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ppGpp mediates the growth phase-dependent regulation of agn43, a phase variable gene, by stimulating its promoter activity.

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  • معلومة اضافية
    • المصدر:
      Publisher: Society for Applied Microbiology and Blackwell Pub Country of Publication: United States NLM ID: 101499207 Publication Model: Print Cited Medium: Internet ISSN: 1758-2229 (Electronic) Linking ISSN: 17582229 NLM ISO Abbreviation: Environ Microbiol Rep Subsets: MEDLINE
    • بيانات النشر:
      Original Publication: [Hoboken, N.J.] : Society for Applied Microbiology and Blackwell Pub., c2009-
    • الموضوع:
    • نبذة مختصرة :
      Antigen 43 (Ag43) is a self-recognizing outer membrane protein of Escherichia coli expressed during intracellular growth and biofilm formation, suggesting a role in infection. The expression of agn43 is under phase variation control, meaning that there are regulatory mechanisms adjusting the percentage of agn43-expressing cells in the population, in addition to mechanisms modulating the transcriptional expression level in each expressing cell. Phenotypic and transcriptional studies indicate that Ag43 expression is induced upon entry into the stationary phase in a ppGpp-dependent and RpoS-independent manner. The use of single-cell approaches and phase variation deficient strains let to conclude that ppGpp stimulates agn43 promoter activity, rather than affecting the percentage of agn43-expressing cells. The data highlight the relevance that promoter activity regulation may have, without any involvement of the phase variation state, in the final Ag43 expression output. The agn43 promoter of the MG1655 strain carries an AT-rich discriminator between positions -10 and +1, which is highly conserved among the agn43 genes present in the different pathotypes of E. coli. Remarkably, the AT-rich discriminator is required for the positive transcriptional control mediated by ppGpp.
      (© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.)
    • Comments:
      Erratum in: Environ Microbiol Rep. 2021 Dec;13(6):958. (PMID: 34811936)
    • References:
      Aberg, A., Fernandez-Vazquez, J., Cabrer-Panes, J.D., Sanchez, A., and Balsalobre, C. (2009) Similar and divergent effects of ppGpp and DksA deficiencies on transcription in Escherichia coli. J Bacteriol 191: 3226-3236.
      Aberg, A., Shingler, V., and Balsalobre, C. (2006) (p)ppGpp regulates type 1 fimbriation of Escherichia coli by modulating the expression of the site-specific recombinase FimB. Mol Microbiol 60: 1520-1533.
      Aberg, A., Shingler, V., and Balsalobre, C. (2008) Regulation of the fimB promoter: a case of differential regulation by ppGpp and DksA in vivo. Mol Microbiol 67: 1223-1241.
      Al-Hasani, K., Rajakumar, K., Bulach, D., Robins-Browne, R., Adler, B., and Sakellaris, H. (2001) Genetic organization of the she pathogenicity Island in Shigella flexneri 2a. Microb Pathog 30: 1-8.
      Anderson, G.G., Palermo, J.J., Schilling, J.D., Roth, R., Heuser, J., and Hultgren, S.J. (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science (80-.) 301: 105-107.
      Beloin, C., Michaelis, K., Lindner, K., Landini, P., Hacker, J., Ghigo, J.M., and Dobrindt, U. (2006) The transcriptional antiterminator RfaH represses biofilm formation in Escherichia coli. J Bacteriol 188: 1316-1331.
      Blomfield, I.C. (2001) The regulation of pap and type 1 fimbriation in Escherichia coli. Adv Microb Physiol 45: 1-49.
      Casadesús, J., and Low, D. (2006) Epigenetic gene regulation in the bacterial world. Microbiol. Mol Biol Rev 70: 830-856.
      Chauhan, A., Sakamoto, C., Ghigo, J.-M., and Beloin, C. (2013) Did I pick the right colony? Pitfalls in the study of regulation of the phase variable antigen 43 adhesin. PLoS One 8: e73568.
      Correnti, J., Munster, V., Chan, T., and Woude, M. (2002) Dam-dependent phase variation of Ag43 in Escherichia coli is altered in a seqA mutant. Mol Microbiol 44: 521-532.
      Diderichsen, B. (1980) flu, a metastable gene controlling surface properties of Escherichia coli. J Bacteriol 141: 858-867.
