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Metabolism

Biosynthesis and Insertion of the Molybdenum Cofactor

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  • Authors: Axel Magalon1, and Ralf R. Mendel2
  • Editor: Valley Stewart3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: CNRS, Aix Marseille Université, IMM FR3479, Laboratoire de Chimie Bactérienne UMR 7283, F-13402 Marseille Cedex 20, France; 2: Department of Plant Biology, Technical University, 38106 Braunschweig, Germany; 3: University of California–Davis, Davis, CA
  • Received 03 February 2014 Accepted 14 April 2015 Published 15 June 2015
  • Address correspondence to Axel Magalon, magalon@imm.cnrs.fr
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  • Abstract:

    The transition element molybdenum (Mo) is of primordial importance for biological systems, because it is required by enzymes catalyzing key reactions in the global carbon, sulfur, and nitrogen metabolism. To gain biological activity, Mo has to be complexed by a special cofactor. With the exception of bacterial nitrogenase, all Mo-dependent enzymes contain a unique pyranopterin-based cofactor coordinating a Mo atom at their catalytic site. Various types of reactions are catalyzed by Mo-enzymes in prokaryotes including oxygen atom transfer, sulfur or proton transfer, hydroxylation, or even nonredox reactions. Mo-enzymes are widespread in prokaryotes and many of them were likely present in the Last Universal Common Ancestor. To date, more than 50 – mostly bacterial – Mo-enzymes are described in nature. In a few eubacteria and in many archaea, Mo is replaced by tungsten bound to the same unique pyranopterin. How Mo-cofactor is synthesized in bacteria is reviewed as well as the way until its insertion into apo-Mo-enzymes.

  • Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013

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References

1. Mendel RR, Kruse T. 2012. Cell biology of molybdenum in plants and humans. Biochim Biophys Acta 1823:1568–1579. [PubMed][CrossRef]
2. Grimaldi S, Schoepp-Cothenet B, Ceccaldi P, Guigliarelli B, Magalon A. 2013. The prokaryotic Mo/W-bisPGD enzymes family: a catalytic workhorse in bioenergetic. Biochim Biophys Acta 1827:1048–1085. [PubMed][CrossRef]
3. Williams RJ, Frausto da Silva JJ. 2002. The involvement of molybdenum in life. Biochem Biophys Res Commun 292:293–299. [PubMed][CrossRef]
4. Hille R. 2002. Molybdenum enzymes containing the pyranopterin cofactor: an overview. Met Ions Biol Syst 39:187–226. [PubMed][CrossRef]
5. Cvetkovic A, Menon AL, Thorgersen MP, Scott JW, Poole FL, 2nd, Jenney FE, Jr., Lancaster WA, Praissman JL, Shanmukh S, Vaccaro BJ, Trauger SA, Kalisiak E, Apon JV, Siuzdak G, Yannone SM, Tainer JA, Adams MW. 2010. Microbial metalloproteomes are largely uncharacterized. Nature 466:779–782. [PubMed][CrossRef]
6. Bevers LE, Hagedoorn PL, Hagen WR. 2009. The bioinorganic chemistry of tungsten. Coord Chem Rev 253:269–290. [CrossRef]
7. Schneider F, Lowe J, Huber R, Schindelin H, Kisker C, Knablein J. 1996. Crystal structure of dimethyl sulfoxide reductase from Rhodobacter capsulatus at 1.88 A resolution. J Mol Biol 263:53–69. [PubMed][CrossRef]
8. Rothery RA, Workun GJ, Weiner JH. 2008. The prokaryotic complex iron-sulfur molybdoenzyme family. Biochim Biophys Acta 1778:1897–1929. [PubMed][CrossRef]
9. Schoepp-Cothenet B, van Lis R, Philippot P, Magalon A, Russell MJ, Nitschke W. 2012. The ineluctable requirement for the trans-iron elements molybdenum and/or tungsten in the origin of life. Sci Rep 2:263. doi:10.1038/srep00263 [PubMed][CrossRef]
10. Magalon A, Fedor JG, Walburger A, Weiner JH. 2011. Molybdenum enzymes in bacteria and their maturation. Coord Chem Rev 255:1159–1178. [CrossRef]
11. Pateman JA, Cove DJ, Rever BM, Roberts DB. 1964. A common co-factor for nitrate reductase and xanthine dehydrogenase which also regulates the synthesis of nitrate reductase. Nature 201:58–60. [PubMed][CrossRef]
12. Cove DJ, Pateman JA. 1963. Independently segregating genetic loci concerned with nitrate reductase activity in Aspergillus nidulans. Nature 198:262–263. [PubMed][CrossRef]
13. Johnson JL, Hainline BE, Rajagopalan KV. 1980. Characterization of the molybdenum cofactor of sulfite oxidase, xanthine, oxidase, and nitrate reductase. Identification of a pteridine as a structural component. J Biol Chem 255:1783–1786. [PubMed]
14. Pichinoty F, Puig J, Chippaux M, Bigliardi-Rouvier J, Gendre J. 1969. [Studies of bacterial mutants that have lost catalytic activities associated with nitrate reductase A. II. Behavior toward chlorate and chlorite]. Ann Inst Pasteur (Paris) 116:409–432.
15. Piechaud M, Pichinoty F, Azoulay E, Couchoud-Beaumont P, Gendre J. 1969. [Study of bacterial mutants that have lost catalytic activity associated with nitrate reductase A. I. Description of isolation methods]. Ann Inst Pasteur (Paris) 116:276–287. [PubMed]
16. Stewart V, MacGregor CH. 1982. Nitrate reductase in Escherichia coli K-12: involvement of chlC, chlE, and chlG loci. J Bacteriol 151:788–799. [PubMed]
17. Shanmugam KT, Stewart V, Gunsalus RP, Boxer DH, Cole JA, Chippaux M, DeMoss JA, Giordano G, Lin EC, Rajagopalan KV. 1992. Proposed nomenclature for the genes involved in molybdenum metabolism in Escherichia coli and Salmonella typhimurium. Mol Microbiol 6:3452–3454. [PubMed][CrossRef]
18. Hagen W. 2011. Cellular uptake of molybdenum and tungsten. Coord Chem Rev 255:1117–1128. [CrossRef]
19. Glaser JH, DeMoss JA. 1971. Phenotypic restoration by molybdate of nitrate reductase activity in chlD mutants of Escherichia coli. J Bacteriol 108:854–860. [PubMed]
20. Scott D, Amy NK. 1989. Molybdenum accumulation in chlD mutants of Escherichia coli. J Bacteriol 171:1284–1287. [PubMed]
21. Pau RN, Lawson DM. 2002. Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. Met Ions Biol Syst 39:31–74. [PubMed][CrossRef]
22. McNicholas PM, Rech SA, Gunsalus RP. 1997. Characterization of the ModE DNA-binding sites in the control regions of modABCD and moaABCDE of Escherichia coli. Mol Microbiol 23:515–524. [PubMed][CrossRef]
23. Anderson LA, Palmer T, Price NC, Bornemann S, Boxer DH, Pau RN. 1997. Characterisation of the molybdenum-responsive ModE regulatory protein and its binding to the promoter region of the modABCD (molybdenum transport) operon of Escherichia coli. Eur J Biochem 246:119–126. [PubMed][CrossRef]
24. Hall DR, Gourley DG, Duke EM, Leonard GA, Anderson LA, Pau RN, Boxer DH, Hunter WN. 1999. Two crystal forms of ModE, the molybdate-dependent transcriptional regulator from Escherichia coli. Acta Crystallogr D Biol Crystallogr 55(Pt 2):542–543. [PubMed][CrossRef]
25. Gourley DG, Schuttelkopf AW, Anderson LA, Price NC, Boxer DH, Hunter WN. 2001. Oxyanion binding alters conformation and quaternary structure of the c-terminal domain of the transcriptional regulator mode. Implications for molybdate-dependent regulation, signaling, storage, and transport. J Biol Chem 276:20641–20647. [PubMed][CrossRef]
26. Schuttelkopf AW, Boxer DH, Hunter WN. 2003. Crystal structure of activated ModE reveals conformational changes involving both oxyanion and DNA-binding domains. J Mol Biol 326:761–767. [PubMed][CrossRef]
27. McNicholas PM, Chiang RC, Gunsalus RP. 1998. Anaerobic regulation of the Escherichia coli dmsABC operon requires the molybdate-responsive regulator ModE. Mol Microbiol 27:197–208. [PubMed][CrossRef]
28. Self WT, Grunden AM, Hasona A, Shanmugam KT. 1999. 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):41–55. [PubMed][CrossRef]
29. Anderson LA, McNairn E, Leubke T, Pau RN, Boxer DH. 2000. ModE-dependent molybdate regulation of the molybdenum cofactor operon moa in Escherichia coli. J Bacteriol 182:7035–7043. [PubMed][CrossRef]
30. Grunden AM, Ray RM, Rosentel JK, Healy FG, Shanmugam KT. 1996. Repression of the Escherichia coli modABCD (molybdate transport) operon by ModE. J Bacteriol 178:735–744. [PubMed]
31. Makdessi K, Andreesen JR, Pich A. 2001. Tungstate uptake by a highly specific ABC transporter in Eubacterium acidaminophilum. J Biol Chem 276:24557–24564. [PubMed][CrossRef]
32. Andreesen JR, Makdessi K. 2008. Tungsten, the surprisingly positively acting heavy metal element for prokaryotes. Ann N Y Acad Sci 1125:215–229. [PubMed][CrossRef]
33. Bevers LE, Hagedoorn PL, Krijger GC, Hagen WR. 2006. Tungsten transport protein A (WtpA) in Pyrococcus furiosus: the first member of a new class of tungstate and molybdate transporters. J Bacteriol 188:6498–6505. [PubMed][CrossRef]
34. Grunden AM, Shanmugam KT. 1997. Molybdate transport and regulation in bacteria. Arch Microbiol 168:345–354. [PubMed][CrossRef]
35. Rosentel JK, Healy F, Maupin-Furlow JA, Lee JH, Shanmugam KT. 1995. Molybdate and regulation of mod (molybdate transport), fdhF, and hyc (formate hydrogenlyase) operons in Escherichia coli. J Bacteriol 177:4857–4864. [PubMed]
36. Baker KP, Boxer DH. 1991. Regulation of the chlA locus of Escherichia coli K12: involvement of molybdenum cofactor. Mol Microbiol 5:901–907. [PubMed][CrossRef]
37. Regulski EE, Moy RH, Weinberg Z, Barrick JE, Yao Z, Ruzzo WL, Breaker RR. 2008. A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Mol Microbiol 68:918–932. [PubMed][CrossRef]
38. Serganov A, Patel DJ. 2009. Amino acid recognition and gene regulation by riboswitches. Biochim Biophys Acta 1789:592–611. [PubMed][CrossRef]
39. Patterson-Fortin LM, Vakulskas CA, Yakhnin H, Babitzke P, Romeo T. 2013. Dual posttranscriptional regulation via a cofactor-responsive mRNA leader. J Mol Biol 425:3662–3677. [PubMed][CrossRef]
40. Timmermans J, Van Melderen L. 2010. Post-transcriptional global regulation by CsrA in bacteria. Cell Mol Life Sci 67:2897–2908. [PubMed][CrossRef]
