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Biochemistry Research International
Volume 2011, Article ID 850924, 13 pages
http://dx.doi.org/10.1155/2011/850924
Review Article

The Role of System-Specific Molecular Chaperones in the Maturation of Molybdoenzymes in Bacteria

Department of Molecular Enzymology, Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany

Received 30 June 2010; Accepted 31 August 2010

Academic Editor: Emil Pai

Copyright © 2011 Meina Neumann and Silke Leimkühler. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Hille, “The mononuclear molybdenum enzymes,” Chemical Reviews, vol. 96, no. 7, pp. 2757–2816, 1996. View at Google Scholar · View at Scopus
  2. K. V. Rajagopalan and J. L. Johnson, “The pterin molybdenum cofactors,” Journal of Biological Chemistry, vol. 267, no. 15, pp. 10199–10202, 1992. View at Google Scholar · View at Scopus
  3. G. Schwarz, “Molybdenum cofactor biosynthesis and deficiency,” Cellular and Molecular Life Sciences, vol. 62, no. 23, pp. 2792–2810, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Hille, “Molybdenum-containing hydroxylases,” Archives of Biochemistry and Biophysics, vol. 433, no. 1, pp. 107–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. M. J. Romão, M. Archer, I. Moura et al., “Crystal structure of the xanthine oxidase-related aldehyde oxido-reductase from D. gigas,” Science, vol. 270, no. 5239, pp. 1170–1176, 1995. View at Google Scholar · View at Scopus
  6. J. Rebelo, S. Macieira, J. M. Dias et al., “Gene sequence and crystal structure of the aldehyde oxidoreductase from Desulfovibrio desulfuricans ATCC 27774,” Journal of Molecular Biology, vol. 297, no. 1, pp. 135–146, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Enroth, B. T. Eger, K. Okamoto, T. Nishino, T. Nishino, and E. F. Pai, “Crystal structures of bovinemilk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 20, pp. 10723–10728, 2000. View at Google Scholar
  8. J. J. Truglio, K. Theis, S. Leimkühler, R. Rappa, K. V. Rajagopalan, and C. Kisker, “Crystal structures of the active and alloxanthine-inhibited forms of xanthine dehydrogenase from Rhodobacter capsulatus,” Structure, vol. 10, no. 1, pp. 115–125, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. I. Bonin, B. M. Martins, V. Purvanov, S. Fetzner, R. Huber, and H. Dobbek, “Active site geometry and substrate recognition of the molybdenum hydroxylase quinoline 2-oxidoreductase,” Structure, vol. 12, no. 8, pp. 1425–1435, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Unciuleac, E. Warkentin, C. C. Page, M. Boll, and U. Ermler, “Structure of a xanthine oxidase-related 4-hydroxybenzoyl-CoA reductase with an additional [4Fe-4S] cluster and an inverted electron flow,” Structure, vol. 12, no. 12, pp. 2249–2256, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. H. Dobbek, L. Gremer, O. Meyer, and R. Huber, “Crystal structure and mechanism of CO dehydrogenase, a molybdo iron-sulfur flavoprotein containing S-selanylcysteine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 16, pp. 8884–8889, 1999. View at Google Scholar · View at Scopus
  12. P. Hänzelmann, H. Dobbek, L. Gremer, R. Huber, and O. Meyer, “The effect of intracellular molybdenum in Hydrogenophaga pseudoflava on the crystallographic structure of the seleno-molybdo-iron-sulfur flavoenzyme carbon monoxide dehydrogenase,” Journal of Molecular Biology, vol. 301, no. 5, pp. 1221–1235, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. C. D. Brondino, M. J. Romão, I. Moura, and J. J. G. Moura, “Molybdenum and tungsten enzymes: the xanthine oxidase family,” Current Opinion in Chemical Biology, vol. 10, no. 2, pp. 109–114, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Garattini, R. Mendel, M. J. Romão, R. Wright, and M. Terao, “Mammalian molybdo-flavoenzymes, an expanding family of proteins: structure, genetics, regulation, function and pathophysiology,” Biochemical Journal, vol. 372, no. 1, pp. 15–32, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Dobbek, L. Gremer, R. Kiefersauer, R. Huber, and O. Meyer, “Catalysis at a dinuclear [CuSMo(=O)OH] cluster in a CO dehydrogenase resolved at 1.1-Å resolution,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 25, pp. 15971–15976, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Garattini, M. Fratelli, and M. Terao, “Mammalian aldehyde oxidases: genetics, evolution and biochemistry,” Cellular and Molecular Life Sciences, vol. 65, no. 7-8, pp. 1019–1048, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Nishino, “The conversion of xanthine dehydrogenase to xanthine oxidase and the role of the enzyme in reperfusion injury,” Journal of Biochemistry, vol. 116, no. 1, pp. 1–6, 1994. View at Google Scholar · View at Scopus
