The causes of reduced proton-pumping efficiency in type B and C respiratory heme-copper oxidases, and in some mutated variants of type A

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 7, 2014, Pages 999-1003

  Rauhamäki, Virve ^a   Wikström, Mårten ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Cellular respiration; Heme copper oxidase; Heme copper oxygen reductase; Proton pumping

Indexed keywords

ASPARAGINE DERIVATIVE; ASPARTIC ACID; CYTOCHROME C OXIDASE; OXIDOREDUCTASE; PROTON PUMP; RESPIRATORY HEME COPPER OXIDASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CONTROLLED STUDY; ENZYME MODIFICATION; GENE MUTATION; GENETIC VARIABILITY; NONHUMAN; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTON TRANSPORT; RHODOBACTER SPHAEROIDES; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA; RHODOBACTER SPHAEROIDES;

CELLULAR RESPIRATION; HEME-COPPER OXIDASE; HEME-COPPER OXYGEN REDUCTASE; PROTON PUMPING;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ELECTRON TRANSPORT COMPLEX IV; MOLECULAR SEQUENCE DATA; MUTATION; OXIDOREDUCTASES; PROTONS; RHODOBACTER SPHAEROIDES;

EID: 84901823829     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2014.02.020     Document Type: Article

References (46)

1. M.M. Pereira, M. Santana, and M. Teixeira A novel scenario for the evolution of heme-copper oxygen reductases Biochim. Biophys. Acta 1505 2001 185 208 (Pubitemid 32378771)
2. M. Wikström, and M.I. Verkhovsky Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases Biochim. Biophys. Acta 1767 2007 1200 1214 (Pubitemid 47498307)
3. A. Puustinen, M. Finel, M. Virkki, and M. Wikström Cytochrome o (bo) is a proton pump in Paracoccus denitrificans and Escherichia coli FEBS Lett. 249 1989 163 167
4. M. Raitio, and M. Wikström An alternative cytochrome oxidase of Paracoccus denitrificans functions as a proton pump Biochim. Biophys. Acta 1186 1994 100 106 (Pubitemid 24213679)
5. 3-type cytochrome c oxidases of Paracoccus denitrificans reveals significant differences in proton-pump design Mol. Microbiol. 20 1996 1247 1260 (Pubitemid 26225432)
6. 3-type cytochrome c oxidase from Rhodobacter sphaeroides, a proton-pumping heme-copper oxidase Biochim. Biophys. Acta 1365 1998 421 434 (Pubitemid 29012399)
7. J.-W.L. de Gier, M. Lübben, W.N.M. Reijnders, C.A. Tipker, D.-J. Slotboom, R.J.M. van Spanning, A.H. Stouthamer, and J. van der Oost The terminal oxidases of Paracoccus denitrificans Mol. Microbiol. 13 1994 183 196
8. 3 Proc. Natl. Acad. Sci. U. S. A. 109 2012 7286 7291
9. 2 environments Proc. Natl. Acad. Sci. U. S. A. 108 2011 14109 14114
10. + per electron Proc. Natl. Acad. Sci. U. S. A. 109 2012 E2144
11. 3-type cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 109 2012 E2145
12. C.M. Gomes, C. Backgren, M. Teixeira, A. Puustinen, M.L. Verkhovskaya, M. Wikström, and M.I. Verkhovsky Heme-copper oxidases with modified D- and K-pathways are yet efficient proton pumps FEBS Lett. 497 2001 159 164 (Pubitemid 32476896)
13. 3-type cytochrome c oxidase from Thermus thermophilus FEBS Lett. 434 1998 17 22 (Pubitemid 28404654)
14. P. Brzezinski, and A.L. Johansson Variable proton-pumping stoichiometry in structural variants of cytochrome c oxidase Biochim. Biophys. Acta 1797 2010 710 723
15. J.W. Thomas, A. Puustinen, J.O. Alben, R.B. Gennis, and M. Wikström Substitution of asparagine for aspartate-135 in subunit I of the cytochrome bo ubiquinol oxidase of Escherichia coli eliminates proton-pumping activity Biochemistry 32 1993 10923 10928 (Pubitemid 23327830)
16. U. Pfitzner, K. Hoffmeier, A. Harrenga, A. Kannt, H. Michel, E. Bamberg, O.M.H. Richter, and B. Ludwig Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans Biochemistry 39 2000 6756 6762 (Pubitemid 30390366)
17. A.S. Pawate, J. Morgan, A. Namslauer, D. Mills, P. Brzezinski, S. Ferguson-Miller, and R.B.B. Gennis 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 (Pubitemid 35303901)
18. A. Namslauer, A.S. Pawate, R.B. Gennis, and P. Brzezinski Redox-coupled proton translocation in biological systems: proton shuttling in cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 100 2003 15543 15547 (Pubitemid 38021026)
