1887

Microbiology Society logo

Volume 155, Issue 3

Exploring the antimicrobial action of a carbon monoxide-releasing compound through whole-genome transcription profiling of Free

Abstract

We recently reported that carbon monoxide (CO) has bactericidal activity. To understand its mode of action we analysed the gene expression changes occurring when , grown aerobically and anaerobically, is treated with the CO-releasing molecule CORM-2 (tricarbonyldichlororuthenium(II) dimer). Microarray analysis shows that the CORM-2 response is multifaceted, with a high number of differentially regulated genes spread through several functional categories, namely genes involved in inorganic ion transport and metabolism, regulators, and genes implicated in post-translational modification, such as chaperones. CORM-2 has a higher impact in cells grown anaerobically, as judged by the repression of genes belonging to eight functional classes which are not seen in the response of aerobically CORM-2-treated cells. The biological relevance of the variations caused by CORM-2 was substantiated by studying the CORM-2 sensitivity of selected mutants. The results show that the deletion of redox-sensing regulators SoxS and OxyR increased the sensitivity to CORM-2 and suggest that while SoxS plays an important role in protection against CORM-2 under both growth conditions, OxyR seems to participate only in the aerobic CORM-2 response. Under anaerobic conditions, we found that the heat-shock proteins IbpA and IbpB contribute to CORM-2 defence since the deletion of these genes increases the sensitivity of the strain. The induction of several genes and the hypersensitivity to CORM-2 of the Δ, Δ and Δ mutant strains suggest that CO has effects on the methionine metabolism of . CORM-2 also affects the transcription of several biofilm-related genes and increases biofilm formation in . In particular, the absence of or increases the resistance of to CORM-2, and deletion of leads to a strain that has lost its capacity to form biofilm upon treatment with CORM-2. In spite of the relatively stable nature of the CO molecule, our results show that CO is able to trigger a significant alteration in the transcriptome of which necessarily has effects in several key metabolic pathways.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): CORM, CO-releasing molecule , CORM-2, tricarbonyldichlororuthenium(II) dimer and FDR, false discovery rate
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.023911-0
2009-03-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/3/813.html?itemId=/content/journal/micro/10.1099/mic.0.023911-0&mimeType=html&fmt=ahah