  18. T. Nishino, K. Okamoto, Y. Kawaguchi et al., “Mechanism of the conversion of xanthine dehydrogenase to xanthine oxidase: identification of the two cysteine disulfide bonds and crystal structure of a non-convertible rat liver xanthine dehydrogenase mutant,” Journal of Biological Chemistry, vol. 280, no. 26, pp. 24888–24894, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Leimkühler, M. Kern, P. S. Solomon et al., “Xanthine dehydrogenase from the phototrophic purple bacterium Rhodobacter capsulatus is more similar to its eukaryotic counterparts than to prokaryotic molybdenum enzymes,” Molecular Microbiology, vol. 27, no. 4, pp. 853–869, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Neumann, G. Mittelstädt, C. Iobbi-Nivol et al., “A periplasmic aldehyde oxidoreductase represents the first molybdopterin cytosine dinucleotide cofactor containing molybdo-flavoenzyme from Escherichia coli,” FEBS Journal, vol. 276, no. 10, pp. 2762–2774, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Kisker, H. Schindelin, and D. C. Rees, “Molybdenum-cofactor-containing enzymes: structure and mechanism,” Annual Review of Biochemistry, vol. 66, pp. 233–267, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Leimkühler and W. Klipp, “Role of XDHC in molybdenum cofactor insertion into xanthine dehydrogenase of Rhodobacter capsulatus,” Journal of Bacteriology, vol. 181, no. 9, pp. 2745–2751, 1999. View at Google Scholar · View at Scopus
  23. F. Blasco, J.-P. Dos Santos, A. Magalon et al., “NarJ is a specific chaperone required for molybdenum cofactor assembly in nitrate reductase A of Escherichia coli,” Molecular Microbiology, vol. 28, no. 3, pp. 435–447, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Ilbert, V. Méjean, M.-T. Giudici-Orticoni, J.-P. Samama, and C. Iobbi-Nivol, “Involvement of a mate chaperone (TorD) in the maturation pathway of molybdoenzyme TorA,” Journal of Biological Chemistry, vol. 278, no. 31, pp. 28787–28792, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Tranier, C. Iobbi-Nivol, C. Birck et al., “A novel protein fold and extreme domain swapping in the dimeric TorD chaperone from Shewanella massilia,” Structure, vol. 11, no. 2, pp. 165–174, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. O. Genest, V. Méjean, and C. Iobbi-Nivol, “Multiple roles of TorD-like chaperones in the biogenesis of molybdoenzymes,” FEMS Microbiology Letters, vol. 297, no. 1, pp. 1–9, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Santiago, U. Schübel, C. Egelseer, and O. Meyer, “Sequence analysis, characterization and CO-specific transcription of the cox gene cluster on the megaplasmid pHCG3 of Oligotropha carboxidovorans,” Gene, vol. 236, no. 1, pp. 115–124, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Neumann, M. Schulte, N. Jünemann, W. Stöcklein, and S. Leimkühler, “Rhodobacter capsulatus XdhC is involved in molybdenum cofactor binding and insertion into xanthine dehydrogenase,” Journal of Biological Chemistry, vol. 281, no. 23, pp. 15701–15708, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. N. V. Ivanov, F. Hubálek, M. Trani, and D. E. Edmondson, “Factors involved in the assembly of a functional molybdopyranopterin center in recombinant Comamonas acidovorans xanthine dehydrogenase,” European Journal of Biochemistry, vol. 270, no. 23, pp. 4744–4754, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. S. G. Kozmin and R. M. Schaaper, “Molybdenum cofactor-dependent resistance to N-hydroxylated base analogs in Escherichia coli is independent of MobA function,” Mutation Research, vol. 619, no. 1-2, pp. 9–15, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Xi, B. L. Schneider, and L. Reitzer, “Purine catabolism in Escherichia coli and function of xanthine dehydrogenase in purine salvage,” Journal of Bacteriology, vol. 182, no. 19, pp. 5332–5341, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Pelzmann, M. Ferner, M. Gnida, W. Meyer-Klaucke, and