Low-spin heme b3 in the catalytic center of nitric oxide reductase from pseudomonas nautica

Biochemistry

Volumn 50, Issue 20, 2011, Pages 4251-4262

  Timóteo, Cristina G ^a   Pereira, Alice S ^a   Martins, Carlos E ^a   Naik, Sunil G ^b   Duarte, Américo G ^a   Moura, José J G ^a   Tavares, Pedro ^a   Huynh, Boi Hanh ^b   Moura, Isabel ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY ASSAYS; AMINO ACID SEQUENCE; BINUCLEAR CENTER; CATALYTIC CENTER; ELECTRON TRANSFER; FERROUS STATE; HEME GROUP; HETERODIMERS; HIGH SPIN STATE; MOSSBAUER; NITRIC OXIDE REDUCTASE; NO MOLECULE; NO REDUCTION; OXIDATION STATE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PURIFIED PROTEIN; REDOX-ACTIVE; REDUCING CONDITIONS; SMALL SUBUNITS; SPECTROSCOPIC DATA; SPECTROSCOPIC MEASUREMENTS; SPIN-SPIN;

AMINO ACIDS; BACTERIA; CATALYSTS; CHARGE TRANSFER; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTROPHORESIS; ENZYMES; GENE ENCODING; IRON; NITRIC OXIDE; PURIFICATION; REACTION INTERMEDIATES; REDUCTION; RESONANCE;

PORPHYRINS;

AMINO ACID; ASCORBIC ACID; CELL EXTRACT; DITHIONITE; HEME; HEME B3; HEME C; HETERODIMER; IRON; NITRIC OXIDE REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BIOCHEMISTRY; CATALYSIS; CELL GROWTH; ELECTRON TRANSPORT; ENZYME ASSAY; GENE SEQUENCE; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; OXIDATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PSEUDOMONAS; PSEUDOMONAS NAUTICA; SEQUENCE HOMOLOGY; ULTRAVIOLET SPECTROSCOPY;

ABSORPTION; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEME; MOLECULAR SEQUENCE DATA; OPTICAL PROCESSES; OXIDATION-REDUCTION; OXIDOREDUCTASES; PSEUDOMONAS; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTROSCOPY, MOSSBAUER;

MARINOBACTER HYDROCARBONOCLASTICUS; PSEUDOMONAS;

EID: 79956198337     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101605p     Document Type: Article

References (60)