41. Edwards AN, Patterson-Fortin LM, Vakulskas CA, Mercante JW, Potrykus K, Vinella D, Camacho MI, Fields JA, Thompson SA, Georgellis D, Cashel M, Babitzke P, Romeo T. 2011. Circuitry linking the Csr and stringent response global regulatory systems. Mol Microbiol 80:1561–1580. [PubMed][CrossRef]
42. Hasona A, Self WT, Shanmugam KT. 2001. Transcriptional regulation of the moe (molybdate metabolism) operon of Escherichia coli. Arch Microbiol 175:178–188. [PubMed][CrossRef]
43. Hasona A, Self WT, Ray RM, Shanmugam KT. 1998. Molybdate-dependent transcription of hyc and nar operons of Escherichia coli requires MoeA protein and ModE-molybdate. FEMS Microbiol Lett 169:111–116. [PubMed][CrossRef]
44. Iobbi-Nivol C, Palmer T, Whitty PW, McNairn E, Boxer DH. 1995. The mob locus of Escherichia coli K12 required for molybdenum cofactor biosynthesis is expressed at very low levels. Microbiology 141(Pt 7):1663–1671. [PubMed][CrossRef]
45. Rajagopalan KV, Johnson JL. 1992. The pterin molybdenum cofactors. J Biol Chem 267:10199–10202. [PubMed]
46. Rajagopalan KV, Johnson JL, Wuebbens MM, Pitterle DM, Hilton JC, Zurick TR, Garrett RM. 1993. Chemistry and biology of the molybdenum cofactors. Adv Exp Med Biol 338:355–362. [PubMed][CrossRef]
47. Thony B, Auerbach G, Blau N. 2000. Tetrahydrobiopterin biosynthesis, regeneration and functions. Biochem J 347(Pt 1):1–16. [PubMed][CrossRef]
48. Bacher A, Eberhardt S, Eisenreich W, Fischer M, Herz S, Illarionov B, Kis K, Richter G. 2001. Biosynthesis of riboflavin. Vitam Horm 61:1–49. [PubMed][CrossRef]
49. Wuebbens MM, Rajagopalan KV. 1995. Investigation of the early steps of molybdopterin biosynthesis in Escherichia coli through the use of in vivo labeling studies. J Biol Chem 270:1082–1087. [PubMed][CrossRef]
50. Rieder C, Eisenreich W, O’Brien J, Richter G, Gotze E, Boyle P, Blanchard S, Bacher A, Simon H. 1998. Rearrangement reactions in the biosynthesis of molybdopterin–an NMR study with multiply 13C/15N labelled precursors. Eur J Biochem 255:24–36. [PubMed][CrossRef]
51. Wuebbens MM, Rajagopalan KV. 1993. Structural characterization of a molybdopterin precursor. J Biol Chem 268:13493–13498. [PubMed]
52. Santamaria-Araujo JA, Fischer B, Otte T, Nimtz M, Mendel RR, Wray V, Schwarz G. 2004. The tetrahydropyranopterin structure of the sulfur-free and metal-free molybdenum cofactor precursor. J Biol Chem 279:15994–15999. [PubMed][CrossRef]
53. Santamaria-Araujo JA, Wray V, Schwarz G. 2012. Structure and stability of the molybdenum cofactor intermediate cyclic pyranopterin monophosphate. J Biol Inorg Chem 17:113–122. [PubMed][CrossRef]
54. Hanzelmann P, Hernandez HL, Menzel C, Garcia-Serres R, Huynh BH, Johnson MK, Mendel RR, Schindelin H. 2004. Characterization of MOCS1A, an oxygen-sensitive iron-sulfur protein involved in human molybdenum cofactor biosynthesis. J Biol Chem 279:34721–34732. [PubMed][CrossRef]
55. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE. 2001. 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 29:1097–1106. [PubMed][CrossRef]
56. Hanzelmann P, Schindelin H. 2004. Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc Natl Acad Sci USA 101:12870–12875. [PubMed][CrossRef]
57. Hanzelmann P, Schindelin H. 2006. 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 USA 103:6829–6834. [PubMed][CrossRef]
58. Wuebbens MM, Liu MT, Rajagopalan K, Schindelin H. 2000. Insights into molybdenum cofactor deficiency provided by the crystal structure of the molybdenum cofactor biosynthesis protein MoaC. Structure Fold Des 8:709–718. [PubMed][CrossRef]
59. Clinch K, Watt DK, Dixon RA, Baars SM, Gainsford GJ, Tiwari A, Schwarz G, Saotome Y, Storek M, Belaidi AA, Santamaria-Araujo JA. 2013. Synthesis of cyclic pyranopterin monophosphate, a biosynthetic intermediate in the molybdenum cofactor pathway. J Med Chem 56:1730–1738. [PubMed][CrossRef]
60. Schwarz G, Santamaria-Araujo JA, Wolf S, Lee HJ, Adham IM, Grone HJ, Schwegler H, Sass JO, Otte T, Hanzelmann P, Mendel RR, Engel W, Reiss J. 2004. Rescue of lethal molybdenum cofactor deficiency by a biosynthetic precursor from Escherichia coli. Hum Mol Genet 13:1249–1255. [PubMed][CrossRef]
61. Veldman A, Santamaria-Araujo JA, Sollazzo S, Pitt J, Gianello R, Yaplito-Lee J, Wong F, Ramsden CA, Reiss J, Cook I, Fairweather J, Schwarz G. 2010. Successful treatment of molybdenum cofactor deficiency type A with cPMP. Pediatrics 125:e1249–e1254. [PubMed][CrossRef]
62. Gutzke G, Fischer B, Mendel RR, Schwarz G. 2001. Thiocarboxylation of molybdopterin synthase provides evidence for the mechanism of dithiolene formation in metal-binding pterins. J Biol Chem 276:36268–36274. [PubMed][CrossRef]
63. Rudolph MJ, Wuebbens MM, Rajagopalan KV, Schindelin H. 2001. Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation. Nat Struct Biol 8:42–46. [PubMed][CrossRef]
64. Tong Y, Wuebbens MM, Rajagopalan KV, Fitzgerald MC. 2005. Thermodynamic analysis of subunit interactions in Escherichia coli molybdopterin synthase. Biochemistry 44:2595–2601. [PubMed][CrossRef]
65. Daniels JN, Wuebbens MM, Rajagopalan KV, Schindelin H. 2008. Crystal structure of a molybdopterin synthase-precursor Z complex: insight into its sulfur transfer mechanism and its role in molybdenum cofactor deficiency. Biochemistry 47:615–626. [PubMed][CrossRef]
66. Wuebbens MM, Rajagopalan KV. 2003. Mechanistic and mutational studies of Escherichia coli molybdopterin synthase clarify the final step of molybdopterin biosynthesis. J Biol Chem 278:14523–14532. [PubMed][CrossRef]
67. Leimkuhler S, Wuebbens MM, Rajagopalan KV. 2001. Characterization of Escherichia coli MoeB and its involvement in the activation of molybdopterin synthase for the biosynthesis of the molybdenum cofactor. J Biol Chem 276:34695–34701. [PubMed][CrossRef]
68. Lake MW, Wuebbens MM, Rajagopalan KV, Schindelin H. 2001. Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB-MoaD complex. Nature 414:325–329. [PubMed][CrossRef]
69. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu Rev Biochem 67:425–479. [PubMed][CrossRef]
70. Schmitz J, Wuebbens MM, Rajagopalan KV, Leimkuhler S. 2007. Role of the C-terminal Gly-Gly motif of Escherichia coli MoaD, a molybdenum cofactor biosynthesis protein with a ubiquitin fold. Biochemistry 46:909–916. [PubMed][CrossRef]
71. Taylor SV, Kelleher NL, Kinsland C, Chiu HJ, Costello CA, Backstrom AD, McLafferty FW, Begley TP. 1998. Thiamin biosynthesis in Escherichia coli. Identification of ThiS thiocarboxylate as the immediate sulfur donor in the thiazole formation. J Biol Chem 273:16555–16560. [PubMed][CrossRef]
72. Wang C, Xi J, Begley TP, Nicholson LK. 2001. Solution structure of ThiS and implications for the evolutionary roots of ubiquitin. Nat Struct Biol 8:47–51. [PubMed][CrossRef]
73. Lehmann C, Begley TP, Ealick SE. 2006. Structure of the Escherichia coli ThiS-ThiF complex, a key component of the sulfur transfer system in thiamin biosynthesis. Biochemistry 45:11–19. [PubMed][CrossRef]
74. Jurgenson CT, Ealick SE, Begley TP. 2009. Biosynthesis of thiamin pyrophosphate. In Kaper JB (ed), EcoSal PLus doi:10.1128/ecosalplus.3.6.3.7. [CrossRef]
75. Cronan JE, Jr. 2014. Biotin and Lipoic acid: synthesis, attachment, and regulation. In Kaper JB (ed), EcoSal Plus doi:10.1128/ecosalplus.3.6.3.5. [CrossRef]
76. Zhang W, Urban A, Mihara H, Leimkuhler S, Kurihara T, Esaki N. 2010. 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 285:2302–2308. [PubMed][CrossRef]
77. Shi R, Proteau A, Villarroya M, Moukadiri I, Zhang L, Trempe JF, Matte A, Armengod ME, Cygler M. 2010. Structural basis for Fe-S cluster assembly and tRNA thiolation mediated by IscS protein-protein interactions. PLoS Biol 8:e1000354. doi:10.1371/journal.pbio.1000354. [CrossRef]
