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Regulation of Activity of the Response Regulator RssB

Response Regulator RssB의 활성 조절

  • Park, Hee Jeong (Department of Microbiology and Immunology, Chosun University School of Dentistry) ;
  • Bang, Iel Soo (Department of Microbiology and Immunology, Chosun University School of Dentistry)
  • 박희정 (조선대학교 치의학전문대학원 미생물학 및 면역학 교실) ;
  • 방일수 (조선대학교 치의학전문대학원 미생물학 및 면역학 교실)
  • Received : 2013.09.04
  • Accepted : 2013.09.23
  • Published : 2013.09.30

Abstract

Against environmental stresses, many bacteria utilize the alternate sigma factor RpoS that induces transcription of the specific set of genes helpful in promoting bacterial survival. Intracellular levels of RpoS are determined mainly by its turnover through proteolysis of ClpXP protease. Delivery of RpoS to ClpXP strictly requires the adaptor protein RssB. The two-component-type response regulator RssB constantly interacts with RpoS, but diverse environmental changes inhibit this interaction through modification of RssB activity, which increases RpoS levels in bacteria. This review discusses and summarizes recent findings on regulatory factors in RssB-RpoS interactions, including IraD, IraM, IraP anti-adaptor proteins of RssB and phosphorylation of N-terminal receiver domain of RssB. New information shows that the coordinated regulation of RssB activity in controlling RpoS turnover confers efficient bacterial defense against stresses.

많은 세균들은 환경적 스트레스에 대항하기 위해 세균 생존에 유용한 특정 유전자들의 전사를 유도하는 대체시그마 인자 RpoS를 활용한다. 세포 내 RpoS 단백질의 농도는 주로 ClpXP 단백질 분해효소의 조절을 통해 결정된다. RpoS를 ClpXP로 전달하기 위해서는 adaptor 단백질 RssB가 반드시 필요하다. Two-component-type response regulator RssB는 RpoS와 지속적으로 상호작용을 하지만, 다양한 환경변화에 의해 RssB-RpoS 상호작용이 억제되어 세균에서 RpoS 양을 증가시킨다. 본 총설에서는 최근까지 연구 된 RssB-RpoS 상호작용에 관여하는 RssB의 anti-adaptor 단백질 IraD, IraM, IraP 등의 조절인자들과 RssB의 N-terminal 수용체 도메인의 인산화에 대해 설명하고 요약하였다. 이러한 RssB의 정교한 활성을 통한 RpoS 분해조절 과정은 외부환경 스트레스로부터 보다 효율적으로 세균을 보호할 수 있다.

