Molybdenum enzymes, their maturation and molybdenum cofactor biosynthesis in Escherichia coli

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1827, Issue 8-9, 2013, Pages 1086-1101

  Iobbi Nivol, Chantal ^a   Leimkühler, Silke ^b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Bis MGD; Dithiolene; Moco; Molybdenum; Molybdenum cofactor; Molybdopterin

Indexed keywords

BACTERIAL ENZYME; CHAPERONE; CYTIDINE PHOSPHATE; DIMETHYL SULFOXIDE REDUCTASE; DINUCLEOTIDE; GUANOSINE PHOSPHATE; MOLYBDENUM; MOLYBDENUM COFACTOR; MOLYBDOPTERIN; SULFITE OXIDASE; UNCLASSIFIED DRUG; XANTHINE OXIDASE; ENZYME; METALLOPROTEIN; PTERIDINE DERIVATIVE;

BIOGENESIS; BIOSYNTHESIS; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; BIS-MGD; COENZYME; DITHIOLENE; METABOLISM; MOCO;

ESCHERICHIA COLI;

BIS-MGD; DITHIOLENE; MOCO; MOLYBDENUM; MOLYBDENUM COFACTOR; MOLYBDOPTERIN;

COENZYMES; ENZYMES; ESCHERICHIA COLI; METALLOPROTEINS; MOLYBDENUM; PTERIDINES;

EID: 84884343748     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.11.007     Document Type: Review

References (160)

1. H. Bortels, Molybdenum as a catalyst in the bioogical fixation of nitrogen, Arch. Mikrobiol. 1 (1930) 333-342.
2. M.P. Coughlan, The role of molybdenum in human biology, J. Inherit. Metab. Dis. 6 (Suppl. 1) (1983) 70-77. (Pubitemid 14226356)
3. D.A. Richert, W.W. Westerfeld, Isolation and identification of the xanthine oxidase factor as molybdenum, J. Biol. Chem. 203 (1953) 915-923.
4. E.C. De Renzo, E. Kaleita, P.G. Heytler, J.J. Oleson, B.L. Hutchings, J.H. Williams, Identification of the xanthine oxidase factor as molybdenum, Arch. Biochem. Biophys. 45 (1953) 247-253.
5. C.Andreini, I. Bertini, G. Cavallaro, G.L. Holliday, J.M.Thornton,Metal ions inbiological catalysis: from enzyme databases to general principles, JBIC 13 (2008) 1205-1218.
6. R. Hille, The mononuclear molybdenum enzymes, Chem. Rev. 96 (1996) 2757-2816. (Pubitemid 126641117)
7. R. Hille, Molybdenum and tungsten in biology, Trends Biochem. Sci. 27 (2002) 360-367. (Pubitemid 34756519)
8. Y. Zhang, S. Rump, V.N. Gladyshev, Comparative genomics and evolution of molybdenum utilization, Coord. Chem. Rev. 255 (2011) 1206-1217.
9. G. Schwarz, R.R. Mendel, M.W. Ribbe, Molybdenum cofactors, enzymes and pathways, Nature 460 (2009) 839-847.
10. K.V. Rajagopalan, J.L. Johnson, The pterin molybdenum cofactors, J. Biol. Chem. 267 (1992) 10199-10202.
11. H. Dobbek, L. Gremer, R. Kiefersauer, R. Huber, O. Meyer, Catalysis at a dinuclear CuSMo(==O)OH cluster in a CO dehydrogenase resolved at 1.1-A resolution, Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 15971-15976. (Pubitemid 35462733)
12. W.T. Self, A.M. Grunden, A. Hasona, K.T. Shanmugam, Molybdate transport, Res. Microbiol. 152 (2001) 311-321. (Pubitemid 32436489)
13. E. Aguilar-Barajas, C. Diaz-Perez, M.I. Ramirez-Diaz, H. Riveros-Rosas, C. Cervantes, Bacterial transport of sulfate, molybdate, and related oxyanions, Biometals 24 (2011) 687-707.
14. J.A. Maupin-Furlow, J.K. Rosentel, J.H. Lee, U. Deppenmeier, R.P. Gunsalus, K.T. Shanmugam, Genetic analysis of the modABCD (molybdate transport) operon of Escherichia coli, J. Bacteriol. 177 (1995) 4851-4856.
15. J.K. Rosentel, F. Healy, J.A. Maupin-Furlow, J.H. Lee, K.T. Shanmugam, Molybdate and regulation of mod (molybdate transport), fdhF, and hyc (formate hydrogenlyase) operons in Escherichia coli, J. Bacteriol. 177 (1995) 4857-4864.
16. C.F. Higgins, ABC transporters: from microorganisms to man, Annu. Rev. Cell Biol. 8 (1992) 67-113. (Pubitemid 23000992)
17. A.L. Davidson, J. Chen, ATP-binding cassette transporters in bacteria, Annu. Rev. Biochem. 73 (2004) 241-268. (Pubitemid 39050369)
18. W.R. Hagen, Cellular uptake of molybdenum and tungsten, Coord. Chem. Rev. 255 (2011) 1117-1128.
19. J. Imperial, M. Hadi, N.K. Amy, Molybdate binding by ModA, the periplasmic component of the Escherichia coli mod molybdate transport system, Biochim. Biophys. Acta 1370 (1998) 337-346. (Pubitemid 28183986)
20. Y. Hu, S. Rech, R.P. Gunsalus, D.C. Rees, Crystal structure of the molybdate binding protein ModA, Nat. Struct. Biol. 4 (1997) 703-707.
