Heme-heme and heme-ligand interactions in the di-heme oxygen-reducing site of cytochrome bd from Escherichia coli revealed by nanosecond absorption spectroscopy

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 9, 2010, Pages 1657-1664

  Rappaport, Fabrice ^a   Zhang, Jie ^b   Vos, Marten H ^c,d   Gennis, Robert B ^b   Borisov, Vitaliy B ^e  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

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

^c CNRS   (France)

^d INSERM   (France)

^e MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Chlorin; Cytochrome; Gas molecule; Ligand binding; Photobiology; Respiration

Indexed keywords

CARBON MONOXIDE; CYTOCHROME B; CYTOCHROME BD; CYTOCHROME D; HEME; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ARTICLE; ELECTRON TRANSPORT; ESCHERICHIA COLI; NANOSECOND ABSORPTION SPECTROSCOPY; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOLYSIS; PRIORITY JOURNAL;

CARBON MONOXIDE; CYTOCHROMES; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEME; LIGANDS; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHOTOLYSIS; SPECTRUM ANALYSIS;

ESCHERICHIA COLI;

EID: 77954761715     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.05.010     Document Type: Article

References (59)

1. Poole R.K., Cook G.M. Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv. Microb. Physiol. 2000, 43:165-224.
2. Junemann S. Cytochrome bd terminal oxidase. Biochim. Biophys. Acta 1997, 1321:107-127.
3. Borisov V.B. Cytochrome bd: structure and properties. Biochemistry (Moscow) 1996, 61:565-574. (translated from Biokhimiya (in Russian) (1996), 61, 786-799.
4. Tsubaki M., Hori H., Mogi T. Probing molecular structure of dioxygen reduction site of bacterial quinol oxidases through ligand binding to the redox metal centers. J. Inorg. Biochem. 2000, 82:19-25.
5. Borisov V.B., Verkhovsky M.I. Oxygen as acceptor. EcoSal - Escherichia coli and Salmonella: Cellular and Molecular Biology 2009, ASM Press, Washington, DC, [Chapter 3.2.7]. . A. Böck, R. Curtiss, J.B. Kaper, F.C. Neidhardt, T. Nyström, K.E. Rudd, C.L. Squires (Eds.).
6. Puustinen A., Finel M., Haltia T., Gennis R.B., Wikstrom M. Properties of the two terminal oxidases of Escherichia coli. Biochemistry 1991, 30:3936-3942.
7. Jasaitis A., Borisov V.B., Belevich N.P., Morgan J.E., Konstantinov A.A., Verkhovsky M.I. Electrogenic reactions of cytochrome bd. Biochemistry 2000, 39:13800-13809.
8. Belevich I., Borisov V.B., Zhang J., Yang K., Konstantinov A.A., Gennis R.B., Verkhovsky M.I. 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 2005, 102:3657-3662.
9. Belevich I., Borisov V.B., Verkhovsky M.I. Discovery of the true peroxy intermediate in the catalytic cycle of terminal oxidases by real-time measurement. J. Biol. Chem. 2007, 282:28514-28519.
10. 595/heme d active site. Biochemistry 2008, 47:7907-7914.
11. Baughn A.D., Malamy M.H. The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature 2004, 427:441-444.
12. Shi L., Sohaskey C.D., Kana B.D., Dawes S., North R.J., Mizrahi V., Gennaro M.L. Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc. Natl Acad. Sci. USA 2005, 102:15629-15634.
13. Loisel-Meyer S., Jimenez de Bagues M.P., Kohler S., Liautard J.P., Jubier-Maurin V. Differential use of the two high-oxygen-affinity terminal oxidases of Brucella suis for in vitro and intramacrophagic multiplication. Infect. Immun. 2005, 73:7768-7771.
14. Jones S.A., Chowdhury F.Z., Fabich A.J., Anderson A., Schreiner D.M., House A.L., Autieri S.M., Leatham M.P., Lins J.J., Jorgensen M., Cohen P.S., Conway T. Respiration of Escherichia coli in the mouse intestine. Infect. Immun. 2007, 75:4891-4899.
15. 2 fixation and microaerobiosis. J. Bacteriol. 1990, 172:2071-2078.
