The σR regulon of Streptomyces coelicolor A3(2) reveals a key role in protein quality control during disulphide stress

Microbiology

Volumn 156, Issue 6, 2010, Pages 1661-1672

  Kallifidas, Dimitris ^a,b   Thomas, Derek ^a   Doughty, Phillip ^a   Paget, Mark S B ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAMIDE; METHIONINE SULFOXIDE REDUCTASE; RIBOFLAVIN; RIBONUCLEOTIDE REDUCTASE; SIGMA FACTOR; THIOL; THIOREDOXIN; BACTERIAL PROTEIN; DISULFIDE; HEAT SHOCK PROTEIN; HSPR PROTEIN, BACTERIA; PROTEIN; REPRESSOR PROTEIN; RNA; RSRA PROTEIN, STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GROWTH; GENE REPRESSION; HEAT SHOCK; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN QUALITY; REGULON; RNA SYNTHESIS; STIMULON; STREPTOMYCES COELICOLOR; WILD TYPE; CHEMISTRY; DRUG EFFECT; GENETICS; METABOLISM;

BACTERIAL PROTEINS; DIAMIDE; DISULFIDES; HEAT-SHOCK PROTEINS; PROTEIN FOLDING; PROTEINS; REGULON; REPRESSOR PROTEINS; RNA; SIGMA FACTOR; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS;

EID: 77953220053     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.037804-0     Document Type: Article

References (55)

