Inverse regulation of Fe-And Ni-containing SOD genes by a fur family regulator Nur through small RNA processed from 3′UTR of the sodF mRNA

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 2003-2014

  Kim, Hae Mi ^a   Shin, Jung Ho ^a   Cho, Yoo Bok ^a   Roe, Jung Hye ^a  

^a Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

5' PHOSPHATE SPECIFIC EXONUCLEASE; EXONUCLEASE; FERRIC UPTAKE REGULATOR; IRON SUPEROXIDE DISMUTASE; MESSENGER RNA; NICKEL; NICKEL SUPEROXIDE DISMUTASE; PROTEIN NUR; RNA; SMALL RNA; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; BIOINFORMATICS; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENOME SIZE; HALF LIFE TIME; MESSENGER RNA SYNTHESIS; MESSENGER RNA SYNTHESIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RIBOSOME; RNA PROCESSING; RNA STABILITY; SODF GENE; SODN GENE; STREPTOMYCES COELICOLOR; TRANSCRIPTION TERMINATION;

3' UNTRANSLATED REGIONS; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; STREPTOMYCES COELICOLOR; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS;

EID: 84896716623     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1071     Document Type: Article

References (58)

1. Fridovich, I. (1997) Superoxide anion radical (O2-.), superoxide dismutases, and related matters. J. Biol. Chem., 272, 18515-18517.
2. Perry, J.J., Shin, D.S., Getzoff, E.D. and Tainer, J.A. (2010) The structural biochemistry of the superoxide dismutases. Biochim. Biophys. Acta, 1804, 245-262.
3. Miller, A.F. (2004) Superoxide dismutases: active sites that save, but a protein that kills. Curr. Opin. Chem. Biol., 8, 162-168.
4. Miller, A.F. (2012) Superoxide dismutases: ancient enzymes and new insights. FEBS Lett., 586, 585-595.
5. Storz, G. and Imlay, J.A. (1999) Oxidative stress. Curr. Opin. Microbiol., 2, 188-194.
6. Gort, A.S., Ferber, D.M. and Imlay, J.A. (1999) The regulation and role of the periplasmic copper, zinc superoxide dismutase of Escherichia coli. Mol. Microbiol., 32, 179-191.
7. Hassan, H.M. and Schrum, L.W. (1994) Roles of manganese and iron in the regulation of the biosynthesis of manganesesuperoxide dismutase in Escherichia coli. FEMS Microbiol. Rev., 14, 315-323.
8. Dubrac, S. and Touati, D. (2000) Fur positive regulation of iron superoxide dismutase in Escherichia coli: functional analysis of the sodB promoter. J. Bacteriol., 182, 3802-3808.
9. Masse, E. and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl Acad. Sci. USA, 99, 4620-4625.
10. Tardat, B. and Touati, D. (1991) Two global regulators repress the anaerobic expression of MnSOD in Escherichia coli::Fur (ferric uptake regulation) and Arc (aerobic respiration control). Mol. Microbiol., 5, 455-465.
11. Hassett, D.J., Howell, M.L., Ochsner, U.A., Vasil, M.L., Johnson, Z. and Dean, G.E. (1997) An operon containing fumC and sodA encoding fumarase C and manganese superoxide dismutase is controlled by the ferric uptake regulator in Pseudomonas aeruginosa: fur mutants produce elevated alginate levels. J. Bacteriol., 179, 1452-1459.
12. Polack, B., Dacheux, D., Delic-Attree, I., Toussaint, B. and Vignais, P.M. (1996) The Pseudomonas aeruginosa fumc and soda genes belong to an iron-responsive operon. Biochem. Biophys. Res. Commun., 226, 555-560.
13. Wilderman, P.J., Sowa, N.A., FitzGerald, D.J., FitzGerald, P.C., Gottesman, S., Ochsner, U.A. and Vasil, M.L. (2004) Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc. Natl Acad. Sci. USA, 101, 9792-9797.
14. Gaballa, A., Antelmann, H., Aguilar, C., Khakh, S.K., Song, K.B., Smaldone, G.T. and Helmann, J.D. (2008) The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc. Natl Acad. Sci. USA, 105, 11927-11932.
15. Youn, H.D., Kim, E.J., Roe, J.H., Hah, Y.C. and Kang, S.O. (1996) A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem. J., 318(Pt 3), 889-896.
