Exploring pathways and barriers for coupled ET/PT in cytochrome c oxidase: A general framework for examining energetics and mechanistic alternatives

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1767, Issue 3, 2007, Pages 244-260

  Olsson, Mats H M ^a   Siegbahn, Per E M ^b   Blomberg, Margareta R A ^b   Warshel, Arieh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Computer simulations; Coupled electron transfer proton transfer; Cytochrome c oxidase; Dielectric of proteins; Electrostatic effects; Protonpumps

Indexed keywords

CYTOCHROME C OXIDASE;

ARTICLE; ELECTRON TRANSPORT; ENERGY TRANSFER; ENZYME ACTIVITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; SIMULATION; THEORETICAL STUDY;

COMPUTER SIMULATION; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; ELECTROSTATICS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTON PUMPS;

EID: 33947285426     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2007.01.015     Document Type: Article

References (74)

1. Wikstrom M.K.F. Proton pump coupled to cytochrome-C oxidase in mitochondria. Nature 266 (1977) 271-273
2. Michel H., Behr J., Harrenga A., and Kannt A. Cytochrome c oxidase: structure and spectroscopy. Ann. Rev. Biophys. Biomol. Struct. 27 (1998) 329-356
3. 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
4. Ostermeier C., Harrenga A., Ermler U., and Michel H. Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10547-10553
5. Yoshikawa S., Shinzawa-Itoh K., Nakashima R., Yaono R., Yamashita E., Inoue N., Yao M., Fei M.J., Libeu C.P., Mizushima T., Yamaguchi H., Tomizaki T., and Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280 (1998) 1723-1729
6. 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
7. Pfitzner U., Hoffmeier K., Harrenga A., Kannt A., Michel H., Bamberg E., Richter O.M., and Ludwig B. Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39 (2000) 6756-6762
8. Han D., Morgan J.E., and Gennis R.B. G204D, a mutation that blocks the proton-conducting D-channel of the aa(3)-type cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry 44 (2005) 12767-12774
9. Ferguson-Miller S., and Babcock G.T. Heme/copper terminal oxidases. Chem. Rev. 96 (1996) 2889-2907
10. Brzezinski P., and Larsson G. Redox-driven proton pumping by heme-copper oxidases. Biochim. Biophys. Acta 1605 (2003) 1-13
11. Wikstrom M., Verkhovsky M.I., and Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1604 (2003) 61-65
12. Olkhova E., Hutter M.C., Lill M.A., Helms V., and Michel H. Dynamic water networks in cytochrome c oxidase from Paracoccus denitrificans investigated by molecular dynamics simulations. Biophys. J. 86 (2004) 1873-1889
13. Hofacker I., and Schulten K. Oxygen and proton pathways in cytochrome c oxidase. Proteins: Struct., Funct., Bioinf. 30 (1998) 100-107
14. Song Y.F., Mao J.J., and Gunner M.R. Electrostatic environment of hemes in proteins: pK(a)s of hydroxyl ligands. Biochemistry 45 (2006) 7949-7958
15. Xu J.C., and Voth G.A. Computer simulation of explicit proton translocation in cytochrome c oxidase: The D-pathway. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 6795-6800
16. 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
17. Zheng X.H., Medvedev D.M., Swanson J., and Stuchebrukhov A.A. Computer simulation of water in cytochrome c oxidase. Biochim. Biophys. Acta - Bioenerg. 1557 (2003) 99-107
18. 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
19. Namslauer A., and Brzezinski P. Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase. FEBS Lett. 567 (2004) 103-110
20. Olsson M.H.M., Sharma P.K., and Warshel A. Simulating redox coupled proton transfer in cytochrome c oxidase: looking for the proton bottleneck. FEBS Lett. 579 (2005) 2026-2034
21. Olsson M.H.M., 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. U. S. A. 103 (2006) 6500-6505
22. Proshlyakov D.A., Pressler M.A., and Babcock G.T. Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 8020-8025
23. Wikstrom 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 - Bioenerg. 1459 (2000) 514-520
24. Karpefors M., Adelroth P., Namslauer A., Zhen Y.J., and Brzezinski P. Formation of the "peroxy" intermediate in cytochrome c oxidase is associated with internal proton/hydrogen transfer. Biochemistry 39 (2000) 14664-14669