78. Dahl JU, Urban A, Bolte A, Sriyabhaya P, Donahue JL, Nimtz M, Larson TJ, Leimkuhler S. 2011. The identification of a novel protein involved in molybdenum cofactor biosynthesis in Escherichia coli. J Biol Chem 286:35801–35812. [PubMed][CrossRef]
79. Ikeuchi Y, Shigi N, Kato J, Nishimura A, Suzuki T. 2006. Mechanistic insights into sulfur relay by multiple sulfur mediators involved in thiouridine biosynthesis at tRNA wobble positions. Mol Cell 21:97–108. [PubMed][CrossRef]
80. Dahl JU, Radon C, Buhning M, Nimtz M, Leichert LI, Denis Y, Jourlin-Castelli C, Iobbi-Nivol C, Mejean V, Leimkuhler S. 2013. The sulfur carrier protein TusA has a pleiotropic role in Escherichia coli that also affects molybdenum cofactor biosynthesis. J Biol Chem 288:5426–5442. [PubMed][CrossRef]
81. Schwarz G, Mendel RR, Ribbe MW. 2009. Molybdenum cofactors, enzymes and pathways. Nature 460:839–847. [PubMed][CrossRef]
82. Llamas A, Mendel RR, Schwarz G. 2004. Synthesis of adenylated molybdopterin: an essential step for molybdenum insertion. J Biol Chem 279:55241–55246. [PubMed][CrossRef]
83. Schwarz G, Boxer DH, Mendel RR. 1997. Molybdenum cofactor biosynthesis. The plant protein Cnx1 binds molybdopterin with high affinity. J Biol Chem 272:26811–26814. [PubMed][CrossRef]
84. Kuper J, Llamas A, Hecht HJ, Mendel RR, Schwarz G. 2004. Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430:803–806. [PubMed][CrossRef]
85. Kuper J, Winking J, Hecht HJ, Mendel RR, Schwarz G. 2003. The active site of the molybdenum cofactor biosynthetic protein domain Cnx1G. Arch Biochem Biophys 411:36–46. [CrossRef]
86. Schwarz G, Schrader N, Mendel RR, Hecht HJ, Schindelin H. 2001. Crystal structures of human gephyrin and plant Cnx1 G domains: comparative analysis and functional implications. J Mol Biol 312:405–418. [PubMed][CrossRef]
87. Llamas A, Otte T, Multhaup G, Mendel RR, Schwarz G. 2006. The Mechanism of nucleotide-assisted molybdenum insertion into molybdopterin. A novel route toward metal cofactor assembly. J Biol Chem 281:18343–18350. [PubMed][CrossRef]
88. Leimkuhler S, Rajagopalan KV. 2001. In vitro incorporation of nascent molybdenum cofactor into human sulfite oxidase. J Biol Chem 276:1837–1844. [PubMed][CrossRef]
89. Bader G, Gomez-Ortiz M, Haussmann C, Bacher A, Huber R, Fischer M. 2004. Structure of the molybdenum-cofactor biosynthesis protein MoaB of Escherichia coli. Acta Crystallogr D Biol Crystallogr 60:1068–1075. [PubMed][CrossRef]
90. Sanishvili R, Beasley S, Skarina T, Glesne D, Joachimiak A, Edwards A, Savchenko A. 2004. The crystal structure of Escherichia coli MoaB suggests a probable role in molybdenum cofactor synthesis. J Biol Chem 279:42139–42146. [PubMed][CrossRef]
91. Liu MT, Wuebbens MM, Rajagopalan KV, Schindelin H. 2000. Crystal structure of the gephyrin-related molybdenum cofactor biosynthesis protein MogA from Escherichia coli. J Biol Chem 275:1814–1822. [PubMed][CrossRef]
92. Kozmin SG, Schaaper RM. 2013. Genetic characterization of moaB mutants of Escherichia coli. Res Microbiol 164:689–694. [PubMed][CrossRef]
93. Bevers LE, Hagedoorn PL, Santamaria-Araujo JA, Magalon A, Hagen WR, Schwarz G. 2008. Function of MoaB proteins in the biosynthesis of the molybdenum and tungsten cofactors. Biochemistry 47:949–956. [PubMed][CrossRef]
94. Neumann M, Mittelstadt G, Iobbi-Nivol C, Saggu M, Lendzian F, Hildebrandt P, Leimkuhler S. 2009. A periplasmic aldehyde oxidoreductase represents the first molybdopterin cytosine dinucleotide cofactor containing molybdo-flavoenzyme from Escherichia coli. FEBS J 276:2762–2774. [PubMed][CrossRef]
95. Neumann M, Mittelstadt G, Seduk F, Iobbi-Nivol C, Leimkuhler S. 2009. MocA is a specific cytidylyltransferase involved in molybdopterin cytosine dinucleotide biosynthesis in Escherichia coli. J Biol Chem 284:21891–21898. [PubMed][CrossRef]
96. Leimkuhler S, Angermuller S, Schwarz G, Mendel RR, Klipp W. 1999. 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 181:5930–5939. [PubMed]
97. Nichols J, Rajagopalan KV. 2002. Escherichia coli MoeA and MogA. Function in metal incorporation step of molybdenum cofactor biosynthesis. J Biol Chem 277:24995–25000. [PubMed][CrossRef]
98. Neumann M, Leimkuhler S. 2008. Heavy metal ions inhibit molybdoenzyme activity by binding to the dithiolene moiety of molybdopterin in Escherichia coli. FEBS J 275:5678–5689. [PubMed][CrossRef]
99. Hasona A, Ray RM, Shanmugam KT. 1998. Physiological and genetic analyses leading to identification of a biochemical role for the moeA (molybdate metabolism) gene product in Escherichia coli. J Bacteriol 180:1466–1472. [PubMed]
100. Brokx SJ, Rothery RA, Zhang G, Ng DP, Weiner JH. 2005. Characterization of an Escherichia coli sulfite oxidase homologue reveals the role of a conserved active site cysteine in assembly and function. Biochemistry 44:10339–10348. [PubMed][CrossRef]
101. Loschi L, Brokx SJ, Hills TL, Zhang G, Bertero MG, Lovering AL, Weiner JH, Strynadka NC. 2004. Structural and biochemical identification of a novel bacterial oxidoreductase. J Biol Chem 279:50391–50400. [PubMed][CrossRef]
102. Xi H, Schneider BL, Reitzer L. 2000. Purine catabolism in Escherichia coli and function of xanthine dehydrogenase in purine salvage. J Bacteriol 182:5332–5341. [PubMed][CrossRef]
103. Kozmin SG, Schaaper RM. 2007. Molybdenum cofactor-dependent resistance to N-hydroxylated base analogs in Escherichia coli is independent of MobA function. Mutat Res 619:9–15. [PubMed][CrossRef]
104. Nichols JD, Rajagopalan KV. 2005. In vitro molybdenum ligation to molybdopterin using purified components. J Biol Chem 280:7817–7822. [PubMed][CrossRef]
105. Magalon A, Frixon C, Pommier J, Giordano G, Blasco F. 2002. In vivo interactions between gene products involved in the final stages of molybdenum cofactor biosynthesis in Escherichia coli. J Biol Chem 277:48199–48204. [PubMed][CrossRef]
106. Belaidi AA, Schwarz G. 2013. Metal insertion into the molybdenum cofactor: product-substrate channelling demonstrates the functional origin of domain fusion in gephyrin. Biochem J 450:149–157. [PubMed][CrossRef]
107. Palmer T, Vasishta A, Whitty PW, Boxer DH. 1994. Isolation of protein FA, a product of the mob locus required for molybdenum cofactor biosynthesis in Escherichia coli. Eur J Biochem 222:687–692. [PubMed][CrossRef]
108. Palmer T, Santini CL, Iobbi-Nivol C, Eaves DJ, Boxer DH, Giordano G. 1996. Involvement of the narJ and mob gene products in distinct steps in the biosynthesis of the molybdoenzyme nitrate reductase in Escherichia coli. Mol Microbiol 20:875–884. [PubMed][CrossRef]
109. Temple CA, Rajagopalan KV. 2000. Mechanism of assembly of the bis(molybdopterin guanine dinucleotide)molybdenum cofactor in Rhodobacter sphaeroides dimethyl sulfoxide reductase. J Biol Chem 275:40202–40210. [PubMed][CrossRef]
110. Rizzi M, Schindelin H. 2002. Structural biology of enzymes involved in NAD and molybdenum cofactor biosynthesis. Curr Opin Struct Biol 12:709–720. [PubMed][CrossRef]
111. Lake MW, Temple CA, Rajagopalan KV, Schindelin H. 2000. The crystal structure of the Escherichia coli MobA protein provides insight into molybdopterin guanine dinucleotide biosynthesis. J Biol Chem 275:40211–40217. [PubMed][CrossRef]
112. Stevenson CE, Sargent F, Buchanan G, Palmer T, Lawson DM. 2000. Crystal structure of the molybdenum cofactor biosynthesis protein MobA from Escherichia coli at near-atomic resolution. Struct Fold Des 8:1115–1125. [PubMed][CrossRef]
113. Guse A, Stevenson CE, Kuper J, Buchanan G, Schwarz G, Giordano G, Magalon A, Mendel RR, Lawson DM, Palmer T. 2003. Biochemical and structural analysis of the molybdenum cofactor biosynthesis protein MobA. J Biol Chem 278:25302–25307. [PubMed][CrossRef]
114. McLuskey K, Harrison JA, Schuttelkopf AW, Boxer DH, Hunter WN. 2003. Insight into the role of Escherichia coli MobB in molybdenum cofactor biosynthesis based on the high resolution crystal structure. J Biol Chem 278:23706–23713. [PubMed][CrossRef]
