Structural Changes and Proton Transfer in Cytochrome c Oxidase

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Vilhjálmsdóttir, Jóhanna ^a   Johansson, Ann Louise ^a,b   Brzezinski, Peter ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; OXYGEN; PHENOLSULFONPHTHALEIN; PROTON; PROTON PUMP;

CHEMISTRY; ELECTRON TRANSPORT; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PH; RHODOBACTER SPHAEROIDES;

ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; OXYGEN; PHENOLSULFONPHTHALEIN; PROTON PUMPS; PROTONS; RHODOBACTER SPHAEROIDES;

EID: 84940398767     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12047     Document Type: Article

References (73)

1. Hosler, J. P., Ferguson-Miller, S., Mills, D. A. Energy transduction: Proton transfer through the respiratory complexes. Annual Review of Biochemistry 75, 165-187 (2006).
2. Yoshikawa, S. et al. Proton pumping mechanism of bovine heart cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1757, 1110-1116 (2006).
3. Namslauer, A., Brzezinski, P. Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase. FEBS Lett 567, 103-110 (2004).
4. Brzezinski, P., Gennis, R. B. Cytochrome c oxidase: exciting progress and remaining mysteries. J Bioenerg Biomembr 40, 521-531 (2008).
5. Brzezinski, P., Ädelroth, P. Design principles of proton-pumping haem-copper oxidases. Curr Opin Struct Biol 16, 465-472 (2006).
6. Richter, O. M. H., Ludwig, B. Electron transfer and energy transduction in the terminal part of the respiratory chain-Lessons from bacterial model systems. Biochimica et Biophysica Acta-Bioenergetics 1787, 626-634 (2009).
7. Belevich, I., Verkhovsky, M. I. Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid Redox Signal 10, 1-29 (2008).
8. Ferguson-Miller, S., Hiser, C., Liu, J. Gating and regulation of the cytochrome c oxidase proton pump. Biochimica et Biophysica Acta 1817, 489-494 (2012).
9. Rich, P. R., Maréchal, A. Functions of the hydrophilic channels in protonmotive cytochrome c oxidase. Journal of the Royal Society Interface 10, 183-196 (2013).
10. Kaila, V. R. I., Verkhovsky, M. I., Wikström, M. Proton-coupled electron transfer in cytochrome oxidase. Chem Rev 110, 7062-7081 (2010).
11. Konstantinov, A. A. Cytochrome c oxidase: Intermediates of the catalytic cycle and their energy-coupled interconversion. FEBS Lett 586, 630-639 (2012).
12. Blomberg, M. R. A., Siegbahn, P. E. M. Proton pumping in Cytochrome c oxidase: Energetic requirements and the role of two proton channels. Biochimica et Biophysica Acta 1837, 1165-1177 (2014).
13. Popovi?, D. M., Leontyev, I. V., Beech, D. G., Stuchebrukhov, A. A. Similarity of cytochrome c oxidases in different organisms. Proteins: Structure, Function and Bioinformatics 78, 2691-2698 (2010).
14. Lu, J., Gunner, M. R. Characterizing the proton loading site in cytochrome c oxidase. Proceedings of the National Academy of Sciences 111, 12414-12419 (2014).
15. Popovi?, D. M., Stuchebrukhov, A. A. Electrostatic study of the proton pumping mechanism in bovine heart cytochrome c oxidase. J Am Chem Soc 126, 1858-1871 (2004).
16. Seibold, S. A., Mills, D. A., Ferguson-Miller, S., Cukier, R. I. Water chain formation and possible proton pumping routes in Rhodobacter sphaeroides cytochrome c oxidase: A molecular dynamics comparison of the wild type and R481K mutant. Biochemistry 44, 10475-10485 (2005).
17. Wraight, C. A. Chance and design-Proton transfer in water, channels and bioenergetic proteins. Biochimica et Biophysica Acta-Bioenergetics 1757, 886-912 (2006).
18. Harrenga, A., Michel, H. The cytochrome c oxidase from Paracoccus denitrificans does not change the metal center ligation upon reduction. J Biol Chem 274, 33296-33299 (1999).