1. Bae, J. B., Park, J. H., Hahn, M. Y., Kim, M. S. & Roe, J. H. (2004). Redox-dependent changes in RsrA, an anti-sigma factor in Streptomyces coelicolor: zinc release and disulfide bond formation. J Mol Biol 335, 425-435.
2. Barends, S., Zehl, M., Bialek, S., de Waal, E., Traag, B. A., Willemse, J., Jensen, O. N., Vijgenboom, E. & van Wezel, G. P. (2010). Transfer-messenger RNA controls the translation of cell-cycle and stress proteins in Streptomyces. EMBO Rep 11, 119-125.
3. Bellier, A. & Mazodier, P. (2004). ClgR, a novel regulator of clp and lon expression in Streptomyces. J Bacteriol 186, 3238-3248.
4. Borovok, I., Kreisberg-Zakarin, R., Yanko, M., Schreiber, R., Myslovati, M., Aslund, F., Holmgren, A., Cohen, G. & Aharonowitz, Y. (2002). Streptomyces spp. contain class Ia and class II ribonucleotide reductases: expression analysis of the genes in vegetative growth. Microbiology 148, 391-404. (Pubitemid 34162782)
5. Borovok, I., Gorovitz, B., Yanku, M., Schreiber, R., Gust, B., Chater, K., Aharonowitz, Y. & Cohen, G. (2004). Alternative oxygen-dependent and oxygen-independent ribonucleotide reductases in Streptomyces: cross-regulation and physiological role in response to oxygen limitation. Mol Microbiol 54, 1022-1035.
6. Bota, D. A. & Davies, K. J. (2002). Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 4, 674-680.
7. Bucca, G., Hindle, Z. & Smith, C. P. (1997). Regulation of the dnaK operon of Streptomyces coelicolor A3(2) is governed by HspR, an autoregulatory repressor protein. J Bacteriol 179, 5999-6004. (Pubitemid 27419020)
8. Bucca, G., Brassington, A. M., Schonfeld, H. J. & Smith, C. P. (2000). The HspR regulon of Streptomyces coelicolor: a role for the DnaK chaperone as a transcriptional co-repressor. Mol Microbiol 38, 1093-1103.
9. Bucca, G., Brassington, A. M., Hotchkiss, G., Mersinias, V. & Smith, C. P. (2003). Negative feedback regulation of dnaK, clpB and lon expression by the DnaK chaperone machine in Streptomyces coelicolor, identified by transcriptome and in vivo DnaK-depletion analysis. Mol Microbiol 50, 153-166.
10. Buchmeier, N. & Fahey, R. C. (2006). The mshA gene encoding the glycosyltransferase of mycothiol biosynthesis is essential in Mycobacterium tuberculosis Erdman. FEMS Microbiol Lett 264, 74-79.
11. Buchmeier, N. A., Newton, G. L. & Fahey, R. C. (2006). A mycothiol synthase mutant of Mycobacterium tuberculosis has an altered thioldisulfide content and limited tolerance to stress. J Bacteriol 188, 6245-6252.
12. Buttner, M. J., Smith, A. M. & Bibb, M. J. (1988). At least three different RNA polymerase holoenzymes direct transcription of the agarase gene (dagA) of Streptomyces coelicolor A3(2). Cell 52, 599-607.
13. de Crecy-Lagard, V., Servant-Moisson, P., Viala, J., Grandvalet, C. & Mazodier, P. (1999). Alteration of the synthesis of the Clp ATP-dependent protease affects morphological and physiological differentiation in Streptomyces. Mol Microbiol 32, 505-517.
14. Engels, S., Schweitzer, J. E., Ludwig, C., Bott, M. & Schaffer, S. (2004). clpC and clpP1P2 gene expression in Corynebacterium glutamicum is controlled by a regulatory network involving the transcriptional regulators ClgR and HspR as well as the ECF sigma factor sH. Mol Microbiol 52, 285-302.
15. Engels, S., Ludwig, C., Schweitzer, J. E., Mack, C., Bott, M. & Schaffer, S. (2005). The transcriptional activator ClgR controls transcription of genes involved in proteolysis and DNA repair in Corynebacterium glutamicum. Mol Microbiol 57, 576-591.
16. Ezraty, B., Aussel, L. & Barras, F. (2005). Methionine sulfoxide reductases in prokaryotes. Biochim Biophys Acta 1703, 221-229.
17. Freeman, M. L., Borrelli, M. J., Syed, K., Senisterra, G., Stafford, D. M. & Lepock, J. R. (1995). Characterization of a signal generated by oxidation of protein thiols that activates the heat shock transcription factor. J Cell Physiol 164, 356-366.
18. Furukawa, Y., Torres, A. S. & O'Halloran, T. V. (2004). Oxygen-induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS. EMBO J 23, 2872-2881.
19. Gallardo-Madueno, R., Leal, J. F., Dorado, G., Holmgren, A., Lopez-Barea, J. & Pueyo, C. (1998). In vivo transcription of nrdAB operon and of grxA and fpg genes is triggered in Escherichia coli lacking both thioredoxin and glutaredoxin 1 or thioredoxin and glutathione, respectively. J Biol Chem 273, 18382-18388.
20. Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D. & Brown, P. O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11, 4241-4257.
21. Goloubinoff, P., Mogk, A., Zvi, A. P., Tomoyasu, T. & Bukau, B. (1999). Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 96, 13732-13737.
22. Grinberg, I., Shteinberg, T., Gorovitz, B., Aharonowitz, Y., Cohen, G. & Borovok, I. (2006). The Streptomyces NrdR transcriptional regulator is a Zn ribbon/ATP cone protein that binds to the promoter regions of class Ia and class II ribonucleotide reductase operons. J Bacteriol 188, 7635-7644.
23. 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. (1999). RsrA, an anti-sigma factor regulated by redox change. EMBO J 18, 4292-4298.
