Replacing Asn207 by aspartate at the neck of the D channel in the aa 3-type cytochrome c oxidase from Rhodobacter sphaeroides results in decoupling the proton pump

Biochemistry

Volumn 45, Issue 47, 2006, Pages 14064-14074

  Han, Dan ^a   Namslauer, Andreas ^b   Pawate, Ashtamurthy ^a   Morgan, Joel E ^a,c   Nagy, Stanislav ^a,d   Vakkasoglu, Ahmet S ^a   Brzezinski, Peter ^b   Gennis, Robert B ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c Research Rensselaer Polytechnic Institute   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CATALYSIS; FREE ENERGY; MOLECULAR DYNAMICS; PROTONS; REACTION KINETICS;

CYTOCHROME C OXIDASE; DECOUPLING; PROTON PUMPS; RHODOBACTER SPHAEROIDES;

ENZYME KINETICS;

ASPARAGINE; ASPARTIC ACID; CYTOCHROME C OXIDASE; OXYGEN; PROTON PUMP; WATER;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENZYME ACTIVITY; ENZYME MECHANISM; FORCE; MEMBRANE TRANSPORT; MUTANT; MUTATION; NONHUMAN; PKA; PRIORITY JOURNAL; PROTON TRANSPORT; REDUCTION; RHODOBACTER SPHAEROIDES;

ASPARAGINE; ASPARTIC ACID; ELECTRON TRANSPORT COMPLEX IV; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MUTATION; PROTON PUMPS; RHODOBACTER SPHAEROIDES; SPECTROPHOTOMETRY, ULTRAVIOLET;

RHODOBACTER SPHAEROIDES;

EID: 33751569076     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061465q     Document Type: Article

References (39)