21. K. Hollenstein, D.C. Frei, K.P. Locher, Structure of an ABC transporter in complex with its binding protein, Nature 446 (2007) 213-216. (Pubitemid 46398672)
22. P.M. McNicholas, S.A. Rech, R.P. Gunsalus, Characterization of the ModE DNA-binding sites in the control regions of modABCD and moaABCDE of Escherichia coli, Mol. Microbiol. 23 (1997) 515-524. (Pubitemid 27051381)
23. P.M. McNicholas, M.M. Mazzotta, S.A. Rech, R.P. Gunsalus, Functional dissection of the molybdate-responsive transcription regulator, ModE, from Escherichia coli, J. Bacteriol. 180 (1998) 4638-4643. (Pubitemid 28405592)
24. W.T. Self, A.M. Grunden, A. Hasona, K.T. Shanmugam, Transcriptional regulation of molybdoenzyme synthesis in Escherichia coli in response to molybdenum: ModE-molybdate, a repressor of the modABCD (molybdate transport) operon is a secondary transcriptional activator for the hyc and nar operons, Microbiology 145 (Pt 1) (1999) 41-55. (Pubitemid 29043576)
25. L.A. Anderson, E. McNairn, T. Lubke, R.N. Pau, D.H. Boxer, ModE-dependent molybdate regulation of the molybdenum cofactor operon moa in Escherichia coli, J. Bacteriol. 182 (2000) 7035-7043. (Pubitemid 32259608)
26. H. Tao, A. Hasona, P.M. Do, L.O. Ingram, K.T. Shanmugam, Global gene expression analysis revealed an unsuspected deo operon under the control of molybdate sensor, ModE protein, in Escherichia coli, Arch. Microbiol. 184 (2005) 225-233. (Pubitemid 41627638)
27. A.W. Schüttelkopf, D.H. Boxer, W.N. Hunter, Crystal structure of activated ModE reveals conformational changes involving both oxyanion and DNA-binding domains, J. Mol. Biol. 326 (2003) 761-767. (Pubitemid 36279317)
28. E.E. Regulski, R.H. Moy, Z. Weinberg, J.E. Barrick, Z. Yao, W.L. Ruzzo, R.R. Breaker, A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism, Mol. Microbiol. 68 (2008) 918-932. (Pubitemid 351581064)
29. G. Börner, M. Karrasch, R.K. Thauer, Molybdopterin adenine dinucleotide and molybdopterin hypoxanthine dinucleotide in formylmethanofuran dehydrogenase from Methanobacterium thermoautotrophicum (Marburg), FEBS Lett. 290 (1991) 31-34.
30. M.K. Chan, S. Mukund, A. Kletzin, M.W.W. Adams, D.C. Rees, Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase, Science 267 (1995) 1463-1469.
31. C. Kisker, H. Schindelin, D.C. Rees, Molybdenum-cofactor-containing enzymes: structure and mechanism, Annu. Rev. Biochem. 66 (1997) 233-267. (Pubitemid 27274657)
32. M.J. Ramão, M. Archer, I. Moura, J.J.G. Moura, J. LeGall, R. Engh, M. Schneider, P. Hof, R. Huber, Crystal structure of the xanthine oxidase-related aldehyde oxido-reductase from D. gigas, Science 270 (1995) 1170-1176.
33. H. Schindelin, C. Kisker, J. Hilton, K.V. Rajagopalan, D.C. Rees, Crystal structure of DMSO reductase: redox-linked changes in molybdopterin coordination, Science 272 (1996) 1615-1621. (Pubitemid 26200018)
34. A. Magalon, J.G. Fedor, A. Walburger, J.A. Weiner, Molybdenum enzymes in bacteria and their maturation, Coord. Chem. Rev. 255 (2011) 1159-1178.
35. S. Gutteridge, S.J. Tanner, R.C. Bray, Comparison of the molybdenum centres of native and desulpho xanthine oxidase, The nature of the cyanide-labile sulphur atom and the nature of the proton-accepting group, Biochem. J. 175 (1978) 887-897.
36. R.C. Wahl, K.V. Rajagopalan, Evidence for the inorganic nature of the cyanolyzable sulfur of molybdenum hydroxylases, J. Biol. Chem. 257 (1982) 1354-1359.
37. M. Neumann, S. Leimkühler, The role of system-specific molecular chaperones in the maturation of molybdoenzymes in bacteria, Biochemistry research international 2011 (2011) 850924.
38. M. Neumann, G.Mittelstadt, C. Iobbi-Nivol,M. Saggu, F. Lendzian, P. Hildebrandt, S. Leimkühler, A periplasmic aldehyde oxidoreductase represents the first molybdopterin cytosine dinucleotide cofactor containing molybdo-flavoenzyme from Escherichia coli, FEBS J. 276 (2009) 2762-2774.
39. S. Leimkühler, M. Kern, P.S. Solomon, A.G. McEwan, G. Schwarz, R.R. Mendel, W. Klipp, Xanthine dehydrogenase from the phototrophic purple bacterium Rhodobacter capsulatus is more similar to its eukaryotic counterparts than to prokaryotic molybdenum enzymes, Mol. Microbiol. 27 (1998) 853-869. (Pubitemid 28081993)
40. A.M. Sevcenco, M.W. Pinkse, H.T. Wolterbeek, P.D. Verhaert, W.R. Hagen, P.L. Hagedoorn, Exploring the microbialmetalloproteome usingMIRAGE,Metallomics: Integrated Biometal Science 3 (2011) 1324-1330.
