Novel Bacterial MerR-Like Regulators. Their Role in the Response to Carbonyl and Nitrosative Stress.

Advances in Microbial Physiology

Volumn 58, Issue , 2011, Pages 1-22

  McEwan, Alastair G ^a   Djoko, Karrera Y ^a   Chen, Nathan H ^a   Couñago, Rafael L M ^a   Kidd, Stephen P ^b   Potter, Adam J ^b   Jennings, Michael P ^c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c GRIFFITH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADHC PROTEIN; ALCOHOL DEHYDROGENASE; ALDEHYDE; BACTERIAL PROTEIN; CARBONYL DERIVATIVE; CARBOXYLESTERASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; INDUCIBLE NITRIC OXIDE SYNTHASE; MERR PROTEIN; NEISSERIA MERR LIKE REGULATOR PROTEIN; S NITROSOGLUTATHIONE; SUPEROXIDE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

BACILLUS SUBTILIS; BACTERIAL CELL; BOOK; CARBONYL STRESS; CELL STRESS; CELLULAR STRESS RESPONSE; EPITHELIUM CELL; GENE EXPRESSION; GONORRHEA; NEISSERIA; NEISSERIA GONORRHOEAE; NITROSATIVE STRESS; NONHUMAN; OXIDATION; PATHOGENESIS; PROTEIN FUNCTION; REGULON; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION REGULATION;

BACTERIA (MICROORGANISMS); NEISSERIA; NEISSERIA GONORRHOEAE; STREPTOCOCCUS PNEUMONIAE;

EID: 79959692852     PISSN: 00652911     EISSN: 00652911     Source Type: Book Series    
DOI: 10.1016/B978-0-12-381043-4.00001-5     Document Type: Chapter

References (75)

