Alternative initial proton acceptors for the D pathway of rhodobacter sphaeroides cytochrome c oxidase

Biochemistry

Volumn 50, Issue 14, 2011, Pages 2820-2828

  Varanasi, Lakshman ^a   Hosler, Jonathan ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BULK SOLVENTS; CARBOXYL GROUPS; CYTOCHROME C OXIDASE; DIRECT CONTACT; ENTRY REGION; IN-LINE; PH RANGE; PROTEIN STRUCTURES; PROTON ACCEPTORS; PROTON UPTAKE; RHODOBACTER SPHAEROIDES; THIOL GROUPS; WILD TYPES;

PROTONS;

ARACHIDONIC ACID; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CARBOXYL GROUP; CYTOCHROME C OXIDASE; PROTEIN SUBUNIT; THIOL GROUP; VALINOMYCIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROGEN BOND; LIPID VESICLE; MOLECULAR DYNAMICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; RHODOBACTER SPHAEROIDES; STEADY STATE; STRUCTURE ANALYSIS; WILD TYPE;

ASPARTIC ACID; BACTERIAL PROTEINS; BINDING SITES; BIOCATALYSIS; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MUTATION; PROTEIN SUBUNITS; PROTONS; RHODOBACTER SPHAEROIDES;

RHODOBACTER SPHAEROIDES;

EID: 79953712351     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi102002v     Document Type: Article

References (46)