24. Kidd, S. P., Potter, A. J., Apicella, M. A., Jennings, M. P. & McEwan, A. G. (2005). NmlR of Neisseria gonorrhoeae: a novel redox responsive transcription factor from the MerR family. Mol Microbiol 57, 1676-1689.
25. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. A. (2000). Practical Streptomyces Genetics. Norwich: The John Innes Foundation.
26. R in actinomycetes. Mol Microbiol 73, 815-825.
27. Leichert, L. I., Scharf, C. & Hecker, M. (2003). Global characterization of disulfide stress in Bacillus subtilis. J Bacteriol 185, 1967-1975.
28. Li, P. P., Nakanishi, A., Clark, S. W. & Kasamatsu, H. (2002). Formation of transitory intrachain and interchain disulfide bonds accompanies the folding and oligomerization of simian virus 40 Vp1 in the cytoplasm. Proc Natl Acad Sci U S A 99, 1353-1358.
29. Li, W., Bottrill, A. R., Bibb, M. J., Buttner, M. J., Paget, M. S. & Kleanthous, C. (2003). The role of zinc in the disulphide stress-regulated anti-sigma factor RsrA from Streptomyces coelicolor. J Mol Biol 333, 461-472.
30. Luo, S. & Levine, R. L. (2009). Methionine in proteins defends against oxidative stress. FASEB J 23, 464-472.
31. H in Mycobacterium tuberculosis global gene expression. Mol Microbiol 45, 365-374.
32. H. J Bacteriol 191, 3965-3980.
33. Newell, K. V., Thomas, D. P., Brekasis, D. & Paget, M. S. (2006). The RNA polymerase-binding protein RbpA confers basal levels of rifampicin resistance on Streptomyces coelicolor. Mol Microbiol 60, 687-696.
34. Newton, G. L., Av-Gay, Y. & Fahey, R. C. (2000). A novel mycothiol-dependent detoxification pathway in Mycobacteria involving mycothiol S-conjugate amidase. Biochemistry 39, 10739-10746.
35. Newton, G. L., Koledin, T., Gorovitz, B., Rawat, M., Fahey, R. C. & Av-Gay, Y. (2003). The glycosyltransferase gene encoding the enzyme catalyzing the first step of mycothiol biosynthesis (mshA). J Bacteriol 185, 3476-3479.
36. O'Connor, T. J., Kanellis, P. & Nodwell, J. R. (2002). The ramC gene is required for morphogenesis in Streptomyces coelicolor and expressed in a cell type-specific manner under the direct control of RamR. Mol Microbiol 45, 45-57.
37. Owen, G. A., Pascoe, B., Kallifidas, D. & Paget, M. S. (2007). Zinc-responsive regulation of alternative ribosomal protein genes in Streptomyces coelicolor involves Zur and sR. J Bacteriol 189, 4078-4086.
38. Paget, M. S. & Buttner, M. J. (2003). Thiol-based regulatory switches. Annu Rev Genet 37, 91-121.
39. R, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J 17, 5776-5782.
40. Paget, M. S., Bae, J. B., Hahn, M. Y., Li, W., Kleanthous, C., Roe, J. H. & Buttner, M. J. (2001a). Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch. Mol Microbiol 39, 1036-1047.
41. Paget, M. S., Molle, V., Cohen, G., Aharonowitz, Y. & Buttner, M. J. (2001b). Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sR regulon. Mol Microbiol 42, 1007-1020.
42. R in Streptomyces coelicolor. Mol Microbiol 68, 861-870.
43. Porankiewicz, J., Wang, J. & Clarke, A. K. (1999). New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 32, 449-458.
44. Schmidt, R., Bukau, B. & Mogk, A. (2009). Principles of general and regulatory proteolysis by AAA+ proteases in Escherichia coli. Res Microbiol 160, 629-636.
45. Sobczyk, A., Bellier, A., Viala, J. & Mazodier, P. (2002). The lon gene, encoding an ATP-dependent protease, is a novel member of the HAIR/HspR stress-response regulon in actinomycetes. Microbiology 148, 1931-1937. (Pubitemid 34679046)
46. Tomoyasu, T., Mogk, A., Langen, H., Goloubinoff, P. & Bukau, B. (2001). Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40, 397-413.
47. Viala, J. & Mazodier, P. (2003). The ATPase ClpX is conditionally involved in the morphological differentiation of Streptomyces lividans. Mol Genet Genomics 268, 563-569. (Pubitemid 36286500)
48. Viala, J., Rapoport, G. & Mazodier, P. (2000). The clpP multigenic family in Streptomyces lividans: conditional expression of the clpP3 clpP4 operon is controlled by PopR, a novel transcriptional activator. Mol Microbiol 38, 602-612.
49. Vitreschak, A. G., Rodionov, D. A., Mironov, A. A. & Gelfand, M. S. (2002). Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res 30, 3141-3151.
50. Wickner, S., Maurizi, M. R. & Gottesman, S. (1999). Posttranslational quality control: folding, refolding, and degrading proteins. Science 286, 1888-1893. (Pubitemid 129515889)
51. Winkler, W. C., Cohen-Chalamish, S. & Breaker, R. R. (2002). An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci U S A 99, 15908-15913.
52. Winter, J., Linke, K., Jatzek, A. & Jakob, U. (2005). Severe oxidative stress causes inactivation of DnaK and activation of the redox-regulated chaperone Hsp33. Mol Cell 17, 381-392.
53. Zdanowski, K., Doughty, P., Jakimowicz, P., O'Hara, L., Buttner, M. J., Paget, M. S. & Kleanthous, C. (2006). Assignment of the zinc ligands in RsrA, a redox-sensing ZAS protein from Streptomyces coelicolor. Biochemistry 45, 8294-8300.
54. Zhang, Y. & Zuber, P. (2007). Requirement of the zinc-binding domain of ClpX for Spx proteolysis in Bacillus subtilis and effects of disulfide stress on ClpXP activity. J Bacteriol 189, 7669-7680.
55. 32 in vivo. J Biol Chem 280, 17758-17768.