41. S.J. Brokx, R.A. Rothery, G. Zhang, D.P. Ng, J.H. Weiner, Characterization of an Escherichia coli sulfite oxidase homologue reveals the role of a conserved active site cysteine in assembly and function, Biochemistry 44 (2005) 10339-10348. (Pubitemid 41076829)
42. L. Loschi, S.J. Brokx, T.L. Hills, G. Zhang, M.G. Bertero, A.L. Lovering, J.H. Weiner, N.C. Strynadka, Structural and biochemical identification of a novel bacterial oxidoreductase, J. Biol. Chem. 279 (2004) 50391-50400. (Pubitemid 39577857)
43. K.G. Havelius, S. Reschke, S. Horn, A. Doring, D. Niks, R. Hille, C. Schulzke, S. Leimkühler, M. Haumann, Structure of the molybdenumsite in YedY, a sulfite oxidase homologue from Escherichia coli, Inorg. Chem. 50 (2011) 741-748.
44. H.C. Raaijmakers, M.J. Romao, Formate-reduced E. coli formate dehydrogenase H: the reinterpretation of the crystal structure suggests a new reaction mechanism, JBIC 11 (2006) 849-854. (Pubitemid 44337586)
45. B.C. Berks, A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22 (1996) 393-404. (Pubitemid 26373825)
46. B.C. Berks, T. Palmer, F. Sargent, Protein targeting by the bacterial twin-arginine translocation (Tat) pathway, Curr. Opin. Microbiol. 8 (2005) 174-181. (Pubitemid 40417959)
47. J. Cole, Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol. Lett. 136 (1996) 1-11. (Pubitemid 26063443)
48. V. Stewart, Nitrate respiration in relation to facultative metabolism in enterobacteria, Microbiol. Rev. 52 (1988) 190-232.
49. T.H. Brondijk, A. Nilavongse, N. Filenko, D.J. Richardson, J.A. Cole, NapGH components of the periplasmic nitrate reductase of Escherichia coli K-12: location, topology and physiological roles in quinol oxidation and redox balancing, Biochem. J. 379 (2004) 47-55. (Pubitemid 38491358)
50. L. Chang, L.I. Wei, J.P. Audia, R.A. Morton, H.E. Schellhorn, Expression of the Escherichia coli NRZ nitrate reductase is highly growth phase dependent and is controlled by RpoS, the alternative vegetative sigma factor, Mol. Microbiol. 34 (1999) 756-766.
51. P.T. Bilous, J.H. Weiner, Molecular cloning and expression of the Escherichia coli dimethyl sulfoxide reductase operon, J. Bacteriol. 170 (1988) 1511-1518.
52. V. Mejean, C. Iobbi-Nivol, M. Lepelletier, G. Giordano, M. Chippaux, M.C. Pascal, TMAO anaerobic respiration in Escherichia coli: involvement of the tor operon, Mol. Microbiol. 11 (1994) 1169-1179. (Pubitemid 24201632)
53. M. Jormakka, B. Byrne, S. Iwata, Formate dehydrogenase-a versatile enzyme in changing environments, Curr. Opin. Struct. Biol. 13 (2003) 418-423. (Pubitemid 37011446)
54. M. Jormakka, S. Tornroth, B. Byrne, S. Iwata, Molecular basis of proton motive force generation: structure of formate dehydrogenase-N, Science 295 (2002) 1863-1868. (Pubitemid 34214117)
55. H. Abaibou, J. Pommier, S. Benoit, G. Giordano, M.A. Mandrand-Berthelot, Expression and characterization of the Escherichia coli fdo locus and a possible physiological role for aerobic formate dehydrogenase, J. Bacteriol. 177 (1995) 7141-7149.
56. S. Benoit, H. Abaibou, M.A. Mandrand-Berthelot, Topological analysis of the aerobic membrane-bound formate dehydrogenase of Escherichia coli, J. Bacteriol. 180 (1998) 6625-6634. (Pubitemid 29006077)
57. J.C. Boyington, V.N. Gladyshev, S.V. Khangulov, T.C. Stadtman, P.D. Sun, Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster, Science 275 (1997) 1305-1308. (Pubitemid 27114158)
58. B. Ezraty, J. Bos, F. Barras, L. Aussel,Methionine sulfoxide reduction and assimilation in Escherichia coli: new role for the biotin sulfoxide reductase BisC, J. Bacteriol. 187 (2005) 231-237. (Pubitemid 40024199)
59. D. Guymer, J. Maillard, F. Sargent, A genetic analysis of in vivo selenate reduction by Salmonella enterica serovar Typhimurium LT2 and Escherichia coli K12, Arch. Microbiol. 191 (2009) 519-528.
60. C.M. Stevens, T.M.Winstone, R.J. Turner, M. Paetzel, Structural analysis of a monomeric form of the twin-arginine leader peptide binding chaperone Escherichia coli DmsD, J. Mol. Biol. 389 (2009) 124-133.
