Deuterium isotope effect of proton pumping in cytochrome c oxidase

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1777, Issue 4, 2008, Pages 343-350

  Salomonsson, Lina ^a   Brändén, Gisela ^a   Brzezinski, Peter ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Cytochrome aa3; Electron transfer; Kinetics; Membrane protein; Mitochondria; Proton transfer; Spectroscopy; Transmembrane transport

Indexed keywords

CYTOCHROME C OXIDASE; DEUTERIUM; PROTON; PROTON PUMP;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ELECTRON; ELECTRON TRANSPORT; ENZYME ANALYSIS; ENZYME STRUCTURE; PH; PRIORITY JOURNAL; PROTON TRANSPORT; TRANSPORT KINETICS; WILD TYPE;

CRYSTALLOGRAPHY, X-RAY; DEUTERIUM; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN-ION CONCENTRATION; KINETICS; PROTON PUMPS;

EID: 40949134606     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2007.09.009     Document Type: Article

References (68)

1. Mills D.A., and Ferguson-Miller S. Understanding the mechanism of proton movement linked to oxygen reduction in cytochrome c oxidase: lessons from other proteins. FEBS Lett. 545 (2003) 47-51
2. Brzezinski P. Redox-driven membrane-bound proton pumps. Trends Biochem. Sci. 29 (2004) 380-387
3. Gennis R.B. Coupled proton and electron transfer reactions in cytochrome oxidase. Front. Biosci. 9 (2004) 581-591
4. Wikström M. Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim. Biophys. Acta 1655 (2004) 241-247
5. Brunori M., Giuffre A., and Sarti P. Cytochrome c oxidase, ligands and electrons. J. Inorg. Biochem. 99 (2005) 324-336
6. Brzezinski P., and Ädelroth P. Design principles of proton-pumping haem-copper oxidases. Curr. Opin. Struct. Biol. 16 (2006) 465-472
7. Papa S., Capitanio G., and Luca Martino P. Concerted involvement of cooperative proton-electron linkage and water production in the proton pump of cytochrome c oxidase. Biochim. Biophys. Acta, Bioenerg. 1757 (2006) 1133-1143
8. Yoshikawa S., Muramoto K., Shinzawa-Itoh K., Aoyama H., Tsukihara T., Shimokata K., Katayama Y., and Shimada H. Proton pumping mechanism of bovine heart cytochrome c oxidase. Biochim. Biophys. Acta, Bioenerg. 1757 (2006) 1110-1116
9. Quenneville J., Popovic D.M., and Stuchebrukhov A.A. Combined DFT and electrostatics study of the proton pumping mechanism in cytochrome c oxidase. Biochim. Biophys. Acta, Bioenerg. 1757 (2006) 1035-1046
10. Hosler J.P., Ferguson-Miller S., and Mills D.A. Energy transduction: proton transfer through the respiratory complexes. Ann. Rev. Biochem. 75 (2006) 165-187
11. Iwata S., Ostermeier C., Ludwig B., and Michel H. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376 (1995) 660-669
12. Svensson-Ek M., Abramson J., Larsson G., Törnroth S., Brzezinski P., and Iwata S. The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321 (2002) 329-339
13. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272 (1996) 1136-1144
14. Shimokata K., Katayama Y., Murayama H., Suematsu M., Tsukihara T., Muramoto K., Aoyama H., Yoshikawa S., and Shimada H. The proton pumping pathway of bovine heart cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 4200-4205
15. Konstantinov A.A., Siletsky S., Mitchell D., Kaulen A., and Gennis R.B. 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. U. S. A. 94 (1997) 9085-9090
16. Brzezinski P., and Ädelroth P. Pathways of proton transfer in cytochrome c oxidase. J. Bioenerg. Biomembranes 30 (1998) 99-107
17. Wikström M., Jasaitis A., Backgren C., Puustinen A., and Verkhovsky M.I. The role of the D- and K-pathways of proton transfer in the function of the haem-copper oxidases. Biochim. Biophys. Acta 1459 (2000) 514-520
18. Brändén G., Brändén M., Schmidt B., Mills D.A., Ferguson-Miller S., and Brzezinski P. The protonation state of a heme propionate controls electron transfer in cytochrome c oxidase. Biochemistry 44 (2005) 10466-10474
19. Olsson M.H., Siegbahn P.E., Blomberg M.R., and Warshel A. Exploring pathways and barriers for coupled ET/PT in cytochrome c oxidase: a general framework for examining energetics and mechanistic alternatives. Biochim. Biophys. Acta 1767 (2007) 244-260
20. Hofacker I., and Schulten K. Oxygen and proton pathways in cytochrome c oxidase. Proteins 30 (1998) 100-107
21. Puustinen A., and Wikström M. Proton exit from the heme-copper oxidase of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 35-37
