Antagonistic regulation of dgkA and plsB genes of phospholipid synthesis by multiple stress responses in Escherichia coli

Molecular Microbiology

Volumn 80, Issue 5, 2011, Pages 1260-1275

  Wahl, Astrid ^a   My, Laetitia ^a   Dumoulin, Romain ^a   Sturgis, James N ^a,b   Bouveret, Emmanuelle ^a  

^a CNRS   (France)

^b UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DIACYLGLYCEROL KINASE; GLYCEROL 3 PHOSPHATE ACYLTRANSFERASE; PROTEIN BASR; PROTEIN DGKA; PROTEIN PLSB; PROTEIN RPOE; RNA POLYMERASE; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE LOCUS; GENETIC REGULATION; LIPOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STRESS;

ACETYLTRANSFERASES; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCEROL-3-PHOSPHATE O-ACYLTRANSFERASE; PHOSPHOLIPIDS; SIGMA FACTOR; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 79957532899     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07641.x     Document Type: Article

References (59)

1. 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.
2. Al-Khodor, S., Kalachikov, S., Morozova, I., Price, C.T., and Abu Kwaik, Y. (2009) The PmrA/PmrB two-component system of Legionella pneumophila is a global regulator required for intracellular replication within macrophages and protozoa. Infect Immun 77: 374-386.
3. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
4. Bachmann, B.J. (1996) Derivations and genotypes of some mutant derivates of E. coli K-12. In Escerichia coli and Salmonella: Cellular and Molecular Biology. Neidhart, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., and Magasanik, B., etal. (eds). Washington, DC: American Society for Microbiology, pp. 2460-2488.
5. Badola, P., and Sanders, C.R.N. (1997) Escherichia coli diacylglycerol kinase is an evolutionarily optimized membrane enzyme and catalyzes direct phosphoryl transfer. J Biol Chem 272: 24176-24182.
6. Baracchini, E., and Bremer, H. (1988) Stringent and growth control of rRNA synthesis in Escherichia coli are both mediated by ppGpp. J Biol Chem 263: 2597-2602.
7. Cherepanov, P.P., and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14.
8. Coornaert, A., Lu, A., Mandin, P., Springer, M., Gottesman, S., and Guillier, M. (2010) MicA sRNA links the PhoP regulon to cell envelope stress. Mol Microbiol 76: 467-479.
9. Costanzo, A., and Ades, S.E. (2006) Growth phase-dependent regulation of the extracytoplasmic stress factor, sigmaE, by guanosine 3', 5'-bispyrophosphate (ppGpp). J Bacteriol 188: 4627-4634.
10. Costanzo, A., Nicoloff, H., Barchinger, S.E., Banta, A.B., Gourse, R.L., and Ades, S.E. (2008) ppGpp and DksA likely regulate the activity of the extracytoplasmic stress factor sigma(E) in Escherichia coli by both direct and indirect mechanisms. Mol Microbiol 67: 619-632.
11. Cronan, J.E. (2003) Bacterial membrane lipids: where do we stand? Annu Rev Microbiol 57: 203-224.
12. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
13. Durfee, T., Hansen, A.M., Zhi, H., Blattner, F.R., and Jin, D.J. (2008) Transcription profiling of the stringent response in Escherichia coli. J Bacteriol 190: 1084-1096.
14. Eichel, J., Chang, Y.Y., Riesenberg, D., and Cronan, J.E.J. (1999) Effect of ppGpp on Escherichia coli cyclopropane fatty acid synthesis is mediated through the RpoS sigma factor (sigmaS). J Bacteriol 181: 572-576.
15. Fernandez, L., Gooderham, W.J., Bains, M., McPhee, J.B., Wiegand, I., and Hancock, R.E. (2010) Adaptive resistance to the 'last hope' antibiotics polymyxin B and colistin in Pseudomonas aeruginosa is mediated by the novel two-component regulatory system ParR-ParS. Antimicrob Agents Chemother 54: 3372-3382.
