Computational study of the activated OH state in the catalytic mechanism of cytochrome c oxidase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 42, 2013, Pages 16844-16849

  Sharma, Vivek ^a,b   Karlin, Kenneth D ^c   Wikström, Mårten ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Electron transfer; Oxygen reduction

Indexed keywords

ADENOSINE TRIPHOSPHATE; CUPRIC ION; CUPROUS ION; CYTOCHROME C OXIDASE; FERRIC ION; HEME; OXYGEN; PROTON; TYROSINE;

ARTICLE; CALCULATION; CATALYSIS; DENSITY FUNCTIONAL THEORY; ELECTRON; HYDRATION; LEISURE; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; RESPIRATORY CHAIN;

ELECTRON TRANSFER; OXYGEN REDUCTION;

ANIMALS; BACTERIAL PROTEINS; CATALYSIS; CATTLE; COMPUTER SIMULATION; ELECTRON TRANSPORT COMPLEX IV; MODELS, CHEMICAL; OXYGEN; PARACOCCUS DENITRIFICANS;

EID: 84885699008     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220379110     Document Type: Article

References (54)

1. Ferguson-Miller S, Babcock GT (1996) Heme-copper terminal oxidases. Chem Rev 96(7): 2889-2908.
2. Kaila VRI, Verkhovsky MI, Wikström M (2010) Proton-coupled electron transfer in cytochrome oxidase. Chem Rev 110(12): 7062-7081.
3. Yoshikawa S, et al. (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280(5370): 1723-1729.
4. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376(6542): 660-669.
5. Konstantinov AA, Siletsky S, Mitchell D, Kaulen A, Gennis RB (1997) 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 94(17): 9085-9090.
6. Wikström M, Krab K (1979) Proton-pumping cytochrome c oxidase. Biochim Biophys Acta 549(2): 177-22.
7. Wikström M, Verkhovsky MI, Hummer G (2003) Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim Biophys Acta 1604(2): 61-65.
8. Wikström M (2004) Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim Biophys Acta 1655(1-3): 241-247.
9. Popović DM, Stuchebrukhov AA (2004) Electrostatic study of the proton pumping mechanism in bovine heart cytochrome C oxidase. J Am Chem Soc 126(6): 1858-1871.
10. Popović DM, Stuchebrukhov AA (2004) Proton pumping mechanism and catalytic cycle of cytochrome c oxidase: Coulomb pump model with kinetic gating. FEBS Lett 566(1-3): 126-130.
11. Morgan JE, Verkhovsky MI, Wikström M (1994) The histidine cycle: A new model for proton translocation in the respiratory heme-copper oxidases. J Bioenerg Biomembr 26(6): 599-608.
12. Rich PR (1995) Towards an understanding of the chemistry of oxygen reduction. Aust J Plant Physiol 22(3): 479-486.
13. Chance B, Saronio C, Leigh JS, Jr. (1975) Functional intermediates in reaction of cytochrome oxidase with oxygen. Proc Natl Acad Sci USA 72(4): 1635-1640.
14. Wikström M (1981) Energy-dependent reversal of the cytochrome oxidase reaction. Proc Natl Acad Sci USA 78(7): 4051-4054.
15. Weng LC, Baker GM (1991) Reaction of hydrogen peroxide with the rapid form of resting cytochrome oxidase. Biochemistry 30(23): 5727-5733.
16. Proshlyakov DA, et al. (1994) Selective resonance Raman observation of the "607 nm" form generated in the reaction of oxidized cytochrome c oxidase with hydrogen peroxide. J Biol Chem 269(47): 29385-29388.
17. Wikström M (2012) Active site intermediates in the reduction of O(2) by cytochrome oxidase, and their derivatives. Biochim Biophys Acta 1817(4): 468-475.
18. Brzezinski P, Gennis RB (2008) Cytochrome c oxidase: Exciting progress and remaining mysteries. J Bioenerg Biomembr 40(5): 521-531.
19. Morgan JE, Verkhovsky MI, Palmer G, Wikström M (2001) Role of the PR intermediate in the reaction of cytochrome c oxidase with O2. Biochemistry 40(23): 6882-6892.
20. Blair DF, Witt SN, Chan SI (1985) Mechanism of cytochrome c oxidase-catalyzed dioxygen reduction at low temperatures. Evidence for two intermediates at the threeelectron level and entropic promotion of the bond-breaking step. J Am Chem Soc 107(25): 7389-7399.
21. Gorbikova EA, Wikström M, Verkhovsky MI (2008) The protonation state of the crosslinked tyrosine during the catalytic cycle of cytochrome c oxidase. J Biol Chem 283(50): 34907-34912.
22. Antonini E, Brunori M, Colosimo A, Greenwood C, Wilson MT (1977) Oxygen "pulsed" cytochrome c oxidase: Functional properties and catalytic relevance. Proc Natl Acad Sci USA 74(8): 3128-3132.
23. Belevich I, Verkhovsky MI (2008) Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid Redox Signal 10(1): 1-29.
24. Verkhovsky MI, Jasaitis A, Verkhovskaya ML, Morgan JE, Wikström M (1999) Proton translocation by cytochrome c oxidase. Nature 400(6743): 480-483.
25. Bloch D, et al. (2004) The catalytic cycle of cytochrome c oxidase is not the sum of its two halves. Proc Natl Acad Sci USA 101(2): 529-533.
26. Wikström M, Verkhovsky MI (2006) Towards the mechanism of proton pumping by the haem-copper oxidases. Biochim Biophys Acta 1757(8): 1047-1051.