61. N. Masuda, G.M. Church, Regulatory network of acid resistance genes in Escherichia coli, Mol. Microbiol. 48 (2003) 699-712. (Pubitemid 36819056)
62. J.D. Partridge, D.F. Browning, M. Xu, L.J. Newnham, C. Scott, R.E. Roberts, R.K. Poole, J. Green, Characterization of the Escherichia coli K-12 ydhYVWXUT operon: regulation by FNR, NarL and NarP, Microbiology 154 (2008) 608-618. (Pubitemid 351292314)
63. S.G. Kozmin, P. Leroy, Y.I. Pavlov, R.M. Schaaper, YcbX and yiiM, two novel determinants for resistance of Escherichia coli to N-hydroxylated base analogues, Mol. Microbiol. 68 (2008) 51-65. (Pubitemid 351363775)
64. V. Anantharaman, L. Aravind, MOSC domains: ancient, predicted sulfurcarrier domains, present in diverse metal-sulfur cluster biosynthesis proteins including Molybdenum cofactor sulfurases, FEMS Microbiol. Lett. 207 (2002) 55-61. (Pubitemid 34214806)
65. K.V. Rajagopalan, Biosynthesis of the molybdenum cofactor, in: F.C. Neidhardt (Ed.), Escherichia coli and Salmonella, ASM Press, Washington, DC, Cellular and Molecular Biology, 1996, pp. 674-679.
66. K.T. Shanmugam, V. Stewart, R.P. Gunsalus, D.H. Boxer, J.A. Cole, M. Chippaux, J.A. DeMoss, G. Giordano, E.C.C. Lin, K.V. Rajagopalan, Proposed nomenclature for the genes involved in molybdenum metabolism in Escherichia coli and Salmonella typhimurium, Mol. Microbiol. 6 (1992) 3452-3454.
67. M.M.Wuebbens, K.V. Rajagopalan, Investigation of the early steps ofmolybdopterin biosynthesis in Escherichia coli through the use of in vivo labeling studies, J. Biol. Chem. 270 (1995) 1082-1087.
68. C. Rieder, W. Eisenreich, J. O'Brien, G. Richter, E. Götze, P. Boyle, S. Blanchard, A. Bacher, H. Simon, Rearrangement reactions in the biosynthesis of molybdopterin. An NMR study with multiply 13C/15N labelled precursors, Eur. J. Biochem. 255 (1998) 24-36. (Pubitemid 28316831)
69. P. Hänzelmann, H. Schindelin, Crystal structure of the S-adenosylmethioninedependent enzymeMoaA and its implications formolybdenumcofactor deficiency in humans, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 12870-12875. (Pubitemid 39167550)
70. P. Hänzelmann, H. Schindelin, Binding of 5'-GTP to the C-terminal FeS cluster of the radical S-adenosylmethionine enzyme MoaA provides insights into its mechanism, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6829-6834.
71. N.S. Lees, P. Hänzelmann, H.L. Hernandez, S. Subramanian, H. Schindelin, M.K. Johnson, B.M. Hoffman, ENDOR spectroscopy shows that guanine N1 binds to 4Fe-4S cluster II of the S-adenosylmethionine-dependent enzyme MoaA: mechanistic implications, J. Am. Chem. Soc. 131 (2009) 9184-9185.
72. H.J. Sofia, G. Chen, B.G. Hetzler, J.F. Reyes-Spindola, N.E. Miller, Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods, Nucleic Acids Res. 29 (2001) 1097-1106. (Pubitemid 32186195)
73. P. Hänzelmann, H.L. Hernandez, C. Menzel, R. Garcia-Serres, B.H. Huynh, M.K. Johnson, R.R. Mendel, H. Schindelin, Characterization of MOCS1A, an oxygensensitive iron-sulfur protein involved in human molybdenum cofactor biosynthesis, J. Biol. Chem. 279 (2004) 34721-34732. (Pubitemid 39318103)
74. D.M. Pitterle, K.V. Rajagopalan, Two proteins encoded at the chlA locus constitute the converting factor of Escherichia coli chlA1, J. Bacteriol. 171 (1989) 3373-3378. (Pubitemid 19145694)
75. D.M. Pitterle, J.L. Johnson, K.V. Rajagopalan, In vitro synthesis ofmolybdopterin from precursor Z using purified converting factor. Role of protein-bound sulfur in formation of the dithiolene, J. Biol. Chem. 268 (1993) 13506-13509. (Pubitemid 23307778)
76. D.M. Pitterle, K.V. Rajagopalan, The biosynthesis ofmolybdopterin in Escherichia coli. Purification and characterization of the converting factor, J. Biol. Chem. 268 (1993) 13499-13505. (Pubitemid 23307777)
77. G. Gutzke, B. Fischer, R.R.Mendel, G. Schwarz, Thiocarboxylation ofmolybdopterin synthase provides evidence for the mechanism of dithiolene formation in metalbinding pterins, J. Biol. Chem. 276 (2001) 36268-36274.
78. J.N. Daniels, M.M. Wuebbens, K.V. Rajagopalan, H. Schindelin, Crystal structure of a molybdopterin synthase-precursor Z complex: insight into its sulfur transfer mechanism and its role in molybdenum cofactor deficiency, Biochemistry 47 (2008) 615-626. (Pubitemid 351195433)
79. M.M. Wuebbens, K.V. Rajagopalan, Mechanistic and mutational studies of Escherichia coli molybdopterin synthase clarify the final step of molybdopterin biosynthesis, J. Biol. Chem. 278 (2003) 14523-14532. (Pubitemid 36800006)
80. S. Leimkühler, M.M. Wuebbens, K.V. Rajagopalan, Characterization of Escherichia coli MoeB and its involvement in the activation of MPT synthase for the biosynthesis of the molybdenum cofactor, J. Biol. Chem. 276 (2001) 34695-34701.