      Ferenci, T., Zhou, Z., Betteridge, T., Ren, Y., Liu, Y., Feng, L., et al. (2009) Genomic sequencing reveals regulatory mutations and recombinational events in the widely used MC4100 lineage of Escherichia coli K-12. J Bacteriol 191: 4025-4029.
      Fexby, S., Bjarnsholt, T., Jensen, P.O., Roos, V., Hoiby, N., Givskov, M., and Klemm, P. (2007) Biological Trojan horse: antigen 43 provides specific bacterial uptake and survival in human neutrophils. Infect Immun 75: 30-34.
      Gummesson, B., Lovmar, M., and Nyström, T. (2013) A proximal promoter element required for positive transcriptional control by guanosine tetraphosphate and DksA protein during the stringent response. J Biol Chem 288: 21055-21064.
      Haagmans, W., and van der Woude, M. (2000) Phase variation of Ag43 in Escherichia coli: dam-dependent methylation abrogates OxyR binding and OxyR-mediated repression of transcription. Mol Microbiol 35: 877-887.
      Haugen, S.P., Ross, W., Manrique, M., and Gourse, R.L. (2008) Fine structure of the promoter-sigma region 1.2 interaction. Proc Natl Acad Sci U S A 105: 3292-3297.
      Hauryliuk, V., Atkinson, G.C., Murakami, K.S., Tenson, T., and Gerdes, K. (2015) Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol 13: 298-309.
      Henderson, I.R., Meehan, M., and Owen, P. (1997) Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. FEMS Microbiol Lett 149: 115-120.
      Henderson, I.R., and Owen, P. (1999) The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving dam and OxyR. J Bacteriol 181: 2132-2141.
      Herzberg, M., Kaye, I.K., Peti, W., and Wood, T.K. (2006) YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J Bacteriol 188: 587-598.
      Justice, S.S., Hung, C., Theriot, J.A., Fletcher, D.A., Anderson, G.G., Footer, M.J., and Hultgren, S.J. (2004) Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc Natl Acad Sci U S A 101: 1333-1338.
      Kjaergaard, K., Hasman, H., Schembri, M.A., and Klemm, P. (2002) Antigen 43-mediated autotransporter display, a versatile bacterial cell surface presentation system. J Bacteriol 184: 4197-4204.
      Kjaergaard, K., Schembri, M.A., Ramos, C., Molin, S., and Klemm, P. (2000) Antigen 43 facilitates formation of multispecies biofilms. Env Microbiol 2: 695-702.
      Klemm, P., Hjerrild, L., Gjermansen, M., and Schembri, M.A. (2004) Structure-function analysis of the self-recognizing antigen 43 autotransporter protein from Escherichia coli. Mol Microbiol 51: 283-296.
      Landini, P., Egli, T., Wolf, J., and Lacour, S. (2014) sigmaS, a major player in the response to environmental stresses in Escherichia coli: role, regulation and mechanisms of promoter recognition. Environ Microbiol Rep 6: 1-13.
      Lim, H.N., and van Oudenaarden, A. (2007) A multistep epigenetic switch enables the stable inheritance of DNA methylation states. Nat Genet 39: 269-275.
      Magnusson, L.U., Farewell, A., and Nyström, T. (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13: 236-242.
      Magnusson, L.U., Gummesson, B., Joksimovic, P., Farewell, A., and Nystrom, T. (2007) Identical, independent, and opposing roles of ppGpp and DksA in Escherichia coli. J Bacteriol 189: 5193-5202.
      Mechold, U., Potrykus, K., Murphy, H., Murakami, K.S., and Cashel, M. (2013) Differential regulation by ppGpp versus pppGpp in Escherichia coli. Nucleic Acids Res 41: 6175-6189.
      Molodtsov, V., Sineva, E., Zhang, L., Huang, X., Cashel, M., Ades, S.E., and Murakami, K.S. (2018) Allosteric effector ppGpp potentiates the inhibition of transcript initiation by DksA. Mol Cell 69: 828-839.
      Owen, P., Meehan, M., de Loughry-Doherty, H., and Henderson, I. (1996) Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol Med Microbiol 16: 63-76.
      Restieri, C., Garriss, G., Locas, M.C., and Dozois, C.M. (2007) Autotransporter-encoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl Env Microbiol 73: 1553-1562.
