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Abstract

YedVW is one of the uncharacterized two-component systems (TCSs) of . In order to identify the regulation targets of YedVW, we performed genomic SELEX (systematic evolution of ligands by exponential enrichment) screening using phosphorylated YedW and an DNA library, and identified YedW-binding sites within three intergenic spacers, , and , along the genome. Using a reporter assay system, we found that transcription of encoding 5-hydroxyisourate hydrolase, was induced at high concentrations of either Cu or HO. Cu-dependent expression of was observed in the knockout mutant, but was reduced markedly in the -null mutant. However, HO-induced expression was observed in the -null mutant, but not in the -null mutant. Gel mobility shift and DNase I footprinting analyses showed binding of both YedW and CusR to essentially the same sequence within the promoter region. Taken together, we concluded that YedVW and CusSR formed a unique cooperative TCS pair by recognizing and regulating the same targets, but under different environmental conditions – YedVW played a role in HO response regulation, whilst CusSR played a role in Cu response regulation.

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2015-04-01
2021-07-23
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References

  1. Anraku Y., Gennis R. B.(1987). The aerobic respiratory chain of Escherichia coli. Trends Biochem Sci 12, 262266. [View Article] [Google Scholar]
  2. Bouzat J. L., Hoostal M. J.(2013). Evolutionary analysis and lateral gene transfer of two-component regulatory systems associated with heavy-metal tolerance in bacteria. J Mol Evol 76, 267279. [View Article][PubMed] [Google Scholar]
  3. Cooper R. A., Knowles P. F., Brown D. E., McGuirl M. A., Dooley D. M.(1992). Evidence for copper and 3,4,6-trihydroxyphenylalanine quinone cofactors in an amine oxidase from the gram-negative bacterium Escherichia coli K-12. Biochem J 288, 337340.[PubMed] [Google Scholar]
  4. Filipe P., Haigle J., Freitas J., Fernandes A., Mazière J.-C., Mazière C., Santus R., Morlière P.(2002). Anti- and pro-oxidant effects of urate in copper-induced low-density lipoprotein oxidation. Eur J Biochem 269, 54745483. [View Article][PubMed] [Google Scholar]
  5. Gort A. S., Ferber D. M., Imlay J. A.(1999). The regulation and role of the periplasmic copper, zinc superoxide dismutase of Escherichia coli. Mol Microbiol 32, 179191. [View Article][PubMed] [Google Scholar]
  6. Hasegawa A., Ogasawara H., Kori A., Teramoto J., Ishihama A.(2008). The transcription regulator AllR senses both allantoin and glyoxylate and controls a set of genes for degradation and reutilization of purines. Microbiology 154, 33663378. [View Article][PubMed] [Google Scholar]
  7. Hennebry S. C., Wright H. M., Likic V. A., Richardson S. J.(2006). Structural and functional evolution of transthyretin and transthyretin-like proteins. Proteins 64, 10241045. [View Article][PubMed] [Google Scholar]
  8. Hennebry S. C., Sait L. C., Mantena R., Humphrey T. J., Yang J., Scott T., Kupz A., Richardson S. J., Strugnell R. A.(2012). Salmonella typhimurium’s transthyretin-like protein is a host-specific factor important in fecal survival in chickens. PLoS One 7, e46675. [View Article][PubMed] [Google Scholar]
  9. Hodgkinson V., Petris M. J.(2012). Copper homeostasis at the host–pathogen interface. J Biol Chem 287, 1354913555. [View Article][PubMed] [Google Scholar]
  10. Ishihama A.(2010). Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol Rev 34, 628645.[PubMed] [Google Scholar]
  11. Ishihama A.(2012). Prokaryotic genome regulation: a revolutionary paradigm. Proc Jpn Acad, Ser B, Phys Biol Sci 88, 485508. [View Article][PubMed] [Google Scholar]
  12. Ishihama A., Kori A., Koshio E., Yamada K., Maeda H., Shimada T., Makinoshima H., Iwata A., Fujita N.(2014). Intracellular concentrations of 65 species of transcription factors with known regulatory functions in Escherichia coli. J Bacteriol 196, 27182727. [View Article][PubMed] [Google Scholar]
  13. Keyer K., Imlay J. A.(1996). Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci U S A 93, 1363513640. [View Article][PubMed] [Google Scholar]
  14. Lee Y., Lee D. H., Kho C. W., Lee A. Y., Jang M., Cho S., Lee C. H., Lee J. S., Myung P. K. et al.(2005). Transthyretin-related proteins function to facilitate the hydrolysis of 5-hydroxyisourate, the end product of the uricase reaction. FEBS Lett 579, 47694774. [View Article][PubMed] [Google Scholar]