16. Figueroa-Bossi, N., Lemire, S., Maloriol, D., Balbontin, R., Casadesus, J., and Bossi, L. (2006) Loss of Hfq activates the sigmaE-dependent envelope stress response in Salmonella enterica. Mol Microbiol 62: 838-852.
17. Froelich, J.M., Tran, K., and Wall, D. (2006) A pmrA constitutive mutant sensitizes Escherichia coli to deoxycholic acid. J Bacteriol 188: 1180-1183.
18. Fujita, Y., Matsuoka, H., and Hirooka, K. (2007) Regulation of fatty acid metabolism in bacteria. Mol Microbiol 66: 829-839.
19. Gordon, L., Chervonenkis, A.Y., Gammerman, A.J., Shahmuradov, I.A., and Solovyev, V.V. (2003) Sequence alignment kernel for recognition of promoter regions. Bioinformatics 19: 1964-1971.
20. Gully, D., Moinier, D., Loiseau, L., and Bouveret, E. (2003) New partners of acyl carrier protein detected in Escherichia coli by tandem affinity purification. FEBS Lett 548: 90-96.
21. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
22. Hagiwara, D., Yamashino, T., and Mizuno, T. (2004) A Genome-wide view of the Escherichia coli BasS-BasR two-component system implicated in iron-responses. Biosci Biotechnol Biochem 68: 1758-1767.
23. Heath, R.J., Jackowski, S., and Rock, C.O. (1994) Guanosine tetraphosphate inhibition of fatty acid and phospholipid synthesis in Escherichia coli is relieved by overexpression of glycerol-3-phosphate acyltransferase (plsB). J Biol Chem 269: 26584-26590.
24. Hernandez, V.J., and Bremer, H. (1990) Guanosine tetraphosphate (ppGpp) dependence of the growth rate control of rrnB P1 promoter activity in Escherichia coli. J Biol Chem 265: 11605-11614.
25. Jensen, L.J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., etal. (2009) STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 37: D412-D416.
26. Kivistik, P.A., Kivi, R., Kivisaar, M., and Horak, R. (2009) Identification of ColR binding consensus and prediction of regulon of ColRS two-component system. BMC Mol Biol 10: 46.
27. Kox, L.F., Wosten, M.M., and Groisman, E.A. (2000) A small protein that mediates the activation of a two-component system by another two-component system. EMBO J 19: 1861-1872.
28. Lee, H., Hsu, F.F., Turk, J., and Groisman, E.A. (2004) The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J Bacteriol 186: 4124-4133.
29. Link, A.J., Phillips, D., and Church, G.M. (1997) Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 179: 6228-6237.
30. Lu, Y.J., Zhang, Y.M., Grimes, K.D., Qi, J., Lee, R.E., and Rock, C.O. (2006) Acyl-phosphates initiate membrane phospholipid synthesis in Gram-positive pathogens. Mol Cell 23: 765-772.
31. Marchal, K., De Keersmaecker, S., Monsieurs, P., van Boxel, N., Lemmens, K., Thijs, G., etal. (2004) In silico identification and experimental validation of PmrAB targets in Salmonella typhimurium by regulatory motif detection. Genome Biol 5: R9.
32. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia Coli and Related Bacteria. Plainview, NY: Cold Spring Harbor Laboratory Press, p. 2 v.
33. Moon, K., and Gottesman, S. (2009) A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 74: 1314-1330.
34. Overgaard, M., Kallipolitis, B., and Valentin-Hansen, P. (2009) Modulating the bacterial surface with small RNAs: a new twist on PhoP/Q-mediated lipopolysaccharide modification. Mol Microbiol 74: 1289-1294.
35. Perez, J.C., and Groisman, E.A. (2009) Evolution of transcriptional regulatory circuits in bacteria. Cell 138: 233-244.
36. Potrykus, K., and Cashel, M. (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62: 35-51.
37. Potrykus, K., Murphy, H., Philippe, N., and Cashel, M. (2010) ppGpp is the major source of growth rate control in E. coli. Environ Microbiol 13: 563-575.