19. Busenlehner, L. S., Brändén, G., Namslauer, I., Brzezinski, P., Armstrong, R. N. Structural elements involved in proton translocation by cytochrome c oxidase as revealed by backbone amide hydrogen-deuterium exchange of the E286H mutant. Biochemistry 47, 73-83 (2008).
20. Busenlehner, L. S., Salomonsson, L., Brzezinski, P., Armstrong, R. N. Mapping protein dynamics in catalytic intermediates of the redox-driven proton pump cytochrome c oxidase. Proc Natl Acad Sci USA 103, 15398-15403 (2006).
21. Qin, L., Liu, J., Mills, D. A., Proshlyakov, D. A., Hiser, C., Ferguson-Miller, S. Redox-dependent conformational changes in cytochrome c oxidase suggest a gating mechanism for proton uptake. Biochemistry 48, 5121-5130 (2009).
22. Liu, J., Qin, L., Ferguson-Miller, S. Crystallographic and online spectral evidence for role of conformational change and conserved water in cytochrome oxidase proton pump. Proc Natl Acad Sci USA 108, 1284-1289 (2011).
23. Muramoto, K. et al. Bovine cytochrome c oxidase structures enable O2 reduction with minimization of reactive oxygens and provide a proton-pumping gate. Proc Natl Acad Sci USA 107, 7740-7745 (2010).
24. Tsukihara, T. 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, 15304-15309 (2003).
25. Durr, K. L. et al. 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, 865-877 (2008).
26. Svensson-Ek, M., Abramson, J., Larsson, G., Törnroth, S., Brzezinski, P., 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, 329-339 (2002).
27. Yoshikawa, S., Muramoto, K., Shinzawa-Itoh, K. Proton-pumping mechanism of cytochrome c oxidase. Annu Rev Biophys Biomolec Struct 40, 205-223 (2011).
28. Sugitani, R., Medvedev, E. S., Stuchebrukhov, A. A. Theoretical and computational analysis of the membrane potential generated by cytochrome c oxidase upon single electron injection into the enzyme. Biochimica et Biophysica Acta-Bioenergetics 1777, 1129-1139 (2008).
29. Goyal, P., Lu, J., Yang, S., Gunner, M. R., Cui, Q. Changing hydration level in an internal cavity modulates the proton affinity of a key glutamate in cytochrome c oxidase. Proc Natl Acad Sci USA 110, 18886-18891 (2013).
30. Belevich, I., Bloch, D. A., Belevich, N., Wikström, M., Verkhovsky, M. I. Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc Natl Acad Sci USA 104, 2685-2690 (2007).
31. Kaila, V. R. I., Sharma, V., Wikström, M. The identity of the transient proton loading site of the proton-pumping mechanism of cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1807, 80-84 (2011).
32. Quenneville, J., Popovic, D. M., Stuchebrukhov, A. A. Combined DFT and electrostatics study of the proton pumping mechanism in cytochrome c oxidase. Biochim Biophys Acta 1757, 1035-1046 (2006).
33. Von Ballmoos, C., Gennis, R. B., Ädelroth, P., Brzezinski, P. Kinetic design of the respiratory oxidases. Proc Natl Acad Sci USA 108, 11057-11062 (2011).
34. Brzezinski, P., Öjemyr, L. N., Ädelroth, P. Intermediates generated during the reaction of reduced Rhodobacter sphaeroides cytochrome c oxidase with dioxygen. Biochimica et Biophysica Acta-Bioenergetics 1827, 843-847 (2013).
35. Näsvik, Öjemyr L, Maréchal, A., Vestin, H., Meunier, B., Rich, P. R., Brzezinski, P. Reaction of wild-type and Glu243Asp variant yeast cytochrome c oxidase with O2. Biochimica et Biophysica Actaz-Bioenergetics 1837, 1012-1018 (2014).
36. Ädelroth, P., Brzezinski, P., Malmström, B. G. Internal electron transfer in cytochrome c oxidase from Rhodobacter sphaeroides. Biochemistry 34, 2844-2849 (1995).
