Molecular dynamics simulation of water in cytochrome c oxidase reveals two water exit pathways and the mechanism of transport

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 9, 2009, Pages 1140-1150

  Sugitani, Ryogo ^a   Stuchebrukhov, Alexei A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Computer simulation; Cytochrome c oxidase; Molecular dynamics; Potential of mean force; Proton pumping mechanism; Water exit channel

Indexed keywords

ARGININE; ASPARTIC ACID; COPPER; CYTOCHROME C OXIDASE; HISTIDINE; LYSINE; MAGNESIUM ION; PROTON PUMP; THREONINE; WATER;

ARTICLE; CATALYSIS; COMPUTER SIMULATION; ENZYME ACTIVITY; ENZYME STRUCTURE; FREE ENERGY; MOLECULAR DYNAMICS; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTON TRANSPORT; STRUCTURE ANALYSIS; WATER ANALYSIS; WATER STRUCTURE; WATER TRANSPORT;

ANIMALS; CATTLE; COMPUTER SIMULATION; ELECTRON TRANSPORT COMPLEX IV; MODELS, MOLECULAR; THERMODYNAMICS; WATER;

BOVINAE;

EID: 67649511725     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.04.004     Document Type: Article

References (70)

1. Wikström M. Proton pump coupled to cytochrome c oxidase in mitochondria. Nature 266 (1977) 271-273
2. Babcock G.T., and Wikström M. Oxygen activation and the conservation of energy in cell respiration. Nature 356 (1992) 301-308
3. Ferguson-Miller S., and Babcock G.T. Heme/copper terminal oxidases. Chem. Rev. 96 (1996) 2889-2907
4. Gennis R.B. How does cytochrome oxidase pump protons?. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 12747-12749
5. Michel H., Behr J., Harrenga A., and Kannt A. Cytochrome c oxidase: structure and spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 27 (1998)
6. Wikström M. Proton translocation by bacteriorhodopsin and heme-copper oxidases. Curr. Opin. Struct. Biol. 8 (1998) 480-488
7. Schmidt B., McCracken J., and Ferguson-Miller S. A discrete water exit pathway in the membrane protein cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15539-15542
8. 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
9. Qin L., Hiser C., Mulichak A., Garavito R.M., and Ferguson-Miller S. Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 16117-16122
10. 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 (1999) 180-187
11. Michel H. The mechanism of proton pumping by cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 12819-12824
12. 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) 1995
13. Verkhovsky M.I., Jasaitis A., Verkhovskaya M.L., Morgan J.E., and Wikstrom M. Proton translocation by cytochrome c oxidase. Nature 400 (1999) 480-483
14. Hofacker I., and Schulten K. Oxygen and proton pathways in cytochrome c oxidase. Proteins 30 (1998) 100-107
15. Sugitani R., Medvedev E.S., and Stuchebrukhov A.A. Theoretical and computational analysis of the membrane potential generated by cytochrome c oxidase upon single electron injection into the enzyme. Biochim. Biophys. Acta 1777 (2008) 1129-1139
16. Kaila R.I., Verkhovsky M.I., Hummer G., and Wikstrom M. Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 6255-6259
17. Fadda E., Yu C.-H., and Pomés R. Electrostatic control of proton pumping in cytochrome c oxidase. Biochim. Biophys. Acta 1777 (2008) 277-284
18. Popovic D.M., and Stuchebrukhov A.A. Proton exit channels in bovine cytochrome c oxidase. J. Phys. Chem. B. 109 (2005) 1999-2006
19. Pawate A.S., Morgan J., Namaslauer 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
20. Humphrey W., Dalke A., and Schulten K. VMD - visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38
21. Sanner M.F., Olson A.J., and Sphener J.-C. Proc. 11th Annu. ACM Sympos. Comput. Geom. (1995) C6-C7
22. Connolly M.L. Solvent-accessible surfaces of proteins and nucleic acids. Science 221 (1983) 709-713
23. Johansson M.P., Kaila V.R.I., and Laakkonen L. Charge parameterization of the metal centers in cytochrome c oxidase. J. Comput. Chem. 29 (2008) 753-767
24. Tashiro M., and Stuchebrukhov A.A. Thermodynamic properties of internal water molecules in the hydrophobic cavity around the catalytic center of cytochrome c oxidase. J. Phys. Chem. B 109 (2005) 1015-1022
25. Duan Y., Wu C., Chowdhury S., Lee M.C., Xiong G., Zhang W., Yang R., Cieplak P., Luo R., Lee T., Caldwell J., Wang J., and Kollman P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24 (2003) 1999-2012
26. Popovic D.M., and Stuchebrukhov A.A. Electrostatic study of the proton pumping mechanism in cytochrome c oxidase. J. Am. Chem. Soc. 126 (2004) 1858-1871
27. Lindahl E., Hess B., and Spoel D.V.D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7 (2001) 306-317
28. Sorin E.J., and Pande V.S. Empirical force-field assessment: the interplay between backbone torsions and noncovalent term scaling. J. Comput. Chem. 26 (2005) 682-690
29. Mahoney M.W., and Jorgensen W.L. A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions. J. Chem. Phys. 112 (2000) 8910-8922
30. Darden T., York D., and Pedersen L. Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J. Chem. Phys. 98 (1993) 10089-10092
31. Essmann U., Perera L., Berkowitz M., Darden T., Lee H., and Pedersen L.G. A smooth particle mesh Ewald method. J. Chem. Phys. 103 (1995) 8577-8593
32. Hoover W.G. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A. 31 (1985) 1695-1697
33. Parrinello M., and Rahman A. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52 (1981) 7182-7190