1. Anderson M.M., Hazen S.L., Hsu F.F., Heinecke J.W. The myeloperoxidase system of human phagocytes generates N-epsilon-(carboxymethyl)lysine on proteins: a mechanism for producing advances glycation end products at sites of inflammation. J. Clin. Investig. 1997, 99:424-432.
2. Angeli V., Tacito A., Paolicchi A., Barsacchi R., Franzini M., Baldassini R., Vecoli C., Pompella A., Bramanti E. A kinetic study of gamma-glutamyltransferase (GGT)-mediated S-nitrosoglutathione catabolism. Arch. Biochem. Biophys. 2009, 481:191-196.
3. Ansari A.Z., Chael M.L., O'Halloran T.V. Allosteric underwinding of DNA is a critical step in positive control of transcription by Hg-MerR. Nature 1992, 355:87-89.
4. Ansari A.Z., Bradner J.E., O'Halloran T.V. DNA-bend modulation in a repressor-to-activator switching mechanism. Nature 1995, 374:371-375.
5. Aslund F., Zheng M., Beckwith J., Storz G. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. USA 1999, 96:6161-6165.
6. Atichartpongkul S., Fuangthong M., Vattanaviboon P., Mongkolsuk S. Analyses of the regulatory mechanism and physiological roles of Pseudomonas aeruginosa OhrR, a transcription regulator and a sensor of organic hydroperoxides. J. Bacteriol. 2010, 192:2093-2101.
7. Bae J.B., Park J.H., Hahn M.Y., Kim M.S., Roe J.H. Redox-dependent changes in RsrA, an anti-sigma factor in Streptomyces coelicolor: zinc release and disulfide bond formation. J. Mol. Biol. 2004, 335:425-435.
8. Barber R.D., Donohue T.J. Function of a glutathione-dependent formaldehyde dehydrogenase in Rhodobacter sphaeroides formaldehyde oxidation and assimilation. Biochemistry 1998, 37:530-537.
9. Brown J.D., Thomas K.R. Rapid enzyme system for the identification of pathogenic Neisseria spp. J. Clin. Microbiol. 1985, 21:857-858.
10. Brown N.L., Ford S.J., Pridmore R.D., Fritzinger D.C. Nucleotide-sequence of a gene from the Pseudomonas transposon-Tn501 encoding mercuric reductase. Biochemistry 1983, 22:4089-4095.
11. Brown N.L., Misra T.K., Winnie J.N., Schmidt A., Seiff M., Silver S. The nucleotide-sequence of the mercuric resistance operons of plasmid R100 and transposon Tn501-further evidence for mer genes which enhance the activity of the mercuric ion detoxification system. Mol. Gen. Genet. 1986, 202:143-151.
12. Brown N.L., Stoyanov J.V., Kidd S.P., Hobman J.L. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 2003, 27:145-163.
13. Cardinale J.A., Clark V.L. Determinants of nitric oxide steady-state levels during anaerobic respiration by Neisseria gonorrhoeae. Mol. Microbiol. 2005, 58:177-188.
14. Changela A., Chen K., Xue Y., Holschen J., Outten C.E., O'Halloran T.V., Mondragon A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 2003, 301:1383-1387.
15. Chiueh C.C. Neuroprotective properties of nitric oxide 1999, 301-311. (Vol. 890, pp. 301-311).
16. Christman M.F., Storz G., Ames B.N. OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc. Natl. Acad. Sci. USA 1989, 86:3484-3488.
17. Cummins I., McAuley K., Fordham-Skelton A., Schwoerer R., Steel P.G., Davis B.G., Edwards R. Unique regulation of the active site of the serine esterase S-formylglutathione hydrolase. J. Mol. Biol. 2006, 359:422-432.
18. Ding H., Hidalgo E., Demple B. The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor. J. Biol. Chem. 1996, 271:33173-33175.
19. Djoko, K.Y., Chen, N.H., Potter, A.J., Kidd, S.P., Jennings, M.J. and McEwan, A.G. (Manuscript in preparation). Molecular characterization of NmlR, the redox-responsive transcription regulator from Neisseria gonorrhoeae.
20. Edwards J.L. Neisseria gonorrhoeae survival during primary human cervical epithelial cell Infection requires nitric oxide and is augmented by progesterone. Infect. Immun. 2010, 78:1202-1213.
21. Edwards J.L., Apicella M.A. Neisseria gonorrhoeae PLD directly interacts with Akt kinase upon infection of primary, human, cervical epithelial cells. Cell. Microbiol. 2006, 8:1253-1271.
22. Edwards J.S., Palsson B.O. Systems properties of the Haemophilus influenzae Rd metabolic genotype. J. Biol. Chem. 1999, 274:17410-17416.
23. Edwards J.L., Shao J.Q., Ault K.A., Apicella M.A. Neisseria gonorrhoeae elicits membrane ruffling and cytoskeletal rearrangements upon infection of primary human endocervical and ectocervical cells. Infect. Immun. 2000, 68:5354-5363.
24. Falsetta M.L., Bair T.B., Ku S.C., Hoven R.N.V., Steichen C.T., McEwan A.G., Jennings M.P., Apicella M.A. Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms. Infect. Immun. 2009, 77:3522-3532.
25. Franiek, J.A., Potter, A.J., Djoko, K.Y., Edwards, J.L., Chen, N.H., Kidd, S. P., Falsetta, M. L., Apicella, M.A., Jennings, M.P. and McEwan, A.G. (Manuscript in preparation). The copA gene of Neisseria gonorrhoeae is required for copper tolerance and survival of the gonococcus within cervical epithelial cells.
