Cytochrome bd oxidase and bacterial tolerance to oxidative and nitrosative stress

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 7, 2014, Pages 1178-1187

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

^a CNR   (Italy)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Bacterial virulence; Heme reactivity; Host pathogen relationship; Hydrogen peroxide; Nitric oxide; Respiratory chain

Indexed keywords

CATALASE; CYTOCHROME BD OXIDASE; HYDROGEN PEROXIDE; NITRIC OXIDE; OXIDOREDUCTASE; OXYGEN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

BACTERIAL VIRULENCE; ENZYME ACTIVITY; ESCHERICHIA COLI; MICROBIAL ACTIVITY; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

BACTERIAL VIRULENCE; HEME REACTIVITY; HOST-PATHOGEN RELATIONSHIP; HYDROGEN PEROXIDE; NITRIC OXIDE; RESPIRATORY CHAIN;

BACTERIA; BACTERIAL PROTEINS; CYTOCHROMES; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; NITRIC OXIDE; OXIDATIVE STRESS; OXIDOREDUCTASES;

EID: 84901845126     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2014.01.016     Document Type: Review

References (116)

1. V.B. Borisov Cytochrome bd: structure and properties Biochem. Mosc. 61 1996 565 574 (translated from Biokhimiya (in Russian) (1996), 61, 1786-1799)
2. S. Jünemann Cytochrome bd terminal oxidase Biochim. Biophys. Acta 1321 1997 107 127 (Pubitemid 27390501)
3. V.B. Borisov, R.B. Gennis, J. Hemp, and M.I. Verkhovsky The cytochrome bd respiratory oxygen reductases Biochim. Biophys. Acta 1807 2011 1398 1413
4. M. Brunori, A. Giuffrè, and P. Sarti Cytochrome c oxidase, ligands and electrons J. Inorg. Biochem. 99 2005 324 336 (Pubitemid 39642985)
5. M.M. Pereira, F.L. Sousa, A.F. Verissimo, and M. Teixeira Looking for the minimum common denominator in haem-copper oxygen reductases: towards a unified catalytic mechanism Biochim. Biophys. Acta 1777 2008 929 934
6. P. Brzezinski, and R.B. Gennis Cytochrome c oxidase: exciting progress and remaining mysteries J. Bioenerg. Biomembr. 40 2008 521 531
7. O.M. Richter, and B. Ludwig Electron transfer and energy transduction in the terminal part of the respiratory chain - lessons from bacterial model systems Biochim. Biophys. Acta 1787 2009 626 634
8. 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
9. 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
10. 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. U. S. A. 102 2005 3657 3662 (Pubitemid 40354667)
11. 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)
12. 595/heme d active site Biochemistry 47 2008 7907 7914
13. 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)
14. 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)
15. 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. U. S. A. 102 2005 15629 15634 (Pubitemid 41528107)
16. 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)
17. 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)
18. 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)
19. 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)
20. 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)
21. 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)
22. 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)
23. 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)
24. B.K. Hassani, A.S. Steunou, S. Liotenberg, F. Reiss-Husson, C. Astier, and S. Ouchane Adaptation to oxygen: role of terminal oxidases in photosynthesis initiation in the purple photosynthetic bacterium, Rubrivivax gelatinosus J. Biol. Chem. 285 2010 19891 19899
25. 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)
26. 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)
27. 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. U. S. A. 107 2010 10436 10441
28. Y.H. Sun, M.F. de Jong, A.B. den Hartigh, C.M. Roux, H.G. Rolan, and R.M. Tsolis The small protein CydX is required for function of cytochrome bd oxidase in Brucella abortus Front. Cell. Infect. Microbiol. 2 2012 47
