Heme-mediated oxygen activation in biology: Cytochrome c oxidase and nitric oxide synthase

Current Opinion in Chemical Biology

Volumn 3, Issue 2, 1999, Pages 131-137

  Poulos, Thomas L ^a   Li, Huiying ^a   Raman, C S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; HEME; HEMOPROTEIN; NITRIC OXIDE SYNTHASE; OXIDOREDUCTASE; OXYGEN; PROTON PUMP; TETRAHYDROBIOPTERIN;

CRYSTAL STRUCTURE; ENZYME MECHANISM; REVIEW;

EID: 0033120861     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1367-5931(99)80024-6     Document Type: Article

References (41)

1. Yoshikawa Y: Beef heart cytochrome c oxidase. Curr Opin Struct Biol 1997, 7:574-579.
2. Fergusson-Miller S, Babbock G: Heme/copper terminal oxidases. Chem Rev 1996, 96:2889-2907.
3. Michel H, Behr J, Harrenga A, Kannt A: Cytochrome c oxidase: Structure and spectroscopy. Annu Rev Biophys Biomol Struct 1998, 27:329-356. This is the most recent review on cytochrome c oxidase, with an emphasis on structure.
4. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S: Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 1995, 269:1069-1074.
5. Iwata S, Ostermeier C, Ludwig B, Michel H: Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 1995, 376:660-669.
6. Kitagawa T, Ogura T: Oxygen activation mechanism at the binuclear site of heme-copper oxidase superfamily as revealed by time-resolved resonance Raman spectroscopy. Prog Inorg Chem 1997, 45:431-479. This is an excellent summary of resonance Raman work on cytochrome c oxidase.
7. B histidine ligand forms a radical during the catalytic cycle.
8. Sucheta A, Szundi I, Einarsdottir O: Intermediates in the reaction for fully reduced cytochrome c oxidase with dioxygen. Biochemistry 1999, in press. Rapid reaction methods are utilized to identify spectral-distinct intermediates during the oxidase catalytic cycle. Rate constants for the individual steps are provided. It is especially useful to correlate the work in this paper with the resonance Raman studies.
9. Sucheta A, Georgiadis K, Einarsdottir O: Mechanism of cytochrome c oxidase-catalyzed reduction of dioxygen to water: Evidence for peroxy and ferryl intermediates at room temperature. Biochemistry 1997, 36:554-565.
10. IV oxidation level. J Am Chem Soc 1996, 118:5543-5549.
11. Stubbe J, van der Donk W: Protein radicals in enzyme catalysis. Chem Rev 1998, 98:705-762.
12. Wikstrom M: Identification of the electron transfers in cytochrome oxidase that are coupled to proton-pumping. Nature 1989, 338:776-778.
13. 2. Biochemistry 1998, 37:3062-3067.
14. Konstantinov A, Siletsky S, Mitchell D, Kaulen A, Gennis R: The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. Proc Natl Acad Sci USA 1997, 94:9085-9090.
15. Brezinski P, Adelroth P: Pathways of proton transfer in cytochrome c oxidase. J Bioenerg Biomem 1998, 30:99-107. This is a brief but excellent and clear description of current views on how protons are pumped in cytochrome c oxidase.
16. Pfitzner O, Odenwald A, Ostermann T, Weingard L, Ludwig B, Richter O: Cytochrome c oxidase (heme aa3) from Paracoccus denitrificans: Analysis of mutations in putative proton channels of subunit I. J Bioenerg Biomem 1998, 30:89-97.
17. Kannt A, Lancaster R, Michel H: The coupling of electron transfer and proton translocation: Electrostatic calculations on Paracoccus denitrificans cytochrome c oxidase. Biophys J 1998, 74:708-721.
18. Puustinen A, Bailey J, Dyer R, Mecklenburg S, Wikstrom M, Woodruff W: Fourier transform infrared evidence for connectivity between CuB and glutamic acid 286 in cytochrome bo3 from Escherichia coli. Biochemistry 1998, 36:13195-13200.
19. Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Fei M, Libeu C, Mizushima T et al.: Redox-coupled crystal structural changes in bovine heart cytochrome c. Science 1998, 280:1723-1729. The bovine heart cytochrome c oxidase structure in the fully reduced state, as well as in a complex with azide and carbon monoxide is described here. A most remarkable and unexpected feature is a large conformational change quite different from the heme centers involving an aspartic acid residue. These observations provide the basis for a possible novel proton transfer pathway.
20. Griffith O, Stuehr D: Nitric oxide synthase: Properties and catalytic mechanism. Annu Rev Physiol 1995, 57:707-736.
21. McMillan K, Bredt D, Hirsch D, Snyder S, Clark J, Masters B: Cloned, expressed rat cerebellar nitric oxide synthase contains stoichiometric amounts of heme, which binds carbon monoxide. Proc Natl Acad Sci USA 1992, 89:11141-11145.
22. White K, Marletta M: Nitric oxide synthase is a cytochrome P-450 type hemoprotein. Biochemistry 1992, 31:6627-6631.
23. Stuehr D, Ikeda-Saito M: Spectral characterization of brain and macrophage nitric oxide synthases. Cytochrome P-450-like hemeproteins that contain a flavin semiquinone radical. J Biol Chem 1992, 267:20547-20550.