1. Richter, O. M. and Ludwig, B. (2003) Cytochrome c oxidase: Structure, function, and physiology of a redox-driven molecular machine Rev. Physiol. Biochem. Pharmacol. 147, 47-74
2. Hosler, J. P., Ferguson-Miller, S., and Mills, D. A. (2006) Energy transduction: Proton transfer through the respiratory complexes Annu. Rev. Biochem. 75, 165-187 (Pubitemid 44118030)
3. Brzezinski, P. and Gennis, R. B. (2008) Cytochrome c oxidase: Exciting progress and remaining mysteries J. Bioenerg. Biomembr. 40, 521-531
4. Brzezinski, P. and Ädelroth, P. (2006) Design principles of proton-pumping haem-copper oxidases Curr. Opin. Struct. Biol. 16, 465-472 (Pubitemid 44149073)
5. Wikström, M. and Verkhovsky, M. I. (2007) Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases Biochim. Biophys. Acta 1767, 1200-1214 (Pubitemid 47498307)
6. Sharpe, M. A. and Ferguson-Miller, S. (2008) A chemically explicit model for the mechanism of proton pumping in heme-copper oxidases J. Bioenerg. Biomembr. 40, 541-549
7. 3 and cytochrome bo J. Bioenerg. Biomembr. 25, 121-136 (Pubitemid 23133520)
8. Richter, O. M. and Ludwig, B. (2009) Electron transfer and energy transduction in the terminal part of the respiratory chain: Lessons from bacterial model systems Biochim. Biophys. Acta 1787, 626-634
9. Sharpe, M., Qin, L., and Ferguson-Miller, S. (2005) Proton Entry, Exit and Pathways in Cytochrome Oxidase: Insight from "Conserved" Water. In Biophysical and Structural Aspects of Bioenergetics (Wikström, M., Ed.), pp 26 - 54, Royal Society of Chemistry Publishing, Cambridge, U.K.
10. Wraight, C. A. (2006) Chance and design: Proton transfer in water, channels and bioenergetic proteins Biochim. Biophys. Acta 1757, 886-912 (Pubitemid 44462697)
11. Wikström, M., Jasaitis, A., Backgren, C., Puustinen, A., and Verkhovsky, M. I. (2000) The role of the D- and K-pathways of proton transfer in the function of the haem-copper oxidases Biochim. Biophys. Acta 1459, 514-520 (Pubitemid 30612427)
12. Brzezinski, P. and Ädelroth, P. (1998) Pathways of proton transfer in cytochrome c oxidase J. Bioenerg. Biomembr. 30, 99-107 (Pubitemid 28262413)
13. Henry, R. M., Yu, C. H., Rodinger, T., and Pomes, R. (2009) Functional hydration and conformational gating of proton uptake in cytochrome c oxidase J. Mol. Biol. 387, 1165-1185
14. Koepke, J., Olkhova, E., Angerer, H., Müller, H., Peng, G., and Michel, H. (2009) High resolution crystal structure of Paracoccus denitrificans cytochrome c oxidase: New insights into the active site and the proton transfer pathways Biochim. Biophys. Acta 1787, 635-645
15. Kaila, V. R., Sharma, V., and Wikström, M. (2011) The identity of the transient proton loading site of the proton-pumping mechanism of cytochrome c oxidase Biochim. Biophys. Acta 1807, 80-84
16. Wikström, M., Verkhovsky, M. I., and Hummer, G. (2003) Water-gated mechanism of proton translocation by cytochrome c oxidase Biochim. Biophys. Acta 1604, 61-65 (Pubitemid 36588691)
17. Qin, L., Liu, J., Mills, D. A., Proshlyakov, D. A., Hiser, C., and Ferguson-Miller, S. (2009) Redox-dependent conformational changes in cytochrome c oxidase suggest a gating mechanism for proton uptake Biochemistry 48, 5121-5130
18. Tomson, F. L., Morgan, J. E., Gu, G., Barquera, B., Vygodina, T. V., and Gennis, R. B. (2003) Substitutions for glutamate 101 in subunit II of cytochrome c oxidase from Rhodobacter sphaeroides result in blocking the proton-conducting K-channel Biochemistry 42, 1711-1717 (Pubitemid 36205980)
19. Smirnova, I. A., Ädelroth, P., Gennis, R. B., and Brzezinski, P. (1999) Aspartate-132 in Cytochrome c Oxidase from Rhodobacter sphaeroides is Involved in a Two-Step Proton Transfer during Oxo-Ferryl Formation Biochemistry 38, 6826-6833
20. Ädelroth, P. and Hosler, J. (2006) Surface proton donors for the D-pathway of cytochrome c oxidase in the absence of subunit III Biochemistry 45, 8308-8318 (Pubitemid 44036537)
21. Hosler, J. P. (2004) 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, 332-339 (Pubitemid 38526196)
22. Svensson-Ek, M., Abramson, J., Larsson, G., Törnroth, S., Brzezinski, P., and Iwata, S. (2002) 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
23. Yoshikawa, S., Shinzawa-Itoh, K., and Tsukihara, T. (1998) Crystal structure of bovine heart cytochrome c oxidase at 2.8 Å resolution J. Bioenerg. Biomembr. 30, 7-14 (Pubitemid 28262402)