81. S. Leimkühler, K.V. Rajagopalan, An Escherichia coli NifS-like sulfurtransferase is required for the transfer of cysteine sulfur in the in vitro synthesis ofmolybdopterin from precursor Z, J. Biol. Chem. 276 (2001) 22024-22031.
82. W. Zhang, A. Urban, H. Mihara, S. Leimkühler, T. Kurihara, N. Esaki, IscS functions as a primary sulfur-donating enzyme by interacting specifically with MoeB and MoaD in the biosynthesis of molybdopterin in Escherichia coli, J. Biol. Chem. 285 (2010) 2302-2308.
83. A. Marquet, Enzymology of carbon-sulfur bond formation, Curr. Opin. Chem. Biol. 5 (2001) 541-549. (Pubitemid 32907605)
84. R. Shi, A. Proteau, M. Villarroya, I. Moukadiri, L. Zhang, J.F. Trempe, A. Matte, M.E. Armengod, M. Cygler, Structural basis for Fe-S cluster assembly and tRNA thiolation mediated by IscS protein-protein interactions, PLoS Biol. 8 (2010) e1000354.
85. J.U. Dahl, A. Urban, A. Bolte, P. Sriyabhaya, J.L. Donahue, M. Nimtz, T.J. Larson, S. Leimkühler, The identification of a novel protein involved in molybdenum cofactor biosynthesis in Escherichia coli, J. Biol. Chem. 286 (2011) 35801-35812.
86. A. Matthies, K.V. Rajagopalan, R.R. Mendel, S. Leimkühler, Evidence for the physiological role of a rhodanese-like protein for the biosynthesis of the molybdenum cofactor in humans, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 5946-5951. (Pubitemid 38520508)
87. J. Schmitz, M.M. Wuebbens, K.V. Rajagopalan, S. Leimkühler, Role of the C-terminal Gly-Gly motif of Escherichia coli MoaD, a molybdenum cofactor biosynthesis protein with a ubiquitin fold, Biochemistry 46 (2007) 909-916. (Pubitemid 46133607)
88. M.E. Johnson, K.V. Rajagopalan, Involvement of chlA, E, M, and N loci in Escherichia coli molybdopterin biosynthesis, J. Bacteriol. 169 (1987) 117-125. (Pubitemid 17228697)
89. M.S. Joshi, J.L. Johnson, K.V. Rajagopalan, Molybdenum cofactor biosynthesis in Escherichia coli mod and mog mutants, J. Bacteriol. 178 (1996) 4310-4312. (Pubitemid 26240917)
90. M.T. Liu, M.M. Wuebbens, K.V. Rajagopalan, H. Schindelin, Crystal structure of the gephyrin-related molybdenum cofactor biosynthesis protein MogA from Escherichia coli, J. Biol. Chem. 275 (2000) 1814-1822. (Pubitemid 30060804)
91. S. Xiang, J. Nichols, K.V. Rajagopalan, H. Schindelin, The crystal structure of Escherichia coli MoeA and its relationship to the multifunctional protein gephyrin, Structure 9 (2001) 299-310. (Pubitemid 32772575)
92. J.D. Schrag, W. Huang, J. Sivaraman, C. Smith, J. Plamondon, R. Larocque, A. Matte, M. Cygler, The crystal structureof Escherichia coli MoeA, a protein from the molybdopterin synthesis pathway, J. Mol. Biol. 310 (2001) 419-431.
93. J.D. Nichols, K.V. Rajagopalan, In vitro molybdenum ligation to molybdopterin using purified components, J. Biol. Chem. 280 (2005) 7817-7822. (Pubitemid 40349676)
94. A. Llamas, R.R. Mendel, G. Schwarz, Synthesis of adenylated molybdopterin: an essential step for molybdenum insertion, J. Biol. Chem. 279 (2004) 55241-55246. (Pubitemid 40066520)
95. A. Llamas, T. Otte, G. Multhaup, R.R. Mendel, G. Schwarz, The Mechanism of nucleotide-assisted molybdenum insertion into molybdopterin. A novel route toward metal cofactor assembly, J. Biol. Chem. 281 (2006) 18343-18350. (Pubitemid 44035491)
96. J. Kuper, A. Llamas, H.J. Hecht, R.R. Mendel, G. Schwarz, Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism, Nature 430 (2004) 803-806. (Pubitemid 39071353)
97. S. Leimkühler, K.V. Rajagopalan, In vitro incorporation of nascent molybdenum cofactor into human sulfite oxidase, J. Biol. Chem. 276 (2001) 1837-1844. (Pubitemid 32109658)
98. M. Neumann, S. Leimkühler, Heavy metal ions inhibit molybdoenzyme activity by binding to the dithiolene moiety of molybdopterin in Escherichia coli, FEBS J. 275 (2008) 5678-5689.
99. J.L. Johnson, N.R. Bastian, K.V. Rajagopalan, Molybdopterin guanine dinucleotide: a modified form of molybdopterin identified in the molybdenum cofactor of dimethyl sulfoxide reductase from Rhodobacter sphaeroides forma specialis denitrificans, Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 3190-3194.