O. Meyer, “The CoxD protein of Oligotropha carboxidovorans is a predicted AAA+ ATPase chaperone involved in the biogenesis of the CO dehydrogenase [CuSMoO2] cluster,” Journal of Biological Chemistry, vol. 284, no. 14, pp. 9578–9586, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. A. C. Schultz, P. Nygaard, and H. H. Saxild, “Functional analysis of 14 genes that constitute the purine catabolic pathway in Bacillus subtilis and evidence for a novel regulon controlled by the PucR transcription activator,” Journal of Bacteriology, vol. 183, no. 11, pp. 3293–3302, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Neumann, G. Mittelstädt, F. Seduk, C. Iobbi-Nivol, and S. Leimkühler, “MocA is a specific cytidylyltransferase involved in molybdopterin cytosine dinucleotide biosynthesis in Escherichia coli,” Journal of Biological Chemistry, vol. 284, no. 33, pp. 21891–21898, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Parschat, B. Hauer, R. Kappl, R. Kraft, J. Hüttermann, and S. Fetzner, “Gene cluster of Arthrobacter ilicis Ru61a involved in the degradation of quinaldine to anthranilate. Characterization and functional expression of the quinaldine 4-oxidase qoxLMS genes,” Journal of Biological Chemistry, vol. 278, no. 30, pp. 27483–27494, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Menéndez, G. Igloi, H. Henninger, and R. Brandsch, “A pAO1-encoded molybdopterin cofactor gene (moaA) of Arthrobacter nicotinovorans: characterization and site-directed mutagenesis of the encoded protein,” Archives of Microbiology, vol. 164, no. 2, pp. 142–151, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Baitsch, C. Sandu, R. Brandsch, and G. L. Igloi, “Gene cluster on pAO1 of Arthrobacter nicotinovorans involved in degradation of the plant alkaloid nicotine: cloning, purification, and characterization of 2,6-dihydroxypyridine 3-hydroxylase,” Journal of Bacteriology, vol. 183, no. 18, pp. 5262–5267, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Fuhrmann, M. Ferner, T. Jeffke, A. Henne, G. Gottschalk, and O. Meyer, “Complete nucleotide sequence of the circular megaplasmid pHCG3 of Oligotropha carboxidovorans: function in the chemolithoautotrophic utilization of CO, H2 and CO2,” Gene, vol. 322, no. 1-2, pp. 67–75, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Leimkühler, R. Hodson, G. N. George, and K. V. Rajagopalan, “Recombinant Rhodobacter capsulatus xanthine dehydrogenase, a useful model system for the characterization of protein variants leading to xanthinuria I in humans,” Journal of Biological Chemistry, vol. 278, no. 23, pp. 20802–20811, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Leimkühler, A. L. Stockert, K. Igarashi, T. Nishino, and R. Hille, “The role of active site glutamate residues in catalysis of Rhodobacter capsulatus xanthine dehydrogenase,” Journal of Biological Chemistry, vol. 279, no. 39, pp. 40437–40444, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Palmer, A. Vasishta, P. W. Whitty, and D. H. Boxer, “Isolation of protein FA, a product of the mob locus required for molybdenum cofactor biosynthesis in Escherichia coli,” European Journal of Biochemistry, vol. 222, no. 2, pp. 687–692, 1994. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Leimkühler, S. Angermüller, G. Schwarz, R. R. Mendel, and 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,” Journal of Bacteriology, vol. 181, no. 19, pp. 5930–5939, 1999. View at Google Scholar · View at Scopus
  43. M. Neumann, W. Stöcklein, and S. Leimkühler, “Transfer of the molybdenum cofactor synthesized by Rhodobacter capsulatus MoeA to XdhC and MobA,” Journal of Biological Chemistry, vol. 282, no. 39, pp. 28493–28500, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. R. C. Wahl, C. K. Warner, V. Finnerty, and K. V. Rajagopalan, “Drosophila melanogaster ma-l mutants are defective in the sulfuration of desulfo Mo hydroxylases,” Journal of Biological Chemistry, vol. 257, no. 7, pp. 3958–3962, 1982. View at Google Scholar · View at Scopus
  45. V. Finnerty, M. McCarron, and G. B. Johnson, “Gene expression in Drosophila: post-translational modification of aldehyde oxidase and xanthine dehydrogenase,” Molecular and General Genetics, vol. 172, no. 1, pp. 37–43, 1979. View at Google Scholar · View at Scopus
