Design principles of proton-pumping haem-copper oxidases

Current Opinion in Structural Biology

Volumn 16, Issue 4, 2006, Pages 465-472

  Brzezinski, Peter ^a   Ädelroth, Pia ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYTOCHROME C OXIDASE; OXIDOREDUCTASE; PROTON PUMP;

ELECTRON TRANSPORT; LIGHT; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; REVIEW;

ANIMALS; COPPER; HEME; HUMANS; OXIDOREDUCTASES; PROTON PUMPS; PROTONS;

EID: 33746601087     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2006.06.012     Document Type: Review

References (61)

1. DeCoursey T.E. Voltage-gated proton channels and other proton transfer pathways. Physiol Rev 83 (2003) 475-579
2. Grotthuss C.J.T. Mémoire sur la décomposition de l'eau et des corps qu'elle tient en dissolution à l'aide de l'électricité galvanique. Ann Chim 58 (1806) 54-74
3. Pomès R: Memoir on the decomposition of water and of the bodies that it holds in solution by means of galvanic electricity. Biochim Biophys Acta 2006, in press.
4. Nagle J.F., and Morowitz H.J. Molecular mechanisms for proton transport in membranes. Proc Natl Acad Sci USA 75 (1978) 298-302
5. Dencher N.A., Sass H.J., and Buldt G. Water and bacteriorhodopsin: structure, dynamics, and function. Biochim Biophys Acta 1460 (2000) 192-203
6. 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
7. Olkhova E., Michel H., Hutter M.C., Lill M.A., and Helms V. Dynamic water networks in cytochrome c oxidase from Paracoccus denitrificans investigated by molecular dynamics simulations. Biophys J 86 (2004) 1873-1889
8. Hofacker I., and Schulten K. Oxygen and proton pathways in cytochrome c oxidase. Proteins 30 (1998) 100-107
9. Sham Y.Y., Muegge I., and Warshel A. Simulating proton translocations in proteins: probing proton transfer pathways in the Rhodobacter sphaeroides reaction center. Proteins 36 (1999) 484-500
10. Ernst J.A., Clubb R.T., Zhou H.X., Gronenborn A.M., and Clore G.M. Demonstration of positionally disordered water within a protein hydrophobic cavity by NMR. Science 267 (1995) 1813-1817
11. Garczarek F., and Gerwert K. Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439 (2006) 109-112. Time-resolved Fourier transform IR spectroscopy was used to investigate the role of intraprotein water clusters in bacteriorhodopsin. A specific arrangement of water molecules within the protein results in controlled proton transfer. The findings can be generalised to other proton transporters and show that intraprotein water molecules are essential for biological function.
12. Fujiyoshi Y., Mitsuoka K., de Groot B.L., Philippsen A., Grubmuller H., Agre P., and Engel A. Structure and function of water channels. Curr Opin Struct Biol 12 (2002) 509-515
13. Kato M, Pisliakov AV, Warshel A: Barrier for proton transport in aquaporins as a challenge for electrostatic models: the role of protein relaxation in mutational calculations. Proteins 2006, in press. A thorough theoretical analysis of proton transfer through aquaporins. The results are also applicable to other biological systems.
14. + symport in LacY. EMBO J 25 (2006) 2038. Two X-ray structures of lactose permease were determined at acidic and neutral pH. On the basis of earlier mechanistic studies and the novel structural information, a model is proposed for the mechanism of coupling between proton and lactose translocation.
15. Schobert B., Brown L.S., and Lanyi J.K. Crystallographic structures of the M and N intermediates of bacteriorhodopsin: assembly of a hydrogen-bonded chain of water molecules between Asp-96 and the retinal Schiff base. J Mol Biol 330 (2003) 553-570
16. Song Y., Mao J., and Gunner M.R. Calculation of proton transfers in bacteriorhodopsin bR and M intermediates. Biochemistry 42 (2003) 9875-9888
17. Onufriev A., Smondyrev A., and Bashford D. Proton affinity changes driving unidirectional proton transport in the bacteriorhodopsin photocycle. J Mol Biol 332 (2003) 1183-1193