100. M.W. Lake, C.A. Temple, K.V. Rajagopalan, H. Schindelin, The crystal structure of the Escherichia coli MobA protein provides insight into molybdopterin guanine dinucleotide biosynthesis, J. Biol. Chem. 275 (2000) 40211-40217. (Pubitemid 32064651)
101. T. Palmer, I.P. Goodfellow, R.E. Sockett, A.G. McEwan, D.H. Boxer, Characterisation of the mob locus from Rhodobacter sphaeroides required for molybdenum cofactor biosynthesis, Biochem. Biophys. Acta 1395 (1998) 135-140. (Pubitemid 28105718)
102. T. Palmer, C.-L. Santini, C. Iobbi-Nivol, D.J. Eaves, D.H. Boxer, G. Giordano, Involvement of the narJ and mob gene products in the biosynthesis of the molybdoenzyme nitrate reductase in Escherichia coli, Mol. Microbiol. 20 (1996) 875-884. (Pubitemid 26174891)
103. K. McLuskey, J.A. Harrison, A.W. Schuttelkopf, D.H. Boxer,W.N. Hunter, Insight into the role of Escherichia coli MobB in molybdenum cofactor biosynthesis based on the high resolution crystal structure, J. Biol. Chem. 278 (2003) 23706-23713. (Pubitemid 36830194)
104. C.A. Temple, K.V. Rajagopalan, Mechanism of assembly of the Bis(Molybdopterin guanine Dinucleotide)Molybdenum cofactor in Rhodobacter sphaeroides dimethyl sulfoxide reductase, J. Biol. Chem. 275 (2000) 40202-40210. (Pubitemid 32064650)
105. M. Neumann, W. Stocklein, S. Leimkühler, Transfer of the molybdenum cofactor synthesized by Rhodobacter capsulatus MoeA to XdhC and MobA, J. Biol. Chem. 282 (2007) 28493-28500. (Pubitemid 47606026)
106. C.E. Stevenson, F. Sargent, G. Buchanan, T. Palmer, D.M. Lawson, Crystal structure of the molybdenum cofactor biosynthesis protein MobA from Escherichia coli at near-atomic resolution, Struct. Fold. Des. 8 (2000) 1115-1125. (Pubitemid 32667477)
107. H. Xi, B.L. Schneider, L. Reitzer, Purine catabolism in Escherichia coli and function of xanthine dehydrogenase in purine salvage, J. Bacteriol. 182 (2000) 5332-5341.
108. S.G. Kozmin, R.M. Schaaper, Molybdenum cofactor-dependent resistance to N-hydroxylated base analogs in Escherichia coli is independent of MobA function, Mutat. Res. 619 (2007) 9-15. (Pubitemid 46602444)
109. M. Neumann, G. Mittelstädt, F. Seduk, C. Iobbi-Nivol, S. Leimkühler, MocA is a specific cytidylyl transferase involved in molybdopterin cytosine dinucleotide biosynthesis in Escherichia coli, J. Biol. Chem. 284 (2009) 21891-21898.
110. M. Neumann, F. Seduk, C. Iobbi-Nivol, S. Leimkühler, Molybdopterin dinucleotide biosynthesis in Escherichia coli: identification of amino acid residues of molybdopterin dinucleotide transferases that determine specificity for binding of guanine or cytosine nucleotides, J. Biol. Chem. 286 (2011) 1400-1408.
111. A. Guse, C.E. Stevenson, J. Kuper, G. Buchanan, G. Schwarz, G. Giordano, A. Magalon, R.R. Mendel, D.M. Lawson, T. Palmer, Biochemical and structural analysis of the molybdenum cofactor biosynthesis protein MobA, J. Biol. Chem. 278 (2003) 25302-25307. (Pubitemid 36835278)
112. S. Leimkühler, W. Klipp, Role of XDHC in Molybdenum cofactor insertion into xanthine dehydrogenase of Rhodobacter capsulatus, J. Bacteriol. 181 (1999) 2745-2751. (Pubitemid 29211088)
113. S. Leimkühler, S. Angermüller, G. Schwarz, R.R. Mendel, W. Klipp, Activity of the molybdopterin-containing xanthine dehydrogenase of Rhodobacter capsulatus can be restored by high molybdenum concentrations in a moeA mutant defective in molybdenum cofactor biosynthesis, J. Bacteriol. 181 (1999) 5930-5939. (Pubitemid 29459902)
114. M. Neumann, W. Stocklein, A. Walburger, A. Magalon, S. Leimkühler, 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)
115. M. Neumann, M. Schulte, N. Junemann, W. Stöcklein, S. Leimkühler, Rhodobacter capsulatus XdhC is involved in molybdenum cofactor binding and insertion into xanthine dehydrogenase, J. Biol. Chem. 281 (2006) 15701-15708. (Pubitemid 43848457)
116. J.C. Hilton, K.V. Rajagopalan, Identification of the molybdenum cofactor of dimethyl sulfoxide reductase from Rhodobacter sphaeroides f. sp. denitrificans as bis(molybdopterin guanine dinucleotide)molybdenum, Arch. Biochem. Biophys. 325 (1996) 139-143. (Pubitemid 26029575)
117. O. Genest, V. Mejean, C. Iobbi-Nivol, Multiple roles of TorD-like chaperones in the biogenesis of molybdoenzymes, FEMS Microbiol. Lett. 297 (2009) 1-9.
118. M.J. Axley, D.A. Grahame, T.C. Stadtman, Escherichia coli formate-hydrogen lyase. Purification and properties of the selenium-dependent formate dehydrogenase component, J. Biol. Chem. 265 (1990) 18213-18218.
119. R. Thome, A. Gust, R. Toci, R. Mendel, F. Bittner, A. Magalon, A. Walburger, A sulfurtransferase is essential for activity of formate dehydrogenases in Escherichia coli, J. Biol. Chem. 287 (2012) 4671-4678.