29. C.E. VanOrsdel, S. Bhatt, R.J. Allen, E.P. Brenner, J.J. Hobson, A. Jamil, B.M. Haynes, A.M. Genson, and M.R. Hemm The Escherichia coli CydX protein is a member of the CydAB cytochrome bd oxidase complex and is required for cytochrome bd oxidase activity J. Bacteriol. 195 2013 3640 3650
30. V.B. Borisov, and M.I. Verkhovsky Chapter 3.2.7, oxygen as acceptor R.C.I.A. Bock, J.B. Kaper, P.D. Karp, F.C. Neidhardt, T. Nystrom, J.M. Slauch, C.L. Squires, D. Ussery, EcoSal - Escherichia coli and Salmonella: Cellular and Molecular Biology 2009 ASM Press Washington, DC (< http://ecosal.org/oxygen- as-acceptor.html >)
31. 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. U. S. A. 90 1993 5863 5867 (Pubitemid 23176263)
32. 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
33. V.B. Borisov, R.B. Gennis, and A.A. Konstantinov Interaction of cytochrome bd from Escherichia coli with hydrogen peroxide Biochem. Mosc. 60 1995 231 239 (translated from Biokhimiya (in Russian) (1995), 60, 1315-1327)
34. 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. U. S. A. 97 2000 1554 1559 (Pubitemid 30118480)
35. 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
36. 595 reacts with CO J. Biol. Chem. 276 2001 22095 22099
37. 595 in quinol oxidase bd from Escherichia coli: a photoselection study using femtosecond spectroscopy Biochemistry 41 2002 1654 1662 (Pubitemid 34112756)
38. 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
39. 595 is 10 Å Biochemistry 47 2008 1752 1759 (Pubitemid 351231224)
40. Q. Gibson, and C. Greenwood Reactions of cytochrome oxidase with oxygen and carbon monoxide Biochem. J. 86 1963 541 555
41. 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
42. 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)
43. A. Paulus, S.G. Rossius, M. Dijk, and S. de Vries Oxoferryl-porphyrin radical catalytic intermediate in cytochrome bd oxidases protects cells from formation of reactive oxygen species J. Biol. Chem. 287 2012 8830 8838
44. G.T. Babcock How oxygen is activated and reduced in respiration Proc. Natl. Acad. Sci. U. S. A. 96 1999 12971 12973
45. J.G. Lindsay, C.S. Owen, and D.F. Wilson The invisible copper of cytochrome c oxidase Arch. Biochem. Biophys. 169 1975 492 505
46. 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. Mosc. 59 1994 437 443 (translated from Biokhimiya (in Russian) (1994), 59, 1598-1606)
47. 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)
48. 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)
49. S. Jünemann, J.M. Wrigglesworth, and P.R. Rich Effects of decyl-aurachin D and reversed electron transfer in cytochrome bd Biochemistry 36 1997 9323 9331 (Pubitemid 27346969)
50. V.B. Borisov, E. Forte, P. Sarti, and A. Giuffrè Catalytic intermediates of cytochrome bd terminal oxidase at steady-state: ferryl and oxy-ferrous species dominate Biochim. Biophys. Acta 1807 2011 503 509
51. 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
52. 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
53. A. Lindqvist, J. Membrillo-Hernandez, R.K. Poole, and G.M. Cook Roles of respiratory oxidases in protecting Escherichia coli K12 from oxidative stress Antonie Van Leeuwenhoek 78 2000 23 31
54. D. Wall, J.M. Delaney, O. Fayet, B. Lipinska, T. Yamamoto, and C. Georgopoulos arc-Dependent thermal regulation and extragenic suppression of the Escherichia coli cytochrome d operon J. Bacteriol. 174 1992 6554 6562
55. B.S. Goldman, K.K. Gabbert, and R.G. Kranz The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents J. Bacteriol. 178 1996 6348 6351 (Pubitemid 26365719)