18. Gennis R.B. Coupled proton and electron transfer reactions in cytochrome oxidase. Front Biosci 9 (2004) 581-591. An excellent and timely review of the structure and function of CytcO.
19. Hosler J.P. The influence of subunit III of cytochrome c oxidase on the D pathway, the proton exit pathway and mechanism-based inactivation in subunit I. Biochim Biophys Acta 1655 (2004) 332-339
20. Wikström M. Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim Biophys Acta 1655 (2004) 241-247. In this review, Wikström describes the principles of proton pumping by haem-copper oxidases in general and in particular discusses a previously proposed molecular mechanism for proton pumping [6]. It is proposed that water molecules in hydrophobic cavities conduct protons and that the conductivity is determined by the water-dipole orientations. The orientation is controlled by the local electric field, which is modulated by the redox states of the cofactors.
21. 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
22. Cukier R.I. Theory and simulation of proton-coupled electron transfer, hydrogen-atom transfer, and proton translocation in proteins. Biochim Biophys Acta 1655 (2004) 37-44
23. Song Y., Michonova-Alexova E., and Gunner M.R. Calculated proton uptake on anaerobic reduction of cytochrome c oxidase: is the reaction electroneutral?. Biochemistry 45 (2006) 7959-7975. A recent thorough theoretical analysis of electrostatic interactions in CytcO. Potential proton donors and acceptors are identified in a number of CytcO redox states, ranging from fully oxidised to fully reduced. Most interestingly, it is found that a majority of the changes in the protonation states take place only at a limited number of key protonatable sites.
24. 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
25. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and Yoshikawa S. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 28 Å. Science 269 (1995) 1069-1074
26. 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
27. 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
28. Ostermeier C., Harrenga A., Ermler U., and Michel H. Structure at 2.7 Å resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc Natl Acad Sci USA 94 (1997) 10547-10553
29. 3-cytochrome c oxidase from Thermus thermophilus. EMBO J 19 (2000) 1766-1776
30. Abramson J., Riistama S., Larsson G., Jasaitis A., Svensson-Ek M., Laakkonen L., Puustinen A., Iwata S., and Wikström M. The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat Struct Biol 7 (2000) 910-917
31. Schmidt B., McCracken J., and Ferguson-Miller S. A discrete water exit pathway in the membrane protein cytochrome c oxidase. Proc Natl Acad Sci USA 100 (2003) 15539-15542
32. Jünemann S., Meunier B., Gennis R.B., and Rich P.R. Effects of mutation of the conserved lysine-362 in cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry 36 (1997) 14456-14464
33. 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 USA 98 (2001) 5013-5018
34. Ädelroth P., Gennis R.B., and Brzezinski P. Role of the pathway through K(I-362) in proton transfer in cytochrome c oxidase from R. sphaeroides. Biochemistry 37 (1998) 2470-2476
35. 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 USA 94 (1997) 9085-9090
36. Brzezinski P., and Ädelroth P. Pathways of proton transfer in cytochrome c oxidase. J Bioenerg Biomembr 30 (1998) 99-107
37. 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. Biochemistry 42 (2003) 1488-1498
38. 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 USA 100 (2003) 15543-15547
39. 3. Biochemistry 38 (1999) 2048-2056
40. Pomès R., Hummer G., and Wikström M. Structure and dynamics of a proton shuttle in cytochrome c oxidase. Biochim Biophys Acta 1365 (1998) 255-260
41. Puustinen A., and Wikström M. Proton exit from the heme-copper oxidase of Escherichia coli. Proc Natl Acad Sci USA 96 (1999) 35-37
42. 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
43. Michel H. The mechanism of proton pumping by cytochrome c oxidase. Proc Natl Acad Sci USA 95 (1998) 12819-12824
