Crystal structures of nitric oxide reductases provide key insights into functional conversion of respiratory enzymes

IUBMB Life

Volumn 65, Issue 3, 2013, Pages 217-226

  Tosha, Takehiko ^a   Shiro, Yoshitsugu ^a  

^a RIKEN SPring 8 Center   (Japan)

Author keywords

cytochrome c oxidase; heme protein; nitric oxide reductase; proton transfer; respiratory enzyme; X ray crystallography

Indexed keywords

ARGININE; CALCIUM ION; CYTOCHROME C OXIDASE; NITRIC OXIDE REDUCTASE;

BIOENERGY; BREATHING; CATALYSIS; CELL MEMBRANE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENVIRONMENTAL CHANGE; LIGAND BINDING; MOLECULAR EVOLUTION; NONHUMAN; OXIDATION; PHYLOGENY; PROTON TRANSPORT; REVIEW; SEQUENCE HOMOLOGY;

AEROBIOSIS; ANAEROBIOSIS; ANIMALS; BACTERIA; CELL RESPIRATION; CRYSTALLOGRAPHY, X-RAY; ELECTRON TRANSPORT COMPLEX IV; EVOLUTION, MOLECULAR; HEME; MODELS, MOLECULAR; NITRIC OXIDE; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84874475158     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1135     Document Type: Review

References (48)

