Catalytic intermediates of cytochrome bd terminal oxidase at steady-state: Ferryl and oxy-ferrous species dominate

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 5, 2011, Pages 503-509

  Borisov, Vitaliy B ^a   Forte, Elena ^b   Sarti, Paolo ^b   Giuffrè, Alessandro ^b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

2,3 dimethoxy 5 methyl 6 (3 methyl 2 butenyl) 1,4 benzoquinone; cyt bd; cytochrome bd; dithiothreitol; DTT; F; ferric heme d; ferrous uncomplexed heme d; ferryl heme d; O; OXY; oxy ferrous heme d; P; peroxy heme d; Q1; R

Indexed keywords

CYTOCHROME BD UBIQUINOL OXIDASE; CYTOCHROME C OXIDASE; DITHIOTHREITOL; HEME; IRON; OXYGEN; UBIQUINONE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; STEADY STATE;

BIOCATALYSIS; CYTOCHROMES; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ELECTRON TRANSPORT COMPLEX IV; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FERROUS COMPOUNDS; OXIDOREDUCTASES;

ESCHERICHIA COLI; MAMMALIA;

EID: 79954853196     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.02.007     Document Type: Article

References (71)

1. A. Puustinen, M. Finel, T. Haltia, R.B. Gennis, and M. Wikström Properties of the two terminal oxidases of Escherichia coli Biochemistry 30 1991 3936 3942
2. A. Jasaitis, V.B. Borisov, N.P. Belevich, J.E. Morgan, A.A. Konstantinov, and M.I. Verkhovsky Electrogenic reactions of cytochrome bd Biochemistry 39 2000 13800 13809
3. I. Belevich, V.B. Borisov, J. Zhang, K. Yang, A.A. Konstantinov, R.B. Gennis, and M.I. Verkhovsky Time-resolved electrometric and optical studies on cytochrome bd suggest a mechanism of electron-proton coupling in the di-heme active site Proc. Natl Acad. Sci. USA 102 2005 3657 3662 (Pubitemid 40354667)
4. I. Belevich, V.B. Borisov, and M.I. Verkhovsky Discovery of the true peroxy intermediate in the catalytic cycle of terminal oxidases by real-time measurement J. Biol. Chem. 282 2007 28514 28519 (Pubitemid 47606033)
5. 595/heme d active site Biochemistry 47 2008 7907 7914
6. J.F. Kolonay Jr., and R.J. Maier Formation of pH and potential gradients by the reconstituted Azotobacter vinelandii cytochrome bd respiratory protection oxidase J. Bacteriol. 179 1997 3813 3817 (Pubitemid 27233031)
7. Y.V. Bertsova, A.V. Bogachev, and V.P. Skulachev Generation of protonic potential by the bd-type quinol oxidase of Azotobacter vinelandii FEBS Lett. 414 1997 369 372 (Pubitemid 27389397)
8. A.D. Baughn, and M.H. Malamy The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen Nature 427 2004 441 444 (Pubitemid 38168496)
9. L. Shi, C.D. Sohaskey, B.D. Kana, S. Dawes, R.J. North, V. Mizrahi, and M.L. Gennaro Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration Proc. Natl Acad. Sci. USA 102 2005 15629 15634 (Pubitemid 41528107)
10. S. Loisel-Meyer, M.P. Jimenez de Bagues, S. Kohler, J.P. Liautard, and V. Jubier-Maurin Differential use of the two high-oxygen-affinity terminal oxidases of Brucella suis for in vitro and intramacrophagic multiplication Infect. Immun. 73 2005 7768 7771 (Pubitemid 41587684)
11. S.A. Jones, F.Z. Chowdhury, A.J. Fabich, A. Anderson, D.M. Schreiner, A.L. House, S.M. Autieri, M.P. Leatham, J.J. Lins, M. Jorgensen, P.S. Cohen, and T. Conway Respiration of Escherichia coli in the mouse intestine Infect. Immun. 75 2007 4891 4899 (Pubitemid 47502160)
12. M.J.S. Kelly, R.K. Poole, M.G. Yates, and C. Kennedy Cloning and mutagenesis of genes encoding the cytochrome bd terminal oxidase complex in Azotobacter vinelandii: mutants deficient in the cytochrome d complex are unable to fix nitrogen in air J. Bacteriol. 172 1990 6010 6019 (Pubitemid 20317143)
13. 2 fixation and microaerobiosis J. Bacteriol. 172 1990 2071 2078 (Pubitemid 20112032)
14. A. Smith, S. Hill, and C. Anthony The purification, characterization and role of the d-type cytochrome oxidase of Klebsiella pneumoniae during nitrogen fixation J. Gen. Microbiol. 136 1990 171 180 (Pubitemid 20045984)
