The Escherichia coli Periplasmic Aldehyde Oxidoreductase Is an Exceptional Member of the Xanthine Oxidase Family of Molybdoenzymes

ACS Chemical Biology

Volumn 11, Issue 10, 2016, Pages 2923-2935

  Correia, Márcia A S ^a   Otrelo Cardoso, Ana Rita ^a   Schwuchow, Viola ^b   Sigfridsson Clauss, Kajsa G V ^c,d   Haumann, Michael ^c   Romão, Maria João ^a   Leimkühler, Silke ^b   Santos Silva, Teresa ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b UNIVERSITY OF POTSDAM   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE OXIDOREDUCTASE; ARGININE; CYTOSINE DERIVATIVE; DINUCLEOTIDE; MOLYBDOPTERIN; UNCLASSIFIED DRUG; XANTHINE OXIDASE; ALDEHYDE DEHYDROGENASE; MOLYBDENUM;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME KINETIC ASSAY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GENE TRANSFER; MOLECULAR PHYLOGENY; NONHUMAN; PHYLUM; PRIORITY JOURNAL; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PERIPLASM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

ALDEHYDE DEHYDROGENASE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLYBDENUM; PERIPLASM; PROTEIN CONFORMATION; XANTHINE OXIDASE;

EID: 84992170557     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b00572     Document Type: Article

References (50)