56. S.E. Edwards, C.S. Loder, G. Wu, H. Corker, B.W. Bainbridge, S. Hill, and R.K. Poole Mutation of cytochrome bd quinol oxidase results in reduced stationary phase survival, iron deprivation, metal toxicity and oxidative stress in Azotobacter vinelandii FEMS Microbiol. Lett. 185 2000 71 77 (Pubitemid 30145609)
57. J.L. Small, S.W. Park, B.D. Kana, T.R. Ioerger, J.C. Sacchettini, and S. Ehrt Perturbation of cytochrome c maturation reveals adaptability of the respiratory chain in Mycobacterium tuberculosis MBio 4 2013 (e00475-00413)
58. E. Forte, V.B. Borisov, A. Davletshin, D. Mastronicola, P. Sarti, and A. Giuffrè Cytochrome bd oxidase and hydrogen peroxide resistance in Mycobacterium tuberculosis MBio 4 2013 e01006 e01013
59. S. Korshunov, and J.A. Imlay Two sources of endogenous hydrogen peroxide in Escherichia coli Mol. Microbiol. 75 2010 1389 1401
60. V.B. Borisov, A.I. Davletshin, and A.A. Konstantinov Peroxidase activity of cytochrome bd from Escherichia coli Biochem. Mosc. 75 2010 428 436 (translated from Biokhimiya (in Russian) (2010), 75, 2520-2530)
61. V.B. Borisov, E. Forte, A. Davletshin, D. Mastronicola, P. Sarti, and A. Giuffrè Cytochrome bd oxidase from Escherichia coli displays high catalase activity: an additional defense against oxidative stress FEBS Lett. 587 2013 2214 2218
62. 558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems J. Biol. Chem. 259 1984 3375 3381 (Pubitemid 14130554)
63. A.M. Gardner, R.A. Helmick, and P.R. Gardner Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli J. Biol. Chem. 277 2002 8172 8177 (Pubitemid 34968272)
64. C.M. Gomes, A. Giuffrè, E. Forte, J.B. Vicente, L.M. Saraiva, M. Brunori, and M. Teixeira A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin J. Biol. Chem. 277 2002 25273 25276 (Pubitemid 34951835)
65. P.R. Gardner, A.M. Gardner, L.A. Martin, and A.L. Salzman Nitric oxide dioxygenase: an enzymic function for flavohemoglobin Proc. Natl. Acad. Sci. U. S. A. 95 1998 10378 10383 (Pubitemid 28413075)
66. A. Hausladen, A. Gow, and J.S. Stamler Flavohemoglobin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen Proc. Natl. Acad. Sci. U. S. A. 98 2001 10108 10112 (Pubitemid 32802982)
67. A.M. Gardner, L.A. Martin, P.R. Gardner, Y. Dou, and J.S. Olson Steady-state and transient kinetics of Escherichia coli nitric-oxide dioxygenase (flavohemoglobin). The B10 tyrosine hydroxyl is essential for dioxygen binding and catalysis J. Biol. Chem. 275 2000 12581 12589 (Pubitemid 30241405)
68. C.E. Mills, S. Sedelnikova, B. Soballe, M.N. Hughes, and R.K. Poole Escherichia coli flavohaemoglobin (Hmp) with equistoichiometric FAD and haem contents has a low affinity for dioxygen in the absence or presence of nitric oxide Biochem. J. 353 2001 207 213 (Pubitemid 32096927)
69. D. Mastronicola, F. Testa, E. Forte, E. Bordi, L.P. Pucillo, P. Sarti, and A. Giuffrè Flavohemoglobin and nitric oxide detoxification in the human protozoan parasite Giardia intestinalis Biochem. Biophys. Res. Commun. 399 2010 654 658
70. C.E. Cooper Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector? Trends Biochem. Sci. 27 2002 33 39 (Pubitemid 34131623)
71. P. Sarti, A. Giuffrè, M.C. Barone, E. Forte, D. Mastronicola, and M. Brunori Nitric oxide and cytochrome oxidase: reaction mechanisms from the enzyme to the cell Free Radic. Biol. Med. 34 2003 509 520 (Pubitemid 36254825)
72. M. Brunori, E. Forte, M. Arese, D. Mastronicola, A. Giuffrè, and P. Sarti Nitric oxide and the respiratory enzyme Biochim. Biophys. Acta 1757 2006 1144 1154 (Pubitemid 44442121)
73. C.E. Cooper, and C. Giulivi Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology Am. J. Physiol. Cell Physiol. 292 2007 C1993 C2003
74. P. Sarti, M. Arese, E. Forte, A. Giuffrè, and D. Mastronicola Mitochondria and nitric oxide: chemistry and pathophysiology Adv. Exp. Med. Biol. 942 2012 75 92