15. R. D'Mello, S. Hill, and R.K. Poole Determination of the oxygen affinities of terminal oxidases in Azotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin: cytochrome bd is a low-affinity oxidase Microbiology 140 1994 1395 1402 (Pubitemid 24195911)
16. 2 fixation J. Bacteriol. 178 1996 5989 5994 (Pubitemid 26337784)
17. N.S. Juty, F. Moshiri, M. Merrick, C. Anthony, and S. Hill The Klebsiella pneumoniae cytochrome bd' terminal oxidase complex and its role in microaerobic nitrogen fixation Microbiology 143 1997 2673 2683 (Pubitemid 27389953)
18. R.K. Poole, and S. Hill Respiratory protection of nitrogenase activity in Azotobacter vinelandii-roles of the terminal oxidases Biosci. Rep. 17 1997 307 317
19. Y.V. Bertsova, O.V. Demin, and A.V. Bogachev Respiratory protection of nitrogenase complex in Azotobacter vinelandii Usp. biologicheskoj khimii Russ. 45 2005 205 234
20. M. Bader, W. Muse, D.P. Ballou, C. Gassner, and J.C.A. Bardwell Oxidative protein folding is driven by the electron transport system Cell 98 1999 217 227 (Pubitemid 29344909)
21. K. Mobius, R. Arias-Cartin, D. Breckau, A.L. Hannig, K. Riedmann, R. Biedendieck, S. Schroder, D. Becher, A. Magalon, J. Moser, M. Jahn, and D. Jahn Heme biosynthesis is coupled to electron transport chains for energy generation Proc. Natl Acad. Sci. USA 107 2010 10436 10441
22. V.B. Borisov, A.I. Davletshin, and A.A. Konstantinov Peroxidase activity of cytochrome bd from Escherichia coli Biochem. Moscow 75 2010 428 436 (translated from Biokhimiya (in Russian) (2010), 75, 520-530)
23. V.B. Borisov, E. Forte, A.A. Konstantinov, R.K. Poole, P. Sarti, and A. Giuffrè Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide FEBS Lett. 576 2004 201 204 (Pubitemid 39330483)
24. B-lacking cytochrome bd terminal oxidase FEBS Lett. 580 2006 4823 4826 (Pubitemid 44286838)
25. V.B. Borisov, E. Forte, P. Sarti, M. Brunori, A.A. Konstantinov, and A. Giuffrè Redox control of fast ligand dissociation from Escherichia coli cytochrome bd Biochem. Biophys. Res. Commun. 355 2007 97 102 (Pubitemid 46273371)
26. E. Forte, V.B. Borisov, A.A. Konstantinov, M. Brunori, A. Giuffrè, and P. Sarti Cytochrome bd, a key oxidase in bacterial survival and tolerance to nitrosative stress Ital. J. Biochem. 56 2007 265 269
27. M.G. Mason, M. Shepherd, P. Nicholls, P.S. Dobbin, K.S. Dodsworth, R.K. Poole, and C.E. Cooper Cytochrome bd confers nitric oxide resistance to Escherichia coli Nat. Chem. Biol. 5 2009 94 96
28. V.B. Borisov, E. Forte, A. Giuffrè, A. Konstantinov, and P. Sarti Reaction of nitric oxide with the oxidized di-heme and heme-copper oxygen-reducing centers of terminal oxidases: different reaction pathways and end-products J. Inorg. Biochem. 103 2009 1185 1187
29. S.S. Way, S. Sallustio, R.S. Magliozzo, and M.B. Goldberg Impact of either elevated or decreased levels of cytochrome bd expression on Shigella flexneri virulence J. Bacteriol. 181 1999 1229 1237 (Pubitemid 29119562)
30. S. Endley, D. McMurray, and T.A. Ficht Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection J. Bacteriol. 183 2001 2454 2462 (Pubitemid 32249753)
31. Y. Yamamoto, C. Poyart, P. Trieu-Cuot, G. Lamberet, A. Gruss, and P. Gaudu Respiration metabolism of Group B Streptococcus is activated by environmental haem and quinone and contributes to virulence Mol. Microbiol. 56 2005 525 534 (Pubitemid 40516788)
32. L. Zhang-Barber, A.K. Turner, G. Martin, G. Frankel, G. Dougan, and P.A. Barrow Influence of genes encoding proton-translocating enzymes on suppression of Salmonella typhimurium growth and colonization J. Bacteriol. 179 1997 7186 7190 (Pubitemid 27492508)
