Redox-mediated interactions of VHb ( Vitreoscilla haemoglobin) with OxyR: Novel regulation of VHb biosynthesis under oxidative stress

Biochemical Journal

Volumn 426, Issue 3, 2010, Pages 271-280

  Anand, Arvind ^a   Duk, Brian T ^b   Singh, Sandeep ^a   Akbas, Meltem Y ^c   Webster, Dale A ^b   Stark, Benjamin C ^b   Dikshit, Kanak L ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

^b Illinois Institute of Technology   (United States)

^c GEBZE TECHNICAL UNIVERSITY   (Turkey)

Author keywords

Bacterial haemoglobin; Oxidative stress; OxyR; Protein protein interaction; Vitreoscilla; Vitreoscilla haemoglobin (VHb)

Indexed keywords

CATALASE-PEROXIDASE; E. COLI; HAEMOGLOBINS; HIGH SENSITIVITY; HYPOXIC CONDITION; IN-VITRO; MEDIATED INTERACTION; NITRATE REDUCTASE; OXIDIZED STATE; PROTECTIVE EFFECTS; PROTEIN-PROTEIN INTERACTIONS; REDOX STATE; SUPER OXIDE DISMUTASE; TRANSCRIPTIONAL ACTIVATORS; TRANSCRIPTIONAL CONTROL; TWO-HYBRID SCREENS; VITREOSCILLA; VITREOSCILLA HAEMOGLOBIN (VHB);

BACTERIOLOGY; BINDING ENERGY; BIOCHEMISTRY; BIOSYNTHESIS; CHEMICAL ACTIVATION; ESCHERICHIA COLI; GELS; GENE ENCODING; GENE EXPRESSION; OXYGEN; PLANTS (BOTANY); PROTEINS;

OXIDATIVE STRESS;

CATALASE; FUMARIC ACID; NITRATE REDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUPEROXIDE DISMUTASE; BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN; FNR PROTEIN, E COLI; HEMOGLOBIN PROTEIN, VITREOSCILLA; HYDROGEN PEROXIDE; HYDROPEROXIDASE II; IRON SULFUR PROTEIN; KATG PROTEIN, E COLI; OXYR PROTEIN, E COLI; REPRESSOR PROTEIN; SODA PROTEIN, BACTERIA; TRUNCATED HEMOGLOBIN;

ARTICLE; BIOSYNTHESIS; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; IN VITRO STUDY; MUTANT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; REDOX STRESS; VITREOSCILLA; VITREOSCILLA HAEMOGLOBIN; ANAEROBIC GROWTH; BIOLOGICAL MODEL; DRUG EFFECT; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO HYBRID SYSTEM; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; VITREOSCILLA;

ANAEROBIOSIS; BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; CATALASE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN PEROXIDE; IRON-SULFUR PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; OXIDATION-REDUCTION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPEROXIDE DISMUTASE; TRUNCATED HEMOGLOBINS; TWO-HYBRID SYSTEM TECHNIQUES; VITREOSCILLA;

EID: 77951920428     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20091417     Document Type: Article

References (56)

