseria meningitidis reveals a distinct 5-helix bundle Proteins 55 2004 756 758 (Pubitemid 38620097)
100. R.K. Wierenga, P. Terpstra, and W.G.J. Hol Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint J. Mol. Biol. 187 1986 101 107
101. P.J. Goldman, K.S. Ryan, M.J. Hamill, A.R. Howard-Jones, C.T. Walsh, S.J. Elliott, and C.L. Drennan An Unusual Role for a Mobile Flavin in StaC-like Indolocarbazole Biosynthetic Enzymes Chem. Biol. 19 2012 855 865
102. K.S. Ryan, A.R. Howard-Jones, M.J. Hamill, S.J. Elliott, C.T. Walsh, and C.L. Drennan Crystallographic trapping in the rebeccamycin biosynthetic enzyme RebC Proc. Natl. Acad. Sci. 104 2007 15311 15316 (Pubitemid 47502914)
103. T. Uchida, J.M. Stevens, O. Daltrop, E.M. Harvat, L. Hong, S.J. Ferguson, and T. Kitagawa The interaction of covalently bound heme with the cytochrome c maturation protein CcmE J. Biol. Chem. 279 2004 51981 51988 (Pubitemid 39656568)
104. O. Daltrop, J.M. Stevens, C.W. Higham, and S.J. Ferguson The CcmE protein of the c-type cytochrome biogenesis system: unusual in vitro heme incorporation into apo-CcmE and transfer from holo-CcmE to apocytochrome Proc. Natl. Acad. Sci. U. S. A. 99 2002 9703 9708 (Pubitemid 34831111)
105. D.A. Mavridou, J.M. Stevens, L. Monkemeyer, O. Daltrop, K. di Gleria, B.M. Kessler, S.J. Ferguson, and J.W. Allen A pivotal heme-transfer reaction intermediate in cytochrome c biogenesis J. Biol. Chem. 287 2012 2342 2352
106. A. Sickmann, J. Reinders, Y. Wagner, C. Joppich, R. Zahedi, H.E. Meyer, B. Schonfisch, I. Perschil, A. Chacinska, B. Guiard, P. Rehling, N. Pfanner, and C. Meisinger The proteome of Saccharomyces cerevisiae mitochondria Proc. Natl. Acad. Sci. U. S. A. 100 2003 13207 13212 (Pubitemid 37444720)
107. R.S. Gupta The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes FEMS Microbiol. Rev. 24 2000 367 402
108. S.J. Park, G. Chao, and R.P. Gunsalus Aerobic regulation of the sucABCD genes of Escherichia coli, which encode alpha-ketoglutarate dehydrogenase and succinyl coenzyme A synthetase: roles of ArcA, Fnr, and the upstream sdhCDAB promoter J. Bacteriol. 179 1997 4138 4142 (Pubitemid 27291041)
109. S.-J. Park, C.-P. Tseng, and R.P. Gunsalus Regulation of succinate dehydrogenase (sdhCDAB) operon expression in Escherichia coli in response to carbon supply and anaerobiosis: role of ArcA and Fnr Mol. Microbiol. 15 1995 473 482
110. T.-W. Nam, Y.-H. Park, H.-J. Jeong, S. Ryu, and Y.-J. Seok Glucose repression of the Escherichia coli sdhCDAB operon, revisited: regulation by the CRP·cAMP complex Nucleic Acids Res. 33 2005 6712 6722 (Pubitemid 41830479)
111. J.S. Park, M.T. Marr, and J.W. Roberts E. coli Transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation Cell 109 2002 757 767 (Pubitemid 34722270)
112. H. Masuda, Q. Tan, N. Awano, Y. Yamaguchi, and M. Inouye A novel membrane bound toxin for cell division, CptA (YgfX), inhibits polymerization of cytoskeleton proteins, FtsZ and MreB in Escherichia coli FEMS Microbiol. Lett. 328 2012 174 181
113. N.J. Robinson, and D.R. Winge Copper metallochaperones Annu. Rev. Biochem. 79 2010 537 562
114. M. Blaut, K. Whittaker, A. Valdovinos, B.A. Ackrell, R.P. Gunsalus, and G. Cecchini Fumarate reductase mutants of Escherichia coli that lack covalently bound flavin J. Biol. Chem. 264 1989 13599 13604 (Pubitemid 19198441)