      Ross, W., Sanchez-Vazquez, P., Chen, A.Y., Lee, J.-H., Burgos, H.L., and Gourse, R.L. (2016) ppGpp binding to a site at the RNAP-DksA Interface accounts for its dramatic effects on transcription initiation during the stringent response. Mol Cell 62: 811-823.
      Sanchez-Vazquez, P., Dewey, C.N., Kitten, N., Ross, W., and Gourse, R.L. (2019) Genome-wide effects on Escherichia coli transcription from ppGpp binding to its two sites on RNA polymerase. Proc Natl Acad Sci U S A 116: 8310-8319.
      Sarubbi, E., Rudd, K.E., and Cashel, M. (1988) Basal ppGpp level adjustment shown by new spoT mutants affect steady state growth rates and rrnA ribosomal promoter regulation in Escherichia coli. MGG Mol Gen Genet 213: 214-222.
      Schembri, M.A., Hjerrild, L., Gjermansen, M., and Klemm, P. (2003) Differential expression of the Escherichia coli autoaggregation factor antigen 43. J Bacteriol 185: 2236-2242.
      Steinchen, W., and Bange, G. (2016) The magic dance of the alarmones (p)ppGpp. Mol Microbiol 101: 531-544.
      Traxler, M.F., Zacharia, V.M., Marquardt, S., Summers, S.M., Nguyen, H.-T., Stark, S.E., and Conway, T. (2011) Discretely calibrated regulatory loops controlled by ppGpp partition gene induction across the “feast to famine” gradient in Escherichia coli. Mol Microbiol 79: 830-845.
      Ulett, G.C., Valle, J., Beloin, C., Sherlock, O., Ghigo, J.M., and Schembri, M.A. (2007) Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 75: 3233-3244.
      Varik, V., Oliveira, S.R.A., Hauryliuk, V., and Tenson, T. (2017) HPLC-based quantification of bacterial housekeeping nucleotides and alarmone messengers ppGpp and pppGpp. Sci Rep 7: 11022.
      Waldron, D.E., Owen, P., and Dorman, C.J. (2002) Competitive interaction of the OxyR DNA-binding protein and the dam methylase at the antigen 43 gene regulatory region in Escherichia coli. Mol Microbiol 44: 509-520.
      Wallecha, A., Munster, V., Correnti, J., Chan, T., and van der Woude, M. (2002) Dam- and OxyR-dependent phase variation of agn43: essential elements and evidence for a new role of DNA methylation. J Bacteriol 184: 3338-3347.
      Wallecha, A., Oreh, H., van der Woude, M.W., and deHaseth, P.L. (2014) Control of gene expression at a bacterial leader RNA, the agn43 gene encoding outer membrane protein Ag43 of Escherichia coli. J Bacteriol 196: 2728-2735.
      Wang, B., Dai, P., Ding, D., Del Rosario, A., Grant, R.A., Pentelute, B.L., and Laub, M.T. (2019) Affinity-based capture and identification of protein effectors of the growth regulator ppGpp. Nat Chem Biol 15: 141-150.
      van der Woude, M.W. (2011) Phase variation: how to create and coordinate population diversity. Curr Opin Microbiol 14: 205-211.
      van der Woude, M.W., and Henderson, I.R. (2008) Regulation and function of Ag43 (flu). Annu Rev Microbiol 62: 153-169.
      Zhang, Y., Zborníková, E., Rejman, D., and Gerdes, K. (2018) Novel (p)ppGpp binding and metabolizing proteins of Escherichia coli. MBio 9: e02188-e02117.
    • Grant Information:
      International Ministry of Education; International University of Barcelona; 2012/ACUP/00048 International RecerCaixa Program; 2017SGR499 International Catalonian Government; AGL2013-45339-R International Ministry of Economy and Competitiveness; PGC2018-096958-B-I00 International Ministry of Economy and Competitiveness
    • الرقم المعرف:
      0 (Adhesins, Escherichia coli)
      0 (antigen 43, E coli)
      33503-72-9 (Guanosine Tetraphosphate)
    • الموضوع:
      Date Created: 20200618 Date Completed: 20210513 Latest Revision: 20211123
    • الموضوع:
      20221213
    • الرقم المعرف:
      10.1111/1758-2229.12860
    • الرقم المعرف:
      32548953