26. Fuangthong M., Helmann J.D. The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc. Natl. Acad. Sci. USA 2002, 99:6690-6695.
27. Gaudu P., Weiss B. SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form. Proc. Natl. Acad. Sci. USA 1996, 93:10094-10098.
28. Gaudu P., Moon N., Weiss B. Regulation of the soxRS oxidative stress regulon. Reversible oxidation of the Fe-S centers of SoxR in vivo. J. Biol. Chem. 1997, 272:5082-5086.
29. Gonzalez C., Proudfoot M., Brown G., Korniyenko Y., Mori H., Savchenko A., Yakuin A. Molecular basis of formaldehyde detoxification: characterization of two S-formylglutathione hydrolases from Escherichia coli, FrmB and YeiG. J. Biol. Chem. 2006, 281:14514-14522.
30. Gutheil W.G., Holmquist B., Vallee B.L. Purification, characterization, and partial sequence of the glutathione-dependent formaldehyde dehydrogenase from Escherichia coli-a class-III alcohol-dehydrogenase. Biochemistry 1992, 31:475-481.
31. Gutheil W.G., Kasimoglu E., Nicholson P.C. Induction of glutathione-dependent formaldehyde dehydrogenase activity in Escherichia coli and Hemophilus influenzae. Biochem. Biophys. Res. Commun. 1997, 238:693-696.
32. Harms N., Ras J., Reijnders W.N.M., van Spanning R.J.M., Stouthamer A.H. S-formylglutathione hydrolase of Paracoccus denitrificans is homologous to human esterase D: a universal pathway for formaldehyde detoxification?. J. Bacteriol. 1996, 178:6296-6299.
33. Hedberg J.J., Griffiths W.J., Nilsson S.J.F., Höög J.O. Reduction of S-nitrosoglutathione by human alcohol dehydrogenase 3 is an irreversible reaction as analysed by electrospray mass spectrometry. Eur. J. Biochem. 2003, 270:1249-1256.
34. Heldwein E.E., Brennan R.G. Crystal structure of the transcription activator BmrR bound to DNA and a drug. Nature 2001, 409:378-382.
35. Hobman J.L., Wilkie J., Brown N.L. A design for life: prokaryotic metal-binding MerR family regulators. Biometals 2005, 18:429-436.
36. Hogg N. Biological chemistry and clinical potential of S-nitrosothiols. Free Radic. Biol. Med. 2000, 28:1478-1486.
37. Huyen N.T.T., Eiamphungporn W., Mader U., Liebeke M., Lalk M., Hecker M., Helmann J.D., Antelmann H. Genome-wide responses to carbonyl electrophiles in Bacillus subtilis: control of the thiol-dependent formaldehyde dehydrogenase AdhA and cysteine proteinase YraA by the MerR-family regulator YraB (AdhR). Mol. Microbiol. 2009, 71:876-894.
38. Imlay J.A. How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv. Microb. Physiol. 2002, 46:111-153.
39. Imlay J.A. Pathways of oxidative damage. Annu. Rev. Microbiol. 2003, 57:395-418.
40. Imlay J.A. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 2008, 77:755-776.
41. Jensen D.E., Belka G.K., Du Bois G.C. S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem. J. 1998, 331:659-668.
42. Kaiser R., Fernandez M.R., Pares X., Jornvall H. Origin of the human alcohol-dehydrogenase system-implications from the structure and properties of the octopus protein. Proc. Natl. Acad. Sci. USA 1993, 90:11222-11226.
43. Kang J.G., Paget M.S., Seok Y.J., Hahn M.Y., Bae J.B., Hahn J.S., Kleanthous C., Buttner M.J., Roe J.H. RsrA, an anti-sigma factor regulated by redox change. EMBO J. 1999, 18:4292-4298.
44. Kato N., Sakazawa C., Nishizawa T., Tani Y., Yamada H. Purification and characterization of S-formylglutathione hydrolase from a methanol utilizing yeast, Kloeckera sp, No 2201. Biochim. Biophys. Acta 1980, 611:323-332.
45. Kidd S.P., Potter A.J., Apicella M.A., Jennings M.P., McEwan A.G. NmlR of Neisseria gonorrhoeae: a novel redox responsive transcription factor from the MerR family. Mol. Microbiol. 2005, 57:1676-1689.
46. Kidd S.P., Jiang D., Jennings M.P., McEwan A.G. Glutathione-dependent alcohol dehydrogenase AdhC is required for defense against nitrosative stress in Haemophilus influenzae. Infect. Immun. 2007, 75:4506-4513.
47. Kim S.O., Merchant K., Nudelman R., Beyer W.F., Keng T., DeAngelo J., Hausladen A., Stamler J.S. OxyR: a molecular code for redox-related signaling. Cell 2002, 109:383-396.
48. Lee I.W., Livrelli V., Park S.J., Totis P.A., Summers A.O. In vivo DNA-protein interactions at the divergent mercury resistance (mer) promoters. II. Repressor/activator (MerR)-RNA polymerase interaction with merOP mutants. J. Biol. Chem. 1993, 268:2632-2639.
49. Lee C., Lee S.M., Mukhopadhyay P., Kim S.J., Lee S.C., Ahn W.S., Yu M.H., Storz G., Ryu S.E. Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat. Struct. Mol. Biol. 2004, 11:1179-1185.
50. Liu L.M., Hausladen A., Zeng M., Que L., Heitman J., Stamler J.S. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 2001, 410:490-494.
51. Markham P.N., Ahmed M., Neyfakh A.A. The drug-binding activity of the multidrug-responding transcriptional regulator BmrR resides in its C-terminal domain. J. Bacteriol. 1996, 178:1473-1475.