38. Raetz, C.R., and Newman, K.F. (1978) Neutral lipid accumulation in the membranes of Escherichia coli mutants lacking diglyceride kinase. J Biol Chem 253: 3882-3887.
39. Raetz, C.R., Kantor, G.D., Nishijima, M., and Jones, M.L. (1981) Isolation of Escherichia coli mutants with elevated levels of membrane enzymes. A trans-acting mutation controlling diglyceride kinase. J Biol Chem 256: 2109-2112.
40. Raetz, C.R., Reynolds, C.M., Trent, M.S., and Bishop, R.E. (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76: 295-329.
41. Reese, M.G. (2001) Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem 26: 51-56.
42. Reynolds, C.M., Kalb, S.R., Cotter, R.J., and Raetz, C.R. (2005) A phosphoethanolamine transferase specific for the outer 3-deoxy-D-manno-octulosonic acid residue of Escherichia coli lipopolysaccharide. Identification of the eptB gene and Ca2+ hypersensitivity of an eptB deletion mutant. J Biol Chem 280: 21202-21211.
43. Rhodius, V.A., Suh, W.C., Nonaka, G., West, J., and Gross, C.A. (2006) Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 4: e2.
44. Rotering, H., and Raetz, C.R. (1983) Appearance of monoglyceride and triglyceride in the cell envelope of Escherichia coli mutants defective in diglyceride kinase. J Biol Chem 258: 8068-8073.
45. Saha, S.K., Nishijima, S., Matsuzaki, H., Shibuya, I., and Matsumoto, K. (1996) A regulatory mechanism for the balanced synthesis of membrane phospholipid species in Escherichia coli. Biosci Biotechnol Biochem 60: 111-116.
46. Sparrow, C.P., and Raetz, C.R. (1983) A trans-acting regulatory mutation that causes overproduction of phosphatidylserine synthase in Escherichia coli. J Biol Chem 258: 9963-9967.
47. Srivatsan, A., and Wang, J.D. (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11: 100-105.
48. Travers, A.A. (1980) Promoter sequence for stringent control of bacterial ribonucleic acid synthesis. J Bacteriol 141: 973-976.
49. Traxler, M.F., Summers, S.M., Nguyen, H.T., Zacharia, V.M., Hightower, G.A., Smith, J.T., and Conway, T. (2008) The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Mol Microbiol 68: 1128-1148.
50. Walsh, J.P., Loomis, C.R., and Bell, R.M. (1986) Regulation of diacylglycerol kinase biosynthesis in Escherichia coli. A trans-acting dgkR mutation increases transcription of the structural gene. J Biol Chem 261: 11021-11027.
51. Wosten, M.M., and Groisman, E.A. (1999) Molecular characterization of the PmrA regulon. J Biol Chem 274: 27185-27190.
52. Xiao, H., Kalman, M., Ikehara, K., Zemel, S., Glaser, G., and Cashel, M. (1991) Residual guanosine 3', 5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J Biol Chem 266: 5980-5990.
53. Yoshimura, M., Oshima, T., and Ogasawara, N. (2007) Involvement of the YneS/YgiH and PlsX proteins in phospholipid biosynthesis in both Bacillus subtilis and Escherichia coli. BMC Microbiol 7: 69.
54. Zaslaver, A., Bren, A., Ronen, M., Itzkovitz, S., Kikoin, I., Shavit, S., etal. (2006) A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods 3: 623-628.
55. Zaslaver, A., Kaplan, S., Bren, A., Jinich, A., Mayo, A., Dekel, E., etal. (2009) Invariant distribution of promoter activities in Escherichia coli. PLoS Comput Biol 5: e1000545.
56. Zeghouf, M., Li, J., Butland, G., Borkowska, A., Canadien, V., Richards, D., etal. (2004) Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J Proteome Res 3: 463-468.
57. Zhang, Y.M., and Rock, C.O. (2008a) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6: 222-233.
58. Zhang, Y.M., and Rock, C.O. (2008b) Acyltransferases in bacterial glycerophospholipid synthesis. J Lipid Res 49: 1867-1874.
59. Zhu, K., Zhang, Y.M., and Rock, C.O. (2009) Transcriptional regulation of membrane lipid homeostasis in Escherichia coli. J Biol Chem 284: 34880-34888.