1. Lawson, D. M. and Smith, B. E. (2002) Molybdenum nitrogenases: a crystallographic and mechanistic view, Metal Ions in Biological Systems, CRC Press, Boca Raton, FL, Vol 39, pp 75-119, DOI: 10.1201/9780203909331.ch3.
2. Rajagopalan, K. V. and Johnson, J. L. (1992) The pterin molybdenum cofactors J. Biol. Chem. 267, 10199-10202
3. Romão, M. J. (2009) Molybdenum and tungsten enzymes: a crystallographic and mechanistic overview Dalton Trans. 21, 4053-4068 10.1039/b821108f
4. Börner, G., Karrasch, M., and Thauer, R. K. (1991) Molybdopterin adenine dinucleotide and molybdopterin hypoxanthine dinucleotide in formylmethanofuran dehydrogenase from Methanobacterium thermoautotrophicum (Marburg) FEBS Lett. 290, 31-34 10.1016/0014-5793(91)81218-W
5. Johnson, J., Indermaur, L., and Rajagopalan, K. (1991) Molybdenum cofactor biosynthesis in Escherichia coli. Requirement of the chlB gene product for the formation of molybdopterin guanine dinucleotide J. Biol. Chem. 266, 12140-12145
6. Johnson, J. L., Bastian, N. R., and Rajagopalan, K. V. (1990) 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, 3190-3194 10.1073/pnas.87.8.3190
7. Leimkühler, S., Wuebbens, M. M., and Rajagopalan, K. V. (2011) The History of the Discovery of the Molybdenum Cofactor and Novel Aspects of its Biosynthesis in Bacteria Coord. Chem. Rev. 255, 1129-1144 10.1016/j.ccr.2010.12.003
8. Neumann, M. and Leimkühler, S. (2011) The Role of System-Specific Molecular Chaperones in the Maturation of Molybdoenzymes in Bacteria Biochem. Res. Int. 2011, 1-13 10.1155/2011/850924
9. Neumann, M., Seduk, F., Iobbi-Nivol, C., and Leimkühler, 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 10.1074/jbc.M110.155671
10. Otrelo-Cardoso, A. R., da Silva Correia, M. A., Schwuchow, V., Svergun, D. I., Romão, M. J., Leimkühler, S., and Santos-Silva, T. (2014) Structural data on the periplasmic aldehyde oxidoreductase PaoABC from Escherichia coli: SAXS and preliminary X-ray crystallography analysis Int. J. Mol. Sci. 15, 2223-2236 10.3390/ijms15022223
11. Hille, R. (1996) The Mononuclear Molybdenum Enzymes Chem. Rev. 96, 2757-2816 10.1021/cr950061t
12. Hille, R., Hall, J., and Basu, P. (2014) The mononuclear molybdenum enzymes Chem. Rev. 114, 3963-4038 10.1021/cr400443z
13. Kisker, C., Schindelin, H., and Rees, D. C. (1997) Molybdenum-cofactor-containing enzymes: structure and mechanism Annu. Rev. Biochem. 66, 233-267 10.1146/annurev.biochem.66.1.233
14. Schindelin, H., Kisker, C., Hilton, J., Rajagopalan, K. V., and Rees, D. C. (1996) Crystal structure of DMSO reductase: Redox-linked changes in molybdopterin coordination Science 272, 1615-1621 10.1126/science.272.5268.1615
15. Woolfolk, C. A. (1985) Purification and properties of a novel ferricyanide-linked xanthine dehydrogenase from Pseudomonas putida 40 J. Bacteriol. 163, 600-609
16. Xiang, Q. and Edmondson, D. E. (1996) Purification and characterization of a prokaryotic xanthine dehydrogenase from Comamonas acidovorans Biochemistry 35, 5441-5450 10.1021/bi952880d
17. Hettrich, D. and Lingens, F. (1991) Microbial metabolism of quinoline and related compounds. VIII. Xanthine dehydrogenase from a quinoline utilizing Pseudomonas putida strain Biol. Chem. Hoppe-Seyler 372, 203-211 10.1515/bchm3.1991.372.1.203
18. Neumann, M., Mittelstädt, G., Iobbi-Nivol, C., Saggu, M., Lendzian, F., Hildebrandt, P., and Leimkühler, S. (2009) A periplasmic aldehyde oxidoreductase represents the first molybdopterin cytosine dinucleotide cofactor containing molybdo-flavoenzyme from Escherichia coli FEBS J. 276, 2762-2774 10.1111/j.1742-4658.2009.07000.x
19. Enroth, C., Eger, B. T., Okamoto, K., Nishino, T., and Pai, E. F. (2000) Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion Proc. Natl. Acad. Sci. U. S. A. 97, 10723-10728 10.1073/pnas.97.20.10723
20. Truglio, J. J., Theis, K., Leimkühler, S., Rappa, R., Rajagopalan, K. V., and Kisker, C. (2002) Crystal structures of the active and alloxanthine-inhibited forms of xanthine dehydrogenase from Rhodobacter capsulatus Structure 10, 115-125 10.1016/S0969-2126(01)00697-9
21. Dobbek, H., Gremer, L., Kiefersauer, R., Huber, R., and Meyer, O. (2002) 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, 15971-15976 10.1073/pnas.212640899
22. Hänzelmann, P., Dobbek, H., Gremer, L., Huber, R., and 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 10.1006/jmbi.2000.4023
23. Bonin, I., Martins, B. M., Purvanov, V., Fetzner, S., Huber, R., and Dobbek, H. (2004) Active site geometry and substrate recognition of the molybdenum hydroxylase quinoline 2-oxidoreductase Structure 12, 1425-1435 10.1016/j.str.2004.05.014
24. Unciuleac, M., Warkentin, E., Page, C. C., Boll, M., and Ermler, U. (2004) Structure of a xanthine oxidase-related 4-hydroxybenzoyl-CoA reductase with an additional [4Fe-4S] cluster and an inverted electron flow Structure 12, 2249-2256 10.1016/j.str.2004.10.008
25. Loschi, L., Brokx, S. J., Hills, T. L., Zhang, G., Bertero, M. G., Lovering, A. L., Weiner, J. H., and Strynadka, N. C. J. (2004) Structural and biochemical identification of a novel bacterial oxidoreductase J. Biol. Chem. 279, 50391-50400 10.1074/jbc.M408876200