Acknowledgement

Supported by : 한국학술진흥재단

References

  1. Barth, M., Marschall, C., Muffler, A., Fischer, D., and Hengge-Aronis, R. 1995. Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of sigma S and many sigma S-dependent genes in Escherichia coli. J. Bacteriol. 177, 3455-3464. https://doi.org/10.1128/jb.177.12.3455-3464.1995
  2. Battesti, A., Tsegaye, Y.M., Packer, D.G., Majdalani, N., and Gottesman, S. 2012. H-NS regulation of IraD and IraM antiadaptors for control of RpoS degradation. J. Bacteriol. 194, 2470-2478. https://doi.org/10.1128/JB.00132-12
  3. Bearson, S.M., Benjamin, W.H., Jr., Swords, W.E., and Foster, J.W. 1996. Acid shock induction of RpoS is mediated by the mouse virulence gene mviA of Salmonella typhimurium. J. Bacteriol. 178, 2572-2579. https://doi.org/10.1128/jb.178.9.2572-2579.1996
  4. Becker, G., Klauck, E., and Hengge-Aronis, R. 1999. Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc. Natl. Acad. Sci. USA 96, 6439-6444. https://doi.org/10.1073/pnas.96.11.6439
  5. Becker, G., Klauck, E., and Hengge-Aronis, R. 2000. The response regulator RssB, a recognition factor for sigmaS proteolysis in Escherichia coli, can act like an anti-sigmaS factor. Mol. Microbiol. 35, 657-666.
  6. Blum, E., Carpousis, A.J., and Higgins, C.F. 1999. Polyadenylation promotes degradation of 3'-structured RNA by the Escherichia coli mRNA degradosome in vitro. J. Biol. Chem. 274, 4009-4016. https://doi.org/10.1074/jbc.274.7.4009
  7. Bouche, S., Klauck, E., Fischer, D., Lucassen, M., Jung, K., and Hengge-Aronis, R. 1998. Regulation of RssB-dependent proteolysis in Escherichia coli: a role for acetyl phosphate in a response regulator-controlled process. Mol. Microbiol. 27, 787-795. https://doi.org/10.1046/j.1365-2958.1998.00725.x
  8. Bougdour, A., Cunning, C., Baptiste, P.J., Elliott, T., and Gottesman, S. 2008. Multiple pathways for regulation of sigmaS (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol. Microbiol. 68, 298-313. https://doi.org/10.1111/j.1365-2958.2008.06146.x
  9. Bougdour, A., Wickner, S., and Gottesman, S. 2006. Modulating RssB activity: IraP, a novel regulator of sigma(S) stability in Escherichia coli. Genes Dev. 20, 884-897. https://doi.org/10.1101/gad.1400306
  10. Carabetta, V.J., Mohanty, B.K., Kushner, S.R., and Silhavy, T.J. 2009. The response regulator SprE (RssB) modulates polyadenylation and mRNA stability in Escherichia coli. J. Bacteriol. 191, 6812-6821. https://doi.org/10.1128/JB.00870-09
  11. Carabetta, V.J., Silhavy, T.J., and Cristea, I.M. 2010. The response regulator SprE (RssB) is required for maintaining poly(A) polymerase I-degradosome association during stationary phase. J. Bacteriol. 192, 3713-3721. https://doi.org/10.1128/JB.00300-10
  12. Cheng, Y. and Sun, B. 2009. Polyphosphate kinase affects oxidative stress response by modulating cAMP receptor protein and rpoS expression in Salmonella typhimurium. J. Microbiol. Biotechnol. 19, 1527-1535. https://doi.org/10.4014/jmb.0903.03030
  13. Dong, T., Kirchhof, M.G., and Schellhorn, H.E. 2008. RpoS regulation of gene expression during exponential growth of Escherichia coli K12. Mol. Genet. Genomics 279, 267-277. https://doi.org/10.1007/s00438-007-0311-4
  14. Eguchi, Y., Ishii, E., Hata, K., and Utsumi, R. 2011. Regulation of acid resistance by connectors of two-component signal transduction systems in Escherichia coli. J. Bacteriol. 193, 1222-1228. https://doi.org/10.1128/JB.01124-10
  15. Gottesman, S. 2004. The small RNA regulators of Escherichia coli: roles and mechanisms. Annu. Rev. Microbiol. 58, 303-328. https://doi.org/10.1146/annurev.micro.58.030603.123841
  16. Gruber, T.M. and Gross, C.A. 2003. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57, 441-466. https://doi.org/10.1146/annurev.micro.57.030502.090913
  17. Heithoff, D.M., Conner, C.P., Hentschel, U., Govantes, F., Hanna, P.C., and Mahan, M.J. 1999. Coordinate intracellular expression of Salmonella genes induced during infection. J. Bacteriol. 181, 799-807.
  18. Hengge, R. 2009. Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res. Microbiol. 160, 667-676. https://doi.org/10.1016/j.resmic.2009.08.014
  19. Hengge-Aronis, R. 1999. Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Curr. Opin. Microbiol. 2, 148-152. https://doi.org/10.1016/S1369-5274(99)80026-5
  20. Hengge-Aronis, R. 2002. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66, 373-395, table of contents. https://doi.org/10.1128/MMBR.66.3.373-395.2002
  21. Ishihama, A. 1997. Adaptation of gene expression in stationary phase bacteria. Curr. Opin. Genet. Dev. 7, 582-588. https://doi.org/10.1016/S0959-437X(97)80003-2
  22. Jenal, U. and Hengge-Aronis, R. 2003. Regulation by proteolysis in bacterial cells. Curr. Opin. Microbiol. 6, 163-172. https://doi.org/10.1016/S1369-5274(03)00029-8
  23. Klauck, E., Lingnau, M., and Hengge-Aronis, R. 2001. Role of the response regulator RssB in sigma recognition and initiation of sigma proteolysis in Escherichia coli. Mol. Microbiol. 40, 1381-1390. https://doi.org/10.1046/j.1365-2958.2001.02482.x
  24. Lange, R. and Hengge-Aronis, R. 1994. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 8, 1600-1612. https://doi.org/10.1101/gad.8.13.1600