115. C. Luna-Chavez, T.M. Iverson, D.C. Rees, and G. Cecchini Overexpression, Purification, and Crystallization of the Membrane-Bound Fumarate Reductase from Escherichia coli Protein Expr. Purif. 19 2000 188 196 (Pubitemid 30387910)
116. H. Ashkenazy, E. Erez, E. Martz, T. Pupko, and N. Ben-Tal ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids Nucleic Acids Res. 38 2010 W529 W533
117. C. Singleton, S. Hearnshaw, L. Zhou, N.E. Le Brun, and A.M. Hemmings Mechanistic insights into Cu(I) cluster transfer between the chaperone CopZ and its cognate Cu(I)-transporting P-type ATPase, CopA Biochem. J. 424 2009 347 356
118. M. Gonzalez-Guerrero, and J.M. Arguello Mechanism of Cu+-transporting ATPases: soluble Cu + chaperones directly transfer Cu + to transmembrane transport sites Proc. Natl. Acad. Sci. U. S. A. 105 2008 5992 5997 (Pubitemid 351758387)
119. M.A. Kihlken, A.P. Leech, and N.E. Le Brun Copper-mediated dimerization of CopZ, a predicted copper chaperone from Bacillus subtilis Biochem. J. 368 2002 729 739 (Pubitemid 36042674)
120. L. Zhou, C. Singleton, and N.E. Le Brun High Cu(I) and low proton affinities of the CXXC motif of Bacillus subtilis CopZ Biochem. J. 413 2008 459 465
121. P. Cobine, W.A. Wickramasinghe, M.D. Harrison, T. Weber, M. Solioz, and C.T. Dameron The Enterococcus hirae copper chaperone CopZ delivers copper(I) to the CopY repressor FEBS Lett. 445 1999 27 30 (Pubitemid 29101529)
122. D. Magnani, and M. Solioz Copper Chaperone Cycling and Degradation in the Regulation of the cop Operon of Enterococcus hirae Biometals 18 2005 407 412 (Pubitemid 41298025)
123. Z.H. Lu, and M. Solioz Copper-induced Proteolysis of the CopZ Copper Chaperone of Enterococcus hirae J. Biol. Chem. 276 2001 47822 47827
124. T. Maeda, V. Sanchez-Torres, and T. Wood Escherichia coli; hydrogenase 3 is a reversible enzyme possessing hydrogen uptake and synthesis activities Appl. Microbiol. Biotechnol. 76 2007 1035 1042 (Pubitemid 47415618)
125. S. Watanabe, R. Matsumi, T. Arai, H. Atomi, T. Imanaka, and K. Miki Crystal structures of [NiFe] hydrogenase maturation proteins HypC, HypD, and HypE: insights into cyanation reaction by thiol redox signaling Mol. Cell 27 2007 29 40 (Pubitemid 46991387)
126. T. Palmer, C.-L. Santini, C. Iobbi-Nivol, D.J. Eaves, D.H. Boxer, and G. Giordano Involvement of the narJ and mob gene products in distinct steps in the biosynthesis of the molybdoenzyme nitrate reductase in Escherichia coli Mol. Microbiol. 20 1996 875
127. M. Neumann, W. Stocklein, and S. Leimkuhler Transfer of the molybdenum cofactor synthesized by Rhodobacter capsulatus MoeA to XdhC and MobA J. Biol. Chem. 282 2007 28493 28500 (Pubitemid 47606026)
128. M. Neumann, W. Stocklein, A. Walburger, A. Magalon, and S. Leimkuhler Identification of a Rhodobacter capsulatus L-cysteine desulfurase that sulfurates the molybdenum cofactor when bound to XdhC and before its insertion into xanthine dehydrogenase Biochemistry 46 2007 9586 9595 (Pubitemid 47291965)
129. M. Neumann, M. Schulte, N. Junemann, W. Stocklein, and S. Leimkuhler Rhodobacter capsulatus XdhC is involved in molybdenum cofactor binding and insertion into xanthine dehydrogenase J. Biol. Chem. 281 2006 15701 15708 (Pubitemid 43848457)