75. P. Sarti, E. Forte, A. Giuffrè, D. Mastronicola, M.C. Magnifico, and M. Arese The chemical interplay between nitric oxide and mitochondrial cytochrome c oxidase: reactions, effectors and pathophysiology Int. J. Cell Biol. 2012 2012 571067
76. P. Sarti, E. Forte, D. Mastronicola, A. Giuffrè, and M. Arese Cytochrome c oxidase and nitric oxide in action: molecular mechanisms and pathophysiological implications Biochim. Biophys. Acta 1817 2012 610 619
77. J.D. Erusalimsky, and S. Moncada Nitric oxide and mitochondrial signaling: from physiology to pathophysiology Arterioscler. Thromb. Vasc. Biol. 27 2007 2524 2531 (Pubitemid 350158901)
78. C.T. Taylor, and S. Moncada Nitric oxide, cytochrome C oxidase, and the cellular response to hypoxia Arterioscler. Thromb. Vasc. Biol. 30 2010 643 647
79. P. Sarti Nitric Oxide in Human Health and Disease April 2013 ELS. John Wiley & Sons, Ltd. Chichester 10.1002/9780470015902.a0003390.pub2
80. C.E. Cooper, J. Torres, M.A. Sharpe, and M.T. Wilson Nitric oxide ejects electrons from the binuclear centre of cytochrome c oxidase by reacting with oxidised copper: a general mechanism for the interaction of copper proteins with nitric oxide? FEBS Lett. 414 1997 281 284 (Pubitemid 27389379)
81. A. Giuffrè, G. Stubauer, M. Brunori, P. Sarti, J. Torres, and M.T. Wilson Chloride bound to oxidized cytochrome c oxidase controls the reaction with nitric oxide J. Biol. Chem. 273 1998 32475 32478 (Pubitemid 28557621)
82. J. Torres, C.E. Cooper, and M.T. Wilson A common mechanism for the interaction of nitric oxide with the oxidized binuclear centre and oxygen intermediates of cytochrome c oxidase J. Biol. Chem. 273 1998 8756 8766 (Pubitemid 28176154)
83. A. Giuffrè, M.C. Barone, D. Mastronicola, E. D'Itri, P. Sarti, and M. Brunori Reaction of nitric oxide with the turnover intermediates of cytochrome c oxidase: reaction pathway and functional effects Biochemistry 39 2000 15446 15453 (Pubitemid 32002771)
84. P. Sarti, A. Giuffrè, E. Forte, D. Mastronicola, M.C. Barone, and M. Brunori Nitric oxide and cytochrome c oxidase: mechanisms of inhibition and NO degradation Biochem. Biophys. Res. Commun. 274 2000 183 187 (Pubitemid 30496777)
85. J. Torres, M.A. Sharpe, A. Rosquist, C.E. Cooper, and M.T. Wilson Cytochrome c oxidase rapidly metabolises nitric oxide to nitrite FEBS Lett. 475 2000 263 266 (Pubitemid 30408465)
86. V.B. Borisov Interaction of bd-type quinol oxidase from Escherichia coli and carbon monoxide: heme d binds CO with high affinity Biochem. Mosc. 73 2008 14 22 (translated from Biokhimiya (in Russian) (2008), 73, 2018-2028) (Pubitemid 351653318)
87. S. Jünemann, and J.M. Wrigglesworth Cytochrome bd oxidase from Azotobacter vinelandii. Purification and quantitation of ligand binding to the oxygen reduction site J. Biol. Chem. 270 1995 16213 16220
88. H. Hori, M. Tsubaki, T. Mogi, and Y. Anraku EPR study of NO complex of bd-type ubiquinol oxidase from Escherichia coli J. Biol. Chem. 271 1996 9254 9258
89. B-lacking cytochrome bd terminal oxidase FEBS Lett. 580 2006 4823 4826 (Pubitemid 44286838)
90. S. Herold, and F.-J.K. Rehmann Kinetic and mechanistic studies of the reactions of nitrogen monoxide and nitrite with ferryl myoglobin J. Biol. Inorg. Chem. 6 2001 543 555 (Pubitemid 32822115)
91. S. Herold, and F.-J.K. Rehmann Kinetic of the reactions of nitrogen monoxide and nitrite with ferryl hemoglobin Free Radic. Biol. Med. 34 2003 531 545 (Pubitemid 36254827)
92. 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
93. F.T. Bonner, M.N. Hughes, R.K. Poole, and R.I. Scott Kinetics of the reactions of trioxodinitrate and nitrite ions with cytochrome d in Escherichia coli Biochim. Biophys. Acta 1056 1991 133 138
94. A. Giuffrè, G. Stubauer, P. Sarti, M. Brunori, W.G. Zumft, G. Buse, and T. Soulimane The heme-copper oxidases of Thermus thermophilus catalyze the reduction of nitric oxide: evolutionary implications Proc. Natl. Acad. Sci. U. S. A. 96 1999 14718 14723 (Pubitemid 30019706)
