DOI QR코드

DOI QR Code

Polyphosphate Kinase Affects Oxidative Stress Response by Modulating cAMP Receptor Protein and rpoS Expression in Salmonella Typhimurium

  • Cheng, Yuanyuan (Hefei National Laboratory for Physical Sciences at Microscale and School of Life Sciences, University of Science and Technology of China) ;
  • Sun, Baolin (Hefei National Laboratory for Physical Sciences at Microscale and School of Life Sciences, University of Science and Technology of China)
  • Published : 2009.12.31

Abstract

Polyphosphate (polyP) plays diverse physiological functions in prokaryotes and eukaryotes, but most of their detailed mechanisms are still obscure. Here, we show that deletion of polyphosphate kinase (PPK), the principal enzyme responsible for synthesis of polyP, resulted in augmented expression of cAMP receptor protein (CRP) and rpoS and lowered $H_2O_2$ sensitivity in Salmonella Typhimurium ATCC14028. The binding of cAMP-CRP complex to rpoS promoter and further stimulation of its transcription were proved through electrophoretic mobility shift assay, lacZ fusion, and exogenous cAMP addition, respectively. The rpoS expression increased in cpdA (cAMP phosphodiesterase coding gene) mutant, further suggesting that cAMP-CRP upregulated rpoS expression. These results demonstrate that PPK affects oxidative stress response by modulating crp and rpoS expression in S. Typhimurium.