1. Bonin, P., Bertrand, J. C., Giordano, G., and Gilewicz, M. (1987) Specific sodium dependence of a nitrate reductase in a marine bacterium FEMS Microbiol. Lett. 48, 5-9
2. Bonin, P., Gilewicz, M., Denis, M., and Bertrand, J. C. (1989) Salt requirements in the denitrifying bacterium Pseudomonas nautica 617 Res. Microbiol. 140, 159-169
3. Tavares, P., Pereira, A. S., Moura, J. J., and Moura, I. (2006) Metalloenzymes of the denitrification pathway J. Inorg. Biochem. 100, 2087-2100 (Pubitemid 44738047)
4. 2O) reductase. Evidence of a bridging inorganic sulfur J. Biol. Chem. 275, 41133-41136 (Pubitemid 32054943)
5. 1 nitrite reductase: regulation of the NO-bound end product J. Biol. Inorg. Chem. 6, 55-62 (Pubitemid 32822157)
6. Brown, K., Tegoni, M., Prudencio, M., Pereira, A. S., Besson, S., Moura, J. J., Moura, I., and Cambillau, C. (2000) A novel type of catalytic copper cluster in nitrous oxide reductase Nat. Struct. Biol. 7, 191-195 (Pubitemid 30140762)
7. Correia, C., Besson, S., Brondino, C. D., Gonzalez, P. J., Fauque, G., Lampreia, J., Moura, I., and Moura, J. J. (2008) Biochemical and spectroscopic characterization of the membrane-bound nitrate reductase from Marinobacter hydrocarbonoclasticus 617 J. Biol. Inorg. Chem. 13, 1321-1333
8. Heiss, B., Frunzke, K., and Zumft, W. G. (1989) Formation of the N-N bond from nitric oxide by a membrane-bound cytochrome bc complex of nitrate-respiring (denitrifying) Pseudomonas stutzeri J. Bacteriol. 171, 3288-3297 (Pubitemid 19145684)
9. Kastrau, D. H., Heiss, B., Kroneck, P. M., and Zumft, W. G. (1994) Nitric oxide reductase from Pseudomonas stutzeri, a novel cytochrome bc complex. Phospholipid requirement, electron paramagnetic resonance and redox properties Eur. J. Biochem. 222, 293-303 (Pubitemid 24204898)
10. Hoglen, J. and Hollocher, T. C. (1989) Purification and some characteristics of nitric oxide reductase-containing vesicles from Paracoccus denitrificans J. Biol. Chem. 264, 7556-7563
11. Carr, G. J. and Ferguson, S. J. (1990) The nitric oxide reductase of Paracoccus denitrificans Biochem. J. 269, 423-429 (Pubitemid 20236034)
12. Sakurai, T., Nakashima, S., Kataoka, K., Seo, D., and Sakurai, N. (2005) Diverse NO reduction by Halomonas halodenitrificans nitric oxide reductase Biochem. Biophys. Res. Commun. 333, 483-487 (Pubitemid 40848317)
13. Sakurai, T., Sakurai, N., Matsumoto, H., Hirota, S., and Yamauchi, O. (1998) Roles of four iron centers in Paracoccus halodenitrificans nitric oxide reductase Biochem. Biophys. Res. Commun. 251, 248-251 (Pubitemid 28498096)
14. Kumita, H., Matsuura, K., Hino, T., Takahashi, S., Hori, H., Fukumori, Y., Morishima, I., and Shiro, Y. (2004) NO reduction by nitric-oxide reductase from denitrifying bacterium Pseudomonas aeruginosa: characterization of reaction intermediates that appear in the single turnover cycle J. Biol. Chem. 279, 55247-55254 (Pubitemid 40066521)
15. Cramm, R., Pohlmann, A., and Friedrich, B. (1999) Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16 FEBS Lett. 460, 6-10 (Pubitemid 29479234)
16. Hendriks, J., Oubrie, A., Castresana, J., Urbani, A., Gemeinhardt, S., and Saraste, M. (2000) Nitric oxide reductases in bacteria Biochim. Biophys. Acta 1459, 266-273 (Pubitemid 30612396)
17. Householder, T. C., Fozo, E. M., Cardinale, J. A., and Clark, V. L. (2000) Gonococcal nitric oxide reductase is encoded by a single gene, norB, which is required for anaerobic growth and is induced by nitric oxide Infect. Immun. 68) 5241-5246
18. 551 Biochemistry 43, 13487-13495 (Pubitemid 39391150)
19. Girsch, P. and de Vries, S. (1997) Purification and initial kinetic and spectroscopic characterization of NO reductase from Paracoccus denitrificans Biochim. Biophys. Acta 1318, 202-216 (Pubitemid 27051234)
20. Hendriks, J., Warne, A., Gohlke, U., Haltia, T., Ludovici, C., Lubben, M., and Saraste, M. (1998) The active site of the bacterial nitric oxide reductase is a dinuclear iron center Biochemistry 37, 13102-13109 (Pubitemid 28449553)