25. Proshlyakov D.A., Pressler M.A., DeMaso C., Leykam J.F., DeWitt D.L., and Babcock G.T. Oxygen activation and reduction in respiration: involvement of redox-active tyrosine 244. Science 290 (2000) 1588-1591
26. Bloch D., Belevich I., Jasaitis A., Ribacka C., Puustinen A., Verkhovsky M.I., and Wikstrom 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
27. Siegbahn P.E.M., and Blomberg M.R.A. Important roles of tyrosines in Photosystem II and cytochrome oxidase. Biochim. Biophys. Acta - Bioenerg. 1655 (2004) 45-50
28. Blomberg M.R.A., and Siegbahn P.E.M. Quantum chemistry applied to the mechanisms of transition metal containing enzymes - Cytochrome c oxidase, a particularly challenging case. J. Comp. Chem. 27 (2006) 1373-1384
29. Warshel A. Computer Modeling of Chemical Reactions in Enzymes and Solutions. 1997 ed. (1991), John Wiley and Sons, New York
30. Warshel A., and Schlosser D.W. Electrostatic control of the efficiency of light-induced electron transfer across membranes. Proc. Natl. Acad. Sci. U. S. A. 78 (1981) 5564-5568
31. Warshel A. Conversion of light energy to electrostatic energy in the proton pump of Halobacterium halobium. Photochem. Photobiol. 30 (1979) 285-290
32. Sham Y., Muegge I., and Warshel A. Simulating proton translocations in proteins: probing proton transfer pathways in the Rhodobacter Sphaeroides Reaction Center. Proteins: Struct., Funct., Bioinf. 36 (1999) 484-500
33. Schutz C.N., and Warshel A. What are the dielectric "constants" of proteins and how to validate electrostatic models. Proteins: Struct., Funct., Bioinf. 44 (2001) 400-417
34. Burykin A., Kato M., and Warshel A. Exploring the origin of the ion selectivity of the KcsA potassium channel. Proteins: Struct., Funct., Bioinf. 52 (2003) 412-426
35. Braun-Sand S., Strajbl M., and Warshel A. Studies of proton translocations in biological systems: simulating proton transport in carbonic anhydrase by EVB based models. Biophys. J. 87 (2004) 2221-2239
36. Carra C., Iordanova N., and Hammes-Schiffer S. Proton-coupled electron transfer in a model for tyrosine oxidation in photosystem II. J. Am. Chem. Soc. 125 (2003) 10429-10436
37. Warshel A., and Hwang J.K. Simulation of the dynamics of electron-transfer reactions in polar-solvents-semiclassical trajectories and dispersed polaron approaches. J. Chem. Phys. 84 (1986) 4938-4957
38. Churg A.K., and Warshel A. Control of redox potential of cytochrome c and microscopic dielectric effects in proteins. Biochemistry 25 (1986) 1675
39. Muegge I., Qi P.X., Wand A.J., Chu Z.T., and Warshel A. The reorganization energy of cytochrome c revisited. J. Phys. Chem. B 101 (1997) 825-836
40. Warshel A., Sharma P.K., Kato M., and Parson W.W. Modeling electrostatic effects in proteins. Biochim. Biophys. Acta 1764 (2006) 1647-1676
41. T.Z. Chu, J. Villà, M. Strajbl, C. Schutz, A. Shurki, A. Warshel. beta 9.05 ed., Los Angeles 2002.
42. Lee F.S., Chu Z.T., and Warshel A. Microscopic and semimicroscopic calculations of electrostatic energies in proteins by the polaris and enzymix programs. J. Comput. Chem. 14 (1993) 161-185
43. Olsson M.H.M., Hong G., and Warshel A. Frozen density functional free energy simulations of redox proteins: computational studies of the reduction potential of plastocyanin and rusticyanin. J. Am. Chem. Soc. 125 (2003) 5025-5039
44. Svensson-Ek M., Abramson J., Larsson G., Tornroth 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
45. Siegbahn P.E.M. Modeling aspects of mechanisms for reactions catalyzed by metalloenzymes. J. Comput. Chem. 22 (2001) 1634-1645
46. Becke A.D. Density-functional exchange-energy approximation with correct asymptotic-behavior. Phys. Rev. A 38 (1988) 3098-3100
47. Becke A.D. A new mixing of hartree-fock and local density-functional theories. J. Chem. Phys. 98 (1993) 1372-1377
48. Becke A.D. Density-functional thermochemistry.3. The role of exact exchange. J. Chem. Phys. 98 (1993) 5648-5652
49. Lee C.T., Yang W.T., and Parr R.G. Development of the colle-salvetti correlation-energy formula into a functional of the electron-density. Phys. Rev. B 37 (1988) 785-789
50. Jaguar. 4.0 ed., Schrodinger Inc., Portland, OR 1991-2000.