44. 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
45. Popovic D.M., and Stuchebrukhov A.A. Proton exit channels in bovine cytochrome c oxidase. J Phys Chem B 109 (2005) 1999-2006
46. Pfitzner U., Hoffmeier K., Harrenga A., Kannt A., Michel H., Bamberg E., Richter O.M.H., and Ludwig B. Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39 (2000) 6756-6762
47. Olsson M.H., and Warshel A. Monte Carlo simulations of proton pumps: on the working principles of the biological valve that controls proton pumping in cytochrome c oxidase. Proc Natl Acad Sci USA 103 (2006) 6500-6505. A Monte Carlo simulation method has been developed to simulate the dynamics of the pumping process in CytcO. The results suggest a mechanism by which the enzyme controls unidirectional proton transfer. The methodology can be generalised to investigations of other proton transporters.
48. Pawate A.S., Morgan J., Namslauer A., Mills D., Brzezinski P., Ferguson-Miller S., and Gennis R.B. A mutation in subunit I of cytochrome oxidase from Rhodobacter sphaeroides results in an increase in steady-state activity but completely eliminates proton pumping. Biochemistry 41 (2002) 13417-13423
49. 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
50. Brändén G., Pawate A.S., Gennis R.B., and Brzezinski P. Controlled uncoupling and recoupling of proton pumping in cytochrome c oxidase. Proc Natl Acad Sci USA 103 (2006) 317-322
51. 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 USA 101 (2004) 529-533. It is shown that each electron transfer to the catalytic site of CytcO is associated with proton pumping. However, proton pumping upon reduction of the oxidised enzyme takes place only under specific conditions when the enzyme is in an 'energised' state.
52. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., et al. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc Natl Acad Sci USA 100 (2003) 15304-15309
53. Papa S., Capitanio N., and Villani G. A cooperative model for protonmotive heme-copper oxidases. The role of heme a in the proton pump of cytochrome c oxidase. FEBS Lett 439 (1998) 1-8
54. Rich P.R., Jünemann S., and Meunier B. Protonmotive mechanism of heme-copper oxidases. J Bioenerg Biomembr 30 (1998) 131-138
55. Siegbahn P.E.M., Blomberg M.R.A., and Blomberg M.L. Theoretical study of the energetics of proton pumping and oxygen reduction in cytochrome oxidase. J Phys Chem B 107 (2003) 10946-10955
56. Wikström M., Ribacka C., Molin M., Laakkonen L., Verkhovsky M., and Puustinen A. Gating of proton and water transfer in the respiratory enzyme cytochrome c oxidase. Proc Natl Acad Sci USA 102 (2005) 10478-10481
57. Faxén K., Gilderson G., Ädelroth P., and Brzezinski P. A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437 (2005) 286-289. Specific proton translocation events are investigated in lipid vesicles, each containing a single CytcO molecule. It is concluded that proton pumping is mechanistically coupled to proton transfer to the catalytic site, rather than to internal electron transfer. The results suggest a principle by which proton pumps might operate.
58. Salomonsson L., Faxén K., Ädelroth P., and Brzezinski P. The timing of proton migration in membrane-reconstituted cytochrome c oxidase. Proc Natl Acad Sci USA 102 (2005) 17624-17629
59. Belevich I., Verkhovsky M.I., and Wikström M. Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase. Nature 440 (2006) 829-832. Proton translocation and electron transfer in CytcO reconstituted in vesicles are investigated. It is concluded that internal electron transfer 'primes' the pump by internal proton relocation, linked to electron transfer.
60. Brzezinski P., and Larsson G. Redox-driven proton pumping by heme-copper oxidases. Biochim Biophys Acta 1605 (2003) 1-13
61. Brandsburg-Zabary S., Fried O., Marantz Y., Nachliel E., and Gutman M. Biophysical aspects of intra-protein proton transfer. Biochim Biophys Acta 1458 (2000) 120-134