Korean Journal of Microbiology (미생물학회지)

The Microbiological Society of Korea (한국미생물학회)
권호 표지
DOI QR코드

DOI QR Code

Implications of Streptomyces coelicolor RraAS1 as an activator of ribonuclease activity of Escherichia coli RNase E

Streptomyces coelicolor RraAS1의 Eschechia coli RNase E의 RNA 분해작용에 대한 활성제로서 기능 암시

  • Heo, Jihune (Department of Life Science, Chung-Ang University) ;
  • Seo, Sojin (Department of Life Science, Chung-Ang University) ;
  • Lee, Boeun (Department of Life Science, Chung-Ang University) ;
  • Yeom, Ji-Hyun (Department of Life Science, Chung-Ang University) ;
  • Lee, Kangseok (Department of Life Science, Chung-Ang University)
  • Received : 2016.08.23
  • Accepted : 2016.08.30
  • Published : 2016.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

RNase E (Rne) is an essential enzyme involved in the processing and degradation of a large portion of RNAs in Escherichia coli. The enzymatic activity of RNase E is controlled by regulators of ribonuclease activity, namely, RraA and RraB. Gram-positive bacterium Streptomyces coelicolor also contains homologs of Rne and RraA, designated as RNase ES (Rns), RraAS1, and RraAS2. In the present study, we investigated the effect of S. coelicolor RraAS1 on the ribonucleolytic activity of RNase E in E. coli. Coexpression of RraAS1 with Rne resulted in the decreased levels of rpsO, ftsZ, and rnhB mRNAs, which are RNase E substrates, and augmented the toxic effect of Rne overexpression on cell growth. These in vivo effects appeared to be induced by the binding of RraAS1 to Rne, as indicated by the results of co-immunoprecipitation analysis. These results suggested that RraAS1 induces ribonucleolytic activity of RNase E in E. coli.

RNase E는 대장균(Escherichia coli)에서 수많은 RNA의 가공 및 분해에 관여하는 필수적인 효소이다. RNase E의 효소 활성은 RraA와 RraB에 의해 조절된다. 그람양성균인 Streptomyces coelicolor는 RNase ES, RraAS1, RraAS2라고 명명되는 RNase E와 RraA의 동족체를 가지고 있다. 이 연구에서는 S. coelicolor 유래의 RraAS1이 E. coli에서 RNase E의 효소활성을 저해하는지 연구하였다. 대장균에서 RraAS1의 발현은 RNase E의 과발현에 의해 감소된 세포생장을 더욱 저하시켰으며, RNase E의 기질인 rpsO, ftsZ, rnhB mRNA의 양을 감소시키는 것을 확인 하였다. 이러한 RraAS1의 효과는 공동면역침전실험을 수행한 결과에서 유추할 수 있듯이, Rne 단백질과 RraAS1의 결합으로 유도되는 것으로 보인다. 이러한 결과는 RraAS1이 대장균에서 RNase E의 리보핵산 가수분해 활성을 유도함을 시사한다.