51. Marten B., Kim K., Cortis C., Friesner R.A., Murphy R.B., Ringnalda M.N., Sitkoff D., and Honig B. New model for calculation of solvation free energies: correction of self-consistent reaction field continuum dielectric theory for short-range hydrogen bonding effects. J. Phys. Chem. 100 (1996) 11775-11788
52. Tannor D.J., Marten B., Murphy R., Friesner R.A., Sitkoff D., Nicholls A., Ringnalda M., Goddard W.A., and Honig B. Accurate first principles calculation of molecular charge-distributions and solvation energies from ab-initio quantum-Mechanics and continuum dielectric theory. J. Am. Chem. Soc. 116 (1994) 11875-11882
53. Curtiss L.A., Raghavachari K., Redfern P.C., and Pople J.A. Assessment of Gaussian-3 and density functional theories for a larger experimental test set. J. Chem. Phys. 112 (2000) 7374-7383
54. Siegbahn P.E.M., and Blomberg M.R.A. Density functional theory of biologically relevant metal centers. Ann. Rev. Phys. Chem. 50 (1999) 221-249
55. Branden M., Namslauer A., Hansson O., Aasa R., and Brzezinski P. Water-hydroxide exchange reactions at the catalytic site of heme-copper oxidases. Biochemistry 42 (2003) 13178-13184
56. Marques H.M., Cukrowski I., and Vashi P.R. Co-ordination of weak field ligands by N-acetylmicroperoxidase-8 (NAcMP8), a ferric haempeptide from cytochrome c, and the influence of the axial ligand on the reduction potential of complexes of NAcMP8. J. Chem. Soc., Dalton Trans. 8 (2000) 1335-1342
57. Brzezinski P. Internal electron-transfer reactions in cytochrome c oxidase. Biochemistry 35 (1996) 5611-5615
58. Salomonsson L., Faxen K., Adelroth P., and Brzezinski P. The timing of proton migration in membrane constituted cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17624-17629
59. Jasaitis A., Rappaport F., Pilet E., Liebl U., and Vos M.H. Activationless electron transfer through the hydrophobic core of cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10882-10886
60. Tan M.L., Balabin I., and Onuchic J.N. Dynamics of electron transfer pathways in cytochrome c oxidase. Biophys. J. 86 (2004) 1813-1819
61. Regan J.J., Ramirez B.E., Winkler J.R., Gray H.B., and Malmstrom B.G. Pathways for electron tunneling in cytochrome c oxidase. J. Bioenerg. Biomembr. 30 (1998) 35-39
62. Warshel A., and Parson W.W. Computer-simulations of electron-transfer reactions in solution and in photosynthetic reaction centers. Ann. Rev. Phys. Chem. 42 (1991) 279-309
63. Namslauer A., Pawatet A.S., Gennis R., 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
64. Paddock M., Adelroot P., Feher G., Okamura M., and Beatty J. Determination of proton transfer rates by chemical rescue: application to Bacterial Reaction Centers. Biochemistry 41 (2002) 14716-14725
65. Williams R.J.P. Multifarious couplings of energy transduction. Biochim. Biophys. Acta 505 (1978) 1-44
66. Mulkidjanian A.Y., Cherepanov D.A., Heberle J., and Junge W. Proton transfer dynamics at membrane/water interface and mechanism of biological energy conversion. Biochemistry (Moscow) 70 (2005) 251-256
67. Georgievskii Y., Medvedev E.S., and Stuchebrukhov A.A. Proton transport via the membrane surface. Biophys. J. 82 (2002) 2833-2846
68. Marantz Y., Nachliel E., Aagaard A., Brzezinski P., and Gutman M. The proton collecting function of the inner surface of cytochrome c oxidase from Rhodobacter sphaeroides. Proc. Nat. Acad. Sci. U. S. A. 95 (1998) 8590-8595
69. Georgievskii Y., Medvedev E.S., and Stuchebrukhov A.A. Proton transport via coupled surface and bulk diffusion. J. Chem. Phys. 116 (2002) 1692-1699
70. Kato M., Pisliakov A.V., and Warshel A. The barrier for proton transport in aquaporins as a challenge for electrostatic models: the role of protein relaxation in mutational calculations. Proteins: Struct., Funct., Bioinf. 64 (2006) 829-844
71. Warshel A., and Weiss R.M. Energetics of heme-protein interactions in hemoglobin. J. Am. Chem. Soc. 103 (1981) 446-451
72. Faxen K., Gilderson G., Adelroth P., and Brzezinski P. A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437 (2005) 286-289
73. 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
74. Busenlehner L.S., Salomonsson L., Brzezinski P., and Armstrong R.N. Mapping protein dynamics in catalytic intermediates of the redox-driven proton pump cytochrome c oxidase. Proc. Nat. Acad. Sci. U. S. A. 103 (2006) 15398-15403