  25. Li, Y., Yamazaki, A., Zou, L., Biddle, E., Zeng, Q., Wang, Y., Lin, H., Wang, Q., and Yang, C.H. 2010. ClpXP protease regulates the type III secretion system of Dickeya dadantii 3937 and is essential for the bacterial virulence. Mol. Plant Microbe Interact. 23, 871-878. https://doi.org/10.1094/MPMI-23-7-0871
  26. Lindahl, T., Sedgwick, B., Sekiguchi, M., and Nakabeppu, Y. 1988. Regulation and expression of the adaptive response to alkylating agents. Annu. Rev. Biochem. 57, 133-157. https://doi.org/10.1146/annurev.bi.57.070188.001025
  27. Loewen, P.C. and Hengge-Aronis, R. 1994. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu. Rev. Microbiol. 48, 53-80. https://doi.org/10.1146/annurev.mi.48.100194.000413
  28. Merrikh, H., Ferrazzoli, A.E., Bougdour, A., Olivier-Mason, A., and Lovett, S.T. 2009. A DNA damage response in Escherichia coli involving the alternative sigma factor, RpoS. Proc. Natl. Acad. Sci. USA 106, 611-616. https://doi.org/10.1073/pnas.0803665106
  29. Mika, F. and Hengge, R. 2005. A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. Genes Dev. 19, 2770-2781. https://doi.org/10.1101/gad.353705
  30. Mitrophanov, A.Y. and Groisman, E.A. 2008. Signal integration in bacterial two-component regulatory systems. Genes Dev. 22, 2601-2611. https://doi.org/10.1101/gad.1700308
  31. Mohanty, B.K. and Kushner, S.R. 1999. Analysis of the function of Escherichia coli poly(A) polymerase I in RNA metabolism. Mol. Microbiol. 34, 1094-1108.
  32. Moreno, M., Audia, J.P., Bearson, S.M., Webb, C., and Foster, J.W. 2000. Regulation of sigma S degradation in Salmonella enterica var typhimurium: in vivo interactions between sigma S, the response regulator MviA(RssB) and ClpX. J. Mol. Microbiol. Biotechnol. 2, 245-254.
  33. Muffler, A., Barth, M., Marschall, C., and Hengge-Aronis, R. 1997. Heat shock regulation of sigmaS turnover: a role for DnaK and relationship between stress responses mediated by sigmaS and sigma32 in Escherichia coli. J. Bacteriol. 179, 445-452. https://doi.org/10.1128/jb.179.2.445-452.1997
  34. Muffler, A., Fischer, D., Altuvia, S., Storz, G., and Hengge-Aronis, R. 1996a. The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. EMBO J. 15, 1333-1339.
  35. Muffler, A., Traulsen, D.D., Lange, R., and Hengge-Aronis, R. 1996b. Posttranscriptional osmotic regulation of the sigma(s) subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 178, 1607-1613. https://doi.org/10.1128/jb.178.6.1607-1613.1996
  36. Palonen, E., Lindstrom, M., Karttunen, R., Somervuo, P., and Korkeala, H. 2011. Expression of signal transduction system encoding genes of Yersinia pseudotuberculosis IP32953 at 28 degrees C and 3 degrees C. PLoS One 6, e25063. https://doi.org/10.1371/journal.pone.0025063
  37. Peterson, C.N., Levchenko, I., Rabinowitz, J.D., Baker, T.A., and Silhavy, T.J. 2012. RpoS proteolysis is controlled directly by ATP levels in Escherichia coli. Genes Dev. 26, 548–553. https://doi.org/10.1101/gad.183517.111
  38. Pratt, L.A. and Silhavy, T.J. 1996. The response regulator SprE controls the stability of RpoS. Proc. Natl. Acad. Sci. USA 93, 2488-2492. https://doi.org/10.1073/pnas.93.6.2488
  39. Sledjeski, D.D., Gupta, A., and Gottesman, S. 1996. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J. 15, 3993-4000.
  40. Studemann, A., Noirclerc-Savoye, M., Klauck, E., Becker, G., Schneider, D., and Hengge, R. 2003. Sequential recognition of two distinct sites in sigma(S) by the proteolytic targeting factor RssB and ClpX. EMBO J. 22, 4111–4120. https://doi.org/10.1093/emboj/cdg411
  41. Tu, X., Latifi, T., Bougdour, A., Gottesman, S., and Groisman, E.A. 2006. The PhoP/PhoQ two-component system stabilizes the alternative sigma factor RpoS in Salmonella enterica. Proc. Natl. Acad. Sci. USA 103, 13503-13508. https://doi.org/10.1073/pnas.0606026103
  42. Weber, H., Polen, T., Heuveling, J., Wendisch, V.F., and Hengge, R. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187, 1591-1603. https://doi.org/10.1128/JB.187.5.1591-1603.2005
  43. Williams, R.M., Rimsky, S., and Buc, H. 1996. Probing the structure, function, and interactions of the Escherichia coli H-NS and StpA proteins by using dominant negative derivatives. J. Bacteriol. 178, 4335-4343. https://doi.org/10.1128/jb.178.15.4335-4343.1996
  44. Yamashino, T., Ueguchi, C., and Mizuno, T. 1995. Quantitative control of the stationary phase-specific sigma factor, sigma S, in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J. 14, 594-602.
  45. Zhang, A., Rimsky, S., Reaban, M.E., Buc, H., and Belfort, M. 1996. Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J. 15, 1340-1349.
  46. Zheng, M., Wang, X., Templeton, L.J., Smulski, D.R., LaRossa, R.A., and Storz, G. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183, 4562-4570. https://doi.org/10.1128/JB.183.15.4562-4570.2001
  47. Zhou, Y. and Gottesman, S. 2006. Modes of regulation of RpoS by H-NS. J. Bacteriol. 188, 7022-7025. https://doi.org/10.1128/JB.00687-06
  48. Zhou, Y., Gottesman, S., Hoskins, J.R., Maurizi, M.R., and Wickner, S. 2001. The RssB response regulator directly targets sigma(S) for degradation by ClpXP. Genes Dev. 15, 627-637. https://doi.org/10.1101/gad.864401