33. A.K. Turner, L.Z. Barber, P. Wigley, S. Muhammad, M.A. Jones, M.A. Lovell, S. Hulme, and P.A. Barrow Contribution of proton-translocating proteins to the virulence of Salmonella enterica Serovars Typhimurium, Gallinarum, and Dublin in chickens and mice Infect. Immun. 71 2003 3392 3401 (Pubitemid 36637567)
34. M.H. Larsen, B.H. Kallipolitis, J.K. Christiansen, J.E. Olsen, and H. Ingmer The response regulator ResD modulates virulence gene expression in response to carbohydrates in Listeria monocytogenes Mol. Microbiol. 61 2006 1622 1635 (Pubitemid 44359388)
35. B.L. Trumpower, and R.B. Gennis Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron transfer reactions to transmembrane proton translocation Annu. Rev. Biochem. 63 1994 675 716 (Pubitemid 24218646)
36. S. Junemann Cytochrome bd terminal oxidase Biochim. Biophys. Acta 1321 1997 107 127 (Pubitemid 27390501)
37. V.B. Borisov Cytochrome bd: structure and properties Biochem. Moscow 61 1996 565 574 (translated from Biokhimiya (in Russian) (1996), 61, 786-799)
38. M. Tsubaki, H. Hori, and T. Mogi Probing molecular structure of dioxygen reduction site of bacterial quinol oxidases through ligand binding to the redox metal centers J. Inorg. Biochem. 82 2000 19 25
39. T. Mogi, M. Tsubaki, H. Hori, H. Miyoshi, H. Nakamura, and Y. Anraku Two terminal quinol oxidase families in Escherichia coli: variations on molecular machinery for dioxygen reduction J. Biochem. Mol. Biol. Biophys. 2 1998 79 110 (Pubitemid 28520273)
40. R.K. Poole, and G.M. Cook Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation Adv. Microb. Physiol. 43 2000 165 224 (Pubitemid 30481125)
41. Vitaliy B. Borisov, and Michael I. Verkhovsky A. Böck, R. Curtiss III J.B. Kaper, P.D. Karp, F.C. Neidhardt, T. Nyström, J.M. Slauch, C.L. Squires, D. Ussery, EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology 2009 ASM Press Washington, DC < http://www.ecosal.org >
42. J.P. Osborne, and R.B. Gennis Sequence analysis of cytochrome bd oxidase suggests a revised topology for subunits I Biochim. Biophys. Acta 1410 1999 32 50 (Pubitemid 29074428)
43. 2 reactive site near the periplasmic surface FEBS Lett. 561 2004 58 62 (Pubitemid 38324607)
44. T.J. Dueweke, and R.B. Gennis Epitopes of monoclonal antibodies which inhibit ubiquinol oxidase activity of Escherichia coli cytochrome d complex localize a functional domain J. Biol. Chem. 265 1990 4273 4277
45. R.G. Kranz, and R.B. Gennis Characterization of the cytochrome d terminal oxidase complex of Escherichia coli using polyclonal and monoclonal antibodies J. Biol. Chem. 259 1984 7998 8003 (Pubitemid 14081225)
46. R.M. Lorence, K. Carter, R.B. Gennis, K. Matsushita, and H.R. Kaback Trypsin proteolysis of the cytochrome d complex of Escherichia coli selectively inhibits ubiquinol oxidase activity while not affecting N, N, N′, N′-tetramethyl-p-phenylenediamine oxidase activity J. Biol. Chem. 11 1988 5271 5276
47. T.J. Dueweke, and R.B. Gennis Proteolysis of the cytochrome d complex with trypsin and chymotrypsin localizes a quinol oxidase domain Biochemistry 30 1991 3401 3406
48. T. Mogi, S. Akimoto, S. Endou, T. Watanabe-Nakayama, E. Mizuochi-Asai, and H. Miyoshi Probing the ubiquinol-binding site in cytochrome bd by site-directed mutagenesis Biochemistry 45 2006 7924 7930 (Pubitemid 44185510)
49. J.J. Hill, J.O. Alben, and R.B. Gennis Spectroscopic evidence for a heme-heme binuclear center in the cytochrome bd ubiquinol oxidase from Escherichia coli Proc. Natl Acad. Sci. USA 90 1993 5863 5867 (Pubitemid 23176263)
50. M. Tsubaki, H. Hori, T. Mogi, and Y. Anraku Cyanide-binding site of bd-type ubiquinol oxidase from Escherichia coli J. Biol. Chem. 270 1995 28565 28569
51. V. Borisov, A.M. Arutyunyan, J.P. Osborne, R.B. Gennis, and A.A. Konstantinov Magnetic circular dichroism used to examine the interaction of Escherichia coli cytochrome bd with ligands Biochemistry 38 1999 740 750