24. Crane B, Arvai A, Ghosh D, Wu C, Getzoff E, Stuehr D, Tainer J: Structure of nitric oxide synthase oxygenase dimer with pterin and substrate. Science 1998, 279:2121-2126. This paper describes the 2.6 Å structure of the mouse inducible nitric oxide synthase dimeric oxygenase domain. In addition to the complex formed with the substrate L-arginine, the structure of the complex formed with the product analog thiocitulline was solved. The authors postulate that the substrate, L-arginine, operates as an acid catalyst during oxygen activation by donating a proton to the iron-linked dioxygen.
25. Raman C, Li H, Martasek P, Kral V, Masters B, Poulos T: Crystal structure of constitutive endothelial nitric oxide synthase: A paradigm for pterin function involving a novel metal center. Cell 1998, 95:939-950. This paper describes the 1.9 Å structure of the bovine endothelial nitric oxide synthase (eNOS) dimeric oxygenase domain. The substrate complex and the complex formed with the inhibitor isothiourea were solved. In addition, the structure of the pterin-free enzyme shows that that pterin site is preformed in eNOS, demonstrating that the binding of pterin does not lead to major structural changes and most likely has very little to do with eNOS dimerization. The substrate L-arginine provides a molecular mimic to the pterin by binding to the pterin site, leading to the postulate that NOS stabilizes a cationic pterin radical during the catalytic cycle. The authors also show that the structures of both inducible NOS and eNOS are very similar, including nearly identical active sites.
26. Ghosh K, Stuehr D: Macrophage NO synthase: Characterization of isolated oxygenase and reductase domains reveals a head-to-head subunit interaction. Biochemistry 1995, 34:801-807.
27. Presta A, Siddhanta U, Wu C, Sennequier N, Huang L, Abu-Soud H, Erzurum S, Stuehr D: Comparative functioning of dihydro- and tetrahydropterins in supporting electron transfer, catalysis, and subunit dimerization in inducible nitric oxide synthase. Biochemistry 1998, 37:298-310.
28. Abu-Soud H, Gachhui R, Raushel F, Stuehr D: The ferrous-dioxy complex of neuronal nitric oxide synthase. J Biol Chem 1997, 272:17349-17353.
29. Bec N, Gorren A, Voelker C, Mayer B, Lange R: Reaction of neuronal nitric-oxide synthase with oxygen at low temperature. Evidence for reductive activation of the oxy-ferrous complex by tetrahydrobiopterin. J Biol Chem 1998, 273:13502-13508. Low temperature rapid reaction kinetics of NOS implicates electron transfer from the pterin to the heme, thereby generating a pterin radical as part of the catalytic cycle.
30. Luykx D, Duine J, de Vries S: Molybdopterin radical in bacterial aldehyde dehydrogenase. Biochemistry 1998, 37:11366-11375.
31. Sundaramoorthy M, Kishi K, Gold M, Poulos T: Crystal structures of substrate binding site mutants of manganese peroxidase. J Biol Chem 1997, 272:17574-17580.
32. Huyett J, Doan P, Gurbriel R, Houseman A, Sivaraja M, Goodin D, Hoffman B: Compound ES of cytochrome c peroxidase contains a Trp pi cation radical: Characterization by CW and pulsed Q-band ENDOR. J Am Chem Soc 1995, 117:9033-9041.
33. Sivaraja M, Goodin D, Smith M, Hoffman B: Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES. Science 1989, 345:738-740.
34. Vidakovic M, Sligar S, Li H, Poulos T: Understanding the role of the essential Asp251 in cytochrome p450cam using site-directed mutagenesis, crystallography, and kinetic solvent isotope effect. Biochemistry 1998, 37:9211-9219.
35. Perry J, Marletta M: Effects of transition metals on nitric oxide synthase catalysis. Proc Natl Acad Sci USA 1998, 95:1101-1106.
36. Goodwill K, Sabatier C, Marks C, Raag R, Fitzpatrick P, Stevens R: Crystal structure of tyrosine hydroxylase at 2.3 Å and its implications for inherited neurodegenerative diseases. Nat Struct Biol 1997, 4:578-585.
37. Pufhal R, Wishnok J, Marletta M: Hydrogen peroxide-supported oxidation of N-hydroxy-L-arginine by nitric oxide synthase. Biochemistry 1995, 34:1930-1941.
38. Abu-Soud H, Presta A, Mayer B, Stuehr D: Analysis of neuronal NO synthase under single-turnover conditions: Conversion of N-omega-hydroxyarginine to nitric oxide and citrulline. Biochemistry 1998, 36:10811-10816. An important set of experiments are described, where it is shown that the conversion of hydroxy-arginine to the final products citrulline and NO requires only one electron.
39. Clague M, Wishnok J, Marletta M: Formation of N-cyanoornithine from N-hydroxy-L-argnine and hydrogen peroxide by neuronal nitric oxide synthase. Biochemistry 1997, 36:14465-14473.
40. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S: The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 1996, 272:1136-1144.
41. Siddhantha U, Presta A, Baochen F, Wolan D, Rousseau D, Steuhr D: Domain swapping in inducible nitric-oxide synthase: Electron transfer occurs between flavin and heme groups located on adjacent subunits in the monomer. J Biol Chem 1998, 273:18950-18958.