24. Harrenga, A. and Michel, H. (1999) The cytochrome c oxidase from Paracoccus denitrificans does not change the metal center ligation upon reduction J. Biol. Chem. 274, 33296-33299 (Pubitemid 129511629)
25. Mills, D. A., Tan, Z., Ferguson-Miller, S., and Hosler, J. (2003) 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, 7410-7417 (Pubitemid 36735818)
26. Gilderson, G., Salomonsson, L., Aagaard, A., Gray, J., Brzezinski, P., and Hosler, J. (2003) Subunit III of cytochrome c oxidase of Rhodobacter sphaeroides is required to maintain rapid proton uptake through the D pathway at physiologic pH Biochemistry 42, 7400-7409 (Pubitemid 36740492)
27. 3-type cytochrome c oxidase from Rhodobacter sphaeroides Biochemistry 44, 12767-12774 (Pubitemid 41377316)
28. Muramoto, K., Hirata, K., Shinzawa-Itoh, K., Yoko-o, S., Yamashita, E., Aoyama, H., Tsukihara, T., and Yoshikawa, S. (2007) 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, 7881-7886 (Pubitemid 47185845)
29. Pfitzner, U., Hoffmeier, K., Harrenga, A., Kannt, A., Michel, H., Bamberg, E., Richter, O. M., and Ludwig, B. (2000) Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans Biochemistry 39, 6756-6762 (Pubitemid 30390366)
30. Pawate, A. S., Morgan, J., Namslauer, A., Mills, D., Brzezinski, P., Ferguson-Miller, S., and Gennis, R. B. (2002) 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, 13417-13423 (Pubitemid 35303901)
31. Namslauer, A., Pawate, A. S., Gennis, R. B., and Brzezinski, P. (2003) Redox-coupled proton translocation in biological systems: Proton shuttling in cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 100, 15543-15547 (Pubitemid 38021026)
32. Brändén, G., Pawate, A. S., Gennis, R. B., and Brzezinski, P. (2006) Controlled uncoupling and recoupling of proton pumping in cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 103, 317-322 (Pubitemid 43122398)
33. Fetter, J., Sharpe, M., Qian, J., Mills, D., Ferguson-Miller, S., and Nicholls, P. (1996) Fatty acids stimulate activity and restore respiratory control in a proton channel mutant of cytochrome c oxidase FEBS Lett. 393, 155-160 (Pubitemid 26298087)
34. Sone, N., Yoshida, M., Hirata, H., and Kagawa, Y. (1977) Asolectin purification procedure J. Biochem. 81, 519-528
35. Keen, N. T., Tamaki, S., Kobayashi, D., and Trollinger, D. (1988) Improved Broad-Host-Range Plasmids for DNA Cloning in Gram-Negative Bacteria Gene 70, 191-197 (Pubitemid 18263496)
36. 3-type cytochrome c oxidase of Rhodobacter sphaeroides Mol. Microbiol. 6, 635-642
37. Zhen, Y., Qian, J., Follmann, K., Hayward, T., Nilsson, T., Dahn, M., Hilmi, Y., Hamer, A. G., Hosler, J. P., and Ferguson-Miller, S. (1998) Overexpression and purification of cytochrome c oxidase from Rhodobacter sphaeroides Protein Expression Purif. 13, 326-336 (Pubitemid 28378826)
38. Fetter, J. R., Qian, J., Shapleigh, J., Thomas, J. W., Garcia-Horsman, A., Schmidt, E., Hosler, J., Babcock, G. T., Gennis, R. B., and Ferguson-Miller, S. (1995) Possible proton relay pathways in cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 92, 1604-1608
39. Qin, L., Hiser, C., Mulichak, A., Garavito, R. M., and Ferguson-Miller, S. (2006) 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, 16117-16122 (Pubitemid 44715161)
40. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling Electrophoresis 18, 2714-2723 (Pubitemid 28059943)
41. Dürr, K. L., Koepke, J., Hellwig, P., Muller, H., Angerer, H., Peng, G., Olkhova, E., Richter, O. M., Ludwig, B., and Michel, H. (2008) 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
42. 3-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
43. Qin, L., Mills, D. A., Hiser, C., Murphree, A., Garavito, R. M., Ferguson-Miller, S., and Hosler, J. (2007) Crystallographic location and mutational analysis of Zn and Cd inhibitory sites and role of lipidic carboxylates in rescuing proton path mutants in cytochrome c oxidase Biochemistry 46, 6239-6248 (Pubitemid 46842867)
44. Mills, D. A. and Hosler, J. P. (2005) Slow proton transfer through the pathways for pumped protons in cytochrome c oxidase induces suicide inactivation of the enzyme Biochemistry 44, 4656-4566
45. Nagle, J. F. and Tristram-Nagle, S. (1983) Hydrogen bonded chain mechanisms for proton conduction and proton pumping J. Membr. Biol. 74, 1-14 (Pubitemid 13069959)
46. Gu, W. and Helms, V. (2009) Tightly connected water wires facilitate fast proton uptake at the proton entrance of proton pumping proteins J. Am. Chem. Soc. 131, 2080-2081