1. Poole, R. K. and Hughes, M. N. (2000) New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36, 775-783
2. Frey, A. D. and Kallio, P. T. (2003) Bacterial hemoglobins and flavohemoglobins: versatile proteins and their impact on microbiology and biotechnology, FEMS Microbiol. Rev. 27, 525-545
3. Ascenzi, P., Bolognesi, M., Milani, M., Guertin, M. and Visca, P. (2007) Mycobacterial truncated hemoglobins: from genes to functions. Gene 398, 42-51 (Pubitemid 47068883)
4. Wakabayasi, S., Matsubara, H. and Webster, D. A. (1986) Primary sequence of a dimeric bacterial hemoglobin from Vitreoscilla. Nature 322, 481-483 (Pubitemid 16034023)
5. Tarricone, C., Galizzi, A., Coda, A., Asenzi, P. and Bolognesi, M. (1997) Unusual sturucture of the oxygen binding site in the dimeric bacterial hemoglobin from Vitreoscilla Sp. Structure 5, 497-507 (Pubitemid 27191226)
6. Kaur, R., Ahuja, S., Anand, A., Singh, B., Stark, B. C., Webster, D. A. and Dikshit, K. L. (2008) Functional implications of the proximal site hydrogen bonding network in Vitreoscilla hemoglobin (VHb): role of Tyr95 (G5) and Tyr126 (H12). FEBS Lett. 15, 3494-3500
7. Khosla, C. and Bailey, J. E. (1988) Heterologous expression of bacterial hemoglobin improves the growth properties of recombinant E. coli Nature 331, 633-635
8. Holmberg, N., Lilius, G., Bailey, J. E. and Bulow, L. (1997) Transgenic tobacco expressing Vitreoscilla hemoglobin exhibits enhanced growth and altered metabolic production. Nat. Biotechnol. 15, 244-247
9. Zhang, L., Li, Y., Wang, Z., Xia, Y., Chen, W. and Tang, K. (2007) Recent developments and future prospects of Vitreoscilla hemoglobin applications in metabolic engineering. Biotechnol. Adv. 25, 123-136
10. Roos, V., Andersson, C. I. J. and Bulow, L. (2004) Gene expression profiling of Escherichia coli expressing double Vitreoscilla haemoglobin. J. Biotechnol. 114, 107-120 (Pubitemid 39298289)
11. Isarankura-Na-Ayudhya, C., Panpumthong, P., Tangkosakul, T., Boonpangrak, S. and Prachayasittikul, V. (2008) Shedding light on the role of Vitreoscilla hemoglobin on cellular catabolic regulation by proteomic analysis. Int. J. Biol. Sci. 4, 71-80
12. Webster, D. A. (1988) Structure and function of bacterial hemoglobin and related proteins. Adv. Inorg. Biochem. 7, 245-265
13. Orri, Y. and Webster, D. A. (1986) Photodissociation of oxygenated cytochrome o(s) ( Vitreoscilla) and kinetic studies of reassociation. J. Biol. Chem. 249, 4261-4266
14. Dikshit, K. L., Spaulding, D., Braun, A. and Webster, D. A. (1989) Oxygen inhibition of globin gene transcription and bacterial hemoglobin production in Vitreoscilla. J. Gen. Microbiol. 135, 2601-2609
15. Dikshit, K. L., Dikshit, R. P. and Webster, D. A. (1990) Study of Vitreoscilla globin (vgb) gene expression and promoter activity in E. coli through transcription fusion. Nucleic Acids Res. 18, 4149-4155
16. Tsai, P. S., Nageli, M. and Bailey, J. E. (2002) Intracellular expression of Vitreoscilla hemoglobin modifies microaerobic Escherichia coli metabolism through elevated concentration and specific activity of cytochrome o. Biotechnol. Bioeng. 79, 558-567
17. Ramandeep, D., Hwang, K. W., Raje, M., Kim, K.J., Stark, B.C., Dikshit, K.L. and Webster, D. A. (2001) Vitreoscilla hemoglobin: intracellular localization and binding to membranes. J. Biol. Chem. 277, 24781-24789
18. Erenler, S. O., Gencer, S., Geckil, H., Stark, B.C. and Webster, D. A. (2004) Cloning and expression of the Vitreoscilla hemoglobin gene in Enterobacter aerogenes: effect on cell growth and oxygen uptake. Appl. Biochem. Microbiol. 40, 241-248