Keywords

References

  1. Ahn, S., Shin, E., Yeom, J.H., and Lee, K. 2008. Modulation of Escherichia coli RNase E action by RraAS2, a Streptomyces coelicolor ortholog of RraA. Korean J. Microbiol. 44, 93-97.
  2. Callaghan, A.J., Aurikko, J.P., Ilag, L.L., Gunter Grossmann, J., Chandran, V., Kuhnel, K., Poljak, L., Carpousis, A.J., Robinson, C.V., Symmons, M.F., et al. 2004. Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J. Mol. Biol. 340, 965-979. https://doi.org/10.1016/j.jmb.2004.05.046
  3. Gao, J., Lee, K., Zhao, M., Qiu, J., Zhan, X., Saxena, A., Moore, C.J., Cohen, S.N., and Georgiou, G. 2006. Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol. Microbiol. 61, 394-406. https://doi.org/10.1111/j.1365-2958.2006.05246.x
  4. Ghora, B.K. and Apirion, D. 1978. Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell 15, 1055-1066. https://doi.org/10.1016/0092-8674(78)90289-1
  5. Gorna, M.W., Pietras, Z., Tsai, Y.C., Callaghan, A.J., Hernandez, H., Robinson, C.V., and Luisi, B.F. 2010. The regulatory protein RraA modulates RNA-binding and helicase activities of the E. coli RNA degradosome. RNA 16, 553-562. https://doi.org/10.1261/rna.1858010
  6. Hagege, J.M. and Cohen, S.N. 1997. A developmentally regulated Streptomyces endoribonuclease resembles ribonuclease E of Escherichia coli. Mol. Microbiol. 25, 1077-1090. https://doi.org/10.1046/j.1365-2958.1997.5311904.x
  7. Jain, C. and Belasco, J.G. 1995. RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev. 9, 84-96. https://doi.org/10.1101/gad.9.1.84
  8. Kido, M., Yamanaka, K., Mitani, T., Niki, H., Ogura, T., and Hiraga, S. 1996. RNase E polypeptides lacking a carboxyl-terminal half suppress a mukB mutation in Escherichia coli. J. Bacteriol. 178, 3917-3925. https://doi.org/10.1128/jb.178.13.3917-3925.1996
  9. Kim, J.M., Song, W.S., Kim, H.L., Go, H., and Lee, K. 2007. Identification and functional analysis of proteins interacting with Streptomyces coelicolor RNase ES. Korean J. Microbiol. 43, 72-75.
  10. Lee, K., Bernstein, J.A., and Cohen, S.N. 2002. RNase G complementation of rne null mutation identifies functional interrelationships with RNase E in Escherichia coli. Mol. Microbiol. 43, 1445-1456. https://doi.org/10.1046/j.1365-2958.2002.02848.x
  11. 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. https://doi.org/10.1046/j.1365-2958.2003.03435.x
  12. Lee, M., Yeom, J.H., Sim, S.H., Ahn, S., and Lee, K. 2009. Effects of Escherichia coli RraA orthologs of Vibrio vulnificus on the ribonucleolytic activity of RNase E in vivo. Curr. Microbiol. 58, 349-353. https://doi.org/10.1007/s00284-009-9360-8
  13. Lee, K., Zhan, X., Gao, J., Qiu, J., Feng, Y., Meganathan, R., Cohen, S.N., and Georgiou, G. 2003. RraA. a protein inhibitor of RNase E activity that globally modulates RNA abundance in E. coli. Cell 114, 623-634. https://doi.org/10.1016/j.cell.2003.08.003
  14. Mudd, E.A. and Higgins, C.F. 1993. Escherichia coli endoribonuclease RNase E: autoregulation of expression and site-specific cleavage of mRNA. Mol. Microbiol. 9, 557-568. https://doi.org/10.1111/j.1365-2958.1993.tb01716.x
  15. Pietras, Z., Hardwick, S.W., Swiezewski, S., and Luisi, B.F. 2013. Potential regulatory interactions of Escherichia coli RraA protein with DEAD-box helicases. J. Biol. Chem. 288, 31919-31929. https://doi.org/10.1074/jbc.M113.502146
  16. Sim, S.H., Yeom, J.H., Shin, C., Song, W.S., Shin, E., Kim, H.M., Cha, C.J., Han, S.H., Ha, N.C., Kim, S.W., et al. 2010. Escherichia coli ribonuclease III activity is downregulated by osmotic stress: consequences for the degradation of bdm mRNA in biofilm formation. Mol. Microbiol. 75, 413-425. https://doi.org/10.1111/j.1365-2958.2009.06986.x
  17. Singh, D., Chang, S.J., Lin, P.H., Averina, O.V., Kaberdin, V.R., and Lin-Chao, S. 2009. Regulation of ribonuclease E activity by the L4 ribosomal protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 106, 864-869. https://doi.org/10.1073/pnas.0810205106
  18. Yeom, J.H., Go, H., Shin, E., Kim, H.L., Han, S.H., Moore, C.J., Bae, J., and Lee, K. 2008b. Inhibitory effects of RraA and RraB on RNAse E-related enzymes imply conserved functions in the regulated enzymatic cleavage of RNA. FEMS Microbiol. Lett. 285, 10-15. https://doi.org/10.1111/j.1574-6968.2008.01205.x
  19. Yeom, J.H. and Lee, K. 2006. RraA rescues Escherichia coli cells over-producing RNase E from growth arrest by modulating the ribonucleolytic activity. Biochem. Biophys. Res. Commun. 345, 1372-1376. https://doi.org/10.1016/j.bbrc.2006.05.018
  20. Yeom, J.H., Shin, E., Go, H., Sim, S.H., Seong, M.J., and Lee, K. 2008a. Functional implications of the conserved action of regulators of ribonuclease activity. J. Microbiol. Biotechnol. 18, 1353-1356.

Cited by

  1. RraAS1 inhibits the ribonucleolytic activity of RNase ES by interacting with its catalytic domain in Streptomyces coelicolor vol.55, pp.1, 2017, https://doi.org/10.1007/s12275-017-6518-0
  2. 퇴비사의 효율적인 운영기술에 대한 고찰 vol.23, pp.4, 2017, https://doi.org/10.7464/ksct.2017.23.4.345