16. Way S.S., Sallustio S., Magliozzo R.S., Goldberg M.B. Impact of either elevated or decreased levels of cytochrome bd expression on Shigella flexneri virulence. J. Bacteriol. 1999, 181:1229-1237.
17. Endley S., McMurray D., Ficht T.A. Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection. J. Bacteriol. 2001, 183:2454-2462.
18. Borisov V.B., Forte E., Konstantinov A.A., Poole R.K., Sarti P., Giuffre A. Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide. FEBS Lett. 2004, 576:201-204.
19. Borisov V.B., Forte E., Sarti P., Brunori M., Konstantinov A.A., Giuffre A. Redox control of fast ligand dissociation from Escherichia coli cytochrome bd. Biochem. Biophys. Res. Commun. 2007, 355:97-102.
20. Mason M.G., Shepherd M., Nicholls P., Dobbin P.S., Dodsworth K.S., Poole R.K., Cooper C.E. Cytochrome bd confers nitric oxide resistance to Escherichia coli. Nat. Chem. Biol. 2009, 5:94-96.
21. Forte E., Borisov V.B., Konstantinov A.A., Brunori M., Giuffre A., Sarti P. Cytochrome bd, a key oxidase in bacterial survival and tolerance to nitrosative stress. Ital. J. Biochem. 2007, 56:265-269.
22. B-lacking cytochrome bd terminal oxidase. FEBS Lett. 2006, 580:4823-4826.
23. Borisov V.B., Forte E., Giuffre A., Konstantinov A., Sarti P. 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. 2009, 103:1185-1187.
24. Bader M., Muse W., Ballou D.P., Gassner C., Bardwell J.C.A. Oxidative protein folding is driven by the electron transport system. Cell 1999, 98:217-227.
25. Borisov V.B., Davletshin A.I., Konstantinov A.A. Peroxidase activity of cytochrome bd from Escherichia coli. Biochemistry (Moscow) 2010, 75:428-436. (translated from Biokhimiya (in Russian) (2010), 75, 520-530).
26. Green G.N., Fang H., Lin R.-J., Newton G., Mather M., Georgiou C.D., Gennis R.B. The nucleotide sequence of the cyd locus encoding the two subunits of the cytochrome d terminal oxidase complex of Escherichia coli. J. Biol. Chem. 1988, 263:13138-13143.
27. Poole R.K. Oxygen reactions with bacterial oxidases and globins: binding, reduction and regulation. Anthonie van Leeuwenhoek 1994, 65:289-310.
28. Mogi T., Tsubaki M., Hori H., Miyoshi H., Nakamura H., Anraku Y. Two terminal quinol oxidase families in Escherichia coli: variations on molecular machinery for dioxygen reduction. J. Biochem. Mol. Biol. Biophys. 1998, 2:79-110.
29. Junemann S., Wrigglesworth J.M. Antimycin inhibition of the cytochrome bd complex from Azotobacter vinelandii indicates the presence of a branched electron transfer pathway for the oxidation of ubiquinol. FEBS Lett. 1994, 345:198-202.
30. 558 component of the cytochrome bd quinol oxidase complex from Escherichia coli has histidine-methionine axial ligation. Biochem. J. 1995, 308:641-644.
31. Belevich I., Borisov V.B., Konstantinov A.A., Verkhovsky M.I. Oxygenated complex of cytochrome bd from Escherichia coli: stability and photolability. FEBS Lett. 2005, 579:4567-4570.
32. Belevich I., Borisov V.B., Bloch D.A., Konstantinov A.A., Verkhovsky M.I. Cytochrome bd from Azotobacter vinelandii: evidence for high-affinity oxygen binding. Biochemistry 2007, 46:11177-11184.
33. 1-like haemoprotein (cytochrome b-595) in Escherichia coli is a direct electron donation to cytochrome d. FEBS Lett. 1987, 217:49-52.
34. Kobayashi K., Tagawa S., Mogi T. Electron transfer process in cytochrome bd-type ubiquinol oxidase from Escherichia coli revealed by pulse radiolysis. Biochemistry 1999, 38:5913-5917.
35. Krasnoselskaya I., Arutjunjan A.M., Smirnova I., Gennis R., Konstantinov A.A. Cyanide-reactive sites in cytochrome bd complex from E. coli. FEBS Lett. 1993, 327:279-283.
36. Hill J.J., Alben J.O., Gennis R.B. Spectroscopic evidence for a heme-heme binuclear center in the cytochrome bd ubiquinol oxidase from Escherichia coli. Proc. Natl Acad. Sci. USA 1993, 90:5863-5867.