21. Cheesman, M. R., Zumft, W. G., and Thomson, A. J. (1998) The MCD and EPR of the heme centers of nitric oxide reductase from Pseudomonas stutzeri: Evidence that the enzyme is structurally related to the heme-copper oxidases Biochemistry 37, 3994-4000 (Pubitemid 28162957)
22. Moenne-Loccoz, P., Richter, O. M. H., Huang, H. W., Wasser, I. M., Ghiladi, R. A., Karlin, K. D., and de Vries, S. (2000) Nitric oxide reductase from Paracoccus denitrificans contains an oxo-bridged heme/non-heme diiron center J. Am. Chem. Soc. 122 (38) 9344-9345
23. Moenne-Loccoz, P. (2007) Spectroscopic characterization of heme iron-nitrosyl species and their role in NO reductase mechanisms in diiron proteins Nat. Prod. Rep. 24 (3) 610-620 (Pubitemid 46848713)
24. Zumft, W. G. (2005) Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type J. Inorg. Biochem. 99, 194-215 (Pubitemid 39642979)
25. Watmough, N. J., Field, S. J., Hughes, R. J., and Richardson, D. J. (2009) The bacterial respiratory nitric oxide reductase Biochem. Soc. Trans. 37, 392-399
26. Field, S. J., Thorndycroft, F. H., Matorin, A. D., Richardson, D. J., and Watmough, N. J. (2008) The respiratory nitric oxide reductase (NorBC) from Paracoccus denitrificans Methods Enzymol. 437, 79-101
27. Collman, J. P., Dey, A., Yang, Y., Decreau, R. A., Ohta, T., and Solomon, E. I. (2008) Intermediates Involved in the Two Electron Reduction of NO to N(2)O by a Functional Synthetic Model of Heme Containing Bacterial NO Reductase J. Am. Chem. Soc. 130, 16498-16499
28. Gronberg, K. L., Roldan, M. D., Prior, L., Butland, G., Cheesman, M. R., Richardson, D. J., Spiro, S., Thomson, A. J., and Watmough, N. J. (1999) A low-redox potential heme in the dinuclear center of bacterial nitric oxide reductase: implications for the evolution of energy-conserving heme-copper oxidases Biochemistry 38, 13780-13786 (Pubitemid 29504207)
29. Gronberg, K. L., Watmough, N. J., Thomson, A. J., Richardson, D. J., and Field, S. J. (2004) Redox-dependent open and closed forms of the active site of the bacterial respiratory nitric-oxide reductase revealed by cyanide binding studies J. Biol. Chem. 279, 17120-17125 (Pubitemid 38560467)
30. Schagger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa Anal. Biochem. 166, 368-379 (Pubitemid 18004907)
31. Saraiva, L. M., Besson, S., Moura, I., and Fauque, G. (1995) Purification and preliminary characterization of three c -type cytochromes from Pseudomonas nautica strain 617 Biochem. Biophys. Res. Commun. 212, 1088-1097
32. 552 from Pseudomonas nautica 617 Eur. J. Biochem. 224, 1011-1017 (Pubitemid 24288865)
33. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein Measurement with the Folin Phenol Reagent J. Biol. Chem. 193, 265-275
34. Berry, E. A. and Trumpower, B. L. (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra Anal. Biochem. 161, 1-15
35. Fischer, D. S. and Price, D. C. (1964) A simple serum iron method using the new sensitive chromogen tripyridyl-S-triazine Clin. Chem. 10, 21-31
36. Moore, S. and Stein, W. H. (1963) Chromatographic determination of amino acids by the use of automatic recording equipment Methods Enzymol. 6, 819-831
37. Ausubel, F. M., Brent, R., Kingston, R. E., Seidman, J. G., Smith, J. A., and Struhl, K., (Eds.) (1989) Current Protocols in Molecular Biology, Greene Pub. Associates and Wiley-Interscience, New York.
38. Butland, G., Spiro, S., Watmough, N. J., and Richardson, D. J. (2001) Two conserved glutamates in the bacterial nitric oxide reductase are essential for activity but not assembly of the enzyme J. Bacteriol. 183, 189-199 (Pubitemid 32003123)
39. Flock, U., Thorndycroft, F. H., Matorin, A. D., Richardson, D. J., Watmough, N. J., and Adelroth, P. (2008) Defining the proton entry point in the bacterial respiratory nitric-oxide reductase J. Biol. Chem. 283, 3839-3845