Keywords

References

  1. Ahn, K. and A. Kornberg. 1990. Polyphosphate kinase from Escherichia coli. Purification and demonstration of a phosphoenzyme intermediate. J. Biol. Chem. 265: 11734-11739
  2. Akiyama, M., E. Crooke, and A. Kornberg. 1993. An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. J. Biol. Chem. 268: 633-639
  3. Ault-Riche, D., C. D. Fraley, C. M. Tzeng, and A. Kornberg. 1998. Novel assay reveals multiple pathways regulating stressinduced accumulations of inorganic polyphosphate in Escherichia coli. J. Bacteriol. 180: 1841-1847
  4. Botsford, J. L. and J. G. Harman. 1992. Cyclic AMP in prokaryotes. Microbiol. Rev. 56: 100-122
  5. Campoy, S., M. Jara, N. Busquets, A. M. de Rozas, I. Badiola, and J. Barbe. 2002. Intracellular cyclic AMP concentration is decreased in Salmonella Typhimurium fur mutants. Microbiology 148: 1039-1048
  6. Coynault, C., V. Robbe-Saule, and F. Norel. 1996. Virulence and vaccine potential of Salmonella Typhimurium mutants deficient in the expression of the RpoS (sigma S) regulon. Mol. Microbiol. 22: 149-160 https://doi.org/10.1111/j.1365-2958.1996.tb02664.x
  7. Datsenko, K. A. and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97: 6640-6645 https://doi.org/10.1073/pnas.120163297
  8. Fang, F. C., S. J. Libby, N. A. Buchmeier, P. C. Loewen, J. Switala, J. Harwood, and D. G. Guiney. 1992. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc. Natl. Acad. Sci. U.S.A. 89: 11978-11982 https://doi.org/10.1073/pnas.89.24.11978
  9. Giebel, L. B. and R. A. Spritz. 1990. Site-directed mutagenesis using a double-stranded DNA fragment as a PCR primer. Nucleic Acids Res. 18: 4947 https://doi.org/10.1093/nar/18.16.4947
  10. 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
  11. Hirsch, M. and T. Elliott. 2005. Fis regulates transcriptional induction of RpoS in Salmonella enterica. J. Bacteriol. 187: 1568-1580 https://doi.org/10.1128/JB.187.5.1568-1580.2005
  12. Hirsch, M. and T. Elliott. 2002. Role of ppGpp in rpoS stationary-phase regulation in Escherichia coli. J. Bacteriol. 184: 5077-5087 https://doi.org/10.1128/JB.184.18.5077-5087.2002
  13. Ibanez-Ruiz, M., V. Robbe-Saule, D. Hermant, S. Labrude, and F. Norel. 2000. Identification of RpoS (sigma(S))-regulated genes in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182: 5749-5756 https://doi.org/10.1128/JB.182.20.5749-5756.2000
  14. Imamura, R., K. Yamanaka, T. Ogura, S. Hiraga, N. Fujita, A. Ishihama, and H. Niki. 1996. Identification of the cpdA gene encoding cyclic 3',5'-adenosine monophosphate phosphodiesterase in Escherichia coli. J. Biol. Chem. 271: 25423-25429 https://doi.org/10.1074/jbc.271.41.25423
  15. Ivanova, A., C. Miller, G. Glinsky, and A. Eisenstark. 1994. Role of rpoS (katF) in oxyR-independent regulation of hydroperoxidase I in Escherichia coli. Mol. Microbiol. 12: 571-578 https://doi.org/10.1111/j.1365-2958.1994.tb01043.x
  16. Jain, R. and S. Shuman. 2008. Polyphosphatase activity of CthTTM, a bacterial triphosphate tunnel metalloenzyme. J. Biol. Chem. 283: 31047-31057 https://doi.org/10.1074/jbc.M805392200
  17. Kim, H. S., S. M. Kim, H. J. Lee, S. J. Park, and K. H. Lee. 2009. Expression of the cpdA gene, encoding a 3',5'-cyclic AMP (cAMP) phosphodiesterase, is positively regulated by the cAMPcAMP receptor protein complex. J. Bacteriol. 191: 922-930 https://doi.org/10.1128/JB.01350-08
  18. Koop, A. H., M. E. Hartley, and S. Bourgeois. 1987. A lowcopy-number vector utilizing beta-galactosidase for the analysis of gene control elements. Gene 52: 245-256 https://doi.org/10.1016/0378-1119(87)90051-5
  19. Kuroda, A., K. Nomura, R. Ohtomo, J. Kato, T. Ikeda, N. Takiguchi, et al. 2001. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293: 705-708 https://doi.org/10.1126/science.1061315
  20. Lange, R., D. Fischer, and R. Hengge-Aronis. 1995. Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the sigma S subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 177: 4676-4680
  21. Lange, R. and R. Hengge-Aronis. 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
  22. Loewen, P. C., B. Hu, J. Strutinsky, and R. Sparling. 1998. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 44: 707-717 https://doi.org/10.1139/cjm-44-8-707
  23. Loewen, P. C., J. Switala, and B. L. Triggs-Raine. 1985. Catalases HPI and HPII in Escherichia coli are induced independently. Arch. Biochem. Biophys. 243: 144-149 https://doi.org/10.1016/0003-9861(85)90782-9
  24. McCann, M. P., C. D. Fraley, and A. Matin. 1993. The putative sigma factor KatF is regulated posttranscriptionally during carbon starvation. J. Bacteriol. 175: 2143-2149
  25. McInerney, P., T. Mizutani, and T. Shiba. 2006. Inorganic polyphosphate interacts with ribosomes and promotes translation fidelity in vitro and in vivo. Mol. Microbiol. 60: 438-447 https://doi.org/10.1111/j.1365-2958.2006.05103.x
  26. McMeechan, A., M. A. Lovell, T. A. Cogan, K. L. Marston, T. J. Humphrey, and P. A. Barrow. 2007. Inactivation of ppk differentially affects virulence and disrupts ATP homeostasis in Salmonella enterica serovars Typhimurium and Gallinarum. Res. Microbiol. 158: 79-85 https://doi.org/10.1016/j.resmic.2006.10.008
  27. Mika, F. and R. Hengge. 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
  28. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y
  29. Nickerson, C. A. and R. Curtiss, 3rd. 1997. Role of sigma factor RpoS in initial stages of Salmonella Typhimurium infection. Infect. Immun. 65: 1814-1823
  30. Nomura, K., J. Kato, N. Takiguchi, H. Ohtake, and A. Kuroda. 2004. Effects of inorganic polyphosphate on the proteolytic and DNA-binding activities of Lon in Escherichia coli. J. Biol. Chem. 279: 34406-34410 https://doi.org/10.1074/jbc.M404725200
  31. Paesold, G. and M. Krause. 1999. Analysis of rpoS mRNA in Salmonella Dublin: Identification of multiple transcripts with growth-phase-dependent variation in transcript stability. J. Bacteriol. 181: 1264-1268
  32. Rashid, M. H., K. Rumbaugh, L. Passador, D. G. Davies, A. N. Hamood, B. H. Iglewski, and A. Kornberg. 2000. Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 97: 9636-9641 https://doi.org/10.1073/pnas.170283397
  33. Schellhorn, H. E. and H. M. Hassan. 1988. Transcriptional regulation of katE in Escherichia coli K-12. J. Bacteriol. 170: 4286-4292
  34. Shiba, T., K. Tsutsumi, H. Yano, Y. Ihara, A. Kameda, K. Tanaka, et al. 1997. Inorganic polyphosphate and the induction of rpoS expression. Proc. Natl. Acad. Sci. U.S.A. 94: 11210-11215 https://doi.org/10.1073/pnas.94.21.11210
  35. Stumpf, J. D. and P. L. Foster. 2005. Polyphosphate kinase regulates error-prone replication by DNA polymerase IV in Escherichia coli. Mol. Microbiol. 57: 751-761 https://doi.org/10.1111/j.1365-2958.2005.04724.x
  36. Sureka, K., S. Dey, P. Datta, A. K. Singh, A. Dasgupta, S. Rodrigue, et al. 2007. Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria. Mol. Microbiol. 65: 261-276 https://doi.org/10.1111/j.1365-2958.2007.05814.x
  37. Takayanagi, Y., K. Tanaka, and H. Takahashi. 1994. Structure of the 5' upstream region and the regulation of the rpoS gene of Escherichia coli. Mol. Gen. Genet. 243: 525-531 https://doi.org/10.1007/BF00284200
  38. Visick, J. E. and S. Clarke. 1997. RpoS- and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J. Bacteriol. 179: 4158-4163
  39. Weber, H., T. Polen, J. Heuveling, V. F. Wendisch, and R. Hengge. 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
  40. Weichart, D., R. Lange, N. Henneberg, and R. Hengge-Aronis. 1993. Identification and characterization of stationary phaseinducible genes in Escherichia coli. Mol. Microbiol. 10: 407-420 https://doi.org/10.1111/j.1365-2958.1993.tb02672.x