115. Neumann M, Seduk F, Iobbi-Nivol C, Leimkuhler S. 2011. 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 286:1400–1408. [PubMed][CrossRef]
116. Hille R. 1996. The mononuclear molybdenum enzymes. Chem Rev 96:2757–2816. [PubMed][CrossRef]
117. Raaijmakers H, Macieira S, Dias JM, Teixeira S, Bursakov S, Huber R, Moura JJ, Moura I, Romao MJ. 2002. Gene sequence and the 1.8 A crystal structure of the tungsten-containing formate dehydrogenase from Desulfovibrio gigas. Structure 10:1261–1272. [PubMed][CrossRef]
118. Raaijmakers HC, Romao MJ. 2006. Formate-reduced E. coli formate dehydrogenase H: the reinterpretation of the crystal structure suggests a new reaction mechanism. J Biol Inorg Chem 11:849–854. [PubMed][CrossRef]
119. Coelho C, Gonzalez PJ, Moura JG, Moura I, Trincao J, Joao Romao M. 2011. The crystal structure of Cupriavidus necator nitrate reductase in oxidized and partially reduced states. J Mol Biol 408:932–948. [PubMed][CrossRef]
120. Najmudin S, Gonzalez PJ, Trincao J, Coelho C, Mukhopadhyay A, Cerqueira NM, Romao CC, Moura I, Moura JJ, Brondino CD, Romao MJ. 2008. Periplasmic nitrate reductase revisited: a sulfur atom completes the sixth coordination of the catalytic molybdenum. J Biol Inorg Chem 13:737–753. [PubMed][CrossRef]
121. Neumann M, Schulte M, Junemann N, Stocklein W, Leimkuhler S. 2006. Rhodobacter capsulatus XdhC is involved in molybdenum cofactor binding and insertion into xanthine dehydrogenase. J Biol Chem 281:15701–15708. [PubMed][CrossRef]
122. Neumann M, Stocklein W, Walburger A, Magalon A, Leimkuhler S. 2007. 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 46:9586–9595. [PubMed][CrossRef]
123. Neumann M, Stocklein W, Leimkuhler S. 2007. Transfer of the molybdenum cofactor synthesized by Rhodobacter capsulatus MoeA to XdhC and MobA. J Biol Chem 282:28493–28500. [PubMed][CrossRef]
124. Thome R, Gust A, Toci R, Mendel R, Bittner F, Magalon A, Walburger A. 2012. A sulfurtransferase is essential for activity of formate dehydrogenases in Escherichia coli. J Biol Chem 287:4671–4678. [PubMed][CrossRef]
125. Arnoux P, Ruppelt C, Oudouhou F, Lavergne J, Siponen MI, Toci R, Mendel RR, Bittner F, Pignol D, Magalon A, Walburger A. 2015. Sulphur shuttling across a chaperone during molybdenum cofactor maturation. Nat Commun 6:6148. doi:10.1038/ncomms7148. [PubMed][CrossRef]
126. Magalon A, Fedor JG, Walburger A, Weiner JH. 2011. Molybdenum enzymes in bacteria and their maturation. Coord Chem Rev 255:1159–1178. [CrossRef]
127. Dobbek H. 2011. Structural aspects of mononuclear Mo/W enzymes. Coord Chem Rev 255:1104–1116. [CrossRef]
128. Hille R, Nishino T, Bittner F. 2011. Molybdenum enzymes in higher organisms. Coord Chem Rev 255:1179–1205. [PubMed][CrossRef]
129. Aguilar M, Kalakoutskii K, Cardenas J, Fernandez E. 1992. Direct transfer of molybdopterin cofactor to aponitrate reductase from a carrier protein in Chlamydomonas reinhardtii. FEBS Lett 307:162–163. [CrossRef]
130. Witte CP, Igeno MI, Mendel R, Schwarz G, Fernandez E. 1998. The Chlamydomonas reinhardtii MoCo carrier protein is multimeric and stabilizes molybdopterin cofactor in a molybdate charged form. FEBS Lett 431:205–209. [CrossRef]
131. Fischer K, Llamas A, Tejada-Jimenez M, Schrader N, Kuper J, Ataya FS, Galvan A, Mendel RR, Fernandez E, Schwarz G. 2006. Function and structure of the molybdenum cofactor carrier protein from Chlamydomonas reinhardtii. J Biol Chem 281:30186–30194. [PubMed][CrossRef]
132. Kruse T, Gehl C, Geisler M, Lehrke M, Ringel P, Hallier S, Hansch R, Mendel RR. 2010. Identification and biochemical characterization of molybdenum cofactor-binding proteins from Arabidopsis thaliana. J Biol Chem 285:6623–6635. [PubMed][CrossRef]
133. Vergnes A, Gouffi-Belhabich K, Blasco F, Giordano G, Magalon A. 2004. Involvement of the molybdenum cofactor biosynthetic machinery in the maturation of the Escherichia coli nitrate reductase A. J Biol Chem 279:41398–41403. [PubMed][CrossRef]
134. Turner RJ, Papish AL, Sargent F. 2004. Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can J Microbiol 50:225–238. [PubMed][CrossRef]
135. Blasco F, Pommier J, Augier V, Chippaux M, Giordano G. 1992. Involvement of the narJ or narW gene product in the formation of active nitrate reductase in Escherichia coli. Mol Microbiol 6:221–230. [PubMed][CrossRef]
136. Schlindwein C, Giordano G, Santini CL, Mandrand MA. 1990. Identification and expression of the Escherichia coli fdhD and fdhE genes, which are involved in the formation of respiratory formate dehydrogenase. J Bacteriol 172:6112–6121. [PubMed]
137. Schlindwein C, Mandrand MA. 1991. Nucleotide sequence of the fdhE gene involved in respiratory formate dehydrogenase formation in Escherichia coli K-12. Gene 97:147–148. [PubMed][CrossRef]
138. Pommier J, Mejean V, Giordano G, Iobbi-Nivol C. 1998. TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine N-oxide reductase enzyme (TorA) in Escherichia coli. J Biol Chem 273:16615–16620. [PubMed][CrossRef]
139. Shaw AL, Leimkuhler S, Klipp W, Hanson GR, McEwan AG. 1999. Mutational analysis of the dimethylsulfoxide respiratory (dor) operon of Rhodobacter capsulatus. Microbiology 145(Pt 6):1409–1420. [PubMed][CrossRef]
140. Oresnik IJ, Ladner CL, Turner RJ. 2001. Identification of a twin-arginine leader-binding protein. Mol Microbiol 40:323–331. [PubMed][CrossRef]
141. Ray N, Oates J, Turner RJ, Robinson C. 2003. 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 534:156–160. [PubMed][CrossRef]
142. Liu HP, Takio S, Satoh T, Yamamoto I. 1999. Involvement in denitrification of the napKEFDABC genes encoding the periplasmic nitrate reductase system in the denitrifying phototrophic bacterium Rhodobacter sphaeroides f. sp. denitrificans. Biosci Biotechnol Biochem 63:530–536. [PubMed][CrossRef]
143. Potter LC, Cole JA. 1999. Essential roles for the products of the napABCD genes, but not napFGH, in periplasmic nitrate reduction by Escherichia coli K-12. Biochem J 344(Pt 1):69–76. [PubMed][CrossRef]
144. Kern M, Mager AM, Simon J. 2007. Role of individual nap gene cluster products in NapC-independent nitrate respiration of Wolinella succinogenes. Microbiology 153:3739–3747. [PubMed][CrossRef]
145. Coulthurst SJ, Dawson A, Hunter WN, Sargent F. 2012. Conserved signal peptide recognition systems across the prokaryotic domains. Biochemistry 51:1678–1686. [PubMed][CrossRef]
146. Leimkuhler S, Klipp W. 1999. Role of XDHC in Molybdenum cofactor insertion into xanthine dehydrogenase of Rhodobacter capsulatus. J Bacteriol 181:2745–2751. [PubMed]
147. Unden G, Dünnwald P. 2008. The Aerobic and anaerobic respiratory chain of Escherichia coli and Salmonella enterica: enzymes and energetics. In Curtiss RI, Kaper JB, Squires CL, Karp PD, Neidhardt FC, Slauch JM (ed), EcoSal. ASM Press, Washington, DC. [CrossRef]
148. Price CE, Driessen AJ. 2008. YidC is involved in the biogenesis of anaerobic respiratory complexes in the inner membrane of Escherichia coli. J Biol Chem 283:26921–26927. [PubMed][CrossRef]
149. Sargent F. 2007. The twin-arginine transport system: moving folded proteins across membranes. Biochem Soc Trans 35:835–847. [PubMed][CrossRef]
150. Li H, Chang L, Howell JM, Turner RJ. 2010. DmsD, a Tat system specific chaperone, interacts with other general chaperones and proteins involved in the molybdenum cofactor biosynthesis. Biochim Biophys Acta 1804:1301–1309. [PubMed][CrossRef]
151. Matos CF, Robinson C, Di Cola A. 2008. The Tat system proofreads FeS protein substrates and directly initiates the disposal of rejected molecules. EMBO J 27:2055–2063. [PubMed][CrossRef]
152. Matos CF, Di Cola A, Robinson C. 2009. TatD is a central component of a Tat translocon-initiated quality control system for exported FeS proteins in Escherichia coli. EMBO Rep 10:474–479. [PubMed][CrossRef]
153. Lindenstrauss U, Matos CF, Graubner W, Robinson C, Bruser T. 2010. Malfolded recombinant Tat substrates are Tat-independently degraded in Escherichia coli. FEBS Lett 584:3644–3648. [PubMed][CrossRef]