16. Dupont, C.L., Neupane, K., Shearer, J. and Palenik, B. (2008) Diversity, function and evolution of genes coding for putative Nicontaining superoxide dismutases. Environ. Microbiol., 10, 1831-1843.
17. Schmidt, A., Gube, M. and Kothe, E. (2009) In silico analysis of nickel containing superoxide dismutase evolution and regulation. J. Basic Microbiol., 49, 109-118.
18. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I.M., Barbe, V., Duprat, S., Galperin, M.Y., Koonin, E.V., Le Gall, F. et al. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Natl Acad. Sci. USA, 100, 10020-10025.
19. Palenik, B., Brahamsha, B., Larimer, F.W., Land, M., Hauser, L., Chain, P., Lamerdin, J., Regala, W., Allen, E.E., McCarren, J. et al. (2003) The genome of a motile marine Synechococcus. Nature, 424, 1037-1042.
20. Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., Arellano, A., Coleman, M., Hauser, L., Hess, W.R. et al. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424, 1042-1047.
21. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., Nelson, W. et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304, 66-74.
22. Eitinger, T. (2004) In vivo production of active nickel superoxide dismutase from Prochlorococcus marinus MIT9313 is dependent on its cognate peptidase. J. Bacteriol., 186, 7821-7825.
23. Barondeau, D.P., Kassmann, C.J., Bruns, C.K., Tainer, J.A. and Getzoff, E.D. (2004) Nickel superoxide dismutase structure and mechanism. Biochemistry, 43, 8038-8047.
24. Wuerges, J., Lee, J.W., Yim, Y.I., Yim, H.S., Kang, S.O. and Djinovic Carugo, K. (2004) Crystal structure of nickel-containing superoxide dismutase reveals another type of active site. Proc. Natl Acad. Sci. USA, 101, 8569-8574.
25. Priya, B., Premanandh, J., Dhanalakshmi, R.T., Seethalakshmi, T., Uma, L., Prabaharan, D. and Subramanian, G. (2007) Comparative analysis of cyanobacterial superoxide dismutases to discriminate canonical forms. BMC Genomics, 8, 435.
26. Kim, E.J., Chung, H.J., Suh, B., Hah, Y.C. and Roe, J.H. (1998) Expression and regulation of the sodF gene encoding iron-And zinc-containing superoxide dismutase in Streptomyces coelicolor Muller. J. Bacteriol., 180, 2014-2020.
27. Kim, E.J., Chung, H.J., Suh, B., Hah, Y.C. and Roe, J.H. (1998) Transcriptional and post-transcriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Muller. Mol. Microbiol., 27, 187-195.
28. Ahn, B.E., Cha, J., Lee, E.J., Han, A.R., Thompson, C.J. and Roe, J.H. (2006) Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor. Mol. Microbiol., 59, 1848-1858.
29. An, Y.J., Ahn, B.E., Han, A.R., Kim, H.M., Chung, K.M., Shin, J.H., Cho, Y.B., Roe, J.H. and Cha, S.S. (2009) Structural basis for the specialization of Nur, a nickel-specific Fur homolog, in metal sensing and DNA recognition. Nucleic Acids Res., 37, 3442-3451.
30. Chung, H.J., Choi, J.H., Kim, E.J., Cho, Y.H. and Roe, J.H. (1999) Negative regulation of the gene for Fe-containing superoxide dismutase by an Ni-responsive factor in Streptomyces coelicolor. J. Bacteriol., 181, 7381-7384.
31. Chao, Y., Papenfort, K., Reinhardt, R., Sharma, C.M. and Vogel, J. (2012) An atlas of Hfq-bound transcripts reveals 30 UTRs as a genomic reservoir of regulatory small RNAs. EMBO J., 31, 4005-4019.
32. Kroger, C., Dillon, S.C., Cameron, A.D., Papenfort, K., Sivasankaran, S.K., Hokamp, K., Chao, Y., Sittka, A., Hebrard, M., Handler, K. et al. (2012) The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc. Natl Acad. Sci. USA, 109, E1277-E1286.
33. Kieser, T. (2000) Practical Streptomyces Genetics. John Innes Foundation, Norwich.
34. Han, A.-R. (2007), MS thesis. Graduate School, Seoul National University, Seoul.
35. Chung, H.J., Kim, E.J., Suh, B., Choi, J.H. and Roe, J.H. (1999) Duplicate genes for Fe-containing superoxide dismutase in Streptomyces coelicolor A3(2). Gene, 231, 87-93.