52. M.H. Vos, V.B. Borisov, U. Liebl, J.-L. Martin, and A.A. Konstantinov Femtosecond resolution of ligand-heme interactions in the high-affinity quinol oxidase bd: a di-heme active site? Proc. Natl Acad. Sci. USA 97 2000 1554 1559 (Pubitemid 30118480)
53. 595 reacts with CO J. Biol. Chem. 276 2001 22095 22099
54. 595 in quinol oxidase bd from Escherichia coli: a photoselection study using femtosecond spectroscopy Biochemistry 41 2002 1654 1662 (Pubitemid 34112756)
55. 595 is 10 Å Biochemistry 47 2008 1752 1759 (Pubitemid 351231224)
56. F. Rappaport, J. Zhang, M.H. Vos, R.B. Gennis, and V.B. Borisov Heme-heme and heme-ligand interactions in the di-heme oxygen-reducing site of cytochrome bd from Escherichia coli revealed by nanosecond absorption spectroscopy Biochim. Biophys. Acta 1797 2010 1657 1664
57. S. Junemann, P.J. Butterworth, and J.M. Wrigglesworth A suggested mechanism for the catalytic cycle of cytochrome bd terminal oxidase based on kinetic analysis Biochemistry 34 1995 14861 14867
58. Y. Matsumoto, E. Muneyuki, D. Fujita, K. Sakamoto, H. Miyoshi, M. Yoshida, and T. Mogi Kinetic mechanism of quinol oxidation by cytochrome bd studied with ubiquinone-2 analogs J. Biochem. Tokyo 139 2006 779 788 (Pubitemid 43973925)
59. K. Yang, V.B. Borisov, A.A. Konstantinov, and R.B. Gennis The fully oxidized form of the cytochrome bd quinol oxidase from E. coli does not participate in the catalytic cycle: direct evidence from rapid kinetics studies FEBS Lett. 582 2008 3705 3709
60. V.B. Borisov, I.A. Smirnova, I.A. Krasnosel'skaya, and A.A. Konstantinov Oxygenated cytochrome bd from Escherichia coli can be converted into the oxidized form by lipophilic electron acceptors Biochem. Moscow 59 1994 437 443 (translated from Biokhimiya (in Russian) (1994), 59, 598-606)
61. I. Belevich, V.B. Borisov, A.A. Konstantinov, and M.I. Verkhovsky Oxygenated complex of cytochrome bd from Escherichia coli: stability and photolability FEBS Lett. 579 2005 4567 4570 (Pubitemid 41218628)
62. I. Belevich, V.B. Borisov, D.A. Bloch, A.A. Konstantinov, and M.I. Verkhovsky Cytochrome bd from Azotobacter vinelandii: evidence for high-affinity oxygen binding Biochemistry 46 2007 11177 11184 (Pubitemid 47502783)
63. B.C. Hill, J.J. Hill, and R.B. Gennis The room temperature reaction of carbon monoxide and oxygen with the cytochrome bd quinol oxidase from Escherichia coli Biochemistry 33 1994 15110 15115
64. V. Borisov, R. Gennis, and A.A. Konstantinov Peroxide complex of cytochrome bd: kinetics of generation and stability Biochem. Mol. Biol. Int. 37 1995 975 982 (Pubitemid 26177957)
65. V.B. Borisov, R.B. Gennis, and A.A. Konstantinov Interaction of cytochrome bd from Escherichia coli with hydrogen peroxide Biochem. Moscow 60 1995 231 239 (translated from Biokhimiya (in Russian) (1995), 60, 315-327)
66. M.G. Mason, P. Nicholls, and C.E. Cooper The steady-state mechanism of cytochrome c oxidase: redox interactions between metal centres Biochem. J. 422 2009 237 246
67. 558 component of the cytochrome bd ubiquinol oxidase from Escherichia coli Biochemistry 34 1995 13491 13501
68. M.J. Miller, and R.B. Gennis Purification and reconstitution of the cytochrome d terminal oxidase complex from Escherichia coli Meth. Enzymol. 126 1986 87 94
69. V.B. Borisov Interaction of bd-type quinol oxidase from Escherichia coli and carbon monoxide: heme d binds CO with high affinity Biochem. Moscow 73 2008 14 22 (translated from Biokhimiya (in Russian) (2008), 73, 18-28) (Pubitemid 351653318)
70. D.A. Bloch, V.B. Borisov, T. Mogi, and M.I. Verkhovsky Heme/heme redox interaction and resolution of individual optical absorption spectra of the hemes in cytochrome bd from Escherichia coli Biochim. Biophys. Acta 1787 2009 1246 1253
71. N. Azarkina, V. Borisov, and A.A. Konstantinov Spontaneous spectral changes of the reduced cytochrome bd FEBS Lett. 416 1997 171 174 (Pubitemid 27462781)