Roles of cell division control factor SdiA: Recognition of quorum sensing signals and modulation of transcription regulation targets

Genes to Cells

Volumn 19, Issue 5, 2014, Pages 405-418

  Shimada, Tomohiro ^a,b   Shimada, Kaori ^a   Matsui, Makoto ^a   Kitai, Yuichi ^a   Igarashi, Jun ^c   Suga, Hiroaki ^c   Ishihama, Akira ^a  

^a HOSEI UNIVERSITY   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; FLUORESCENT DYE; GENOMIC DNA; N ACYLHOMOSERINE LACTONE; SPACER DNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SDIA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL STRAIN; BINDING AFFINITY; BINDING SITE; CELL COMMUNICATION; CELL DIVISION; DNA BINDING; DNA PROBE; DNA SEQUENCE; ESCHERICHIA COLI; GENOMIC FRAGMENT; NONHUMAN; NORTHERN BLOTTING; OPERON; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; TRANSCRIPTION REGULATION; VIBRIO HARVEYI;

ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

ACYL-BUTYROLACTONES; CELL DIVISION; DNA, BACTERIAL; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; QUORUM SENSING; TRANS-ACTIVATORS;

EID: 84898798578     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/gtc.12139     Document Type: Article

References (69)

1. Ahmer, B.M. (2004) Cell-to-cell signaling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52, 933-945.
2. Ahmer, B.M., Reeuwijk, J.V., Timmers, C.D., Valentine, P.J. & Heffron, F. (1998) Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J. Bacteriol. 180, 1185-1193.
3. Aiba, H., Adhya, S. & de Crombrugghe, B. (1981) Evidence for two functional gal promoters in intact Escherichia coli cells. J. Biol. Chem. 256, 11905-11910.
4. Baba, T., Ara, T., Hasgawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K.A., Tomita, M., Wanner, B.L. & Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 20006.0006.
5. Bassler, B.L. (2002) Small talk: Cell-to-cell communication in bacteria. Cell 109, 421-424.
6. Bougdour, A., Cunning, C., Baptiste, P.J., Elliott, T. & 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.
7. Cao, J.-G. & Meighen, E.A. (1989) Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J. Biol. Chem. 264, 21670-21676.
8. Chu, W., Zere, T.R., Weber, M.M., Wood, T.K., Whiteley, M., Hidalgo-Romano, B., Valenzuela, E. Jr & McLean, R.J.C. (2012) Indole production promoters Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Appl. Environ. Microbiol. 78, 411-419.
9. Chung, J., Goo, E., Yu, S., Choi, O., Lee, J., Kim, J., Kim, H., Igarashi, J., Suuga, H., Moon, J.-S., Hwang, I. & Rhee, S. (2011) Small-molecule inhibitor binding to an N-acyl-homoserine lactone synthase. Proc. Natl Acad. Sci. USA 108, 12089-12094.
10. Dyszel, J.L., Soares, J.A., Swearingen, M.C., Lundsay, A., Smith, J.N. & Ahmer, B.M. (2010) E. coli K-12 and EHEC genes regulated by SdiA. PLoS ONE 5, e8946.
11. Eberhard, A., Brlingame, A.L., Eberhard, C., Kenyon, G.L., Healson, K.H. & Oppenheimer, N.J. (1981) Structural identification of autoinducer Photobacterium fischeri luciferase. Biochemistry 20, 2444-2449.
12. Eberl, L. (1999) N-Acyl homoserinelactone-mediated gene regulation in Gram-negative bacteria. Syst. Appl. Microbiol. 22, 493-506.
13. Ellington, A.D. & Szostak, J.W. (1990) In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818-822.
14. Fuqua, C., Winans, S. & Greenberg, E.P. (1996) Census and consensus in bacterial ecosystems; the LuxR-LuxI family of quorum sensing transcriptional regulators. Annu. Rev. Microbiol. 50, 727-751.
15. Garcia-Lara, J., Shang, L.H. & Rothfield, L.I. (1996) An extracellular factor regulates expression of sdiA, a transcriptional activator of cell division genes in Escherichia coli. J. Bacteriol. 178, 2742-2748.
16. Hale, C.A. & de Boer, P.A. (1997) Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88, 175-185.
17. Hasegawa, A., Ogasawara, H., Kori, A., Teramoto, J. & Ishihama, A. (2008) The transcription regulator AllR senses both allantoin and glyoxylate and controls a set of genes for degradation and reutilization of purines. Microbiology 154, 3366-3378.
18. Houlberg, U. & Jensen, K.F. (1983) Role of hypoxanthine and guanine in regulation of Salmonella typhimurium pur gene expression. J. Bacteriol. 153, 837-845.