120. C. Coelho, P.J. Gonzalez, J.G.Moura, I. Moura, J. Trincao, M. Joao Romao, The crystal structure of Cupriavidus necator nitrate reductase in oxidized and partially reduced states, J. Mol. Biol. 408 (2011) 932-948.
121. S. Najmudin, P.J. Gonzalez, J. Trincao, C. Coelho, A. Mukhopadhyay, N.M. Cerqueira, C.C. Romao, I. Moura, J.J. Moura, C.D. Brondino, M.J. Romao, Periplasmic nitrate reductase revisited: a sulfur atom completes the sixth coordination of the catalytic molybdenum, J. Biol. Inorg. Chem. 13 (2008) 737-753.
122. F. Blasco, J.P. Dos Santos, A. Magalon, C. Frixon, B. Guigliarelli, C.L. Santini, 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)
123. F. Blasco, J. Pommier, V. Augier, M. Chippaux, G. Giordano, Involvement of the narJ or narW gene product in the formation of active nitrate reductase in Escherichia coli, Mol. Microbiol. 6 (1992) 221-230.
124. N. Ray, J. Oates, R.J. Turner, C. Robinson, DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus, FEBS Lett. 534 (2003) 156-160. (Pubitemid 36084534)
125. M. Ilbert, V. Mejean, 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)
126. S. Tranier, C. Iobbi-Nivol, C. Birck, M. Ilbert, I. Mortier-Barriere, V. Mejean, J.P. Samama, A novel protein fold and extreme domain swapping in the dimeric TorD chaperone from Shewanella massilia, Structure (Camb) 11 (2003) 165-174. (Pubitemid 36187418)
127. O. Kirillova, M. Chruszcz, I.A. Shumilin, T. Skarina, E. Gorodichtchenskaia, M. Cymborowski, A. Savchenko, A. Edwards, W. Minor, An extremely SAD case: structure of a putative redox-enzyme maturation protein from Archaeoglobus fulgidus at 3.4 A resolution, Acta Crystallogr. D Biol. Crystallogr. 63 (2007) 348-354.
128. J. Pommier, V. Mejean, G. Giordano, C. Iobbi-Nivol, TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine N-oxide reductase enzyme (TorA) in Escherichia coli, J. Biol. Chem. 273 (1998) 16615-16620. (Pubitemid 28311451)
129. M. Ilbert, V.Mejean, M.T. Giudici-Orticoni, J.P. Samama, 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)
130. K. Hatzixanthis, T.A. Clarke, A. Oubrie, D.J. Richardson, R.J. Turner, F. Sargent, Signal peptide-chaperone interactions on the twin-arginine protein transport pathway, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 8460-8465. (Pubitemid 40862758)
131. R.L. Jack, G. Buchanan, A. Dubini, K. Hatzixanthis, T. Palmer, F. Sargent, Coordinating assembly and export of complex bacterial proteins, EMBO J. 23 (2004) 3962-3972. (Pubitemid 39472418)
132. C.S. Chan, T.M. Winstone, L. Chang, C.M. Stevens, M.L. Workentine, H. Li, Y. Wei, M.J. Ondrechen, M. Paetzel, R.J. Turner, Identification of residues in DmsD for twin-arginine leader peptide binding, defined through random and bioinformaticsdirected mutagenesis, Biochemistry 47 (2008) 2749-2759. (Pubitemid 351328825)
133. O. Genest, M. Ilbert, V. Mejean, C. Iobbi-Nivol, TorD, an essential chaperone for TorA molybdoenzyme maturation at high temperature, J. Biol. Chem. 280 (2005) 15644-15648. (Pubitemid 40616682)
134. O. Genest, F. Seduk, L. Theraulaz, V. Mejean, C. Iobbi-Nivol, Chaperone protection of immature molybdoenzyme during molybdenum cofactor limitation, FEMS Microbiol. Lett. 265 (2006) 51-55. (Pubitemid 44715443)
135. O. Genest, F. Seduk, M. Ilbert, V. Mejean, C. Iobbi-Nivol, Signal peptide protection by specific chaperone, Biochem. Biophys. Res. Commun. 339 (2006) 991-995. (Pubitemid 41772909)
136. A. Vergnes, J. Pommier, R. Toci, F. Blasco, G. Giordano, A. Magalon, NarJ chaperone binds on two distinct sites of the aponitrate reductase of Escherichia coli to coordinate molybdenum cofactor insertion and assembly, J. Biol. Chem. 281 (2006) 2170-2176. (Pubitemid 43845807)
137. I.J. Oresnik, C.L. Ladner, R.J. Turner, Identification of a twin-arginine leaderbinding protein, Mol. Microbiol. 40 (2001) 323-331.
138. C.S. Chan, J.M. Howell, M.L. Workentine, R.J. Turner, Twin-arginine translocase may have a role in the chaperone function of NarJ from Escherichia coli, Biochem. Biophys. Res. Commun. 343 (2006) 244-251.
139. R.J. Turner, A.L. Papish, F. Sargent, Sequence analysis of bacterial redox enzyme maturation proteins (REMPs), Can. J. Microbiol. 50 (2004) 225-238. (Pubitemid 38903410)
140. O. Genest, M. Neumann, F. Seduk, W. Stocklein, V. Mejean, S. Leimkühler, C. Iobbi-Nivol, Dedicated metallochaperone connects apoenzyme and molybdenum cofactor biosynthesis components, J. Biol. Chem. 283 (2008) 21433-21440.