1. Wikström, M., and Verkhovsky, M. I. (2006) Towards the mechanism of proton pumping by the haem-copper oxidases, Biochim. Biophys. Acta, 1757, 1047-1051.
2. Wikström, M. (2004) Cytochrome c oxidase: 25 Years of the elusive proton pump, Biochim. Biophys. Acta 1655, 241-247.
3. Verkhovsky, M. I., Belevich, I., Bloch, D. A., and Wikstrom, M. (2006) Elementary steps of proton translocation in the catalytic cycle of cytochrome oxidase, Biochim. Biophys. Acta 1757, 401-407.
4. Branden, G., Gennis, R. B., and Brzezinski, P. (2006) Transmembrane proton translocation by cytochrome c oxidase, Biochim. Biophys. Acta 1757, 1052-1063.
5. Michel, H. (1999) Cytochrome c oxidase: Catalytic cycle and mechanisms of proton pumping-A discussion, Biochemistry 38, 15129-15140.
6. 2 reduction site, FEBS Lett. 555, 8-12.
7. Pawate, A. S., J., M., Namslauer, A., Mills, D. A., 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.
8. Namslauer, A., Pawate, A., 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.
9. Siletsky, S. A., Pawate, A. S., Weiss, K., Gennis, R. B., and Konstantinov, A. A. (2004) Transmembrane charge separation during the ferryl-oxo ∅ oxidized transition in a nonpumping mutant of cytochrome c oxidase, J. Biol. Chem. 279, 52558-52565.
10. Pfitzner, U., Hoffmeier, K., Harrenga, A., Kannt, A., Michel, H., Bamberg, E., Richter, O.-M. H., and Ludwig, B. (2000) Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans, Biochemistry 39, 6756-6762.
11. 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, 317-22.
12. Olkhova, E., Helms, V., and Michel, H. (2005) 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, 2324-2331.
13. Vakkasoglu, A. S., Morgan, J. E., Han, D., Pawate, A. S., and Gennis, R. B. (2006) Mutations which decouple the proton pump of the cytochrome c oxidase from Rhodobacter sphaeroides perturb the environment of glutamate 286, FEBS Lett. 580, 4613-4617.
14. Sistrom, W. R. (1962) The kinetics of the synthesis of photopigments in Rhodopseudomonas sphaeroides, J. Gen. Microbiol. 28, 607-616.
15. 2+-NTA affinity chromatography, FEBS Lett. 368, 148-150.
16. Hiser, C., Mills, D. A., Schall, M., and Ferguson-Miller, S. (2001) C-Terminal truncation and histidine-tagging of cytochrome c oxidase subunit II reveals the native processing site, shows involvement of the C-terminus in cytochrome c binding, and improves the assay for proton pumping, Biochemistry 40, 1606-1615.
17. A site in cytochrome-c oxidase of Paracoccus denitrificans by replacement of Met227 with isoleucine, Eur. J. Biochem. 234, 686-693.
18. Blair, D. F., Ellis, J., Walther, R., Wang, H., Gray, H. B., and Chan, S. I. (1986) Spectroelectrochemical study of cytochrome c oxidase: pH and temperature dependences of the cytochrome potentials, J. Biol. Chem. 261, 11524-11537.
19. 3 reduction. The neoclassical model revisited, Ann. N.Y. Acad. Sci. 550, 59-67.
20. Jasaitis, A., Verkhovsky, M. I., Morgan, J. E., Verkhovskaya, M. L., and Wikström, M. (1999) Assignment and charge translocation stoichiometries of the major electrogenic phases in the reaction of cytochrome c oxidase with dioxygen, Biochemistry 38, 2697-2706.
21. Rigaud, J.-L., Mosser, G., Lacapere, J.-J., Olofsson, A., Levy, D., and Ranck, J.-L. (1997) Bio-beads: An efficient strategy for two-dimensional crystallization of membrane proteins, J. Struct. Biol. 118, 226-235.
22. Sarti, P., Jones, M. G., Antonini, G., Malatesta, F., Colosimo, A., Wilson, M. T., and Brunori, M. (1985) Kinetics of redox-linked proton pumping activity of native and subunit III-depleted cytochrome c oxidase: A stopped-flow investigation, Proc. Natl. Acad. Sci. U.S.A. 82, 4876-4880.
23. Hummel, B. C. (1959) A modified spectrophotometric determination of chymotrypsin, trypsin, and thrombin, Can. J. Biochem. Physiol. 37, 1393-1399.
24. Verkhovsky, M. I., Morgan, J. E., and Wikström, M. (1995) Control of electron delivery to the oxygen reduction site of cytochrome c oxidase: A role for protons, Biochemistry 34, 7483-7491.
25. Brändén, M., Sigurdson, H., Namslauer, A., Gennis, R. B., Ädelroth, P., and Brzezinski, P. (2001) On the role of the K-proton transfer pathway in cytochrome c oxidase, PNAS 98, 5013-5018.
26. Nyquist, R. M., Heitbrink, D., Bolwien, C., Wells, T. A., Gennis, R. B., and Heberle, J. (2001) Perfusion-induced redox differences in cytochrome c oxidase: ATR/FT-IR spectroscopy, FEBS Lett. 505, 63-67.
27. Nyquist, R. M., Heitbrink, D., Bolwien, C., Gennis, R. B., and Heberle, J. (2003) Direct observation of protonation reactions during the catalytic cycle of cytochrome c oxidase, Proc. Natl. Acad. Sci. U.S.A. 100, 8715-8720.
28. Iwaki, M., Breton, J., and Rich, P. R. (2002) ATR-FTIR difference spectroscopy of the PM intermediate of bovine cytochrome c oxidase, Biochim. Biophys. Acta 1555, 116-121.
29. Salomonsson, L., Faxen, K., Adelroth, P., and Brzezinski, P. (2005) The timing of proton migration in membrane-reconstituted cytochrome c oxidase, Proc. Natl. Acad. Sci. U.S.A. 102, 17624-17629.
30. Namslauer, A., Aagaard, A., Katsonouri, A., and Brzezinski, P. (2003) 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, 1488-1498.
31. Brädén, G., Brädén, M., Schmidt, B., Mills, D. A., Ferguson-Miller, S., and Brzezinski, P. (2005) The protonation state of a heme propionate controls electrontransfer in cytochrome c oxidase, Biochemistry 44, 10466-10474.
32. M and F intermediates of bovine and Paracoccus denitrificans cytochrome c oxidase, Biochemistry 42, 8809-8817.
33. M intermediate of Paracoccus denitrificans cytochrome c oxidase, Biochemistry 43, 14370-14378.
34. Marantz, Y., Nachliel, E., Aagaard, A., Brzezinski, P., and Gutman, M. (1998) The proton collecting function of the inner surface of cytochrome c oxidase from Rhodobacter sphaeroides, Proc. Natl. Acad. Sci. U.S.A. 95, 8590-8595.
35. Marantz, Y., Einarsdóttir, Ó., Nachliel, E., and Gutman, M. (2001) Proton-collecting properties of bovine heart cytochrome c oxidase: Kinetic and electrostatic analysis, Biochemistry 40, 15086-15097.
36. Ruitenberg, M., Kannt, A., Bamberg, E., Fendler, K., and Michel, H. (2002) Reduction of cytochrome c oxidase by a second electron leads to proton translocation, Nature 417, 99-102.
37. Vakkasoglu, A., Morgan, J. E., Han, D., Pawate, A., and Gennis, R. B. (2006) ATR-FTIR investigation of a possible conformational change in the vicinity of Glu286 resulting from the Asn139Asp mutation which decouples the proton pump of the cytochrome c oxidase from Rhodobacter shpaeroides, FEBS Lett. 580, 4613-4617.
38. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graph. 14, 33-38.
39. Svensson-Ek, M., Abramson, J., Larsson, G., Tornroth, 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.