36. Bibb, M.J., Janssen, G.R. and Ward, J.M. (1985) Cloning and analysis of the promoter region of the erythromycin resistance gene (ermE) of Streptomyces erythraeus. Gene, 38, 215-226.
37. Kim, M.S., Hahn, M.Y., Cho, Y., Cho, S.N. and Roe, J.H. (2009) Positive and negative feedback regulatory loops of thiol-oxidative stress response mediated by an unstable isoform of sigmaR in actinomycetes. Mol. Microbiol., 73, 815-825.
38. Swiercz, J.P., Hindra., Bobek, J., Haiser, H.J., Di Berardo, C., Tjaden, B. and Elliot, M.A. (2008) Small non-coding RNAs in Streptomyces coelicolor. Nucleic Acids Res., 36, 7240-7251.
39. Celesnik, H., Deana, A. and Belasco, J.G. (2008) PABLO analysis of RNA: 50-phosphorylation state and 50-end mapping. Methods Enzymol., 447, 83-98.
40. Mitra, A., Angamuthu, K., Jayashree, H.V. and Nagaraja, V. (2009) Occurrence, divergence and evolution of intrinsic terminators across eubacteria. Genomics, 94, 110-116.
41. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
42. Waters, L.S. and Storz, G. (2009) Regulatory RNAs in bacteria. Cell, 136, 615-628.
43. Storz, G., Vogel, J. and Wassarman, K.M. (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell, 43, 880-891.
44. Sun, X., Zhulin, I. and Wartell, R.M. (2002) Predicted structure and phyletic distribution of the RNA-binding protein Hfq. Nucleic Acids Res., 30, 3662-3671.
45. Panek, J., Bobek, J., Mikulik, K., Basler, M. and Vohradsky, J. (2008) Biocomputational prediction of small non-coding RNAs in Streptomyces. BMC Genomics, 9, 217.
46. Vockenhuber, M.P., Sharma, C.M., Statt, M.G., Schmidt, D., Xu, Z., Dietrich, S., Liesegang, H., Mathews, D.H. and Suess, B. (2011) Deep sequencing-based identification of small non-coding RNAs in Streptomyces coelicolor. RNA Biol., 8, 468-477.
47. Tezuka, T., Hara, H., Ohnishi, Y. and Horinouchi, S. (2009) Identification and gene disruption of small noncoding RNAs in Streptomyces griseus. J. Bacteriol., 191, 4896-4904.
48. Moody, M.J., Young, R.A., Jones, S.E. and Elliot, M.A. (2013) Comparative analysis of non-coding RNAs in the antibioticproducing Streptomyces bacteria. BMC Genomics, 14, 558.
49. Vockenhuber, M.P. and Suess, B. (2012) Streptomyces coelicolor sRNA scr5239 inhibits agarase expression by direct base pairing to the dagA coding region. Microbiology, 158, 424-435.
50. Sharma, C.M. and Vogel, J. (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr. Opin. Microbiol., 12, 536-546.
51. Davis, B.M. and Waldor, M.K. (2007) RNase E-dependent processing stabilizes MicX, a Vibrio cholerae sRNA. Mol. Microbiol., 65, 373-385.
52. Papenfort, K., Said, N., Welsink, T., Lucchini, S., Hinton, J.C. and Vogel, J. (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol. Microbiol., 74, 139-158.
53. Price, B., Adamidis, T., Kong, R. and Champness, W. (1999) A Streptomyces coelicolor antibiotic regulatory gene, absB, encodes an RNase III homolog. J. Bacteriol., 181, 6142-6151.
54. Lee, K. and Cohen, S.N. (2003) A Streptomyces coelicolor functional orthologue of Escherichia coli RNase E shows shuffling of catalytic and PNPase-binding domains. Mol. Microbiol., 48, 349-360.
55. Stoof, J., Breijer, S., Pot, R.G.J., van der Neut, D., Kuipers, E.J., Kusters, J.G. and van Vliet, A.H.M. (2008) Inverse nickelresponsive regulation of two urease enzymes in the gastric pathogenHelicobacter mustelae. Environ. Microbiol., 10, 2586-2597.
56. Stoof, J., Kuipers, E.J. and van Vliet, A.H. (2010) Characterization of NikR-responsive promoters of urease and metal transport genes of Helicobacter mustelae. Biometals, 23, 145-159.
57. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
58. Rice, P., Longden, I. and Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet., 16, 276-277.