19. Park, K. W., Kim, K. J., Howard, A. J., Stark, B. C. and Webster, D. A. (2002) Vitreoscilla hemoglobin binds to subunit I of cytochrome boubiquinol oxidases. J. Biol. Chem. 277, 33334-33337
20. Rinaldi, A. C., Bonamore, A., Macone, A., Boffi, A., Bozzi, A. and Di Giulio, A. (2006) Interaction of Vitreoscilla hemoglobin with membrane lipids. Biochemistry 45, 4069-4076
21. Fish, P. A., Webster, D. A. and Stark, B. C. (2001) Vitreoscilla hemoglobin enhances the first step in 2,4-dinitrotoluene degradation in vitroand at low aeration in vivo. J. Mol. Catal. B. Enzym. 9, 75-82
22. Lin, J. M., Stark, B. C. and Webster, D. A. (2003) Effects of Vitreoscilla hemoglobin on the 2,4-dinitrotoluene (DNT) dioxygenase activity of Burkholderia and on DNT degradation in two-phase bioreactors. J. Ind. Microbiol. Biotechnol. 30, 362-368
23. Lee, S. Y., Stark, B. C. and Webster, D. A. (2004) Structure-function studies of the Vitreoscilla hemoglobin D-region. Biochem. Biophys. Res. Comm. 316, 1101-1106
24. Dikshit, R. P., Dikshit, K. L., Liu, Y. and Webster, D. A. (1992) The bacterial hemoglobin from Vitreoscilla can support the aerobic growth of E. coli lacking terminal oxidases. Arch. Biochem. Biophys. 293, 241-245
25. Tsai, P. S., Rao, G. and Bailey, J. E. (1995) Improvement of Escherichia coli microaerobic oxygen metabolism by Vitreoscilla hemoglobin: new insights from NAD(P)H fluorescence and culture redox potential. Biotechnol. Bioeng. 47, 347-354
26. Kaur, R., Pathania, R., Sharma, V., Mande, S. and Dikshit, K. L. (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
27. Frey, A. D., Farres, J., Bollinger, C. J. T. and Kallio, P. T. (2002) Bacterial hemoglobins and flavohemoglobins for alleviation of nitrosative stress in Escherichia coli. Appl. Environ. Microbiol. 68, 4835-4840
28. Geckil, H., Gencer, S., Kahraman, H. and Erenler, S. O. (2003) Genetic engineering of Enterobacter aerogenes with the Vitreoscilla hemoglobin gene: cell growth, survival, and antioxidant enzyme status under oxidative stress. Res. Microbiol. 154, 425-431
29. Kvist, M., Ryabova, E. S., Nordlander, E. and Bulow, L. (2007) An investigation of the peroxidase activity of Vitreoscilla hemoglobin. J. Biol. Inorg. Chem. 12, 324-334
30. Keyer, K. and Imlay, J. A. (1996) Superoxide accelerates DNA damage by elevating free iron levels. Proc. Natl. Acad. Sci. U.S.A. 93, 13635-13640
31. Fridovich, I. (1998) Oxygen: the dark side. Age (Dordr.) 21, 77
32. Kim, Y. J., Sa, S. O., Chang, Y. K., Hong, S. K. and Hong, Y. S. (2007) Overexpression of Shinorhizobium meliloti hemoprotein in Streptomyces lividans to enhance secondary metabolite production. J. Microbiol. Biotechnol. 12, 2066-2070
33. Wang, Z., Xiao, Y., Chen, W., Tang, K. and Zhang, L. (2009) Functional expression of Vitreoscilla hemoglobin (VHb) in Arabidopsis relieves submergence, nitrosative, photo-oxidative stress and enhances antioxidants metabolism. Plant Sci. 176, 66-77
34. Abrams, J. J. and Webster, D. A. (1990) Purification, partial characterization, and possible role of catalase in the bacterium Vitreoscilla.Arch. Biochem. Biophys. 279, 54-59
35. Navani, N. K., Joshi, M. A. and Dikshit, K. L. (1996) Genetic transformation of Vitreoscilla sp. Gene 177, 265-266
36. Benov, L. and Fridovich, I. (1995) A superoxide dismutase mimic protects sodA sodB Escherichia coli against aerobic heating and stationary-phase death. Arch. Biochem. Biophys. 322, 291-294