37. Tsubaki M., Hori H., Mogi T., Anraku Y. Cyanide-binding site of bd-type ubiquinol oxidase from Escherichia coli. J. Biol. Chem. 1995, 270:28565-28569.
38. Borisov V., Arutyunyan A.M., Osborne J.P., Gennis R.B., Konstantinov A.A. Magnetic circular dichroism used to examine the interaction of Escherichia coli cytochrome bd with ligands. Biochemistry 1999, 38:740-750.
39. Vos M.H., Borisov V.B., Liebl U., Martin J.-L., Konstantinov A.A. Femtosecond resolution of ligand-heme interactions in the high-affinity quinol oxidase bd: a di-heme active site?. Proc. Natl Acad. Sci. USA 2000, 97:1554-1559.
40. 595 reacts with CO. J. Biol. Chem. 2001, 276:22095-22099.
41. 595 in quinol oxidase bd from Escherichia coli: a photoselection study using femtosecond spectroscopy. Biochemistry 2002, 41:1654-1662.
42. Hori H., Tsubaki M., Mogi T., Anraku Y. EPR study of NO complex of bd-type ubiquinol oxidase from Escherichia coli. J. Biol. Chem. 1996, 271:9254-9258.
43. 595 is 10 A. Biochemistry 2008, 47:1752-1759.
44. Bloch D.A., Borisov V.B., Mogi T., Verkhovsky M.I. Heme/heme redox interaction and resolution of individual optical absorption spectra of the hemes in cytochrome bd from Escherichia coli. Biochim. Biophys. Acta 2009, 1787:1246-1253.
45. Rothery R.A., Houston A.M., Ingledew W.J. The respiratory chain of anaerobically grown Escherichia coli: reactions with nitrite and oxygen. J. Gen. Microbiol. 1987, 133:3247-3255.
46. D'mello R., Hill S., Poole R.K. The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two-oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 1996, 142:755-763.
47. 595. Biochemistry 2001, 40:8548-8556.
48. 558 component of the cytochrome bd ubiquinol oxidase from Escherichia coli. Biochemistry 1995, 34:13491-13501.
49. Joliot P., Beal D., Frilley B. Une nouvelle methode spectrophotometrique destinee a l'etude des reactions photosynthetiques. J. Chim. Phys. Phys. 1980, 77:209-216.
50. Beal D., Rappaport F., Joliot P. A new high-sensitivity 10-ns time-resolution spectrophotometric technique adapted to in vivo analysis of the photosynthetic apparatus. Rev. Sci. Instrum. 1999, 70:202-207.
51. Koland J.G., Miller M.J., Gennis R.B. Potentiometric analysis of the purified cytochrome d terminal oxidase complex from Escherichia coli. Biochemistry 1984, 23:1051-1056.
52. 595. Biochemistry 1986, 25:2314-2321.
53. Hill B.C., Hill J.J., Gennis R.B. The room temperature reaction of carbon monoxide and oxygen with the cytochrome bd quinol oxidase from Escherichia coli. Biochemistry 1994, 33:15110-15115.
54. Junemann S., Rich P.R., Wrigglesworth J.M. CO flash photolysis of cytochrome bd from Azotobacter vinelandii. Biochem. Soc. Trans. 1995, 23:157S.
55. Junemann S., Wrigglesworth J.M. Cytochrome bd oxidase from Azotobacter vinelandii. Purification and quantitation of ligand binding to the oxygen reduction site. J. Biol. Chem. 1995, 270:16213-16220.
56. Borisov V.B. Interaction of bd-type quinol oxidase from Escherichia coli and carbon monoxide: heme d binds CO with high affinity. Biochemistry (Moscow) 2008, 73:14-22. (translated from Biokhimiya (in Russian) (2008), 73, 18-28).
57. +-motive oxidases of the o-type from Bacillus FTU and of the d-type from Escherichia coli. FEBS Lett. 1993, 327:347-350.
58. Junemann S., Wrigglesworth J.M., Rich P.R. Effects of decyl-aurachin D and reversed electron transfer in cytochrome bd. Biochemistry 1997, 36:9323-9331.
59. Lorence R.M., Miller M.J., Borochov A., Faiman-Weinberg R., Gennis R.B. Effects of pH and detergent on the kinetic and electrochemical properties of the purified cytochrome d terminal oxidase complex of Escherichia coli. Biochim. Biophys. Acta 1984, 790:148-153.