Access to the active site of periplasmic nitrate reductase: Insights from site-directed mutagenesis and zinc inhibition studies

Biochemistry

Volumn 46, Issue 34, 2007, Pages 9713-9721

  Dementin, Sebastien ^a,b,c   Arnoux, Pascal ^a   Frangioni, Bettina ^b   Grosse, Sandrine ^a   Léger, Christophe ^b   Burlat, Bénédicte ^b   Guigliarelli, Bruno ^a   Sabaty, Monique ^a   Pignol, David ^a  

^a IRFM   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; CATALYST ACTIVITY; DENITRIFICATION; DIMERIZATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; MUTAGENESIS;

ACTIVE SITES; HETERODIMERS; NITRATE REDUCTASE (NAPAB); REDOX POTENTIOMETRY;

ENZYME ACTIVITY;

DIMETHYL SULFOXIDE; HETERODIMER; MOLYBDENUM; MUTANT PROTEIN; NITRATE REDUCTASE; PERIPLASMIC PROTEIN; ZINC ION;

ARTICLE; CATALYSIS; CONSERVATION BIOLOGY; ELECTRON SPIN RESONANCE; ENZYMATIC ASSAY; INHIBITION KINETICS; KINETICS; MOLECULE; NONHUMAN; POTENTIOMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; RHODOBACTER SPHAEROIDES; SITE DIRECTED MUTAGENESIS;

BINDING SITES; MOLYBDENUM; MUTAGENESIS, SITE-DIRECTED; MUTATION; NITRATE REDUCTASE; NITRATES; OXIDATION-REDUCTION; PERIPLASM; PROTEIN BINDING; RHODOBACTER SPHAEROIDES; ZINC;

RHODOBACTER SPHAEROIDES;

EID: 34548256727     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700928m     Document Type: Article

References (42)