52. Nunoshiba T., Hidalgo E., Amabile Cuevas C.F., Demple B. Two-stage control of an oxidative stress regulon: the Escherichia coli SoxR protein triggers redox-inducible expression of the soxS regulatory gene. J. Bacteriol. 1992, 174:6054-6060.
53. Okado-Matsumoto A., Fridovich I. The role of alpha, beta-dicarbonyl compounds in the toxicity of short chain sugars. J. Biol. Chem. 2000, 275:34853-34857.
54. Overton T.W., Whitehead R., Li Y., Snyder L.A.S., Saunders N.J., Smith H., Cole J.A. Coordinated regulation of the Neisseria gonorrhoeae-truncated denitrification pathway by the nitric oxide-sensitive repressor, NsrR, and nitrite-insensitive NarQ-NarP. J. Biol. Chem. 2006, 281:33115-33126.
55. Paget M.S., Bae J.B., Hahn M.Y., Li W., Kleanthous C., Roe J.H., Buttner M.J. Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch. Mol. Microbiol. 2001, 39:1036-1047.
56. Parkhill J., Lawley B., Hobman J.L., Brown N.L. Selection and characterization of mercury-independent activation mutants of the Tn501 transcriptional regulator, MerR. Microbiology 1998, 144(Pt 10):2855-2864.
57. Potter A.J., Kidd S.P., Edwards J.L., Falsetta M.L., Apicella M.A., Jennings M.P., McEwan A.G. Esterase D is essential for protection of Neisseria gonorrhoeae against nitrosative stress and for bacterial growth during interaction with cervical epithelial cells. J. Infect. Dis. 2009, 200:273-278.
58. Potter A.J., Kidd S.P., Edwards J.L., Falsetta M.L., Apicella M.A., Jennings M.P., McEwan A.G. Thioredoxin reductase is essential for protection of Neisseria gonorrhoeae against killing by nitric oxide and for bacterial growth during interaction with cervical epithelial cells. J. Infect. Dis. 2009, 199:227-235.
59. Potter A.J., Kidd S.P., McEwan A.G., Paton J.C. The MerR/NmlR family transcription factor of Streptococcus pneumoniae responds to carbonyl stress and modulates hydrogen peroxide production. J. Bacteriol. 2010, 192:4063-4066.
60. Ritz D., Beckwith J. Roles of thiol-redox pathways in bacteria. Annu. Rev. Microbiol. 2001, 55:21-48.
61. Sengupta R., Ryter S.W., Zuckerbraun B.S., Tzeng E., Billiar T.R., Stoyanovsky D.A. Thioredoxin catalyzes the denitrosation of low-molecular mass and protein S-nitrosothiols. Biochemistry 2007, 46:8472-8483.
62. Shafqat J., El-Ahmad M., Danielsson O., Martinez M.C., Persson B., Pares X., Jornvall H. Pea formaldehyde-active class III alcohol dehydrogenase: common derivation of the plant and animal forms but not of the corresponding ethanol-active forms (classes I and P). Proc. Natl. Acad. Sci. USA 1996, 93:5595-5599.
63. Shewchuk L.M., Verdine G.L., Nash H., Walsh C.T. Mutagenesis of the cysteines in the metalloregulatory protein MerR indicates that a metal-bridged dimer activates transcription. Biochemistry 1989, 28:6140-6145.
64. Staab C.A., Alander J., Morgenstern R., Grafstrom R.C., Höög J.O. The Janus face of alcohol dehydrogenase 3. Chem Biol. Interact. 2009, 178:29-35.
65. Stroeher U.H., Kidd S.P., Stafford S.L., Jennings M.P., Paton J.C., McEwan A.G. A pneumococcal MerR-like regulator and S-nitrosoglutathione reductase are required for systemic virulence. J. Infect. Dis. 2007, 196:1820-1826.
66. Takahashi H., Watanabe H. A gonococcal homologue of meningococcal gamma-glutamyl transpeptidase gene is a new type of bacterial pseudogene that is transcriptionally active but phenotypically silent. BMC Microbiol. 2005, 5:56.
67. Thornalley P.J. Pharmacology of methylglyoxal: formation, modification of proteins and nucleic acids, and enzymatic detoxification-a role in pathogenesis and antiproliferative chemotherapy. Gen. Pharmacol. 1996, 27:565-573.
68. Tsaneva I.R., Weiss B. soxR, a locus governing a superoxide response regulon in Escherichia coli K-12. J. Bacteriol. 1990, 172:4197-4205.
69. Uotila L., Koivusal M. Purification and properties of S-formylglutathione hydrolase from human liver. J. Biol. Chem. 1974, 249:7664-7672.
70. Watanabe S., Kita A., Kobayashi K., Miki K. Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc. Natl. Acad. Sci. USA 2008, 105:4121-4126.
71. Williams D.H., Lund P., Krebs H.A. Redox state of free nicotinamide-adenine dinucleotide in cytoplasm and mitochondria of rat liver. Biochem. J. 1967, 103:514-527.
72. Wu D., Li Y., Song G.J., Zhang D., Shaw N., Liu Z.J. Crystal structure of human esterase D: a potential genetic marker of retinoblastoma. FASEB J. 2009, 23:1441-1446.
73. Zeng Q., Stalhandske C., Anderson M.C., Scott R.A., Summers A.O. The core metal-recognition domain of MerR. Biochemistry 1998, 37:15885-15895.
74. Zheleznova E.E., Markham P.N., Neyfakh A.A., Brennan R.G. Structural basis of multidrug recognition by BmrR, a transcription activator of a multidrug transporter. Cell 1999, 96:353-362.
75. Zheng M., Aslund F., Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 1998, 279:1718-1721.