40. Thorndycroft, F. H., Butland, G., Richardson, D. J., and Watmough, N. J. (2007) A new assay for nitric oxide reductase reveals two conserved glutamate residues form the entrance to a proton-conducting channel in the bacterial enzyme Biochem. J. 401, 111-119 (Pubitemid 46114605)
41. Flock, U., Lachmann, P., Reimann, J., Watmough, N. J., and Ädelroth, P. (2009) Exploring the terminal region of the proton pathway in the bacterial nitric oxide reductiase J. Inorg. Biochem. 103, 845-850
42. Sakurai, N. and Sakurai, T. (1997) Isolation and characterization of nitric oxide reductase from Paracoccus halodenitrificans Biochemistry 36, 13809-13815 (Pubitemid 27494886)
43. Field, S. J., Prior, L., Roldan, M. D., Cheesman, M. R., Thomson, A. J., Spiro, S., Butt, J. N., Watmought, N. J., and Richardson, D. J. (2002) Spectral properties of bacterial nitric-oxide reductase-Resolution of pH-dependent forms of the active site heme b (3) J. Biol. Chem. 277 (23) 20146-20150 (Pubitemid 34967305)
44. Fujiwara, T. and Fukumori, Y. (1996) Cytochrome cb -type nitric oxide reductase with cytochrome c oxidase activity from Paracoccus denitrificans ATCC 35512 J. Bacteriol. 178, 1866-1871 (Pubitemid 26110528)
45. Oubrie, A., Gemeinhardt, S., Field, S., Marritt, S., Thomson, A. J., Saraste, M., and Richardson, D. J. (2002) Properties of a soluble domain of subunit C of a bacterial nitric oxide reductase Biochemistry 41, 10858-10865 (Pubitemid 34971063)
46. Aasa, R. and Vanngard, T. (1975) EPR signal intensity and powder shapes: a reexamination J. Magn. Reson. 19, 308-315
47. De Vries, S. and Albracht, S. P. J. (1979) Intensity of highly anisotropic low-spin heme EPR signals Biochim. Biophys. Acta 546, 334-340
48. 549 from the marine denitrifying bacterium Pseudomonas nautica 617 Biochem. Biophys. Res. Commun. 199, 1289-1296
49. Hendrich, M. P. and Debrunner, P. G. (1989) Integer-spin electron paramagnetic resonance of iron proteins Biophys. J. 56, 489-506
50. Moenne-Loccoz, P. and de Vries, S. (1998) Structural characterization of the catalytic high-spin heme b of nitric oxide reductase: A resonance Raman study J. Am. Chem. Soc. 120, 5147-5152 (Pubitemid 28328876)
51. Hino, T., Matsumoto, Y., Nagano, S., Sugimoto, H., Fukumori, Y., Murata, T., Iwata, S., and Shiro, Y. (2010) Structural basis of biological N2O generation by bacterial nitric oxide reductase Science 330, 1666-1670
52. Lachmann, P., Huang, Y., Reimann, J., Flock, U., and Adelroth, P. (2010) Substrate Control of Internal Electron Transfer in Bacterial Nitric-oxide Reductase J. Biol. Chem. 285, 25531-25537
53. 1 nitrite reductase Biochem. Soc. Trans. 36, 1155-1159
54. Ford, P. C. and Lorkovic, I. M. (2002) Mechanistic aspects of the reaction of nitric oxide with transition-metal complexes Chem. Rev. 102, 993-1017 (Pubitemid 35381627)
55. Cooper, C. E. (1999) Nitric oxide and iron proteins Biochim. Biophys. Acta 1411, 290-309 (Pubitemid 29221956)
56. Goodrich, L. E., Paulat, F., Praneeth, V. K. K., and Lehnert, N. (2010) Electronic structure of heme-nytrosyls and its significance for nitric oxide reactivity, sensing, transport, and toxicity in biological systems Inorg. Chem. 49, 6293-6316 and references therein.
57. Wang, Z.-Q., Wei, C.-C., and Stuehr, D. J. (2010) How does a valine residue that modulates heme-NO binding kinetics in inducible NO synthase regulate enzyme catalysis? J. Inorg. Biochem. 104, 349-356
58. Cordas, C. M., Pereira, A. S., Martins, C. E., Timoteo, C. G., Moura, I., Moura, J. J. G., and Tavares, P. (2006) Nitric oxide reductase: Direct electrochemistry and electrocatalytic activity ChemBioChem 7, 1878-1881 (Pubitemid 44893519)
59. Buschmann, S., Warkentin, E., Xie, H., Langer, J. D., Ermler, U., and Michel, H. (2010) The Structure of cbb(3) Cytochrome Oxidase Provides Insights into Proton Pumping Science 329, 327-330
60. Hendriks, J. H., Prior, L., Baker, A. R., Thomson, A. J., Saraste, M., and Watmough, N. J. (2001) Reaction of carbon monoxide with the reduced active site of bacterial nitric oxide reductase Biochemistry 40, 13361-13369 (Pubitemid 33043552)