The heme-copper oxidase superfamily shares a Zn2+-binding motif at the entrance to a proton pathway

FEBS Letters

Volumn 587, Issue 6, 2013, Pages 770-774

  Lee, Hyun Ju ^a,b   Ädelroth, Pia ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

cbb3; K pathway; Liposome; Nickel; Nitric oxide reductase; Proton transfer

Indexed keywords

HEME COPPER OXIDASE; NICKEL; OXIDOREDUCTASE; OXYGEN; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; BINDING SITE; CATALYSIS; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTON TRANSPORT; RHODOBACTER SPHAEROIDES; SITE DIRECTED MUTAGENESIS; STEADY STATE;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; BINDING SITES; ESCHERICHIA COLI; HEME; KINETICS; MODELS, MOLECULAR; MULTIGENE FAMILY; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; PROTEIN BINDING; PROTON-MOTIVE FORCE; PROTONS; RECOMBINANT PROTEINS; RHODOBACTER SPHAEROIDES; THERMODYNAMICS; ZINC;

BACTERIA (MICROORGANISMS);

EID: 84875224636     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.01.069     Document Type: Article

References (26)

1. F.L. Sousa, R.J. Alves, J.B. Pereira-Leal, M. Teixeira, and M.M. Pereira A bioinformatics classifier and database for heme-copper oxygen reductases PLoS One 6 2011 e19117
2. J. Hemp, H. Han, J.H. Roh, S. Kaplan, T.J. Martinez, and R.B. Gennis Comparative genomics and site-directed mutagenesis support the existence of only one input channel for protons in the C-family (cbb(3) oxidase) of heme-copper oxygen reductases Biochemistry 46 2007 9963 9972
3. H.J. Lee, J. Reimann, Y. Huang, and P. Ädelroth Functional proton transfer pathways in the heme-copper oxidase superfamily Biochim. Biophys. Acta 1817 2012 537 544
4. M. Brändén, F. Tomson, R.B. Gennis, and P. Brzezinski The entry point of the K-proton-transfer pathway in cytochrome c oxidase Biochemistry 41 2002 10794 10798
5. J. Ma Glutamate-89 in subunit II of cytochrome bo3 from Escherichia coli is required for the function of the heme-copper oxidase Biochemistry 38 1999 15150 15156
6. H.Y. Chang, J. Hemp, Y. Chen, J.A. Fee, and R.B. Gennis The cytochrome ba3 oxygen reductase from Thermus thermophilus uses a single input channel for proton delivery to the active site and for proton pumping Proc. Natl. Acad. Sci. USA 106 2009 16169 16173
7. S. Buschmann, E. Warkentin, H. Xie, J.D. Langer, U. Ermler, and H. Michel The structure of cbb3 cytochrome oxidase provides insights into proton pumping Science 329 2010 327 330
8. H.J. Lee, R.B. Gennis, and P. Ädelroth Entrance of the proton pathway in cbb3-type heme-copper oxidases Proc. Natl. Acad. Sci. USA 108 2011 17661 17666
9. 2O generation by bacterial nitric oxide reductase Science 330 2010 1666 1670
10. 2+ in bacterial reaction centers Proc. Natl. Acad. Sci. USA 97 2000 1542 1547
11. Y. Marantz, E. Nachliel, A. Aagaard, P. Brzezinski, and M. Gutman The proton collecting function of the inner surface of cytochrome c oxidase from Rhodobacter sphaeroides Proc. Nat. Acad. Sci. USA 95 1998 8590 8595
12. D.A. Mills, B. Schmidt, C. Hiser, E. Westley, and S. Ferguson-Miller Membrane potential-controlled inhibition of cytochrome c oxidase by zinc J. Biol. Chem. 277 2002 14894 14901
13. 2+-binding site at the P-side of the membrane FEBS Lett. 582 2008 4158 4162
14. A. Aagaard, A. Namslauer, and P. Brzezinski Inhibition of proton transfer in cytochrome c oxidase by zinc ions: delayed proton uptake during oxygen reduction Biochim. Biophys. Acta 1555 2002 133 139
15. K. Faxén, L. Salomonsson, P. Ädelroth, and P. Brzezinski Inhibition of proton pumping by zinc ions during specific reaction steps in cytochrome c oxidase Biochim. Biophys. Acta 1757 2006 388 394
16. A. Kannt, T. Ostermann, H. Müller, and M. Ruitenberg Zn(2+) binding to the cytoplasmic side of Paracoccus denitrificans cytochrome c oxidase selectively uncouples electron transfer and proton translocation FEBS Lett. 503 2001 142 146
17. L. Qin, C. Hiser, A. Mulichak, R.M. Garavito, and S. Ferguson-Miller Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase Proc. Natl. Acad. Sci. USA 103 2006 16117 16122
18. K. Muramoto, K. Hirata, K. Shinzawa-Itoh, S. Yoko-o, E. Yamashita, H. Aoyama, T. Tsukihara, and S. Yoshikawa A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase Proc. Natl. Acad. Sci. USA 104 2007 7881 7886
19. J.I. Oh, and S. Kaplan Oxygen adaptation. The role of the CcoQ subunit of the cbb3 cytochrome c oxidase of Rhodobacter sphaeroides 2.4.1 J. Biol. Chem. 277 2002 16220 16228
20. U. Flock, F.H. Thorndycroft, A.D. Matorin, D.J. Richardson, N.J. Watmough, and P. Ädelroth Defining the proton entry point in the bacterial respiratory nitric-oxide reductase J. Biol. Chem. 283 2008 3839 3845
21. V.V. Cherny, and T.E. DeCoursey PH-dependent inhibition of voltage-gated H+ currents in rat alveolar epithelial cells by Zn2+ and other divalent cations J. Gen. Phys. V114 1999 819 838
22. A. Wiedenmann, P. Dimroth, and C. von Ballmoos Deltapsi and DeltapH are equivalent driving forces for proton transport through isolated F(0) complexes of ATP synthases Biochim. Biophys. Acta 1777 2008 1301 1310
23. L. Qin, D.A. Mills, C. Hiser, A. Murphree, R.M. Garavito, S. Ferguson-Miller, and J. Hosler 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 2007 6239 6248
24. M. Svensson-Ek, J. Abramson, G. Larsson, S. Törnroth, P. Brzezinski, and S. Iwata 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
25. P. Ädelroth, M.L. Paddock, A. Tehrani, J.T. Beatty, G. Feher, and M.Y. Okamura Identification of the proton pathway in bacterial reaction centers: decrease of proton transfer rate by mutation of surface histidines at H126 and H128 and chemical rescue by imidazole identifies the initial proton donors Biochemistry 40 2001 14538 14546
26. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38