Bacterial hemoglobins and flavohemoglobins for alleviation of nitrosative stress in Escherichia coli

Applied and Environmental Microbiology

Volumn 68, Issue 10, 2002, Pages 4835-4840

  Frey, Alexander D ^a   Farrés, Judith ^a   Bollinger, Christian J T ^a   Kallio, Pauli T ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; CELL CULTURE; DETOXIFICATION; GENES; GROWTH KINETICS; HEMOGLOBIN; PROTEINS;

OXIDATIVE STRESS;

ESCHERICHIA COLI;

CELL EXTRACT; FLAVOHEMOGLOBIN; HEMOGLOBIN; HEMOGLOBIN DERIVATIVE; NITRIC OXIDE; NITRO DERIVATIVE; NITROPRUSSIDE SODIUM; RADICAL; UNCLASSIFIED DRUG;

BACTERIUM;

ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; DEINOCOCCUS RADIODURANS; DETOXIFICATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE OVEREXPRESSION; KLEBSIELLA PNEUMONIAE; NITROGEN METABOLISM; NONHUMAN; OXIDATIVE STRESS; PSEUDOMONAS AERUGINOSA; VITREOSCILLA;

BACTERIAL PROTEINS; DIHYDROPTERIDINE REDUCTASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION; HEMEPROTEINS; HEMOGLOBINS; NADH, NADPH OXIDOREDUCTASES; NITRIC OXIDE; NITROPRUSSIDE; OXIDATIVE STRESS; OXYGENASES; RECOMBINANT PROTEINS;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; DEINOCOCCUS; DEINOCOCCUS RADIODURANS; ESCHERICHIA COLI; KLEBSIELLA; KLEBSIELLA PNEUMONIAE; NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; VITREOSCILLA; VITREOSCILLA SP.;

EID: 0036794855     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.68.10.4835-4840.2002     Document Type: Article

References (40)