26. Gennaris, A., Ezraty, B., Henry, C., Agrebi, R., Vergnes, A., Oheix, E., Bos, J., Leverrier, P., Espinosa, L., Szewczyk, J., Vertommen, D., Iranzo, O., Collet, J. F., and Barras, F. (2015) Repairing oxidized proteins in the bacterial envelope using respiratory chain electrons Nature 528, 409-412 10.1038/nature15764
27. Coelho, C., Foti, A., Hartmann, T., Santos-Silva, T., Leimkühler, S., and Romão, M. J. (2015) Structural insights into xenobiotic and inhibitor binding to human aldehyde oxidase Nat. Chem. Biol. 11, 779-83 10.1038/nchembio.1895
28. Boll, M. (2005) Key enzymes in the anaerobic aromatic metabolism catalysing Birch-like reductions Biochim. Biophys. Acta, Bioenerg. 1707, 34-50 10.1016/j.bbabio.2004.01.009
29. Leimkühler, S. and Klipp, W. (1999) Role of XDHC in Molybdenum Cofactor Insertion into Xanthine Dehydrogenase of Rhodobacter capsulatus J. Bacteriol. 181, 2745-2751
30. Schumann, S., Saggu, M., Möller, N., Anker, S. D., Lendzian, F., Hildebrandt, P., and Leimkühler, S. (2008) The mechanism of assembly and cofactor insertion into Rhodobacter capsulatus xanthine dehydrogenase J. Biol. Chem. 283, 16602-16611 10.1074/jbc.M709894200
31. Dereeper, A., Audic, S., Claverie, J. M., and Blanc, G. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis BMC Evol. Biol. 10, 1-6 10.1186/1471-2148-10-8
32. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist Nucleic Acids Res. 36, W465-W469 10.1093/nar/gkn180
33. Havelius, K. G. V, Reschke, S., Horn, S., Döring, A., Niks, D., Hille, R., Schulzke, C., Leimkühler, S., and Haumann, M. (2011) Structure of the molybdenum site in YedY, a sulfite oxidase homologue from Escherichia coli Inorg. Chem. 50, 741-748 10.1021/ic101291j
34. Reschke, S., Sigfridsson, K. G., Kaufmann, P., Leidel, N., Horn, S., Gast, K., Schulzke, C., Haumann, M., and Leimkühler, S. (2013) Identification of a bis-molybdopterin intermediate in molybdenum cofactor biosynthesis in Escherichia coli J. Biol. Chem. 288, 29736-29745 10.1074/jbc.M113.497453
35. Schrapers, P., Hartmann, T., Kositzki, R., Dau, H., Reschke, S., Schulzke, C., Leimkühler, S., and Haumann, M. (2015) Sulfido and cysteine ligation changes at the molybdenum cofactor during substrate conversion by formate dehydrogenase (FDH) from Rhodobacter capsulatus Inorg. Chem. 54, 3260-3271 10.1021/ic502880y
36. Samuel, P. P., Horn, S., Döring, A., Havelius, K. G. V., Reschke, S., Leimkühler, S., Haumann, M., and Schulzke, C. (2011) A crystallographic and Mo K-Edge XAS study of molybdenum oxo bis-, mono-, and non-dithiolene complexes-First-sphere coordination geometry and noninnocence of ligands Eur Eur. J. Inorg. Chem. 2011, 4387-4399 10.1002/ejic.201100331
37. Badalyan, A., Neumann-Schaal, M., Leimkühler, S., and Wollenberger, U. (2013) A biosensor for aromatic aldehydes comprising the mediator dependent PaoABC-Aldehyde oxidoreductase Electroanalysis 25, 101-108 10.1002/elan.201200362
38. McKenna, S. M., Leimkühler, S., Herter, S., Turner, N. J., and Carnell, A. J. (2015) Enzyme cascade reactions: synthesis of furandicarboxylic acid (FDCA) and carboxylic acids using oxidases in tandem Green Chem. 17, 3271-3275 10.1039/C5GC00707K
39. Badalyan, A., Dierich, M., Stiba, K., Schwuchow, V., Leimkühler, S., and Wollenberger, U. (2014) Electrical wiring of the aldehyde oxidoreductase PaoABC with a polymer containing osmium redox centers: biosensors for benzaldehyde and GABA Biosensors 4, 403-421 10.3390/bios4040403
40. Powell, H., Leslie, A., and Battye, G. (2007) Mosflm 7.0.1 and its new interface: iMosflm 0.5.3, CCP4 Newsl Protein Crystallogr., BBSRC, Swindon, England, vol 46.
41. Kabsch, W. (1988) Automatic indexing of rotation diffraction patterns J. Appl. Crystallogr. 21, 67-72 10.1107/S0021889887009737
42. Collaborative Computational Project, N. 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50, 760-3, DOI: 10.1107/S0907444994003112
43. Read, R. J. (2001) Pushing the boundaries of molecular replacement with maximum likelihood Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 1373-1382 10.1107/S0907444901012471
44. Cowtan, K. D. and Zhang, K. Y. (1999) Density modification for macromolecular phase improvement Prog. Biophys. Mol. Biol. 72, 245-270 10.1016/S0079-6107(99)00008-5
45. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255 10.1107/S0907444996012255
46. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132 10.1107/S0907444904019158
47. Joosten, R. P., Joosten, K., Murshudov, G. N., and Perrakis, A. (2012) PDB-REDO: constructive validation, more than just looking for errors Acta Crystallogr., Sect. D: Biol. Crystallogr. 68, 484-496 10.1107/S0907444911054515
48. Joosten, R. P., Salzemann, J., Bloch, V., Stockinger, H., Berglund, A.-C., Blanchet, C., Bongcam-Rudloff, E., Combet, C., Da Costa, A. L., Deleage, G., Diarena, M., Fabbretti, R., Fettahi, G., Flegel, V., Gisel, A., Kasam, V., Kervinen, T., Korpelainen, E., Mattila, K., Pagni, M., Reichstadt, M., Breton, V., Tickle, I. J., and Vriend, G. (2009) PDB-REDO: automated re-refinement of X-ray structure models in the PDB J. Appl. Crystallogr. 42, 376-384 10.1107/S0021889809008784
49. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291 10.1107/S0021889892009944
50. Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 12-21 10.1107/S0907444909042073