37. Ädelroth, P., Ek, M., Brzezinski, P. Factors Determining Electron-Transfer Rates in Cytochrome c Oxidase: Investigation of the Oxygen Reaction in the R. sphaeroides and Bovine Enzymes. Biochim Biophys Acta 1367, 107-117 (1998).
38. Namslauer, A., Pawate, A. S., Gennis, R. B., Brzezinski, P. Redox-coupled proton translocation in biological systems: Proton shuttling in cytochrome c oxidase. Proc Natl Acad Sci USA 100, 15543-15547 (2003).
39. Brzezinski, P. Internal electron-transfer reactions in cytochrome c oxidase. Biochemistry 35, 5612-5615 (1996).
40. Pilet, E., Jasaitis, A., Liebl, U., Vos, M. H. Electron transfer between hemes in mammalian cytochrome c oxidase. Proc Natl Acad Sci USA 101, 16198-16203 (2004).
41. Heitbrink, D., Sigurdson, H., Bolwien, C., Brzezinski, P., 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, 1-10 (2002).
42. Faxén, K., Gilderson, G., Ädelroth, P., Brzezinski, P. A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437, 286-289 (2005).
43. Namslauer, A., Aagaard, A., Katsonouri, A., 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, 1488-1498 (2003).
44. Chakrabarty, S., Namslauer, I., Brzezinski, P., Warshel, A. Exploration of the cytochrome c oxidase pathway puzzle and examination of the origin of elusive mutational effects. Biochimica et Biophysica Acta-Bioenergetics 1807, 413-426 (2011).
45. Gunner, M. R., Amin, M., Zhu, X., Lu, J. Molecular mechanisms for generating transmembrane proton gradients. Biochimica et Biophysica Acta-Bioenergetics 1827, 892-913 (2013).
46. Yang, S., Cui, Q. Glu-286 rotation and water wire reorientation are unlikely the gating elements for proton pumping in cytochrome c oxidase. Biophys J 101, 61-69 (2011).
47. Kaila, V. R. I., Verkhovsky, M. I., Hummer, G., Wikström, M. Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc Natl Acad Sci USA 105, 6255-6259 (2008).
48. Pisliakov, A. V., Sharma, P. K., Chu, Z. T., Haranczyk, M., Warshel, A. Electrostatic basis for the unidirectionality of the primary proton transfer in cytochrome c oxidase. Proc Natl Acad Sci USA 105, 7726-7731 (2008).
49. Popovi?, D. M., Stuchebrukhov, A. A. Coupled electron and proton transfer reactions during the O? e transition in bovine cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1817, 506-517 (2012).
50. Popovic, D. M., Stuchebrukhov, A. A. Two conformational states of Glu242 and pKas in bovine cytochrome c oxidase. Photochemical and Photobiological Sciences 5, 611-620 (2006).
51. Brzezinski, P., Johansson, A. L. Variable proton-pumping stoichiometry in structural variants of cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1797, 710-723 (2010).
52. Pomes, R., Hummer, G., Wikström, M. Structure and dynamics of a proton shuttle in cytochrome c oxidase. Biochim Biophys Acta 1365, 255-260 (1998).
53. Fadda, E., Yu, C. H., Pomes, R. Electrostatic control of proton pumping in cytochrome c oxidase. Biochimica et Biophysica Acta-Bioenergetics 1777, 277-284 (2008).
54. Brzezinski, P., Larsson, G. Redox-driven proton pumping by heme-copper oxidases. Biochim Biophys Acta 1605, 1-13 (2003).
55. Johansson, A. L., Chakrabarty, S., Berthold, C. L., Högbom, M., Warshel, A., Brzezinski, P. Proton-transport mechanisms in cytochrome c oxidase revealed by studies of kinetic isotope effects. Biochimica et Biophysica Acta-Bioenergetics 1807, 1083-1094 (2011).