19. 3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I J. Bioenerg. Biomembr. 30 1998 89 97 (Pubitemid 28262412)
20. K.L. Dürr, J. Koepke, P. Hellwig, H. Müller, H. Angerer, G. Peng, E. Olkhova, O.M. Richter, B. Ludwig, and H. Michel 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
21. 3 from Thermus thermophilus Proc. Natl. Acad. Sci. U. S. A. 109 2012 5259 5264
22. 3 oxidase from Thermus thermophilus Biochim. Biophys. Acta 1767 2007 1383 1392 (Pubitemid 350179716)
23. 3 cytochrome c oxidase from Thermus thermophilus Biochim. Biophys. Acta 1817 2012 650 657
24. S.A. Siletsky, A.S. Pawate, K. Weiss, R.B. Gennis, and A.A. Konstantinov Transmembrane charge separation during the ferryl-oxo -> oxidized transition in a nonpumping mutant of cytochrome c oxidase J. Biol. Chem. 279 2004 52558 52565 (Pubitemid 39656632)
25. 3-cytochrome c oxidase from Thermus thermophilus EMBO J. 19 2000 1766 1776 (Pubitemid 30204388)
26. 3 cytochrome oxidase provides insights into proton pumping Science 329 2010 327 330
27. 3 oxidase) of heme-copper oxygen reductases Biochemistry 46 2007 9963 9972 (Pubitemid 47378586)
28. 3 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. U. S. A. 106 2009 16169 16173
29. P.C. Hinkle P/O ratios of mitochondrial oxidative phosphorylation Biochim. Biophys. Acta 1706 2005 1 11 (Pubitemid 40037758)
30. M. Wikström, and G. Hummer Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications Proc. Natl. Acad. Sci. U. S. A. 109 2012 4431 4436
31. 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum J. Bacteriol. 178 1996 1532 1538
32. 3 cytochrome oxidase from Thermus thermophilus Proc. Natl. Acad. Sci. U. S. A. 107 2010 21010 21015
33. B. Chance, C. Saronio, and J.S. Leigh Functional intermediates in reaction of cytochrome oxidase with oxygen Proc. Natl. Acad. Sci. U. S. A. 72 1975 1635 1640
34. M.I. Verkhovsky, J.E. Morgan, A. Puustinen, and M. Wikström Kinetic trapping of oxygen in cell respiration Nature 380 1996 268 270 (Pubitemid 26090653)
35. M. Wikström, M.I. Verkhovsky, and G. Hummer Water-gated mechanism of proton translocation by cytochrome c oxidase Biochim. Biophys. Acta 1604 2003 61 65 (Pubitemid 36588691)
36. P.E. Siegbahn, and M.R. Blomberg Energy diagrams and mechanism for proton pumping in cytochrome c oxidase Biochim. Biophys. Acta 1767 2007 1143 1156 (Pubitemid 47313389)
37. V.R. Kaila, M.I. Verkhovsky, and M. Wikström Proton-coupled electron transfer in cytochrome oxidase Chem. Rev. 110 2010 7062 7081
38. M.R. Blomberg, and P.E. Siegbahn The mechanism for proton pumping in cytochrome c oxidase from an electrostatic and quantum chemical perspective Biochim. Biophys. Acta 1817 2012 495 505
39. Y.C. Kim, M. Wikström, and G. Hummer Kinetic models of redox-coupled proton pumping Proc. Natl. Acad. Sci. U. S. A. 104 2007 2169 2174 (Pubitemid 46391370)
40. Y.C. Kim, M. Wikström, and G. Hummer Kinetic gating of the proton pump in cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 106 2009 13707 13712
41. C. Brochier-Armanet, E. Talla, and S. Gribaldo The multiple evolutionary histories of dioxygen reductases: implications for the origin and evolution of aerobic respiration Mol. Biol. Evol. 26 2009 285 297
42. A.-L. Ducluzeau, B. Schoepp-Cothenet, F. Baymann, M.J. Russell, and W. Nitschke Free energy conversion in the LUCA: quo vadis? Biochim. Biophys. Acta 2014
43. A.-L. Ducluzeau, B. Schoepp-Cothenet, R. van Lis, F. Baymann, S. McGlynn, M.J. Russell, and W. Nitschke J. Roy. Soc. Interface 2014
44. P.K. Glasoe, and F.A. Long Use of glass electrodes to measure acidities in deuterium oxide J. Phys. Chem. U. S. 64 1960 188 190
45. G. Gilderson, L. Salomonsson, A. Aagaard, J. Gray, P. Brzezinski, and J. Hosler 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 2003 7400 7409 (Pubitemid 36740492)
46. C. Backgren, G. Hummer, M. Wikström, and A. Puustinen Proton translocation by cytochrome c oxidase can take place without the conserved glutamic acid in subunit I Biochemistry 39 2000 7863 7867 (Pubitemid 30452358)