19. Hughes, D.T., Terekhova, D.A., Liou, L., Hovde, C.J., Sahl, J.W., Patankar, A.V., Gonzalez, J.E., Edrington, T.S., Rasko, D.A. & Sperandio, V. (2010) Chemical sensing in mammalian host-bacterial commensal associations. Proc. Natl Acad. Sci. USA 107, 9831-9836.
20. Igarashi, J. & Suga, H. (2011) Custom synthesis of autoinducers and their analogs. Methods Mol. Biol. 692, 265-274.
21. Ishihama, A. (2010) Prokaryotic genome regulation: multi-factor promoters, multi-target regulators and hierarchic networks. FEMS Microbiol. Rev. 34, 628-645.
22. Ishihama, A. (2012) Prokaryotic genome regulation: a revolutionary paradigm. Proc. Jpn Acad. Ser. B Phys. Biol. Sci. 88, 485-508.
23. Jenal, U. & Malone, J. (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40, 385-407.
24. Lee, J., Jayaraman, A. & Wood, T.K. (2007) Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7, 42.
25. Lee, J., Maeda, M., Hong, S.H. & Wood, T.K. (2009) Reconfiguring the quorum-sensing regulator SdiA of Escherichia coli to control biofilm formation via indole and N-acylhomoserine lactones. Appl. Environ. Microbiol. 75, 1703-1716.
26. Lorca, G.L., Ezersky, A., Lunin, V.V., Walker, J.R., Altamentova, S., Evdokimova, E., Vedadi, M., Bochkarev, A. & Savchenko, A. (2007) Glyoxylate and pyruvate are antagonistic effectors of the Escherichia coli IclR transcriptional regulator. J. Biol. Chem. 282, 16476-16491.
27. Marbaniang, C.N. & Gowrishankar, J. (2011) Role of ArgP (IciA) in lysine-mediated repression in Escherichia coli. J. Bacteriol. 193, 5985-5996.
28. Michael, B., Smith, J.N., Swift, N., Heffron, F. & Ahmer, B.M. (2001) SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol. 183, 5733-5742.
29. Miethke, M., Hou, J. & Marahiel, M.A. (2011) The siderophore-interacting protein YqjH acts as a ferric reductase in different iron assimilation pathways of Escherichia coli. Biochemistry 50, 10951-10964.
30. Passador, L., Tucker, K.D., Guertin, K.R., Journet, M.P., Kende, A.S. & Iglewski, B.H. (1996) Functional analysis of the Pseudomonas aeruginosa atutoinducer PAI. J. Bacteriol. 178, 5995-6000.
31. Pearson, J.P., Gray, K.M., Passador, L., Tucker, K.D., Eberhard, A., Iglewski, B.H. & Greenberg, E.P. (1994) Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl Acad. Sci. USA 91, 197-201.
32. Pearson, J.P., Passador, L., Igelewski, B.H. & Greenberg, E.P. (1995) A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 92, 1490-1494.
33. Pearson, J.P., Pesci, E.C. & Iglewski, B.H. (1997) Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol. 179, 5756-5767.
34. Pittard, J. (1996) The various strategies within the TyrR regulation of Escherichia coli to modulate gene expression. Genes Cells 1, 717-725.
35. Pratt, L.A. & Silhavy, T.J. (1998) Crl stimulates RpoS activity during stationary phase. Mol. Microbiol. 29, 1225-1236.
36. Rahmati, S., Yang, S., Davidson, A.L. & Zechiedrich, E.L. (2002) Control of the AcrAB multidrug efflux pump by quorum-sensing regulator SdiA. Mol. Microbiol. 43, 677-685.
37. Schaefer, A.L., Hanzelka, B.L., Eberhard, A. & Greenberg, E.P. (1996) Quorum sensing in Vibrio fischeri: probing autoinducer-LuxR interactions with autoinducer analogs. J. Bacteriol. 178, 2897-2901.
38. Schauder, S., Shokat, K., Surette, M.G. & Bassler, B.L. (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41, 463-476.
39. Schreiber, V. & Richet, E. (1999) Self-association of the Escherichia coli transcription activator MalT in the presence of maltotriose and ATP. J. Biol. Chem. 274, 33220-33226.
40. Sharma, V.K., Bearson, S.M.D. & Bearson, B.L. (2010) Evaluation of the effects of sdiA, a luxR homologue, on adherence and motility of Escherichia coli O157:H7. Microbiology 156, 1303-1312.
41. Shimada, K., Ogasawara, H., Yamada, K., Shimura, M., Kori, A., Shimada, T., Yamanaka, Y., Yamamoto, K. & Ishihama, A. (2013) Screening of promoter-specific transcription factors: multiple regulators for the sdiA gene involved in cell division control and quorum sensing. Microbiology 59, 2501-2512.
42. Shimada, T., Bridier, A., Briandet, R. & Ishihama, A. (2011a) Novel roles of LeuO in transcription regulation in E. coli gonome: antagonistic interplay with the universal silencer H-NS. Mol. Microbiol. 82, 378-397.
43. Shimada, T., Fujita, N., Maeda, M. & Ishihama, A. (2005) Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells 10, 907-918.