22. Ädelroth P., Karpefors M., Gilderson G., Tomson F.L., Gennis R.B., and Brzezinski P. Proton transfer from glutamate 286 determines the transition rates between oxygen intermediates in cytochrome c oxidase. Biochim. Biophys. Acta 1459 (2000) 533-539
23. Namslauer A., Pawate A.S., Gennis R.B., and Brzezinski P. Redox-coupled proton translocation in biological systems: proton shuttling in cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15543-15547
24. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., and Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15304-15309
25. Popovic D.M., and Stuchebrukhov A.A. Proton pumping mechanism and catalytic cycle of cytochrome c oxidase: Coulomb pump model with kinetic gating. FEBS Lett. 566 (2004) 126-130
26. Quenneville J., Popovic D.M., and Stuchebrukhov A.A. Combined DFT and electrostatics study of the proton pumping mechanism in cytochrome c oxidase. Biochim. Biophys. Acta 1757 (2006) 1035-1046
27. Brändén G., Gennis R.B., and Brzezinski P. Transmembrane proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1757 (2006) 1052-1063
28. Faxén K., Gilderson G., Ädelroth P., and Brzezinski P. A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437 (2005) 286-289
29. Zaslavsky D., Kaulen A.D., Smirnova I.A., Vygodina T., and Konstantinov A.A. Flash-induced membrane potential generation by cytochrome c oxidase. FEBS Lett. 336 (1993) 389-393
30. Verkhovsky M.I., Morgan J.E., Verkhovskaya M.L., and Wikström M. Translocation of electrical charge during a single turnover of cytochrome-c oxidase. Biochim. Biophys. Acta 1318 (1997) 6-10
31. Bloch D., Belevich I., Jasaitis A., Ribacka C., Puustinen A., Verkhovsky M.I., and Wikström M. The catalytic cycle of cytochrome c oxidase is not the sum of its two halves. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 529-533
32. Smirnova I.A., Ädelroth P., Gennis R.B., and Brzezinski P. Aspartate-132 in cytochrome c oxidase from Rhodobacter sphaeroides is involved in a two-step proton transfer during oxo-ferryl formation. Biochemistry 38 (1999) 6826-6833
33. Namslauer A., Aagaard A., Katsonouri A., and Brzezinski P. Intramolecular proton-transfer reactions in a membrane-bound proton pump: the effect of pH on the peroxy to ferryl transition in cytochrome c oxidase. Biochemsitry 42 (2003) 1488-1498
34. Iwaki M., Puustinen A., Wikström M., and Rich P.R. ATR-FTIR spectroscopy of the PM and F intermediates of bovine and Paracoccus denitrificans cytochrome c oxidase. Biochemistry 42 (2003) 8809-8817
35. Nyquist R.M., Heitbrink D., Bolwien C., Gennis R.B., and Heberle J. Direct observation of protonation reactions during the catalytic cycle of cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 8715-8720
36. Heitbrink D., Sigurdson H., Bolwien C., Brzezinski P., and Heberle J. Transient binding of CO to Cu-B in cytochrome c oxidase is dynamically linked to structural changes around a carboxyl group: a time-resolved step-scan Fourier transform infrared investigation. Biophys. J. 82 (2002) 1-10
37. Agmon N. The Grotthuss Mechanism. Chem. Phys. Lett. 244 (1995) 456-462
38. Decoursey T.E. Voltage-gated proton channels and other proton transfer pathways. Physiol. Rev. 83 (2003) 475-579
39. Karpefors M., Ädelroth P., Aagaard A., Smirnova I.A., and Brzezinski P. The deuterium isotope effect as a tool to investigate enzyme catalysis: proton-transfer control mechanisms in cytochrome c oxidase. Isr. J. Chem. 39 (1999) 427-437
40. Hallén S., and Nilsson T. Proton transfer during the reaction between fully reduced cytochrome c oxidase and dioxygen: pH and deuterium isotope effects. Biochemistry 31 (1992) 11853-11859
41. Sadoski R.C., Zaslavsky D., Gennis R.B., Durham B., and Millett F. Exposure of bovine cytochrome c oxidase to high triton X-100 or to alkaline conditions causes a dramatic change in the rate of reduction of compound F. J. Biol. Chem. 276 (2001) 33616-33620
42. Zaslavsky D., Sadoski R.C., Wang K.F., Durham B., Gennis R.B., and Millett F. Single electron reduction of cytochrome c oxidase compound F: resolution of partial steps by transient spectroscopy. Biochemistry 37 (1998) 14910-14916
43. Siletsky S.A., Pawate A.S., Weiss K., Gennis R.B., and Konstantinov A.A. Transmembrane charge separation during the ferryl-oxo → oxidized transition in a nonpumping mutant of cytochrome c oxidase. J. Biol. Chem. 279 (2004) 52558-52565
44. Salomonsson L., Faxén K., Ädelroth P., and Brzezinski P. The timing of proton migration in membrane-reconstituted cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17624-17629
