Accommodation of two diatomic molecules in cytochrome bo 3: Insights into NO reductase activity in terminal oxidases

Biochemistry

Volumn 48, Issue 5, 2009, Pages 883-890

  Hayashi, Takahiro ^a   Lin, Myat T ^b   Ganesan, Krithika ^b   Chen, Ying ^c   Fee, James A ^c   Gennis, Robert B ^b   Moënne Loccoz, Pierre ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITES; BINDING CHARACTERISTICS; COMPARATIVE STUDIES; DIATOMIC MOLECULES; FTIR; HEME-COPPER TERMINALS; IRON COPPERS; LOW TEMPERATURES; METAL-METAL DISTANCES; N-O COMPLEXES; NITROSYL COMPLEXES; NO MOLECULES; REACTION MECHANISMS; REDUCTASE ACTIVITIES; RESONANCE RAMAN; TERMINAL OXIDASE; THERMUS THERMOPHILUS; TWO-ELECTRON REDUCTIONS;

BINDING SITES; COORDINATION REACTIONS; COPPER; ESCHERICHIA COLI; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HEMOGLOBIN; MOLECULES; PHOTOLYSIS; PORPHYRINS;

COPPER COMPOUNDS;

COPPER COMPLEX; CYTOCHROME; CYTOCHROME BO 3; HEME; NITRIC OXIDE REDUCTASE; NITROGEN OXIDE; NITROUS OXIDE; UNCLASSIFIED DRUG; CYTOCHROME BO3, E COLI; DUROQUINOL OXIDASE; ESCHERICHIA COLI PROTEIN; NITRIC-OXIDE REDUCTASE; OXIDOREDUCTASE;

ARTICLE; CONTROLLED STUDY; DENITRIFICATION; ENZYME ACTIVITY; ESCHERICHIA COLI; INFRARED SPECTROSCOPY; METAL BINDING; NONHUMAN; PHOTOLYSIS; PRIORITY JOURNAL; RAMAN SPECTROMETRY; CHEMISTRY; COMPARATIVE STUDY; ENZYME ACTIVATION; FREEZING; METABOLISM; OXIDATION REDUCTION REACTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; THERMUS THERMOPHILUS;

CYTOCHROMES; ENZYME ACTIVATION; ESCHERICHIA COLI PROTEINS; FREEZING; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHOTOLYSIS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 61449231809     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801915r     Document Type: Article

References (54)