44. Shimada, T., Fujita, N., Yamamoto, K. & Ishihama, A. (2011b) Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS ONE 6, e20081.
45. Shimada, T., Hirao, K., Kori, A., Yamamoto, K. & Ishihama, A. (2007) RutR is the uracil/thymine-sensing master regulator of a set of genes for synthesis and degradation of pyrimdines. Mol. Microbiol. 66, 744-757.
46. Shimada, T., Ishihama, A., Busby, S.J.W. & Grainger, D.C. (2008) The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res. 36, 3950-3955.
47. Singer, B.S., Shtatland, T., Brown, D. & Gold, L. (1997) Libraries for genomic SELEX. Nucleic Acids Res. 25, 781-786.
48. Sitnikov, D.M., Schineller, J.B. & Moses, R.E. (1996) Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduciton. Proc. Natl Acad. Sci. USA 93, 336-341.
49. Smith, J.N. & Ahmer, B.M. (2003) Detection of other microbial species by Salmonella: expression of the SdiA regulon. J. Bacteriol. 185, 1357-1366.
50. Smith, K., Bu, Y. & Suga, H. (2003a) Library screening for synthetic agonists of Pseudomonas aeruginosa autoinducer. Chem. Biol. 10, 563-571.
51. Smith, K., Bu, Y. & Suga, H. (2003b) Induction and inhibition of Pseudomonas aeruginosa quorum sensing by synthetic autoinducer analogs. Chem. Biol. 10, 81-89.
52. Sperandio, V., Torres, A.G., Jarvis, B., Nataro, J.P. & Kaper, J.B. (2003) Bacteria-host communication: the language of hormones. Proc. Natl Acad. Sci. USA 100, 8951-8956.
53. Studier, F.W. & Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113-130.
54. Tavio, M.M., Aquili, V.D., Poveda, J.B., Antunes, N.T., Sanchez-Cespedes, J. & Vila, J. (2010) Quorum-sensing regulator sdiA and marA overexpression is involved in in vitro-selected multidrug resistance of Escherichia coli. J. Antimicrob. Chemother. 65, 1178-1186.
55. Teramoto, J., Yoshimura, S., Takeyasu, K. & Ishihama, A. (2010) A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions. Nucleic Acids Res. 38, 3605-3618.
56. Tuerk, C. & Gold, L. (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505-510.
57. Van Houdt, R., Aertsen, A., Moons, P., Vanoirbeek, K. & Michiels, C.W. (2006) N-acyl-L-homoserine lactone signal interception by Escherichia coli. FEMS Microbiol. Lett. 256, 83-89.
58. Wang, S., Wu, Y. & Outten, F.W. (2011) Fur and the novel regulator YqiI control transcription of the ferric reductase gene yqjH in Escherichia coli. J. Bacteriol. 193, 563-574.
59. Wang, X.D., de Boer, P.A. & Rothfield, L.I. (1991) A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. EMBO J. 10, 3363-3372.
60. Waters, C.M. & Bassler, B.L. (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319-346.
61. Wei, Y., Lee, J.M., Smulski, D.R. & LaRrossa, R.A. (2001a) Global impact of sdiA amplification revealed by comprehensive gene expression profiling of Escherichia coli. J. Bacteriol. 183, 2265-2272.
62. Wei, Y., Vollmer, A.C. & LaRossa, R.A. (2001b) In vivo titration of mytomycin C action by four Escherichia coli genomic regions on multicopy plasmids. J. Bacteriol. 183, 2259-2264.
63. Weiss, D.S. (2004) Bacterial cell division and the septal ring. Mol. Microbiol. 54, 588-597.
64. Wu, C., Lokanath, N.K., Kim, D.Y., Nguyen, L.D. & Kim, K.K. (2008) Crystallization and preliminary X-ray studies of SdiA from Escherichia coli. Acta Crystallogr. 64, 19-21.
65. Yamamoto, K., Hirao, K., Ohshima, T., Aiba, H., Utsumi, R. & Ishihama, A. (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280, 1448-1456.
66. Yamamoto, K., Yata, K., Fujita, N. & Ishihama, A. (2001) Novel mode of transcription regulation by SdiA, an Escherichia coli homologue of the quorum-sensing regulator. Mol. Microbiol. 41, 1187-1198.
67. Yao, Y., Dickerson, T.J., Hixon, M.S. & Dyson, H.J. (2007) NMR detection of adventitious xylose binding to the quorum-sensing protein SdiA of Escherichia coli. Bioorg. Med. Chem. Lett. 17, 6202-6205.
68. Yao, Y., Martinez-Yamout, M.A., Dickenson, T.J., Brogan, A.P., Wright, P.E. & Dyson, H.J. (2006) Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J. Mol. Biol. 355, 262-273.
69. Zhou, X., Meng, X. & Sun, B. (2008) An EAL domain protein and cyclic AMP contribute to the interaction between the two quorum sensing systems in Escherichia coli. Cell Res. 18, 937-948.