45. Karpefors M., Ädelroth P., and Brzezinski P. Localized control of proton transfer through the D-pathway in cytochrome c oxidase: application of the proton-inventory technique. Biochemistry 39 (2000) 6850-6856
46. Mitchell D.M., and Gennis R.B. Rapid purification of wildtype and mutant cytochrome c oxidase from Rhodobacter sphaeroides by Ni(2+)-NTA affinity chromatography. FEBS Lett. 368 (1995) 148-150
47. Mitchell D.M., Fetter J.R., Mills D.A., Ädelroth P., Pressler M.A., Kim Y., Aasa R., Brzezinski P., Malmström B.G., Alben J.O., Babcock G.T., Ferguson-Miller S., and Gennis R.B. Site-directed mutagenesis of residues lining a putative proton transfer pathway in cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry 35 (1996) 13089-13093
48. Mills D.A., Geren L., Hiser C., Schmidt B., Durham B., Millett F., and Ferguson-Miller S. An arginine to lysine mutation in the vicinity of the heme propionates affects the redox potentials of the hemes and associated electron and proton transfer in cytochrome c oxidase. Biochemistry 44 (2005) 10457-10465
49. Brändén M., Sigurdson H., Namslauer A., Gennis R.B., Ädelroth P., and Brzezinski P. On the role of the K-proton transfer pathway in cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5013-5018
50. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
51. Winn M.D., Isupov M.N., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr., D Biol. Crystallogr. 57 (2001) 122-133
52. Namslauer A., and Brzezinski P. Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase. FEBS Lett. 567 (2004) 103-110
53. Fetter J.R., Qian J., Shapleigh J., Thomas J.W., García-Horsman A., Schmidt E., Hosler J., Babcock G.T., Gennis R.B., and Ferguson-Miller S. Possible proton relay pathways in cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 1604-1608
54. Mills D.A., Tan Z., Ferguson-Miller S., and Hosler J. A role for subunit III in proton uptake into the D pathway and a possible proton exit pathway in Rhodobacter sphaeroides cytochrome c oxidase. Biochemistry 42 (2003) 7410-7417
55. Muramoto K., Hirata K., Shinzawa-Itoh K., Yoko O.S., Yamashita E., Aoyama H., Tsukihara T., and Yoshikawa S. A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 7881-7886
56. Aagaard A., Gilderson G., Mills D.A., Ferguson-Miller S., and Brzezinski P. Redesign of the proton-pumping machinery of cytochrome c oxidase: proton pumping does not require Glu(I-286). Biochemistry 39 (2000) 15847-15850
57. Backgren C., Hummer G., Wikström M., and Puustinen A. Proton translocation by cytochrome c oxidase can take place without the conserved glutamic acid in subunit I. Biochemistry 39 (2000) 7863-7867
58. Schowen R.L. Solvent isotope effects on enzymic reactions. In: Cleland W.W., O'Leary M.H., and Northrop D.B. (Eds). Isotope Effects on Enzyme-Catalyzed Reactions (1977), University Park Press, Baltimore, MD 64-99
59. Karpefors M., Ädelroth P., Zhen Y., Ferguson-Miller S., and Brzezinski P. Proton uptake controls electron transfer in cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 13606-13611
60. Belevich I., Bloch D.A., Belevich N., Wikström M., and Verkhovsky M.I. Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 2685-2690
61. Behr J., Michel H., Mäntele W., and Hellwig P. Functional properties of the heme propionates in cytochrome c oxidase from Paracoccus denitrificans. Evidence from FTIR difference spectroscopy and site-directed mutagenesis. Biochemistry 39 (2000) 1356-1363
62. Brzezinski P., and Larsson G. Redox-driven proton pumping by heme-copper oxidases. Biochim. Biophys. Acta 1605 (2003) 1-13
63. Michel H. The mechanism of proton pumping by cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 12819-12824
64. Popovic D.M., and Stuchebrukhov A.A. Electrostatic study of the proton pumping mechanism in bovine heart cytochrome c oxidase. J. Am. Chem. Soc. 126 (2004) 1858-1871
65. Wikström M., Verkhovsky M.I., and Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1604 (2003) 61-65
66. Schowen K.B., and Schowen R.L. Solvent isotope effects on enzyme systems. Methods Enzymol. 87 (1982) 551-606
67. Mills D.A., Florens L., Hiser C., Qian J., and Ferguson-Miller S. Where is 'outside' in cytochrome c oxidase and how and when do protons get there?. Biochim. Biophys. Acta 1458 (2000) 180-187
68. Mills D.A., and Ferguson-Miller S. Influence of structure, pH and membrane potential on proton movement in cytochrome oxidase. Biochim. Biophys. Acta 1555 (2002) 96-100