1. Lissenden, S., Mohan, S., Overton, T., Regan, T., Crooke, H., Cardinale, J. A., Householder, T. C., Adams, P., O'conner, C. D., Clark, V. L., Smith, H., and Cole, J. A. (2000) Identification of transcription activators that regulate gonococcal adaptation from aerobic to anaerobic or oxygen-limited growth. Mol. Microbiol. 37, 839-855.
2. 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.
3. Anjum, M. F., Stevanin, T. M., Read, R. C., and Moir, J. W. (2002) Nitric oxide metabolism in Neisseria meningitidis. J. Bacteriol. 184, 2987-2993.
4. Castresana, J., Lubben, M., Saraste, M., and Higgins, D. G. (1994) Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J. 13, 2516-2525.
5. Zumft, W. G., Braun, C., and Cuypers, H. (1994) Nitric oxide reductase from Pseudomonas stutzeri. Primary structure and gene organization of a novel bacterial cytochrome bc complex. Eur. J. Biochem. 219, 481-490.
6. van der Oost, J., de Boer, A. P., de Gier, J. W., Zumft, W. G., Stouthamer, A. H., and van Spanning, R. J. (1994) The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase. FEMS Microbiol. Lett. 121, 1-9.
7. 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.
8. Averill, B. A. (1996) Dissimilatory nitrite and nitric oxide reductases. Chem. Rev. 96, 2951-2965.
9. x redox chemistry. Chem. Rev. 102, 1201-1234.
10. Zumft, W. G. (2005) Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J. Inorg. Biochem. 99, 194-215.
11. Moënne-Loccoz, P. (2007) Spectroscopic characterization of heme iron-nitrosyl species and their role in NO reductase mechanisms in diiron proteins. Nat. Prod. Rep. 24, 610-620.
12. Giuffre, A., Stubauer, G., Sarti, P., Brunori, M., Zumft, W. G., Buse, G., and Soulimane, T. (1999) The heme-copper oxidases of Thermus thermophilus catalyze the reduction of nitric oxide: evolutionary implications. Proc. Natl. Acad. Sci. U.S.A. 96, 14718-14723.
13. 3 from Pseudomonas stutzeri displays nitric oxide reductase activity. Eur. J. Biochem. 268, 6486-6491.
14. 3 from Escherichia coli: the binding and turnover of nitric oxide. Biochem. Biophys. Res. Commun. 296, 1272-1278.
15. 2O: a density functional theory study. Inorg. Chem. 45, 3187-3190.
16. 3-type heme-copper oxidase. Biochim. Biophys. Acta 1757, 31-46.
17. 3 from Thermus thermophilus: relevance to NO reductase activity in heme-copper terminal oxidases. J. Am. Chem. Soc. 129, 14952-14958.
18. 3 from Thermus thermophilus. Biochemistry 43, 14118-14127.
19. B. Biochemistry 36, 16259-16266.
20. Miller, L. M., Pedraza, A. J., and Chance, M. R. (1997) Identification of conformational substates involved in nitric oxide binding to ferric and ferrous myoglobin through difference Fourier transform infrared spectroscopy (FTIR). Biochemistry 36, 12199-12207.
21. 3 from Thermus thermophilus HB8. Protein Expression Purif. 40, 299-318.
22. 3 from Escherichia coli and demonstration that associated quinone is not required for the structural integrity of the oxidase. Biochim. Biophys. Acta 1340, 131-142.
23. Zhao, X. J., Sampath, V., and Caughey, W. S. (1995) Cytochrome c oxidase catalysis of the reduction of nitric oxide to nitrous oxide. Biochem. Biophys. Res. Commun. 212, 1054-1060.
24. Cheesman, M. R., Watmough, N. J., Pires, C. A., Turner, R., Brittain, T., Gennis, R. B., Greenwood, C., and Thomson, A. J. (1993) Cytochrome bo from Escherichia coli: identification of haem ligands and reaction of the reduced enzyme with carbon monoxide. Biochem. J. 289, 709-718.
25. 3 from Escherichia coli. J. Biol. Chem. 282, 8777-8775.
26. 3 from Escherichia coli. J. Biol. Chem. 281, 16879-16887.
27. Coyle, C. M., Vogel, K. M., Rush, T. S., 3rd, Kozlowski, P. M., Williams, R., Spiro, T. G., Dou, Y., Ikeda-Saito, M., Olson, J. S., and Zgierski, M. Z. (2003) FeNO structure in distal pocket mutants of myoglobin based on resonance Raman spectroscopy. Biochemistry 42, 4896-4903.
28. Ibrahim, M., Xu, C., and Spiro, T. G. (2006) Differential sensing of protein influences by NO and CO vibrations in heme adducts. J. Am. Chem. Soc. 128, 16834-16845.
29. Xu, C., and Spiro, T. G. (2008) Ambidentate H-bonding by heme-bound NO: structural and spectral effects of -O versus -N H-bonding. J. Biol. Inorg. Chem. 613-621.
30. 3-oxidase from thermus thermophilus. J. Am. Chem. Soc. 127, 15161-15167.
31. 3-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19, 1766-1776.
32. Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., Laakkonen, L., Puustinen, A., Iwata, S., and Wikstrom, M. (2000) The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat. Struct. Biol. 7, 910-917.
33. 3. Biochim. Biophys. Acta 234, 493-498.
34. a3 couple in cytochrome c oxidase as revealed by nitric oxide binding studies. Proc. Natl. Acad. Sci. U.S.A. 76, 3320-3324.
35. Brudvig, G. W., Stevens, T. H., and Chan, S. I. (1980) Reactions of nitric oxide with cytochrome c oxidase. Biochemistry 19, 5275-5285.
36. 3 ligated with nitric oxide and cytochrome a. J. Biol. Chem. 258, 5348-5351.
37. Blackmore, R. S., Greenwood, C., and Gibson, Q. H. (1991) Studies of the primary oxygen intermediate in the reaction of fully reduced cytochrome oxidase. J. Biol. Chem. 266, 19245-19249.
38. 3. Biochemistry 40, 7806-7811.
39. 3 heme and copper observed by low-temperature Fourier transform infrared spectroscopy of the CO complex. Proc. Natl. Acad. Sci. U.S.A. 78, 234-237.
40. 3 from Escherichia coli. Biochemistry 36, 13195-13200.
41. 3 from Thermus thermophilus. J. Biol. Chem. 264, 2405-2408.
42. 3-type cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry 34, 9819-9825.
43. Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660-669.
44. Yoshikawa, S., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., Yamashita, E., Inoue, N., Yao, M., Fei, M. J., Libeu, C. P., Mizushima, T., Yamaguchi, H., Tomizaki, T., and Tsukihara, T. (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280, 1723-1729.
45. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa, I.-K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272, 1136-1144.
46. 3 oxidase from Thermus thermophilus. Acta Crystallogr. D61, 340-343.
47. 3 from Thermus thermophilus. Acta Crystallogr. F63, 1029-1034.
48. 3 oxidase from Thermus thermophilus: stucture of the reduced form of the enzyme. Biochemistry, in press.
49. B upon illumination, with carbonyl stretching frequencies and intensities that are indistinguishable from those observed at low CO concentrations with 5% glycerol. In contrast with the terminal oxidases, the active site of the NO reductase from Bacillus azotoformans was shown to bind two CO molecules: Lu, S., Suharti, de Vries, S., and Moënne-Loccoz, P. (2004) Two CO molecules can bind concomitantly at the diiron site of NO reductase from Bacillus azotoformans. J. Am. Chem. Soc. 126, 15332-15333.
50. Hill, J., Goswitz, V. C., Calhoun, M., Garcia-Horsman, J. A., Lemieux, L., Alben, J. O., and Gennis, R. B. (1992) Demonstration by FTIR that the bo-type ubiquinol oxidase of Escherichia coli contains a heme-copper binuclear center similar to that in cytochrome c oxidase and that proper assembly of the binuclear center requires the cyoE gene product. Biochemistry 31, 11435-11440.
51. Calhoun, M. W., Lemieux, L. J., Thomas, J. W., Hill, J. J., Goswitz, V. C., Alben, J. O., and Gennis, R. B. (1993) Spectroscopic characterization of mutants supports the assignment of histidine-419 as the axial ligand of heme o in the binuclear center of the cytochrome bo ubiquinol oxidase from Escherichia coli. Biochemistry 32, 13254-13261.
52. 3 from Escherichia coli. Is chloride ion a cofactor? Biochemistry 38, 7185-7194.
53. 3. Biochim. Biophys. Acta 1767, 387-392.
54. Zhao, X. J., Sampath, V., and Caughey, W. S. (1994) Infrared characterization of nitric oxide bonding to bovine heart cytochrome c oxidase and myoglobin. Biochem. Biophys. Res. Commun. 204, 537-543.