1. Bertero, M. G., Rothery, R. A., Palak, M., Hou, C., Lim, D., Blasco, F., Weiner, J. H., and Strynadka, N. C. (2003) Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A, Nat. Struct. Biol. 10, 681-687.
2. Richardson, D. J., Berks, B. C., Russell, D. A., Spiro, S., and Taylor, C. J. (2001) Functional, biochemical and genetic diversity of prokaryotic nitrate reductases, Cell. Mol. Life Sci. 58, 165-178.
3. Blasco, F., Guigliarelli, B., Magalon, A., Asso, M., Giordano, G., and Rothery, R. A. (2001) The coordination and function of the redox centres of the membrane-bound nitrate reductases, Cell. Mol. Life Sci. 58, 179-193.
4. Sabaty, M., Schwintner, C., Cahors, S., Richaud, P., and Vermeglio, A. (1999) Nitrite and nitrous oxide reductase regulation by nitrogen oxides in Rhodobacter sphaeroides f. sp. denitrificans IL106, J. Bacteriol. 181, 6028-6032.
5. Cartron, M. L., Roldan, M. D., Ferguson, S. J., Berks, B. C., and Richardson, D. J. (2002) Identification of two domains and distal histidine ligands to the four haems in the bacterial c-type cytochrome NapC; the prototype connector between quinol/quinone and periplasmic oxido-reductases, Biochem. J. 368, 425-432.
6. Dias, J. M., Than, M. E., Humm, A., Huber, R., Bourenkov, G. P., Bartunik, H. D., Bursakov, S., Calvete, J., Caldeira, J., Carneiro, C., Moura, J. J., Moura, I., and Romao, M. J. (1999) Crystal structure of the first dissimilatory nitrate reductase at 1.9 Å solved by MAD methods, Structure 7, 65-79.
7. Arnoux, P., Sabaty, M., Alric, J., Frangioni, B., Guigliarelli, B., Adriano, J. M., and Pignol, D. (2003) Structural and redox plasticity in the heterodimeric periplasmic nitrate reductase, Nat. Struct. Biol. 10, 928-934.
8. Jepson, B. J. N., Mohan, S., Clarke, T. A., Gates, A. J., Cole, J. A., Butler, C. S., Butt, J. N., Hemmings, A. M., and Richardson, D. J. (2007) Spectropotentiometric and structural analysis of the periplasmic nitrate reductase from Escherichia coli, J. Biol. Chem. 282, 6425-6437.
9. Frangioni, B., Arnoux, P., Sabaty, M., Pignol, D., Bertrand, P., Guigliarelli, B., and Leger, C. (2004) In Rhodobacter sphaeroides respiratory nitrate reductase, the kinetics of substrate binding favors intramolecular electron transfer, J. Am. Chem. Soc. 126, 1328-1329.
10. Sabaty, M., Avazeri, C., Pignol, D., and Vermeglio, A. (2001) Characterization of the reduction of selenate and tellurite by nitrate reductases, Appl. Environ. Microbiol. 67, 5122-5126.
11. Butler, C. S., Charnock, J. M., Garner, C. D., Thomson, A. J., Ferguson, S. J., Berks, B. C., and Richardson, D. J. (2000) Thiocyanate binding to the molybdenum centre of the periplasmic nitrate reductase from Paracoccus pantotrophus, Biochem. J. 352 Pt 3, 859-864.
12. Hettmann, T., Siddiqui, R. A., Frey, C., Santos-Silva, T., Romao, M. J., and Diekmann, S. (2004) Mutagenesis study on amino acids around the molybdenum centre of the periplasmic nitrate reductase from Ralstonia eutropha, Biochem. Biophys. Res. Commun. 320, 1211-1219.
13. Clayton, R. K. (1960) Physiology of induced catalase synthesis in Rhodopseudomonas spheroids, J. Cell. Comp. Physiol. 55, 1-7.
14. Pignol, D., Adriano, J. M., Fontecilla-Camps, J. C., and Sabaty, M. (2001) Crystallization and preliminary X-ray analysis of the periplasmic nitrate reductase (NapA-NapB complex) from Rhodobacter sphaeroides f. sp. denitrificans, Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 1900-1902.
15. Nicholas, D. J. D., and Nason, A. (1957) Determination of nitrate and nitrite, Methods Enzymol. 3, 981-984.
16. Gazaryan, I. G., Krasnikov, B. F., Ashby, G. A., Thorneley, R. N., Kristal, B. S., and Brown, A. M. (2002) Zinc is a potent inhibitor of thiol oxidoreductase activity and stimulates reactive oxygen species production by lipoamide dehydrogenase, J. Biol. Chem. 277, 10064-10072.
17. Magalon, A., Asso, M., Guigliarelli, B., Rothery, R. A., Bertrand, P., Giordano, G., and Blasco, F. (1998) Molybdenum cofactor properties and [Fe-S] cluster coordination in Escherichia coli nitrate reductase A: investigation by site-directed mutagenesis of the conserved his-50 residue in the NarG subunit, Biochemistry 37, 7363-7370.
18. Kyritsis, P., Kummerle, R., Huber, J. G., Gaillard, J., Guigliarelli, B., Popescu, C., Munck, E., and Moulis, J. M. (1999) Unusual NMR, EPR, and Mossbauer properties of Chromatium vinosum 2[4Fe-4S] ferredoxin, Biochemistry 38, 6335-6345.
19. Lanciano, P., Magalon, A., Bertrand, P., Guigliarelli, B., and Grimaldi, S. (2007) High-Stability Semiquinone Intermediate in Nitrate Reductase A (NarGHI) from Escherichia coli Is Located in a Quinol Oxidation Site Close to Heme b(D), Biochemistry 46, 5323-5329.
20. Frangioni, B. (2006) in Etude fonctionnelle de la nitrate periplasmique de Rhodobacter sphaeroides par spectroscopic RPE et electrochimie directe, Thesis, Université Aix marseille I, France.
21. Gonzalez, P. J., Rivas, M. G., Brondino, C. D., Bursakov, S. A., Moura, I., and Moura, J. J. G. (2006) EPR and redox properties of periplasmic nitrate reductase from Desulfovibrio desulfuricans ATCC 27774, J. Biol. Inorg. Chem. 11, 609-616.