27. Jancura D, et al. (2006) Spectral and kinetic equivalence of oxidized cytochrome C oxidase as isolated and "activated" by reoxidation. J Biol Chem 281(41): 30319-30325.
28. Brudvig GW, Stevens TH, Morse RH, Chan SI (1981) Conformations of oxidized cytochrome c oxidase. Biochemistry 20(13): 3912-3921.
29. Belevich I, Bloch DA, Belevich N, Wikström M, Verkhovsky MI (2007) Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc Natl Acad Sci USA 104(8): 2685-2690.
30. Gorbikova EA, Vuorilehto K, Wikström M, Verkhovsky MI (2006) Redox titration of all electron carriers of cytochrome c oxidase by Fourier transform infrared spectroscopy. Biochemistry 45(17): 5641-5649.
31. Han S, Takahashi S, Rousseau DL (2000) Time dependence of the catalytic intermediates in cytochrome c oxidase. J Biol Chem 275(3): 1910-1919.
32. Wikström M, Krab K, Saraste M (1981) Cytochrome Oxidase: A Synthesis (Academic, London).
33. Chufán EE, et al. (2010) Differential reactivity between two copper sites in peptidylglycine α-hydroxylating monooxygenase. J Am Chem Soc 132(44): 15565-15572.
34. Himes RA, Park GY, Siluvai GS, Blackburn NJ, Karlin KD (2008) Structural studies of copper(I) complexes of amyloid-beta peptide fragments: Formation of two-coordinate bis(histidine) complexes. Angew Chem Int Ed Engl 47(47): 9084-9087.
35. Himes RA, Park GY, Barry AN, Blackburn NJ, Karlin KD (2007) Synthesis and X-ray absorption spectroscopy structural studies of Cu(I) complexes of histidylhistidine peptides: The predominance of linear 2-coordinate geometry. J Am ChemSoc 129(17): 5352-5353.
36. Gray HB, Malmström BG, Williams RJP (2000) Copper coordination in blue proteins. J Biol Inorg Chem 5(5): 551-559.
37. Dunitz JD (1994) The entropic cost of bound water in crystals and biomolecules. Science 264(5159): 670.
38. Wirstam M, Blomberg MRA, Siegbahn PER (1999) Reaction mechanism of compound I formation in heme peroxidases: A density functional theory study. J Am Chem Soc 121(43): 10178-10185.
39. Heimdal J, Rydberg P, Ryde U (2008) Protonation of the proximal histidine ligand in heme peroxidases. J Phys Chem B 112(8): 2501-2510.
40. Kaukonen M (2007) Calculated reaction cycle of cytochrome c oxidase. J Phys Chem B 111(43): 12543-12550.
41. Baik M, Freisner RA (2002) Computing redox potentials in solution: Density functional theory as a tool for rational design of redox agents. J Phys Chem A 106(32): 7407-7412.
42. Roy LE, Jakubikova E, Guthrie MG, Batista ER (2009) Calculation of one-electron redox potentials revisited. Is it possible to calculate accurate potentials with density functional methods? J Phys Chem A 113(24): 6745-6750.
43. Martens CF, et al. (1993) Redox behaviour of novel copper(II) crown ether-pyrazole complexes. J Chem Soc Chem Commun 1: 88-90.
44. Martens CF, et al. (1995) X-ray structures and redox properties of copper(II) bis(pyrazole) complexes. Inorg Chem 34(19): 4735-4744.
45. Chen P, Bell J, Eipper BA, Solomon EI (2004) Oxygen activation by the noncoupled binuclear copper site in peptidylglycine alpha-hydroxylating monooxygenase. Spectroscopic definition of the resting sites and the putative CuIIM-OOH intermediate. Biochemistry 43(19): 5735-5747.
46. Pettingill TM, Strange RW, Blackburn NJ (1991) Carbonmonoxy dopamine betahydroxylase. Structural characterization by Fourier transform infrared, fluorescence, and x-ray absorption spectroscopy. J Biol Chem 266(26): 16996-17003.
47. Fox S, Nanthakumar A, Wikström M, Karlin KD, Blackburn NJ (1996) XAS structural comparisons of reversible inter-convertible oxo- and hydroxo-bridged heme-copper oxidase model compounds. J Am Chem Soc 118(1): 24-34.
48. Obias HV, et al. (1998) Heterobinucleating ligand-induced structural and chemical variations in [(L)FeIII-O-CuII]+ μ-oxo complexes. J Am Chem Soc 120(37): 9696-9697.
49. Baron R, McCammon JA (2007) Dynamics, hydration, and motional averaging of a loop-gated artificial protein cavity: The W191G mutant of cytochrome c peroxidase in water as revealed by molecular dynamics simulations. Biochemistry 46(37): 10629-10642.
50. Tegoni M, Yu F, Bersellini M, Penner-Hahn JE, Pecoraro VL (2012) Designing a functional type 2 copper center that has nitrite reductase activity within α-helical coiled coils. Proc Natl Acad Sci USA 109(52): 21234-21239.
51. Qin L, et al. (2009) Redox-dependent conformational changes in cytochrome C oxidase suggest a gating mechanism for proton uptake. Biochemistry 48(23): 5121-5130.
52. Brand SE, et al. (2007) A new ruthenium complex to study single-electron reduction of the pulsed O(H) state of detergent-solubilized cytochrome oxidase. Biochemistry 46(50): 14610-14618.
53. Rousseau DL, Ching YC, Brunori M, Giacometti GM (1989) Axial coordination of ferric Aplysia myoglobin. J Biol Chem 264(14): 7878-7881.
54. Sharma V, Wikström M, Kaila VR (2011) Stabilization of the peroxy intermediate in the oxygen splitting reaction of cytochrome cbb(3). Biochim Biophys Acta 1807(7): 813-818.