95. 3 from Pseudomonas stutzeri displays nitric oxide reductase activity Eur. J. Biochem. 268 2001 6486 6491
96. C. Butler, E. Forte, F. Maria Scandurra, M. Arese, A. Giuffrè, C. Greenwood, and P. Sarti Cytochrome bo(3) from Escherichia coli: the binding and turnover of nitric oxide Biochem. Biophys. Res. Commun. 296 2002 1272 1278
97. G. Stubauer, A. Giuffrè, M. Brunori, and P. Sarti Cytochrome c oxidase does not catalyze the anaerobic reduction of NO Biochem. Biophys. Res. Commun. 245 1998 459 465 (Pubitemid 28418525)
98. J. van der Oost, A.P.N. deBoer, J.-W.L. deGier, W.G. Zumft, A.H. Stouthamer, and R.J.M. van Spanning The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase FEMS Microbiol. Lett. 121 1994 1 10 (Pubitemid 2116583)
99. M. Saraste, and J. Castresana Cytochrome oxidase evolved by tinkering with denitrification enzymes FEBS Lett. 341 1994 1 4 (Pubitemid 24089178)
100. 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)
101. T.M. Stevanin, N. Ioannidis, C.E. Mills, S.O. Kim, M.N. Hughes, and R.K. Poole Flavohemoglobin Hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo' or bd, from nitric oxide J. Biol. Chem. 275 2000 35868 35875
102. G.C. Brown, and C.E. Cooper Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase FEBS Lett. 356 1994 295 298 (Pubitemid 24376992)
103. M.G. Mason, P. Nicholls, M.T. Wilson, and C.E. Cooper Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 103 2006 708 713 (Pubitemid 43153090)
104. 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
105. D.D. Lemon, M.W. Calhoun, R.B. Gennis, and W.H. Woodruff The gateway to the active site of heme-copper oxidases Biochemistry 32 1993 11953 11956 (Pubitemid 23353630)
106. S.P. Cary, J.A. Winger, and M.A. Marletta Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP Proc. Natl. Acad. Sci. U. S. A. 102 2005 13064 13069 (Pubitemid 41324979)
107. S. Rinaldo, K.A. Sam, N. Castiglione, V. Stelitano, A. Arcovito, M. Brunori, J.W. Allen, S.J. Ferguson, and F. Cutruzzolà Observation of fast release of NO from ferrous d haem allows formulation of a unified reaction mechanism for cytochrome cd nitrite reductases Biochem. J. 435 2011 217 225
108. 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
109. A. Giuffrè, V.B. Borisov, D. Mastronicola, P. Sarti, and E. Forte Cytochrome bd oxidase and nitric oxide: From reaction mechanisms to bacterial physiology FEBS Lett. 586 2012 622 629
110. H. Fu, H. Chen, J. Wang, G. Zhou, H. Zhang, L. Zhang, and H. Gao Crp-dependent cytochrome bd oxidase confers nitrite resistance to Shewanella oneidensis Environ. Microbiol. 15 2013 2198 2212
111. H. Zhang, H. Fu, J. Wang, L. Sun, Y. Jiang, L. Zhang, and H. Gao Impacts of nitrate and nitrite on physiology of Shewanella oneidensis PLoS One 8 2013 e62629
112. S.T. Pullan, M.D. Gidley, R.A. Jones, J. Barrett, T.M. Stevanin, R.C. Read, J. Green, and R.K. Poole Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S-nitrosation J. Bacteriol. 189 2007 1845 1855 (Pubitemid 46446147)
113. A.R. Richardson, P.M. Dunman, and F.C. Fang The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity Mol. Microbiol. 61 2006 927 939 (Pubitemid 44137205)
114. C.M. Moore, M.M. Nakano, T. Wang, R.W. Ye, and J.D. Helmann Response of Bacillus subtilis to nitric oxide and the nitrosating agent sodium nitroprusside J. Bacteriol. 186 2004 4655 4664 (Pubitemid 38891029)
115. P. Machado, R. Felix, R. Rodrigues, S. Oliveira, and C. Rodrigues-Pousada Characterization and expression analysis of the cytochrome bd oxidase operon from Desulfovibrio gigas Curr. Microbiol. 52 2006 274 281
116. A. Giuffrè, E. Forte, M. Brunori, and P. Sarti Nitric oxide, cytochrome c oxidase and myoglobin: competition and reaction pathways FEBS Lett. 579 2005 2528 2532 (Pubitemid 40569532)