Alkali metals in addition to acidic pH activate the EvgS histidine kinase sensor in Escherichia coli

Journal of Bacteriology

Volumn 196, Issue 17, 2014, Pages 3140-3149

  Eguchi, Yoko ^a   Utsumi, Ryutaro ^a  

^a KINKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALI METAL; BACTERIAL PERIPLASMIC SOLUTE BINDING PROTEIN; BINDING PROTEIN; EVGS HISTIDINE KINASE; LEUCINE; PHOQ HISTIDINE KINAS; POTASSIUM; PROTEIN HISTIDINE KINASE; SODIUM; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EVGA; TRANSCRIPTION FACTOR GADE; TRANSCRIPTION FACTOR YDEO; UNCLASSIFIED DRUG;

ACIDITY; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; CHIMERA; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; PERIPLASM; POTASSIUM; PROTEIN KINASES; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SODIUM;

EID: 84905457460     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01742-14     Document Type: Article

References (41)

1. Gotoh Y, Eguchi Y, Watanabe T, Okamoto S, Doi A, Utsumi R. 2010. Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr. Opin. Microbiol. 13:232-239. http://dx.doi.org/10.1016/j.mib.2010.01.008.
2. Foster JW. 2004. Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2:898-907. http://dx.doi.org/10.1038/nrmicro1021.
3. Smith DK, Kassam T, Singh B, Elliott JF. 1992. Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci. J. Bacteriol. 174:5820-5826.
4. Hersh BM, Farooq FT, Barstad DN, Blankenshorn DL, Slonczewski JL. A glutamate-dependent acid resistance gene in Escherichia coli. J. Bacteriol. 178:3978-3981.
5. Castanie-Cornet MP, Penfound TA, Smith D, Elliot JF, Foster JW. Control of acid resistance in Escherichia coli. J. Bacteriol. 181:3525-3535.
6. Ma Z, Masuda N, Foster JW. 2004. Characterization of EvgAS-YdeOGadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli. J. Bacteriol. 186:7378-7389. http://dx.doi.org/10.1128/JB.186.21.7378-7389.2004.
7. Masuda N, Church GM. 2003. Regulatory network of acid resistance genes in Escherichia coli. Mol. Microbiol. 48:699-712. http://dx.doi.org/10.1046/j.1365-2958.2003.03477.x.
8. Itou J, Eguchi Y, Utsumi R. 2009. Molecular mechanism of transcriptional cascade initiated by the EvgS/EvgA system in Escherichia coli K-12. Biosci. Biotechnol. Biochem. 73:870-878. http://dx.doi.org/10.1271/bbb.80795.
9. Burton NA, Johnson MD, Antczak P, Robinson A, Lund PA. 2010. Novel aspects of the acid response network of E. coli K-12 are revealed by a study of transcriptional dynamics. J. Mol. Biol. 401:726-742. http://dx.doi.org/10.1016/j.jmb.2010.06.054.
10. Eguchi Y, Okada T, Minagawa S, Oshima T, Mori H, Yamamoto K, Ishihama A, Utsumi R. 2004. Signal transduction cascade between EvgA/EvgS and PhoP/PhoQ two-component systems of Escherichia coli. J. Bacteriol. 186:3006-3014. http://dx.doi.org/10.1128/JB.186.10.3006-3014.2004.
11. Eguchi Y, Itou J, Yamane M, Demizu R, Yamato F, Okada A, Mori H, Kato A, Utsumi R. 2007. B1500, a small membrane protein, connects the two-component systems EvgS/EvgA and PhoQ/PhoP in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 104:18712-18717. http://dx.doi.org/10.1073/pnas.0705768104.
12. Eguchi Y, Ishii E, Yamane M, Utsumi R. 2012. The connector SafA interacts with the multi-sensing domain of PhoQ in Escherichia coli. Mol. Microbiol. 85:299-313. http://dx.doi.org/10.1111/j.1365-2958.2012.08114.x.
13. Bougdour A, Cunning C, Baptiste PJ, 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. http://dx.doi.org/10.1111/j.1365-2958.2008.06146.x.
14. Eguchi Y, Ishii E, Hata K, Utsumi R. 2011. Regulation of acid resistance by connectors of two-component signal transduction systems in Escherichia coli. J. Bacteriol. 193:1222-1228. http://dx.doi.org/10.1128/JB.01124-10.
15. Castanié-Cornet MP, Cam K, Bastiat B, Cros A, Bordes P, Gutierrez C. Acid stress response in Escherichia coli: mechanism of regulation of gadA transcription by RcsB and GadE. Nucleic Acids Res. 38:3546-3554. http://dx.doi.org/10.1093/nar/gkq097.
16. Johnson MD, Burton NA, Gutierrez B, Painter K, Lund PA. 2011. RcsB is required for inducible acid resistance in Escherichia coli and acts at gadEdependent and -independent promoters. J. Bacteriol. 193:3653-3656. http://dx.doi.org/10.1128/JB.05040-11.
17. Clarke EJ, Voigt CA. 2011. Characterization of combinatorial patterns generated by multiple two-component sensors in E. coli that respond to many stimuli. Biotechnol. Bioeng. 108:666-675. http://dx.doi.org/10.1002/bit.22966.
18. Perraud AL, Kimmel B, Weiss V, Gross R. 1998. Specificity of the BvgAS and EvgAS phosphorelay is mediated by the C-terminal HPt domains of the sensor proteins. Mol. Microbiol. 27:875-887. http://dx.doi.org/10.1046/j.1365-2958.1998.00716.x.