56. Pfitzner, U., et al. Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39, 6756-6762 (2000).
57. Zhu, J., Han, H., Pawate, A., Gennis, R. B. Decoupling mutations in the D-Channel of the aa3-Type cytochrome c oxidase from Rhodobacter sphaeroides suggest that a continuous hydrogen-bonded chain of waters is essential for proton pumping. Biochemistry 49, 4476-4482 (2010).
58. Lepp, H., Salomonsson, L., Zhu, J. P., Gennis, R. B., Brzezinski, P. Impaired proton pumping in cytochrome c oxidase upon structural alteration of the D pathway. Biochim Biophys Acta 1777, 897-903 (2008).
59. Brändén, G., Pawate, A. S., Gennis, R. B., Brzezinski, P. Controlled uncoupling and recoupling of proton pumping in cytochrome c oxidase. Proc Natl Acad Sci USA 103, 317-322 (2006).
60. Siletsky, S. A., Pawate, A. S., Weiss, K., Gennis, R. B., Konstantinov, A. A. Transmembrane charge separation during the ferryloxo-> oxidized transition in a nonpumping mutant of cytochrome c oxidase. J Biol Chem 279, 52558-52565 (2004).
61. Han, D. et al. Replacing Asn207 by Aspartate at the Neck of the D Channel in the aa3-Type Cytochrome c Oxidase from Rhodobacter sphaeroides Results in Decoupling the Proton Pump. Biochemistry 45, 14064-14074 (2006).
62. Gutman, M., Nachliel, E. Time-resolved dynamics of proton transfer in proteinous systems. Annu Rev Phys Chem 48, 329-356 (1997).
63. Wikström, M., Verkhovsky, M. I. The D-channel of cytochrome oxidase: An alternative view. Biochimica et Biophysica Acta-Bioenergetics 1807, 1273-1278 (2011).
64. Brändén, G., Brändén, M., Schmidt, B., Mills, D. A., Ferguson-Miller, S., Brzezinski, P. The protonation state of a heme propionate controls electron transfer in cytochrome c oxidase. Biochemistry 44, 10466-10474 (2005).
65. Karpefors, M., Ädelroth, P., Zhen, Y., Ferguson-Miller, S., Brzezinski, P. Proton uptake controls electron transfer in cytochrome c oxidase. Proc Natl Acad Sci USA 95, 13606-13611 (1998).
66. Hellwig, P. et al. Involvement of glutamic acid 278 in the redox reaction of the cytochrome c oxidase from Paracoccus denitrificans investigated by FTIR spectroscopy. Biochemistry 37, 7390-7399 (1998).
67. Lübben, M., Prutsch, A., Mamat, B., Gerwert, K. Electron transfer induces side-chain conformational changes of glutamate-286 from cytochrome bo3. Biochemistry 38, 2048-2056 (1999).
68. Mitchell, D. M., Gennis, R. B. Rapid purification of wildtype and mutant cytochrome c oxidase from Rhodobacter sphaeroides by Ni(2+ )-NTA affinity chromatography. FEBS Lett 368, 148-150 (1995).
69. Zhen, Y. et al. Overexpression and purification of cytochrome coxidase from Rhodobacter sphaeroides. Protein Expression and Purification. Protein Expr Purif 13, 326-336 (1998).
70. Brändén, M., Sigurdson, H., Namslauer, A., Gennis, R. B., Ädelroth, P., Brzezinski, P. On the role of the K-proton transfer pathway in cytochrome c oxidase. Proc Natl Acad Sci USA 98, 5013-5018 (2001).
71. Faxén, K., Brzezinski, P. The inside pH determines rates of electron and proton transfer in vesicle-reconstituted cytochrome c oxidase. Biochim Biophys Acta 1767, 381-386 (2007).
72. Namslauer, I., Lee, H. J., Gennis, R. B., Brzezinski, P. A pathogenic mutation in cytochrome c oxidase results in impaired proton pumping while retaining O2-reduction activity. Biochimica et Biophysica Acta-Bioenergetics 1797, 550-556 (2010).
73. DeLano, W. L. The PyMOL Molecular Graphics System DeLano Scientific, Palo Alto, CA, USA (2002).