141. J.L. Johnson, N.R. Bastian, N.L. Schauer, J.G. Ferry, K.V. Rajagopalan, Identification of molybdopterin guanine dinucleotide in formate dehydrogenase from Methanobacterium formicicum, FEMS Microbiol. Lett. 77 (1991) 213-216.
142. T.L. Winstone, M.L. Workentine, K.J. Sarfo, A.J. Binding, B.D. Haslam, R.J. Turner, Physical nature of signal peptide binding to DmsD, Arch. Biochem. Biophys. 455 (2006) 89-97. (Pubitemid 44602004)
143. D. Redelberger, F. Seduk, O. Genest, V. Mejean, S. Leimkühler, C. Iobbi-Nivol, YcdY protein of Escherichia coli, an atypical member of the TorD chaperone family, J. Bacteriol. 193 (2011) 6512-6516.
144. M. Dubourdieu, J.A. DeMoss, The narJ gene product is required for biogenesis of respiratory nitrate reductase in Escherichia coli, J. Bacteriol. 174 (1992) 867-872.
145. X. Liu, J.A. DeMoss, Characterization of NarJ, a system-specific chaperone required for nitrate reductase biogenesis in Escherichia coli, J. Biol. Chem. 272 (1997) 24266-24271. (Pubitemid 27418628)
146. J. Grove, S. Tanapongpipat, G. Thomas, L. Griffiths, H. Crooke, J. Cole, Escherichia coli K-12 genes essential for the synthesis of c-type cytochromes and a third nitrate reductase located in the periplasm, Mol. Microbiol. 19 (1996) 467-481. (Pubitemid 26052134)
147. L. Potter, H. Angove, D. Richardson, J. Cole, Nitrate reduction in the periplasm of gram-negative bacteria, Adv. Microb. Physiol. 45 (2001) 51-112. (Pubitemid 32612190)
148. J. Maillard, C.A. Spronk, G. Buchanan, V. Lyall, D.J. Richardson, T. Palmer, G.W. Vuister, F. Sargent, Structural diversity in twin-arginine signal peptide-binding proteins, Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 15641-15646. (Pubitemid 350035353)
149. D.J. Richardson, B.C. Berks, D.A. Russell, S. Spiro, C.J. Taylor, Functional, biochemical and genetic diversity of prokaryotic nitrate reductases, Cell. Mol. Life Sci. 58 (2001) 165-178. (Pubitemid 32217349)
150. T.H. Brondijk, D. Fiegen, D.J. Richardson, J.A. Cole, Roles of NapF, NapG and NapH, subunits of the Escherichia coli periplasmic nitrate reductase, in ubiquinol oxidation, Mol. Microbiol. 44 (2002) 245-255. (Pubitemid 34429779)
151. B.J. Jepson, A. Marietou, S. Mohan, J.A. Cole, C.S. Butler, D.J. Richardson, Evolution of the soluble nitrate reductase: defining the monomeric periplasmic nitrate reductase subgroup, Biochem. Soc. Trans. 34 (2006) 122-126. (Pubitemid 43235550)
152. G. Thomas, L. Potter, J.A. Cole, The periplasmic nitrate reductase from Escherichia coli: a heterodimericmolybdoproteinwith a double-arginine signal sequence and an unusual leader peptide cleavage site, FEMS Microbiol. Lett. 174 (1999) 167-171. (Pubitemid 29179448)
153. M.F. Olmo-Mira, M. Gavira, D.J. Richardson, F. Castillo, C. Moreno-Vivian, M.D. Roldan, NapF is a cytoplasmic iron-sulfur protein required for Fe-S cluster assembly in the periplasmic nitrate reductase, J. Biol. Chem. 279 (2004) 49727-49735. (Pubitemid 39577776)
154. A. Nilavongse, T.H. Brondijk, T.W. Overton, D.J. Richardson, E.R. Leach, J.A. Cole, The NapF protein of the Escherichia coli periplasmic nitrate reductase system: demonstration of a cytoplasmic location and interaction with the catalytic subunit, NapA, Microbiology 152 (2006) 3227-3237. (Pubitemid 44734327)
155. S. Zakian, D. Lafitte, A. Vergnes, C. Pimentel, C. Sebban-Kreuzer, R. Toci, J.B. Claude, F. Guerlesquin, A. Magalon, Basis of recognition between the NarJ chaperone and the N-terminus of the NarG subunit from Escherichia coli nitrate reductase, FEBS J. 277 (2010) 1886-1895.
156. S. Grahl, J. Maillard, C.A. Spronk, G.W. Vuister, F. Sargent, Overlapping transport and chaperone-binding functions within a bacterial twin-arginine signal peptide, Mol. Microbiol. (2012) 1254-1267.
157. S.J. Coulthurst, A. Dawson, W.N. Hunter, F. Sargent, Conserved signal peptide recognition systems across the prokaryotic domains, Biochemistry 51 (2012) 1678-1686.
158. Y. Zhang, V.N. Glagyshev, Molybdoproteomes and evolution of molybdenum utilization, J. Mol. Biol. 379 (2008) 881-899.
159. G. Schwarz, Molybdenum cofactor biosynthesis and deficiency, Cell. Mol. Life Sci. 62 (2005) 2792-2810. (Pubitemid 41779947)
160. M. Fischer, B. Thöny, S. Leimkühler, The biosynthesis of folate and Pterin and their enzymology, in: Comprehensive natural products chemistry II, vol. 7, 2010, pp. 599-648.