22. Butler, C. S., Charnock, J. M., Bennett, B., Sears, H. J., Reilly, A. J., Ferguson, S. J., Garner, C. D., Lowe, D. J., Thomson, A. J., Berks, B. C., and Richardson, D. J. (1999) Models for molybdenum coordination during the catalytic cycle of periplasmic nitrate reductase from Paracoccus denitrificans derived from EPR and EXAFS spectroscopy, Biochemistry 38, 9000-9012.
23. Butler, C. S., Fairhurst, S. A., Ferguson, S. J., Thomson, A. J., Berks, B. C., Richardson, D. J., and Lowe, D. J. (2002) Mo(V) co-ordination in the periplasmic nitrate reductase from Paracoccus pantotrophus probed by electron nuclear double resonance (ENDOR) spectroscopy, Biochem. J. 363, 817-823.
24. Guigliarelli, B., Asso, M., More, C., Augier, V., Blasco, F., Pommier, J., Giordano, G., and Bertrand, P. (1992) EPR and redox characterization of iron-sulfur centers in nitrate reductases A and Z from Escherichia coli. Evidence for a high-potential and a low-potential class and their relevance in the electron-transfer mechanism, Eur. J. Biochem. 207, 61-68.
25. Vincent, S. P., and Bray, R. C. (1978) Electron-paramagnetic-resonance studies on nitrate reductase from Escherichia coli K12, Biochem. J. 171, 639-647.
26. Jepson, B. J. N., Anderson, L. J., Rubio, L. M., Taylor, C. J., Butler, C. S., Flores, E., Herrero, A., Butt, J. N., and Richardson, D. J. (2004) Tuning a nitrate reductase for function-The first spectropotentiometric characterization of a bacterial assimilatory nitrate reductase reveals novel redox properties, J. Biol. Chem. 279, 32212-32218.
27. Bastian, N. R., Kay, C. J., Barber, M. J., and Rajagopalan, K. V. (1991) Spectroscopic studies of the molybdenum-containing dimethyl sulfoxide reductase from Rhodobacter sphaeroides f. sp. denitrificans, J. Biol. Chem. 266, 45-51.
28. Benson, N., Farrar, J. A., McEwan, A. G., and Thomson, A. J. (1992) Detection of the optical bands of molybdenum(V) in DMSO reductase (Rhodobacter capsulatus) by low-temperature MCD spectroscopy, FEBS Lett. 307, 169-172.
29. Zorin, N. A., Dimon, B., Gagnon, J., Gaillard, J., Carrier, P., and Vignais, P. M. (1996) Inhibition by iodoacetamide and acetylene of the H-D-exchange reaction catalyzed by Thiocapsa roseopersicina hydrogenase, Eur. J. Biochem. 241, 675-681.
30. Dixon, M. (1953) The determination of enzyme inhibitor constants, Biochem. J. 55, 170-171.
31. Cornish-Bowden, A., and Eisenthal, R. (1974) Statistical considerations in the estimation of enzyme kinetic parameters by the direct linear plot andother methods, Biochem. J. 139, 721-730.
32. Mouncey, N. J., and Kaplan, S. (1998) Cascade regulation of dimethyl sulfoxide reductase (dor) gene expression in the facultative phototroph Rhodobacter sphaeroides 2.4. IT, J. Bacteriol. 180, 2924-2930.
33. Karakas, E., Wilson, H. L., Graf, T. N., Xiang, S., Jaramillo-Busquets, S., Rajagopalan, K. V., and Kisker, C. (2005) Structural insights into sulfite oxidase deficiency, J. Biol. Chem. 280, 33506-33515.
34. Bartalesi, I., Bertini, I., Ghosh, K., Rosato, A., and Turano, P. (2002) The unfolding of oxidized c-type cytochromes: the instructive case of Bacillus pasteurii, J. Mol. Biol. 321, 693-701.
35. Barker, P. D., and Freund, S. M. (1996) Bis-methionine ligation to heme iron in mutants of cytochrome b562. 2. Characterization by NMR of heme-ligand interactions, Biochemistry 35, 13627-13635.
36. Romero, A., De la Cerda, B., Varela, P. F., Navarro, J. A., Hervas, M., and De la Rosa, M. A. (1998) The 2.15 A crystal structure of a triple mutant plastocyanin from the cyanobacterium Synechocystis sp. PCC 6803, J. Mol. Biol. 275, 327-336.
37. Williams, P. A., Blackburn, N. J., Sanders, D., Bellamy, H., Stura, E. A., Fee, J. A., and McRee, D. E. (1999) The CuA domain of Thermus thermophilus ba3-type cytochrome c oxidase at 1.6 A resolution, Nat. Struct. Biol. 6, 509-516.
38. D'Angelo, P., Pacello, F., Mancini, G., Proux, O., Hazemann, J. L., Desideri, A., and Battistoni, A. (2005) X-ray absorption investigation of a unique protein domain able to bind both copper(I) and copper(II) at adjacent sites of the N-terminus of Haemophilus ducreyi Cu,Zn superoxide dismutase, Biochemistry 44, 13144-13150.
39. Jobling, M. F., Huang, X., Stewart, L. R., Barnham, K. J., Curtain, C., Volitakis, I., Perugini, M., White, A. R., Cherny, R. A., Masters, C. L., Barrow, C. J., Collins, S. J., Bush, A. I., and Cappai, R. (2001) Copper and zinc binding modulates the aggregation and neurotoxic properties of the prion peptide PrP106-126, Biochemistry 40, 8073-8084.
40. Mathys, W. (1975) Enzymes of heavy-metal resistant and non-resistant populations of Silene cucubalus and their interaction with some heavy metals in vitro and in vivo, Physiol. Plant. 33, 161-175.
41. Tripathi, B. N., Mehta, S. K., and Gaur, J. P. (2004) Recovery of uptake and assimilation of nitrate in Scenedesmus sp. previously exposed to elevated levels of Cu2+ and Zn2+, J. Plant Physiol. 161, 543-549.
42. Fischer, K., Barbier, G. G., Hecht, H. J., Mendel, R. R., Campbell, W. H., and Schwarz, G. (2005) Structural basis of eukaryotic nitrate reduction: crystal structures of the nitrate reductase active site, Plant Cell 17, 1167-1179.