Cited by

  1. Amino Acids Involved in Polyphosphate Synthesis and Its Mobilization Are Distinct in Polyphosphate Kinase-1 from Mycobacterium tuberculosis vol.6, pp.11, 2009, https://doi.org/10.1371/journal.pone.0027398
  2. Response Regulator RssB의 활성 조절 vol.49, pp.3, 2009, https://doi.org/10.7845/kjm.2013.3057
  3. RpoS integrates CRP, Fis, and PhoP signaling pathways to control Salmonella Typhi hlyE expression vol.14, pp.None, 2009, https://doi.org/10.1186/1471-2180-14-139
  4. Expression of a Subset of Heat Stress Induced Genes of Mycobacterium tuberculosis Is Regulated by 3',5'-Cyclic AMP vol.9, pp.2, 2009, https://doi.org/10.1371/journal.pone.0089759
  5. The opposite roles of agdA and glaA on citric acid production in Aspergillus niger vol.100, pp.13, 2009, https://doi.org/10.1007/s00253-016-7324-z
  6. Involvement of C-terminal amino acids of a hyperthermophilic serine racemase in its thermostability vol.22, pp.1, 2009, https://doi.org/10.1007/s00792-017-0980-9
  7. Inorganic Polyphosphate Is Essential for Salmonella Typhimurium Virulence and Survival in Dictyostelium discoideum vol.8, pp.None, 2009, https://doi.org/10.3389/fcimb.2018.00008
  8. Exploration of the effects of a degS mutant on the growth of Vibrio cholerae and the global regulatory function of degS by RNA sequencing vol.7, pp.None, 2009, https://doi.org/10.7717/peerj.7959
  9. Attenuation of Acinetobacter baumannii virulence by inhibition of polyphosphate kinase 1 with repurposed drugs vol.242, pp.None, 2009, https://doi.org/10.1016/j.micres.2020.126627