References

  1. Alessio E., Milani B., Bolle M., Mestroni G., Faleschini P., Todone F., Geremia S., Calligaris M. 1995; Carbonyl derivatives of chloride-dimethyl sulfoxide-ruthenium(II) complexes: synthesis, structural characterization, and reactivity of Ru(CO)x(DMSO)4- xCl2 complexes ( x=1–3. Inorg Chem 34:4722–4734
     [Google Scholar]
  2. Al-Shahrour F., Diaz-Uriarte R., Dopazo J. 2004; FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20:578–580
     [Google Scholar]
  3. Al-Shahrour F., Minguez P., Tarraga J., Montaner D., Alloza E., Vaquerizas J. M., Conde L., Blaschke C., Vera J., Dopazo J. 2006; BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Res 34:W472–W476
     [Google Scholar]
  4. Al-Shahrour F., Minguez P., Tarraga J., Medina I., Alloza E., Montaner D., Dopazo J. 2007; FatiGO+: a functional profiling tool for genomic data. Integration of functional annotation, regulatory motifs and interaction data with microarray experiments. Nucleic Acids Res 35:W91–W96
     [Google Scholar]
  5. Beloin C., Valle J., Latour-Lambert P., Faure P., Kzreminski M., Balestrino D., Haagensen J. A., Molin S., Prensier G. other authors 2004; Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51:659–674
     [Google Scholar]
  6. Danese P. N., Silhavy T. J. 1998; CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180:831–839
     [Google Scholar]
  7. Dulak J., Jozkowicz A., Foresti R., Kasza A., Frick M., Huk I., Green C. J., Pachinger O., Weidinger F., Motterlini R. 2002; Heme oxygenase activity modulates vascular endothelial growth factor synthesis in vascular smooth muscle cells. Antioxid Redox Signal 4:229–240
     [Google Scholar]
  8. Fleischer R., Heermann R., Jung K., Hunke S. 2007; Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli . J Biol Chem 282:8583–8593
     [Google Scholar]
  9. Herzberg M., Kaye I. K., Peti W., Wood T. K. 2006; YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J Bacteriol 188:587–598
     [Google Scholar]
  10. Justino M. C., Vicente J. B., Teixeira M., Saraiva L. M. 2005; New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. J Biol Chem 280:2636–2643
     [Google Scholar]
  11. Lethanh H., Neubauer P., Hoffmann F. 2005; The small heat-shock proteins IbpA and IbpB reduce the stress load of recombinant Escherichia coli and delay degradation of inclusion bodies. Microb Cell Fact 4:6
     [Google Scholar]
  12. Li C., Hung Wong W. 2001; Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2:RESEARCH0032
     [Google Scholar]
  13. Li C., Wong W. H. 2001; Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98:31–36
     [Google Scholar]
  14. Li C., Hossieny P., Wu B. J., Qawasmeh A., Beck K., Stocker R. 2007; Pharmacologic induction of heme oxygenase-1. Antioxid Redox Signal 9:2227–2239
     [Google Scholar]
  15. Motterlini R., Clark J. E., Foresti R., Sarathchandra P., Mann B. E., Green C. J. 2002; Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res 90:E17–E24
     [Google Scholar]
  16. Motterlini R., Mann B. E., Foresti R. 2005; Therapeutic applications of carbon monoxide-releasing molecules. Expert Opin Investig Drugs 14:1305–1318
     [Google Scholar]
  17. Nobre L. S., Seixas J. D., Romao C. C., Saraiva L. M. 2007; Antimicrobial action of carbon monoxide-releasing compounds. Antimicrob Agents Chemother 51:4303–4307
     [Google Scholar]
  18. Otterbein L. E., Choi A. M. 2000; Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 279:L1029–L1037
     [Google Scholar]
  19. Ren D., Bedzyk L. A., Thomas S. M., Ye R. W., Wood T. K. 2004; Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64:515–524
     [Google Scholar]
  20. Ren D., Zuo R., Gonzalez Barrios A. F., Bedzyk L. A., Eldridge G. R., Pasmore M. E., Wood T. K. 2005; Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl Environ Microbiol 71:4022–4034
     [Google Scholar]
  21. Ryter S. W., Alam J., Choi A. M. 2006; Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583–650
     [Google Scholar]
  22. Stupfel M., Bouley G. 1970; Physiological and biochemical effects on rats and mice exposed to small concentrations of carbon monoxide for long periods. Ann N Y Acad Sci 174:342–368
     [Google Scholar]
  23. Thomas J. G., Baneyx F. 1998; Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J Bacteriol 180:5165–5172
     [Google Scholar]
  24. Verma A., Hirsch D. J., Glatt C. E., Ronnett G. V., Snyder S. H. 1993; Carbon monoxide: a putative neural messenger. Science 259:381–384
     [Google Scholar]
  25. Wu L., Wang R. 2005; Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 57:585–630
     [Google Scholar]
  26. Wu J., Weiss B. 1992; Two-stage induction of the soxRS (superoxide response) regulon of Escherichia coli . J Bacteriol 174:3915–3920
     [Google Scholar]
  27. Zhang X. S., Garcia-Contreras R., Wood T. K. 2007; YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol 189:3051–3062
     [Google Scholar]
  28. Zhao K., Liu M., Burgess R. R. 2005; The global transcriptional response of Escherichia coli to induced sigma 32 protein involves sigma 32 regulon activation followed by inactivation and degradation of sigma 32 in vivo . J Biol Chem 280:17758–17768
     [Google Scholar]
  29. Zheng M., Wang X., Templeton L. J., Smulski D. R., LaRossa R. A., Storz G. 2001; DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.023911-0
Loading
Exploring the antimicrobial action of a carbon monoxide-releasing compound through whole-genome transcription profiling of Escherichia coli
Microbiology 155, 813 (2009); https://doi.org/10.1099/mic.0.023911-0
/content/journal/micro/10.1099/mic.0.023911-0
/content/journal/micro/10.1099/mic.0.023911-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF

Supplementary material 4

PDF

Supplementary material 5

PDF

Supplementary material 6

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error