19. Jacob-Dubuisson F, Wintjens R, Herrou J, Dupré E, Antoine R. BvgS of pathogenic Bordetellae: a paradigm for sensor kinases with Venus flytrap perception domains, p 57-83. In Gross R, Beier D (ed), Two-component systems in bacteria. Caister Academic Press, Norfolk, United Kingdom.
20. Petersen TN, Brunak S, Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
21. Herrou J, Bompard C, Wintjens R, Dupre E, Willery E, Villeret V, Locht C, Antoine R, Jacob-Dubuisson F. 2010. Periplasmic domain of the sensor-kinase BvgS reveals a new paradigm for the Venus flytrap mechanism. Proc. Natl. Acad. Sci. U. S. A. 107:17351-17355. http://dx.doi.org/10.1073/pnas.1006267107.
22. Miller JH. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Plainview, NY.
23. Ellermeier CD, Janakiraman A, Slauch JM. 2002. Construction of targeted single copy lac fusions using lambda Red and FLP-mediated sitespecific recombination in bacteria. Gene 290:153-161. http://dx.doi.org/10.1016/S0378-1119(02)00551-6.
24. Datsenko KA, Wanner BL. 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. http://dx.doi.org/10.1073/pnas.120163297.
25. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
26. Masuda N, Church GM. 2002. Escherichia coli gene expression responsive to levels of the response regulator EvgA. J. Bacteriol. 184:6225-6234. http://dx.doi.org/10.1128/JB.184.22.6225-6234.2002.
27. Kato A, Ohnishi H, Yamamoto K, Furuta E, Tanabe H, Utsumi R. 2000. Transcription of emrKY is regulated by the EvgA-EvgS two-component system in Escherichia coli K-12. Biosci. Biotechnol. Biochem. 64:1203-1209. http://dx.doi.org/10.1271/bbb.64.1203.
28. Eguchi Y, Oshima T, Mori H, Aono R, Yamamoto K, Ishihama A, Utsumi R. 2003. Transcriptional regulation of drug efflux genes by EvgAS, a two-component system in Escherichia coli. Microbiology 149:2819-2828. http://dx.doi.org/10.1099/mic.0.26460-0.
29. Prost LR, Daley ME, Le Sage V, Bader MW, Le Moual H, Klevit RE, Miller SI. 2007. Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol. Cell 26:165-174. http://dx.doi.org/10.1016/j.molcel.2007.03.008.
30. Watson N, Dunyak DS, Rosey EL, Slonczewski JL, Olson ER. 1992. Identification of elements involved in transcriptional regulation of the Escherichia coli cad operon by external pH. J. Bacteriol. 174:530-540.
31. Meng SY, Bennett GN. 1992. Regulation of the Escherichia coli cad operon: location of a site required for acid induction. J. Bacteriol. 174:2670-2678.
32. Tetsch L, Koller C, Haneburger I, Jung K. 2008. The membraneintegrated transcriptional activator CadC of Escherichia coli senses lysine indirectly via the interaction with the lysine permease LysP. Mol. Microbiol. 67:570-583. http://dx.doi.org/10.1111/j.1365-2958.2007.06070.x.
33. Haneburger I, Eichinger A, Skerra A, Jung K. 2011. New insights into the signaling mechanism of the pH-responsive, membrane-integrated transcriptional activator CadC of Escherichia coli. J. Biol. Chem. 286:10681-10689. http://dx.doi.org/10.1074/jbc. M110.196923.
34. Lippa AM, Goulian M. 2009. Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet. 5:e1000788. http://dx.doi.org/10.1371/journal.pgen.1000788.
35. Umemura T, Matsumoto Y, Ohnishi K, Homma M, Kawagishi I. 2002. Sensing of cytoplasmicpHby bacterial chemoreceptors involves the linker region that connects the membrane-spanning and the signal-modulating helices. J. Biol. Chem. 277:1593-1598. http://dx.doi.org/10.1074/jbc. M109930200.
36. Slonczewski JL, Rosen BP, Alger JR, Macnab RM. 1981. pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate. Proc. Natl. Acad. Sci. U. S. A. 78: 6271-6275. http://dx.doi.org/10.1073/pnas.78.10.6271.
37. Wilks JC, Slonczewski JL. 2007. pH of the cytoplasm and periplasm of Escherichia coli: rapid measurement by green fluorescent protein fluorimetry. J. Bacteriol. 189:5601-5607. http://dx.doi.org/10.1128/JB.00615-07.
38. Bock A, Gross R. 2002. The unorthodox histidine kinases BvgS and EvgS are responsive to the oxidation status of a quinone electron carrier. Eur. J. Biochem. 269:3479-3484. http://dx.doi.org/10.1046/j.1432-1033.2002.03029.x.
39. Georgellis D, Kwon O, Lin EC. 2001. Quinones as the redox signal for the arc two-component system of bacteria. Science 292:2314-2316. http://dx.doi.org/10.1126/science.1059361.
40. Malpica R, Franco B, Rodriguez C, Kwon O, Georgellis D. 2004. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc. Natl. Acad. Sci. U. S. A. 101:13318-13323. http://dx.doi.org/10.1073/pnas.0403064101.
41. Alvarez AF, Rodriguez C, Georgellis D. 2013. Ubiquinone and menaquinone electron carriers represent the yin and yang in the redox regulation of the ArcB sensor kinase. J. Bacteriol. 195:3054-3061. http://dx.doi.org/10.1128/JB.00406-13.