  46. L. Amrani, J. Primus, A. Glatigny, L. Arcangeli, C. Scazzocchio, and V. Finnerty, “Comparison of the sequences of the Aspergillus nidulans hxB and Drosophila melanogaster ma-I genes with nifS from Azotobacter vinelandii suggests a mechanism for the insertion of the terminal sulphur atom in the molybdopterin cofactor,” Molecular Microbiology, vol. 38, no. 1, pp. 114–125, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. R. R. Mendel and F. Bittner, “Cell biology of molybdenum,” Biochimica et Biophysica Acta, vol. 1763, no. 7, pp. 621–635, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Zheng, R. H. White, V. L. Cash, and D. R. Dean, “Mechanism for the desulfurization of L-cysteine catalyzed by the NIFs gene product,” Biochemistry, vol. 33, no. 15, pp. 4714–4720, 1994. View at Google Scholar · View at Scopus
  49. T. Kurihara, H. Mihara, S.-I. Kato, T. Yoshimura, and N. Esaki, “Assembly of iron-sulfur clusters mediated by cysteine desulfurases, IscS, CsdB and CSD, from Escherichia coli,” Biochimica et Biophysica Acta, vol. 1647, no. 1-2, pp. 303–309, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Neumann, W. Stöcklein, A. Walburger, A. Magalon, and 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, vol. 46, no. 33, pp. 9586–9595, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Schumann, M. Saggu, N. Möller et al., “The mechanism of assembly and cofactor insertion into Rhodobacter capsulatus xanthine dehydrogenase,” Journal of Biological Chemistry, vol. 283, no. 24, pp. 16602–16611, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. K. V. Rajagopalan, “Biosynthesis of the molybdenum cofactor in Escherichia coli and Salmonella,” in Cellular and Molecular Biology, F. C. Neidhardt, Ed., pp. 674–679, ASM Press, Washington, DC, USA, 1996. View at Google Scholar
  53. G. Schwarz, R. R. Mendel, and M. W. Ribbe, “Molybdenum cofactors, enzymes and pathways,” Nature, vol. 460, no. 7257, pp. 839–847, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Nichols and K. V. Rajagopalan, “Escherichia coli MoeA and MogA: function in metal incorporation step of molybdenum cofactor biosynthesis,” Journal of Biological Chemistry, vol. 277, no. 28, pp. 24995–25000, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. J. D. Nichols and K. V. Rajagopalan, “In vitro molybdenum ligation to molybdopterin using purified components,” Journal of Biological Chemistry, vol. 280, no. 9, pp. 7817–7822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Palmer, C.-L. Santini, C. Iobbi-Nivol, D. J. Eaves, D. H. Boxer, and G. Giordano, “Involvement of the narJ and mob gene products in distinct steps in the biosynthesis of the molybdoenzyme nitrate reductase in Escherichia coli,” Molecular Microbiology, vol. 20, no. 4, pp. 875–884, 1996. View at Publisher · View at Google Scholar · View at Scopus
  57. V. Anantharaman and L. Aravind, “MOSC domains: ancient, predicted sulfur-carrier domains, present in diverse metal-sulfur cluster biosynthesis proteins including Molybdenum cofactor sulfurases,” FEMS Microbiology Letters, vol. 207, no. 1, pp. 55–61, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. S. G. Kozmin, P. Leroy, Y. I. Pavlov, and R. M. Schaaper, “YcbX and yiiM, two novel determinants for resistance of Escherichia coli to N-hydroxylated base analogues,” Molecular Microbiology, vol. 68, no. 1, pp. 51–65, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Bittner, M. Oreb, and R. R. Mendel, “ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana,” Journal of Biological Chemistry, vol. 276, no. 44, pp. 40381–40384, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Heidenreich, S. Wollers, R. R. Mendel, and F. Bittner, “Characterization of the NifS-like domain of ABA3 from Arabidopsis thaliana provides insight into the mechanism of molybdenum cofactor sulfuration,” Journal of Biological Chemistry, vol. 280, no. 6, pp. 4213–4218, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Wollers, T. Heidenreich, M. Zarepour et al., “Binding of sulfurated molybdenum cofactor to the C-terminal domain of ABA3 from Arabidopsis thaliana provides insight into the mechanism of molybdenum cofactor sulfuration,” Journal of Biological Chemistry, vol. 283, no. 15, pp. 9642–9650, 2008. View at Publisher · View at Google Scholar · View at Scopus