1. 2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123-125.
2. Stevanin, T. M., Laver, J. R., Poole, R. K., Moir, J. W., and, Read, R. C., (2007) Metabolism of nitric oxide by Neisseria meningitidis modifies release of NO-regulated cytokines and chemokines by human macrophages. Microbes Infect. 9, 981-987.
3. Falsetta, M. L., Steichen, C. T., McEwan, A. G., Cho, C. M., Ketterer, M., et al. (2011) The composition and metabolic phenotype of Neisseria gonorrhoeae biofilms. Front. Microbiol. 2, 75.
4. Saraste, M., and, Castresana, J., (1994) Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett. 341, 1-4.
5. Zumft, W. G., (2005) Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J. Inorg. Biochem. 99, 194-215.
6. Ducluzeau, A. L., van Lis, R., Duval, S., Schoepp-Cothenet, B., Russell, M. J., et al. (2009) Was nitric oxide the first deep electron sink? Trends. Biochem. Sci. 34, 9-15.
7. Pereira, M. M., Santana, M., and, Teixeira, M., (2001) A novel scenario for the evolution of haem-copper oxygen reductases. Biochim. Biophys. Acta 1505, 185-208.
8. 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.
9. Giuffre, A., Stubauer, G., Sarti, P., Brunori, M., Zumft, W. G., et al. (1999) The heme-copper oxidases of Thermus thermophilus catalyze the reduction of nitric oxide: evolutionary implications. Proc. Natl. Acad. Sci. USA 96, 14718-14723.
10. Hayashi, T., Lin, M. T., Ganesan, K., Chen, Y., Fee, J. A., et al. (2009) Accommodation of two diatomic molecules in cytochrome bo: insights into NO reductase activity in terminal oxidases. Biochemistry 48, 883-890.
11. Hendriks, J. H., Jasaitis, A., Saraste, M., and, Verkhovsky, M. I., (2002) Proton and electron pathways in the bacterial nitric oxide reductase. Biochemistry 41, 2331-2340.
12. Reimann, J., Flock, U., Lepp, H., Honigmann, A., and, Adelroth, P., (2007) A pathway for protons in nitric oxide reductase from Paracoccus denitrificans. Biochim. Biophys. Acta 1767, 362-373.
13. 2O generation by bacterial nitric oxide reductase. Science 330, 1666-1670.
14. Matsumoto, Y., Tosha, T., Pisliakov, A. V., Hino, T., Sugimoto, H., et al. (2012) Crystal structure of quinol-dependent nitric oxide reductase from Geobacillus Stearothermophilus. Nat. Struct. Mol. Biol. 19, 238-245.
15. Hendriks, J., Oubrie, A., Castresana, J., Urbani, A., Gemeinhardt, S., et al. (2000) Nitric oxide reductases in bacteria. Biochim. Biophys. Acta 1459, 266-273.
16. 3 cytochrome oxidase provides insights into proton pumping. Science 329, 327-330.
17. 3-type oxygen reductases from Rhodobacter sphaeroides and Vibrio cholerae. Biochemistry 51, 7290-7296.
18. 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.
19. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., et al. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272, 1136-1144.
20. 3-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19, 1766-1776.
21. Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., et al. (2000) The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat. Struct. Biol. 7, 910-917.
22. Sousa, F. L., Alves, R. J., Ribeiro, M. A., Pereira-Leal, J. B., Teixeira, M., et al. (2012) The superfamily of heme-copper oxygen reductases: types and evolutionary considerations. Biochim. Biophys. Acta 1817, 629-637.
23. 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.
24. Lin, Y. W., Yeung, N., Gao, Y. G., Miner, K. D., Tian, S., et al. (2010) Roles of glutamates and metal ions in a rationally designed nitric oxide reductase based on myoglobin. Proc. Natl. Acad. Sci. USA 107, 8581-8586.
25. Hayashi, T., Miner, K. D., Yeung, N., Lin, Y. W., Lu, Y., et al. (2011) Spectroscopic characterization of mononitrosyl complexes in heme-nonheme diiron centers within the myoglobin scaffold (Fe(B)Mbs): relevance to denitrifying NO reductase. Biochemistry 50, 5939-5947.
26. Kumita, H., Matsuura, K., Hino, T., Takahashi, S., Hori, H., et al. (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.
27. 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, 610-620.
28. 2O generation in bacterial nitric oxide reductase: a quantum chemical study. Biochemistry 51, 5173-5186.
29. 3 in the catalytic center of nitric oxide reductase from Pseudomonas nautica. Biochemistry 50, 4251-4262.
30. 2O by a functional synthetic model of heme containing bacterial NO reductase. J. Am. Chem. Soc. 130, 16498-16499.
31. Shiro, Y., (2012) Structure and function of bacterial nitric oxide reductases: nitric oxide reductase, anaerobic enzymes. Biochim. Biophys. Acta 1817, 1907-1913.
32. Shiro, Y., Sugimoto, H., Tosha, T., Nagano, S., and, Hino, T., (2012) Structural basis for nitrous oxide generation by bacterial nitric oxide reductases. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1195-1203.
33. Hunsicker-Wang, L. M., Pacoma, R. L., Chen, Y., Fee, J. A., and, Stout, C. D., (2005) A novel cryoprotection scheme for enhancing the diffraction of crystals of recombinant cytochrome ba3 oxidase from Thermus thermophilus. Acta Crystallogr. D Biol. Crystallogr. 61, 340-343.
34. 3 oxidase from Thermus thermophilus: structure of the reduced form of the enzyme. Biochemistry 48, 820-826.
35. 3-type cytochrome oxidase. Nature 487, 514-518.
36. Harrenga, A., and, Michel H,. (1999) The cytochrome c oxidase from Paracoccus denitrificans does not change the metal center ligation upon reduction. J. Biol. Chem. 274, 33296-33299.
37. Koepke, J., Olkhova, E., Angerer, H., Muller, H., Peng, G., et al. (2009) High resolution crystal structure of Paracoccus denitrificans cytochrome c oxidase: new insights into the active site and the proton transfer pathways. Biochim. Biophys. Acta 1787, 635-645.
38. Svensson-Ek, M., Abramson, J., Larsson, G., Tornroth, S., Brzezinski, P., et al. (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321, 329-339.
39. Qin, L., Liu, J., Mills, D. A., Proshlyakov, D. A., Hiser, C., et al. (2009) Redox-dependent conformational changes in cytochrome C oxidase suggest a gating mechanism for proton uptake. Biochemistry 48, 5121-5130.
40. 2 reduction site of fully oxidized cytochrome c oxidase could suppress the proton pump. Proc. Natl. Acad. Sci. USA 106, 2165-2169.
41. Muramoto, K., Hirata, K., Shinzawa-Itoh, K., Yoko-o, S., Yamashita, E., et al. (2007) A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase. Proc. Natl. Acad. Sci. USA 104, 7881-7886.
42. 2 reduction with minimization of reactive oxygens and provide a proton-pumping gate. Proc. Natl. Acad. Sci. USA 107, 7740-7745.
43. Yoshikawa, S., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., Yamashita, E., et al. (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280, 1723-1729.
44. Petrek, M., Otyepka, M., Banas, P., Kosinova, P., Koca, J., et al. (2006) CAVER: a new tool to explore routes from protein clefts, pockets and cavities. BMC Bioinformatics 7, 316.
45. Pisliakov, A. V., Hino, T., Shiro, Y., and, Sugita, Y., (2012) Molecular dynamics simulations reveal proton transfer pathways in cytochrome C-dependent nitric oxide reductase. PLoS Comput. Biol. 8, e1002674.
46. Salomonsson, L., Reimann, J., Tosha, T., Krause, N., Gonska, N., et al. (2012) Proton transfer in the quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus during reduction of oxygen. Biochim. Biophys. Acta 1817, 1914-1920.
47. Flock, U., Watmough, N. J., and, Adelroth, P., (2005) Electron/proton coupling in bacterial nitric oxide reductase during reduction of oxygen. Biochemistry 44, 10711-10719.
48. Ishigami, I., Nishigaki, K., Shinzawa-Itoh, K., Yoshikawa, S., Nakashima, S., et al. (2012) An intermediate conformational state during ligand binding to cytochrome c oxidase detected by time-resolved resonance Raman analyses of heme peripheral group. Chem. Lett. 2, 178-180.