1. Anjum, M. F., N. Ioannidis, and R. K. Poole. 1998. Response of the NAD(P)H-oxidising flavohaemoglobin (Hmp) to prolonged oxidative stress and implications for its physiological role in Escherichia coli. FEMS Microbiol. Lett. 166:219-223.
2. Bollinger, C. J. T., J. E. Bailey, and P. T. Kallio. 2001. Novel hemoglobins to enhance microaerobic growth and substrate utilization in Escherichia coli. Biotechnol. Prog. 17:798-808.
3. Bolwell, G. P. 1999. Role of active oxygen species and NO in plant defence responses. Curr. Opin. Plant Biol. 2:287-294.
4. Bonner, F. T., M. N. Hughes, R. K. Poole, and R. I. Scott. 1991. Kinetics of the reactions of trioxodinitrate and nitrite ions with cytochrome d in Escherichia coli. Biochim. Biophys. Acta 1056:133-138.
5. Bradford, M. M. 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
6. Crawford, M. J., and D. E. Goldberg. 1998. Role for the Salmonella flavohemoglobin in protection from nitric oxide. J. Biol. Chem. 273:12543-12547.
7. Farr, S. B., and T. Kogoma. 1991. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 55:561-585.
8. Frey, A. D., J. E. Bailey, and P. T. Kallio. 2000. Expression of Alcaligenes eutrophus flavohemoprotein and engineered Vatreoscilla hemoglobin-reductase fusion protein for improved hypoxic growth of Escherichia coli. Appl. Environ. Microbiol. 66:98-104.
9. 13C nuclear magnetic resonance flux distribution analysis in microaerobic bioprocesses. Appl. Environ. Microbiol. 67:680-687.
10. Gardner, P. R., A. M. Gardner, L. A. Martin, Y. Dou, T. Li, J. S. Olson, H. Zhu, and A. F. Riggs. 2000. Nitric oxide dioxygenase activity and function of flavohemoglobins: sensitivity to nitric oxide and carbon monoxide inhibition. J. Biol. Chem. 275:31581-31587.
11. Gardner, P. R., A. M. Gardner, L. A. Martin, and A. L. Salzman. 1998. Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc. Natl. Acad. Sci. USA 95:10378-10383.
12. Gonzales-Prevatt, V., and D. A. Webster. 1980. Purification and properties of NADH-cytochrome o reductase from Vitreoscilla, J. Biol. Chem. 255:1478-1482.
13. González-Flecha, B., and B. Demple. 1995. Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J. Biol. Chem. 270:13681-13687.
14. Goretski, J., O. C. Zafiriou, and T. C. Hollocher. 1990. Steady-state nitric oxide concentrations during denitrification. J. Biol. Chem. 265:11535-11538.
15. Hausladen, A., A. Gow, and J. S. Stamler. 2001. Flavohemoglobin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen. Proc. Natl. Acad. Sci. USA 98:10108-10112.
16. Hausladen, A., A. J. Gow, and J. S. Stamler. 1998. Nitrosative stress: metabolic pathway involving the flavohemoglobin. Proc. Natl. Acad. Sci. USA 95:14100-14105.
17. Hausladen, A., C. T. Privalle, T. Keng, J. DeAngelo, and J. S. Stamler. 1996. Nitrosative stress: activation of the transcription factor OxyR. Cell 86:719-729.
18. Hu, Y. M., P. D. Butcher, J. A. Mangan, M. A. Rajandream, and A. R. M. Coates. 1999. Regulation of hmp gene transcription in Mycobacterium tuberculosis: effects of oxygen limitation and nitrosative and oxidative stress. J. Bacteriol. 181:3486-3493.
19. Imlay, J. A., and I. Fridovich. 1991. Assay of metabolic superoxide production in Escherichia coli. J. Biol. Chem. 266:6957-6965.
20. Kallio, P. T., A. D. Frey, and J. E. Bailey. 2001. From Vitreoscilla hemoglobin (VHb) to a novel class of growth stimulating hemoglobin proteins, p. 75-87. In O.-W. Merten, D. Mattanovich, G. Larsson, P. Neubauer, C. Land, D. Porro, J. Teixeira de Mattos, P. Postma, and J. Cole (ed.), Recombinant protein production with prokaryotic and eukaryotic cells. A comparative view on host physiology. Kluewer Academics Publishers, Dordrecht, The Netherlands.
21. Kallio, P. T., D. J. Kim, P. S. Tsai, and J. E. Bailey. 1994. Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions. Eur. J. Biochem. 219:201-208.
22. Kallio, P. T., P. S. Tsai, and J. E. Bailey. 1996. Expression of Vitreoscilla hemoglobin is superior to horse heart myoglobin or yeast flavohemoglobin expression for enhancing Escherichia coli growth in a microaerobic bioreactor. Biotechnol. Prog. 12:751-757.
23. Kaur, R., R. Pathania, V. Sharma, S. C. Mande, and K. L. Dikshit. 2002. Chimeric Vitreoscilla hemoglobin (VHb) carrying a flavoreductase domain relieves nitrosative stress in Escherichia coli: new insight into the functional role of VHb. Appl. Environ. Microbiol. 68:152-160.
24. Khosla, C., and J. E. Bailey. 1988. The Vitreoscilla hemoglobin gene: molecular cloning, nucleotide sequence and genetic expression in Escherichia coli. Mol. Gen. Genet. 214:158-161.
25. 5 interactions and the kinetic mechanism of metmyoglobin reductase. J. Biol. Chem. 260:15699-15707.
26. Membrillo-Hernández, J., M. D. Coopamah, M. F. Anjum, T. M. Stevanin, A. Kelly, M. N. Hughes, and R. K. Poole. 1999. The flavohemoglobin of Escherichia coli confers resistance to a nitrosating agent, a "nitric oxide releaser," and paraquat and is essential for transcriptional responses to oxidative stress. J. Biol. Chem. 274:748-754.
27. Membrillo-Hernández, J., N. Ioannidis, and R. K. Poole. 1996. The flavohaemoglobin (HMP) of Escherichia coli generates superoxide in vitro and causes oxidative stress in vivo. FEBS Lett. 382:141-144.
28. 5. J. Bacteriol. 179:3164-3170.
29. Mills, C. E., S. Sedelnikova, B. Soballe, M. N. Hughes, and R. K. Poole. 2001. 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. 353:207-213.
30. Patel, S. M., B. C. Stark, K. W. Hwang, K. L. Dikshit, and D. A. Webster. 2000. Cloning and expression of Vitreoscilla hemoglobin gene in Burkholderia sp. strain DNT for enhancement of 2,4-dinitrotoluene degradation. Biotechnol. Prog. 16:26-30.
31. Pomposiello, P. J., and B. Demple. 2001. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol. 19:109-114.
32. Poole, R. K., M. F. Anjum, J. Membrillo-Hernández, S. O. Kim, M. N. Hughes, and V. Stewart. 1996. Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J. Bacteriol. 178:5487-5492.
33. Ramandeep, K. W. Hwang, M. Raje, K. J. Kim, B. C. Stark, K. L. Dikshit, and D. A. Webster. 2001. Vitreoscilla hemoglobin. Intracellular localization and binding to membranes. J. Biol. Chem. 276:24781-24789.
34. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
35. Stevanin, T. M., N. Ioannidis, C. E. Mills, S. O. Kim, M. N. Hughes, and R. K. Poole. 2000. Flavohemoglobin hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo or bd, from nitric oxide. J. Biol. Chem. 275:35868-35875.
36. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
37. Webster, D. A., and C. Y. Liu. 1974. Reduced nicotinamide adenine dinucleotide cytochrome o reductase associated with cytochrome o purified from Vitreoscilla. Evidence for an intermediate oxygenated form of cytochrome o. J. Biol. Chem. 249:4257-4260.
38. 2 reaction. Chem. Res. Toxicol. 6:23-27.
39. Zhao, X. J., D. Raitt, P. V. Burke, A. S. Clewell, K. E. Kwast, and R. O. Poyton. 1996. Function and expression of flavohemoglobin in Saccharomyces cerevisiae - evidence for a role in the oxidative stress response. J. Biol. Chem. 271:25131-25138.
40. Zweier, J. L., P. H. Wang, A. Samouilov, and P. Kuppusamy. 1995. Enzyme-independent formation of nitric oxide in biological tissues. Nat. Med. 1:804809.