  15. Lemire J. A., Harrison J. J., Turner R. J.(2013). Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11, 371384. [View Article][PubMed] [Google Scholar]
  16. Lukat G. S., McCleary W. R., Stock A. M., Stock J. B.(1992). Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci U S A 89, 718722. [View Article][PubMed] [Google Scholar]
  17. Macomber L., Imlay J. A.(2009). The iron–sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci U S A 106, 83448349. [View Article][PubMed] [Google Scholar]
  18. McCleary W. R., Stock J. B.(1994). Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 269, 3156731572.[PubMed] [Google Scholar]
  19. Miller J. H.(1972).Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. [Google Scholar]
  20. Mizuno T.(1997). Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res 4, 161168. [View Article][PubMed] [Google Scholar]
  21. Munson G. P., Lam D. L., Outten F. W., O’Halloran T. V.(2000). Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 182, 58645871. [View Article][PubMed] [Google Scholar]
  22. Ogasawara H., Hasegawa A., Kanda E., Miki T., Yamamoto K., Ishihama A.(2007a). Genomic SELEX search for target promoters under the control of the PhoQP–RstBA signal relay cascade. J Bacteriol 189, 47914799. [View Article][PubMed] [Google Scholar]
  23. Ogasawara H., Ishida Y., Yamada K., Yamamoto K., Ishihama A.(2007b). PdhR (pyruvate dehydrogenase complex regulator) controls the respiratory electron transport system in Escherichia coli. J Bacteriol 189, 55345541. [View Article][PubMed] [Google Scholar]
  24. Ogasawara H., Yamada K., Kori A., Yamamoto K., Ishihama A.(2010). Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. Microbiology 156, 24702483. [View Article][PubMed] [Google Scholar]
  25. Ogasawara H., Shinohara S., Yamamoto K., Ishihama A.(2012). Novel regulation targets of the metal-response BasS–BasR two-component system of Escherichia coli. Microbiology 158, 14821492. [View Article][PubMed] [Google Scholar]
  26. Oshima T., Aiba H., Masuda Y., Kanaya S., Sugiura M., Wanner B. L., Mori H., Mizuno T.(2002). Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46, 281291. [View Article][PubMed] [Google Scholar]
  27. Rensing C., Grass G.(2003). Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27, 197213. [View Article][PubMed] [Google Scholar]
  28. Rensing C., Fan B., Sharma R., Mitra B., Rosen B. P.(2000). CopA: an Escherichia coli Cu(I)-translocating P-type ATPase. Proc Natl Acad Sci U S A 97, 652656. [View Article][PubMed] [Google Scholar]
  29. Rintoul M. R., Cusa E., Baldomà L., Badia J., Reitzer L., Aguilar J.(2002). Regulation of the Escherichia coli allantoin regulon: coordinated function of the repressor AllR and the activator AllS. J Mol Biol 324, 599610. [View Article][PubMed] [Google Scholar]
  30. Shimada T., Fujita N., Maeda M., Ishihama A.(2005). Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells 10, 907918. [View Article][PubMed] [Google Scholar]
  31. Simons R. W., Houman F., Kleckner N.(1987). Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53, 8596. [View Article][PubMed] [Google Scholar]
  32. Vogels G. D., Van der Drift C.(1976). Degradation of purines and pyrimidines by microorganisms. Bacteriol Rev 40, 403468.[PubMed] [Google Scholar]
  33. Walker J. R., Altamentova S., Ezersky A., Lorca G., Skarina T., Kudritska M., Ball L. J., Bochkarev A., Savchenko A.(2006). Structural and biochemical study of effector molecule recognition by the E. coli glyoxylate and allantoin utilization regulatory protein AllR. J Mol Biol 358, 810828. [View Article][PubMed] [Google Scholar]
  34. Xi H., Schneider B. L., Reitzer L.(2000). Purine catabolism in Escherichia coli and function of xanthine dehydrogenase in purine salvage. J Bacteriol 182, 53325341. [View Article][PubMed] [Google Scholar]
  35. Yamamoto K., Ishihama A.(2005). Transcriptional response of Escherichia coli to external copper. Mol Microbiol 56, 215227. [View Article][PubMed] [Google Scholar]
  36. Yamamoto K., Hirao K., Oshima T., Aiba H., Utsumi R., Ishihama A.(2005). Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 280, 14481456. [View Article][PubMed] [Google Scholar]
  37. Yamamoto K., Watanabe H., Ishihama A.(2014). Expression levels of transcription factors in Escherichia coli: growth phase- and growth condition-dependent variation of 90 regulators from six families. Microbiology 160, 19031913. [View Article][PubMed] [Google Scholar]
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