154. Tranier S, Iobbi-Nivol C, Birck C, Ilbert M, Mortier-Barriere I, Mejean V, Samama JP. 2003. A novel protein fold and extreme domain swapping in the dimeric TorD chaperone from Shewanella massilia. Structure (Camb) 11:165–174. [PubMed][CrossRef]
155. Kirillova O, Chruszcz M, Shumilin IA, Skarina T, Gorodichtchenskaia E, Cymborowski M, Savchenko A, Edwards A, Minor W. 2007. 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 63:348–354. [PubMed][CrossRef]
156. Qiu Y, Zhang R, Binkowski TA, Tereshko V, Joachimiak A, Kossiakoff A. 2008. The 1.38 A crystal structure of DmsD protein from Salmonella typhimurium, a proofreading chaperone on the Tat pathway. Proteins 71:525–533. [PubMed][CrossRef]
157. Ramasamy SK, Clemons WM, Jr. 2009. Structure of the twin-arginine signal-binding protein DmsD from Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:746–750. [PubMed][CrossRef]
158. Stevens CM, Winstone TM, Turner RJ, Paetzel M. 2009. Structural analysis of a monomeric form of the twin-arginine leader peptide binding chaperone Escherichia coli DmsD. J Mol Biol 389:124–133. [PubMed][CrossRef]
159. Bertero MG, Rothery RA, Palak M, Hou C, Lim D, Blasco F, Weiner JH, Strynadka NC. 2003. Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat Struct Biol 10:681–687. [PubMed][CrossRef]
160. Jormakka M, Richardson D, Byrne B, Iwata S. 2004. Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes. Structure (Camb) 12:95–104. [PubMed][CrossRef]
161. Dubourdieu M, DeMoss JA. 1992. The narJ gene product is required for biogenesis of respiratory nitrate reductase in Escherichia coli. J Bacteriol 174:867–872. [PubMed]
162. Liu X, DeMoss JA. 1997. Characterization of NarJ, a system-specific chaperone required for nitrate reductase biogenesis in Escherichia coli. J Biol Chem 272:24266–24271. [PubMed][CrossRef]
163. Blasco F, Nunzi F, Pommier J, Brasseur R, Chippaux M, Giordano G. 1992. Formation of active heterologous nitrate reductases between nitrate reductases A and Z of Escherichia coli. Mol Microbiol 6:209–219. [PubMed][CrossRef]
164. Lanciano P, Vergnes A, Grimaldi S, Guigliarelli B, Magalon A. 2007. Biogenesis of a respiratory complex is orchestrated by a single accessory protein. J Biol Chem 282:17468–17474. [PubMed][CrossRef]
165. Zakian S, Lafitte D, Vergnes A, Pimentel C, Sebban-Kreuzer C, Toci R, Claude JB, Guerlesquin F, Magalon A. 2010. Basis of recognition between the NarJ chaperone and the N-terminus of the NarG subunit from Escherichia coli nitrate reductase. FEBS J 277:1886–1895. [PubMed][CrossRef]
166. Lorenzi M, Sylvi L, Gerbaud G, Mileo E, Halgand F, Walburger A, Vezin H, Belle V, Guigliarelli B, Magalon A. 2012. Conformational selection underlies recognition of a molybdoenzyme by its dedicated chaperone. PLoS One 7:e49523. doi:10.1371/journal.pone.0049523 [PubMed][CrossRef]
167. Vergnes A, Pommier J, Toci R, Blasco F, Giordano G, Magalon A. 2006. NarJ chaperone binds on two distinct sites of the aponitrate reductase of Escherichia coli to coordinate molybdenum cofactor insertion and assembly. J Biol Chem 281:2170–2176. [PubMed][CrossRef]
168. Jack RL, Buchanan G, Dubini A, Hatzixanthis K, Palmer T, Sargent F. 2004. Coordinating assembly and export of complex bacterial proteins. EMBO J 23:3962–3972. [PubMed][CrossRef]
169. Ize B, Coulthurst SJ, Hatzixanthis K, Caldelari I, Buchanan G, Barclay EC, Richardson DJ, Palmer T, Sargent F. 2009. Remnant signal peptides on non-exported enzymes: implications for the evolution of prokaryotic respiratory chains. Microbiology 155:3992–4004. [PubMed][CrossRef]
170. Rothery RA, Bertero MG, Spreter T, Bouromand N, Strynadka NC, Weiner JH. 2010. Protein crystallography reveals a Role for the FS0 cluster of Escherichia coli nitrate reductase A (NarGHI) in enzyme maturation. J Biol Chem 285:8801–8807. [PubMed][CrossRef]
171. Winstone TL, Workentine ML, Sarfo KJ, Binding AJ, Haslam BD, Turner RJ. 2006. Physical nature of signal peptide binding to DmsD. Arch Biochem Biophys 455:89–97. [PubMed][CrossRef]
172. Guymer D, Maillard J, Agacan MF, Brearley CA, Sargent F. 2010. Intrinsic GTPase activity of a bacterial twin-arginine translocation proofreading chaperone induced by domain swapping. FEBS J 277:511–525. [PubMed][CrossRef]
173. Tzeng SR, Kalodimos CG. 2011. Protein dynamics and allostery: an NMR view. Curr Opin Struct Biol 21:62–67. [PubMed][CrossRef]
174. Blasco F, Dos Santos JP, Magalon A, Frixon C, Guigliarelli B, Santini CL, Giordano G. 1998. NarJ is a specific chaperone required for molybdenum cofactor assembly in nitrate reductase A of Escherichia coli. Mol Microbiol 28:435–447. [PubMed][CrossRef]
175. Rothery RA, Bertero MG, Cammack R, Palak M, Blasco F, Strynadka NC, Weiner JH. 2004. The Catalytic subunit of Escherichia coli nitrate reductase a contains a novel [4Fe-4S] cluster with a high-spin ground state. Biochemistry 43:5324–5333. [PubMed][CrossRef]
176. Hanzelmann P, Dobbek H, Gremer L, Huber R, Meyer O. 2000. The effect of intracellular molybdenum in Hydrogenophaga pseudoflava on the crystallographic structure of the seleno-molybdo-iron-sulfur flavoenzyme carbon monoxide dehydrogenase. J Mol Biol 301:1221–1235. [PubMed][CrossRef]
177. Weiner JH, Bilous PT, Shaw GM, Lubitz SP, Frost L, Thomas GH, Cole JA, Turner RJ. 1998. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93:93–101. [PubMed][CrossRef]
178. Guymer D, Maillard J, Sargent F. 2009. A genetic analysis of in vivo selenate reduction by Salmonella enterica serovar Typhimurium LT2 and Escherichia coli K12. Arch Microbiol 191:519–528. [PubMed][CrossRef]
179. Papish AL, Ladner CL, Turner RJ. 2003. The twin-arginine leader-binding protein, DmsD, interacts with the TatB and TatC subunits of the Escherichia coli twin-arginine translocase. J Biol Chem 278:32501–32506. [PubMed][CrossRef]
180. Kostecki JS, Li H, Turner RJ, DeLisa MP. 2010. Visualizing interactions along the Escherichia coli twin-arginine translocation pathway using protein fragment complementation. PLoS One 5:e9225. doi:10.1371/journal.pone.0009225. [CrossRef]
181. Chan CS, Winstone TM, Chang L, Stevens CM, Workentine ML, Li H, Wei Y, Ondrechen MJ, Paetzel M, Turner RJ. 2008. Identification of residues in DmsD for twin-arginine leader peptide binding, defined through random and bioinformatics-directed mutagenesis. Biochemistry. 47:2749–2759. [PubMed][CrossRef]
182. Hatzixanthis K, Clarke TA, Oubrie A, Richardson DJ, Turner RJ, Sargent F. 2005. Signal peptide-chaperone interactions on the twin-arginine protein transport pathway. Proc Natl Acad Sci USA 102:8460–8465. [PubMed][CrossRef]
183. Sambasivarao D, Turner RJ, Simala-Grant JL, Shaw G, Hu J, Weiner JH. 2000. Multiple roles for the twin arginine leader sequence of dimethyl sulfoxide reductase of Escherichia coli. J Biol Chem 275:22526–22531. [PubMed][CrossRef]
184. Tang H, Rothery RA, Voss JE, Weiner JH. 2011. Correct assembly of iron-sulfur cluster FS0 into Escherichia coli dimethyl sulfoxide reductase (DmsABC) is a prerequisite for molybdenum cofactor insertion. J Biol Chem 286:15147–15154. [PubMed][CrossRef]
185. Schroder I, Rech S, Krafft T, Macy JM. 1997. Purification and characterization of the selenate reductase from Thauera selenatis. J Biol Chem 272:23765–23768. [PubMed][CrossRef]
186. Martinez-Espinosa RM, Dridge EJ, Bonete MJ, Butt JN, Butler CS, Sargent F, Richardson DJ. 2007. Look on the positive side! The orientation, identification and bioenergetics of ‘Archaeal’ membrane-bound nitrate reductases. FEMS Microbiol Lett 276:129–139. [PubMed][CrossRef]
187. Thorell HD, Stenklo K, Karlsson J, Nilsson T. 2003. A gene cluster for chlorate metabolism in Ideonella dechloratans. Appl Environ Microbiol 69:5585–5592. [PubMed][CrossRef]