34. Miyamoto S., and Kollman P.A. Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water molecules. J. Comput. Chem. 13 (1992) 952-962
35. Hess B., Bekker H., Berendsen H.J.C., and Fraaije J.G.E.M. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18 (1997) 1463-1472
36. Torrie G.M., and Valleau J.P. Nonphysical sampling distributions in Monte Carlo free-energy estimation: umbrella sampling. J. Comp. Phys. 23 (1977) 187-199
37. Kumar S., Bouzida D., Swendsen R.H., Kollman P.A., and Rosenberg J.H. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13 (1992) 1011-1021
38. Berne B.J., Borkovec M., and Straub J.E. Classical and modern methods in reaction rate theory. J. Phys. Chem. 92 (1988) 3711-3725
39. Frauenfelder H., and Wolynes P.G. Rate theories and puzzles of hemeprotein kinetics. Science 229 (1985) 337-345
40. Crouzy S., Woolf T.B., and Roux B. A molecular dynamics study of gating in dioxolane-linked Gramicidin A channels. Biophys. J. 67 (1994) 1370-1386
41. Hummer G. Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium replica molecular dynamics simulations. New J. Phys. 7 (2005) 1-14
42. + inside Gramicidin A: a comparative study of four computational methods. Biophys. Chem. 124 (2006) 268-278
43. Petrek M., Otyepka M., Banás P., Kosinová P., Koca J., and Dambrosky J. CAVER: a new tool to explore routes from protein clefts, pockets, and cavities. B.M.C. Bioinform. 7 (2006) 316-324
44. Ho B.K., and Gruswitz F. HOLLOW: generating accurate representation of channel and interior surfaces in molecular structures. B.M.C. Struct. Biol. 8 (2008) 1-6
45. Zheng X., Medvedev D.M., Swanson J., and Stuchebrukhov A.A. Computer simulation of water in cytochrome c oxidase. Biochim. Biophys. Acta 1557 (2003) 99-107
46. 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
47. Cukier R.I. Quantum molecular dynamics simulation of proton transfer in cytochrome c oxidase. Biochim. Biophys. Acta 1656 (2004) 189-202
48. 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
49. Seibold S.A., Mills D.A., Ferguson-Miller S., and Cukier R.I. Water chain formation and possible proton pumping routes in Rhodobacter sphaeroides cytochrome c oxdiase: a molecular dynamics comparison of the wild type and R481K mutant. Biochemistry 44 (2005) 10475-10485
50. 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. U. S. A. 102 (2005) 10478-10481
51. Harrenga A., and Michel H. The cytochrome c oxidase from Paraccocus denitrificans does not change the metal center ligation upon reduction. J. Biol. Chem. 274 (1999) 33296-33299
52. 3 oxidase from Thermus thermophilus. Acta Cryst. D61 (2005) 340-343
53. Xu J., Sharpe M.A., Qin L., Ferguson-Miller S., and Voth G.A. Storage of an excess proton in the hydrogen-bonded network of the D-pathway of cytochrome c oxidase: identification of a protonated water cluster. J. Am. Chem. Soc. 129 (2007) 2910-2913
54. Belevich I., Bloch D.A., 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
55. Brookes P.S., Rolfe D.F.S., and Brand M.D. The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: comparison with isolated mitochondria. J. Membr. Biol. 155 (1996) 167-174
56. B. Structure 15 (1997) 1339-1359
57. Nagle J.F., and Tristram-Nagle S. Structure of lipid bilayers. Biochim. Biophys. Acta 1469 (2000) 159-195
58. Dürr K.L., Koepke J., Hellwig P., Müller H., Angerer H., Peng G., Olkhova E., Richter O.-M.H., Ludwig B., and Michel H. A D-pathway mutation decouples the Paracoccus denitrificans cytochrome c oxidase by altering the side-chain orientation of a distant conserved glutamate. J. Mol. Biol. 384 (2008) 865-877
59. Wikström M., and Verkhovsky M.I. Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases. Biochim. Biophys. Acta 1767 (2007) 1200-1214
60. Brzezinski P., and Ädelroth P. Design principles of proton-pumping haem-copper oxidases. Curr. Opin. Struct. Biol. 16 (2006) 465-472
61. Faxén K., Gilderson G., Ädelroth P., and Brzezinski P. A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437 (2005) 286-289
62. Sharpe M.A., Krzyaniak M.D., Xu S., McCracken J., and Ferguson-Miller S. EPR evidence of cyanide binding to the Mn(Mg) center of cytochrome c oxidase: support for CuA-Mg involvement in proton pumping. Biochemistry 48 (2009) 328-335
63. Sharpe M.A., and Ferguson-Miller S. A chemically explicit model for the mechanism of proton pumping in heme-copper oxidases. J. Bioenerg. Biomembr. 40 (2008) 541-549
64. 3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I. J. Bioenerg. Biomembr. 30 (1998) 89-97
65. Lepp H., Salomonsson L., Zhu J.-P., Gennis R.B., and Brzezinski P. Impaired proton pumping in cytochrome c oxidase upon structural alteration of the D pathway. Biochim. Biophys. Acta 1777 (2008) 897-903
66. 3-type cytochrome c oxidase from Rhodobacter sphaeroides results in decoupling the proton pump. Biochemistry 45 (2006) 14064-14074
67. 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 (2005) 6500-6505
68. + conduction in the D-pathway of cytochrome c oxidase: a study of the wild type and N98D mutant enzymes. Biochim. Biophys. Acta 1757 (2006) 852-859
69. Olkhova E., Helms V., and Michel H. Titration behavior of residues at the entrance of the D-pathway of cytochrome c oxidase from Paracoccus denitrificans investigated by continuum electrostatic calculations. Biophys. J. 89 (2005) 2324-2331
70. Bränden 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. U. S. A. 103 (2006) 317-322