37. Mukhopadhyay, S. and Schellhorn, H. E. (1994) Identification and characterization of hydrogen peroxide-sensitive mutants of Escherichia coli: genes that require OxyR for expression. J. Bacteriol. 176, 2300-2307
38. Dikshit, K. L. and Webster, D. A. (1988) Cloning, characterization and expression of the bacterial globin gene from Vitreoscilla in Escherichia coli.Gene 70, 377-386
39. Zheng, M., Aslund, F. and Storz, G. (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279, 1718-1721 (Pubitemid 28164467)
40. Lazazzera, B. A., Beinert, H., Khoroshilova, N., Kennedy, M. C. and Kiley, P. J. (1996) DNA binding and dimerization of the Fe-S-containing FNR protein from Escherichia coli are regulated by oxygen. J. Biol. Chem. 271, 2762-2768
41. Verma, S., Patel, S., Kaur, R., Stark, B. C., Diskhit, K. L. and Webster, D. A. (2005) Mutational study of the bacterial hemoglobin distal heme pocket. Biochem. Biophys. Res. Commun. 326, 290-297
42. Miller, J. H. (1972) Experiments in Molecular Genetics, pp, 352-355, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
43. Imlay, J. A. and Linn, S. (1987) Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. J. Bacteriol. 169, 2967-2976 (Pubitemid 17106313)
44. Woodbury, W., Spencer, A. K. and Stahman, M. A. (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal. Biochem. 44, 301-305
45. Tartaglia, A. L., Gimeno, C. J., Storz, G. and Ames, B. N. (1992) Multidegenerate DNA recognition by the OxyR transcriptional regulator. J. Biol. Chem. 267, 2038-2045
46. Khosla, C. and Bailey, J. E. (1989) Characterization of the oxygen-dependent promoter of the Vitreoscilla hemoglobin gene in Escherichia coli. J. Bacteriol. 171, 5995-6004 (Pubitemid 19266922)
47. Yang, J. G., Webster, D. A. and Stark, B. C. (2005) ArcA works with Fnr as a positive regulator of Vitreoscilla (bacterial) hemoglobin gene expression in Escherichia coli. Microbiol. Res. 160, 405-415
48. Joshi, M. and Dikshit, K. L. (1994) Oxygen dependent regulation of Vitreoscilla globin gene: evidence for positive regulation by FNR. Biochem. Biophys. Res. Comm. 202, 535-542
49. Webster, D. A. (1975) The formation of hydrogen peroxide during the oxidation of reduced nicotinamide adenine dinucleotide by cytochrome ofrom Vitreoscilla. J. Biol. Chem. 250, 4955-4958
50. Tao, K. (1999) In vivo oxidation-reduction kinetics of OxyR, the transcriptional activator for an oxidative stress-inducible regulon in Escherichia coli. FEBS Lett. 457, 90-92
51. Zheng, M. and Storz, G. (2000) Redox sensing by prokaryotic transcription factors. Biochem. Pharmacol. 59, 1-6
52. Storz, G., Tartaglia, L. A. and Ames, B. N. (1990) Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248, 189-194
53. Partridge, J. A., Poole, R. K. and Green, J. (2007) The Escherichia coli yhjA gene, encoding a predicted cytochrome c peroxidase, is regulated by FNR and OxyR. Microbiology 153, 1499-1507
54. Constantinidou, C. M., Hobman, J. L., Griffith, L., Patel, M. D., Penn, C. W., Cole, J. A. and Overton, T. W. (2006) A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coliK12 adapts from aerobic to anaerobic growth. J. Biol. Chem. 281, 4802-4815
55. Manchado, M., Michan, C. and Pueyo, C. (2000) Hydrogen peroxide activates the SoxRS regulon in vivo. J. Bacterol. 182, 6842-6844 (Pubitemid 32249272)
56. Orii, Y. and Webster, D. A. (1977) Oxygenated cytochrome o( Vitreoscilla) formed by treating oxidized cytochrome with superoxide anion. Plant Cell Physiol. 18, 521-526