188. Bender KS, Shang C, Chakraborty R, Belchik SM, Coates JD, Achenbach LA. 2005. Identification, characterization, and classification of genes encoding perchlorate reductase. J Bacteriol 187:5090–5096. [PubMed][CrossRef]
189. Kniemeyer O, Heider J. 2001. Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 276:21381–21386. [PubMed][CrossRef]
190. McDevitt CA, Hugenholtz P, Hanson GR, McEwan AG. 2002. Molecular analysis of dimethyl sulphide dehydrogenase from Rhodovulum sulfidophilum: its place in the dimethyl sulphoxide reductase family of microbial molybdopterin-containing enzymes. Mol Microbiol 44:1575–1587. [PubMed][CrossRef]
191. Stolz JF, Basu P, Santini JM, Oremland RS. 2006. Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60:107–130. [PubMed][CrossRef]
192. Duval S, Ducluzeau AL, Nitschke W, Schoepp-Cothenet B. 2008. Enzyme phylogenies as markers for the oxidation state of the environment: the case of respiratory arsenate reductase and related enzymes. BMC Evol Biol 8:206. [PubMed][CrossRef]
193. Jormakka M, Tornroth S, Byrne B, Iwata S. 2002. Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295:1863–1868. [PubMed][CrossRef]
194. Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD. 1997. Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science 275:1305–1308. [PubMed][CrossRef]
195. Mandrand-Berthelot MA, Couchoux-Luthaud G, Santini CL, Giordano G. 1988. Mutants of Escherichia coli specifically deficient in respiratory formate dehydrogenase activity. J Gen Microbiol 134:3129–3139. [PubMed][CrossRef]
196. Stewart V, Lin JT, Berg BL. 1991. Genetic evidence that genes fdhD and fdhE do not control synthesis of formate dehydrogenase-N in Escherichia coli K-12. J Bacteriol 173:4417–4423. [PubMed]
197. Pommier J, Mandrand MA, Holt SE, Boxer DH, Giordano G. 1992. A second phenazine methosulphate-linked formate dehydrogenase isoenzyme in Escherichia coli. Biochim Biophys Acta 1107:305–313. [PubMed][CrossRef]
198. Luke I, Butland G, Moore K, Buchanan G, Lyall V, Fairhurst SA, Greenblatt JF, Emili A, Palmer T, Sargent F. 2008. Biosynthesis of the respiratory formate dehydrogenases from Escherichia coli: characterization of the FdhE protein. Arch Microbiol 190:685–696. [PubMed][CrossRef]
199. Maillard J, Spronk CA, Buchanan G, Lyall V, Richardson DJ, Palmer T, Vuister GW, Sargent F. 2007. Structural diversity in twin-arginine signal peptide-binding proteins. Proc Natl Acad Sci USA 104:15641–15646. [CrossRef]
200. Grahl S, Maillard J, Spronk CA, Vuister GW, Sargent F. 2012. Overlapping transport and chaperone-binding functions within a bacterial twin-arginine signal peptide. Mol Microbiol 83:1254–1267. [PubMed][CrossRef]
201. Nilavongse A, Brondijk TH, Overton TW, Richardson DJ, Leach ER, Cole JA. 2006. The NapF protein of the Escherichia coli periplasmic nitrate reductase system: demonstration of a cytoplasmic location and interaction with the catalytic subunit, NapA. Microbiology 152:3227–3237. [PubMed][CrossRef]
202. Olmo-Mira MF, Gavira M, Richardson DJ, Castillo F, Moreno-Vivian C, Roldan MD. 2004. NapF is a cytoplasmic iron-sulfur protein required for Fe-S cluster assembly in the periplasmic nitrate reductase. J Biol Chem 279:49727–49735. [PubMed][CrossRef]
203. Kern M, Simon J. 2009. Periplasmic nitrate reduction in Wolinella succinogenes: cytoplasmic NapF facilitates NapA maturation and requires the menaquinol dehydrogenase NapH for membrane attachment. Microbiology 155:2784–2794. [PubMed][CrossRef]
204. Arnoux P, Sabaty M, Alric J, Frangioni B, Guigliarelli B, Adriano JM, Pignol D. 2003. Structural and redox plasticity in the heterodimeric periplasmic nitrate reductase. Nat Struct Biol 10:928–934. [PubMed][CrossRef]
205. Jepson BJ, Mohan S, Clarke TA, Gates AJ, Cole JA, Butler CS, Butt JN, Hemmings AM, Richardson DJ. 2007. Spectropotentiometric and structural analysis of the periplasmic nitrate reductase from Escherichia coli. J Biol Chem 282:6425–6437. [PubMed][CrossRef]
206. Bittner F, Oreb M, Mendel RR. 2001. ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana. J Biol Chem 276:40381–40384. [PubMed][CrossRef]
207. Heidenreich T, Wollers S, Mendel RR, Bittner F. 2005. Characterization of the NifS-like domain of ABA3 from Arabidopsis thaliana provides insight into the mechanism of molybdenum cofactor sulfuration. J Biol Chem 280:4213–4218. [PubMed][CrossRef]
208. Wollers S, Heidenreich T, Zarepour M, Zachmann D, Kraft C, Zhao Y, Mendel RR, Bittner F. 2008. Binding of sulfurated molybdenum cofactor to the C-terminal domain of ABA3 from Arabidopsis thaliana provides insight into the mechanism of molybdenum cofactor sulfuration. J Biol Chem 283:9642–9650. [PubMed][CrossRef]
209. Mejean V, Iobbi-Nivol C, Lepelletier M, Giordano G, Chippaux M, Pascal MC. 1994. TMAO anaerobic respiration in Escherichia coli: involvement of the tor operon. Mol Microbiol 11:1169–1179. [PubMed][CrossRef]
210. Silvestro A, Pommier J, Pascal MC, Giordano G. 1989. The inducible trimethylamine N-oxide reductase of Escherichia coli K12: its localization and inducers. Biochim Biophys Acta 999:208–216. [PubMed][CrossRef]
211. Czjzek M, Dos Santos JP, Pommier J, Giordano G, Mejean V, Haser R. 1998. Crystal structure of oxidized trimethylamine N-oxide reductase from Shewanella massilia at 2.5 A resolution. J Mol Biol 284:435–447. [PubMed][CrossRef]
212. Tranier S, Mortier-Barriere I, Ilbert M, Birck C, Iobbi-Nivol C, Mejean V, Samama JP. 2002. Characterization and multiple molecular forms of TorD from Shewanella massilia, the putative chaperone of the molybdoenzyme TorA. Protein Sci 11:2148–2157. [PubMed][CrossRef]
213. Genest O, Ilbert M, Mejean V, Iobbi-Nivol C. 2005. TorD, an essential chaperone for TorA molybdoenzyme maturation at high temperature. J Biol Chem 280:15644–15648. [PubMed][CrossRef]
214. Genest O, Neumann M, Seduk F, Stocklein W, Mejean V, Leimkuhler S, Iobbi-Nivol C. 2008. Dedicated metallochaperone connects apoenzyme and molybdenum cofactor biosynthesis components. J Biol Chem 283:21433–21440. [PubMed][CrossRef]
215. Genest O, Seduk F, Theraulaz L, Mejean V, Iobbi-Nivol C. 2006. Chaperone protection of immature molybdoenzyme during molybdenum cofactor limitation. FEMS Microbiol Lett 265:51–55. [PubMed][CrossRef]
216. Ilbert M, Mejean V, Giudici-Orticoni MT, Samama JP, Iobbi-Nivol C. 2003. Involvement of a mate chaperone (TorD) in the maturation pathway of molybdoenzyme TorA. J Biol Chem 278:28787–28792. [PubMed][CrossRef]
217. Ilbert M, Mejean V, Iobbi-Nivol C. 2004. Functional and structural analysis of members of the TorD family, a large chaperone family dedicated to molybdoproteins. Microbiology 150:935–943. [PubMed][CrossRef]
218. Dow JM, Gabel F, Sargent F, Palmer T. 2013. Characterization of a pre-export enzyme-chaperone complex on the twin-arginine transport pathway. Biochem J 452:57–66. [PubMed]
219. Leimkuhler S, Kern M, Solomon PS, McEwan AG, Schwarz G, Mendel RR, Klipp W. 1998. Xanthine dehydrogenase from the phototrophic purple bacterium Rhodobacter capsulatus is more similar to its eukaryotic counterparts than to prokaryotic molybdenum enzymes. Mol Microbiol 27:853–869. [PubMed][CrossRef]
220. Truglio JJ, Theis K, Leimkuhler S, Rappa R, Rajagopalan KV, Kisker C. 2002. Crystal structures of the active and alloxanthine-inhibited forms of xanthine dehydrogenase from Rhodobacter capsulatus. Structure (Camb) 10:115–125. [CrossRef]
221. Schumann S, Saggu M, Moller N, Anker SD, Lendzian F, Hildebrandt P, Leimkuhler S. 2008. The mechanism of assembly and cofactor insertion into Rhodobacter capsulatus xanthine dehydrogenase. J Biol Chem 283:16602–16611. [PubMed][CrossRef]
222. Xiang S, Nichols J, Rajagopalan KV, Schindelin H. 2001. The crystal structure of Escherichia coli MoeA and its relationship to the multifunctional protein gephyrin. Structure (Camb) 9:299–310. [CrossRef]
223. DeLano WL. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0006-2013
2015-06-15
2017-06-24

Abstract:

The transition element molybdenum (Mo) is of primordial importance for biological systems, because it is required by enzymes catalyzing key reactions in the global carbon, sulfur, and nitrogen metabolism. To gain biological activity, Mo has to be complexed by a special cofactor. With the exception of bacterial nitrogenase, all Mo-dependent enzymes contain a unique pyranopterin-based cofactor coordinating a Mo atom at their catalytic site. Various types of reactions are catalyzed by Mo-enzymes in prokaryotes including oxygen atom transfer, sulfur or proton transfer, hydroxylation, or even nonredox reactions. Mo-enzymes are widespread in prokaryotes and many of them were likely present in the Last Universal Common Ancestor. To date, more than 50 – mostly bacterial – Mo-enzymes are described in nature. In a few eubacteria and in many archaea, Mo is replaced by tungsten bound to the same unique pyranopterin. How Mo-cofactor is synthesized in bacteria is reviewed as well as the way until its insertion into apo-Mo-enzymes.

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Figures

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Figure 1

Shown are the known biosynthetic intermediates dividing the whole pathway into four steps and giving rise to the different forms of cofactor found in the three distinct Mo-enzyme families: the Mo/W-PGD family, the sulfite oxidase family, and the xanthine oxidase family. Ribbon representation of the crystal structures of the Moco biosynthetic proteins are shown: MoaA ( 56 ), MoaC ( 58 ), MoaD-MoaE complex ( 63 ), MoeB-MoaD complex ( 68 ), MogA ( 91 ), MoeA ( 222 ), MobA ( 111 , 112 ), and MobB ( 114 ). Individual figures were generated with PYMOL ( 223 ) using the deposited coordinates from the protein structure data base. doi:10.1128/ecosalplus.ESP-0006-2013.f1

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 2

See the text for a detailed description of the reaction mechanism leading to the two-step conversion of cPMP to PPT. doi:10.1128/ecosalplus.ESP-0006-2013.f2

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 3

See the text for a description of the reaction mechanism leading to MPT adenylylation. doi:10.1128/ecosalplus.ESP-0006-2013.f3

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 4

See the text for description of the reaction mechanism leading to Mo addition and of the different postulated pathways for the nucleotide addition step leading to the Mo-PGD molecule. doi:10.1128/ecosalplus.ESP-0006-2013.f4

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 5

The arrows represent the interactions as detected by using bacterial two-hybrid methodology, TAP-Tag, or biochemical assays (see the text for details and references). doi:10.1128/ecosalplus.ESP-0006-2013.f5

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 6

Identity percentages are indicated by using proteins as reference. doi:10.1128/ecosalplus.ESP-0006-2013.f6

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 7

(A) NarJ-like from (PDB ID code 2o9x). (B) DmsD from (PDB ID code 3efp). (C) TorD monomer from (PDB ID code 1n1c). (D) NapD from (PDB ID code 2jsx). (E) FdhD dimer from in complex with GDP (PDB ID code 4PDE). (F) FdhE from (PDB ID code 2fiy). NarJ-like, DmsD, and TorD belong to the Pfam PF02613 family. Individual figures were generated with PYMOL ( 223 ) by using the deposited coordinates from the protein structure database. The proteins are represented in cartoon with α-helices colored in red and β-sheets colored in yellow. Two GDPs are cocrystallized with FdhD, while two iron atoms are coordinated by FdhE (represented by green spheres). doi:10.1128/ecosalplus.ESP-0006-2013.f7

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 8

The NarGHI complex is surface-represented (PDB ID code 1q16) and represented as a homodimer. NarG is colored in pink and in green, NarH in yellow and in cyan, and NarI in gray and fuchsia. The cytoplasmic membrane is represented as two ellipses, one colored in red at the interface with the periplasm and the other one colored in blue at the interface with the cytoplasm. Metal centers are shown on the left. The Mo-PGD is buried in NarG close to the [Fe-S] cluster (FS0). NarH harbors 4 [Fe-S] clusters: FS1, FS2, FS3, and FS4. NarI harbors two -type hemes: b (P as proximal) and b (D as distal). doi:10.1128/ecosalplus.ESP-0006-2013.f8

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Figure 9

NarG and NarH constitute the catalytic dimer, while NarI is the -type membrane anchor subunit of the complex. NarI maturation takes place in the inner membrane where the two -type and hemes are sequentially inserted. Concomitantly, the apoNarGH complex retained by the enzyme-specific chaperone NarJ in the cytoplasm is maturated. First, [Fe-S] clusters are inserted in the NarH subunit through the action of one of the [Fe-S] biosynthetic machineries. Second, both Moco and its proximal [Fe-S] cluster, FS0, are inserted in the catalytic subunit NarG in a NarJ-dependent manner. On complete maturation of the NarGH complex, NarJ dissociates, allowing membrane anchoring of the NarGH dimer. TorA constitutes the catalytic subunit of the TMAO reductase system and harbors a twin-arginine signal peptide at the N terminus. Early interaction of the enzyme-specific chaperone TorD on apoTorA facilitates Moco insertion. Subsequently, mature TorA is exported to the periplasm through the Tat translocase. TorC, a pentahemic membrane-bound cytochrome , constitutes the electron donor to TorA. Whatever the considered system, Moco insertion proceeds as the action of a multiprotein complex of Moco biosynthetic proteins and chaperones ( 70 , 125 ). doi:10.1128/ecosalplus.ESP-0006-2013.f9

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013
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Tables

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Table 1

Genetic and biochemical characteristics of the proteins involved in Moco biosynthesis in

Citation: Magalon A, Mendel R. 2015. Biosynthesis and Insertion of the Molybdenum Cofactor, EcoSal Plus 2015; doi:10.1128/ecosalplus.ESP-0006-2013

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