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J Bacteriol. Aug 1997; 179(16): 5126–5130.
PMCID: PMC179371

Growth-phase-dependent expression of cspD, encoding a member of the CspA family in Escherichia coli.


The cspD gene of Escherichia coli encodes a protein of high sequence similarity with the cold shock protein CspA, but cspD expression is not induced by cold shock. In this study, we analyzed the regulation of cspD gene expression. By using a cspD-lacZ fusion and primer extension analysis, the expression of cspD was found to be dramatically induced by stationary-phase growth. However, this induction does not depend on the stationary-phase sigma factor sigmaS. Moreover, the expression of cspD is inversely dependent on growth rates and induced upon glucose starvation. Using a (p)ppGpp-depleted strain, we found that (p)ppGpp is one of the positive factors for the regulation of cspD expression.

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  • Aiba H, Adhya S, de Crombrugghe B. Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem. 1981 Nov 25;256(22):11905–11910. [PubMed]
  • Aldea M, Garrido T, Pla J, Vicente M. Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters. EMBO J. 1990 Nov;9(11):3787–3794. [PMC free article] [PubMed]
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Brandi A, Pietroni P, Gualerzi CO, Pon CL. Post-transcriptional regulation of CspA expression in Escherichia coli. Mol Microbiol. 1996 Jan;19(2):231–240. [PubMed]
  • Dersch P, Schmidt K, Bremer E. Synthesis of the Escherichia coli K-12 nucleoid-associated DNA-binding protein H-NS is subjected to growth-phase control and autoregulation. Mol Microbiol. 1993 May;8(5):875–889. [PubMed]
  • Etchegaray JP, Jones PG, Inouye M. Differential thermoregulation of two highly homologous cold-shock genes, cspA and cspB, of Escherichia coli. Genes Cells. 1996 Feb;1(2):171–178. [PubMed]
  • Fang L, Jiang W, Bae W, Inouye M. Promoter-independent cold-shock induction of cspA and its derepression at 37 degrees C by mRNA stabilization. Mol Microbiol. 1997 Jan;23(2):355–364. [PubMed]
  • Gentry DR, Hernandez VJ, Nguyen LH, Jensen DB, Cashel M. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J Bacteriol. 1993 Dec;175(24):7982–7989. [PMC free article] [PubMed]
  • Goldenberg D, Azar I, Oppenheim AB. Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol Microbiol. 1996 Jan;19(2):241–248. [PubMed]
  • Goldstein J, Pollitt NS, Inouye M. Major cold shock protein of Escherichia coli. Proc Natl Acad Sci U S A. 1990 Jan;87(1):283–287. [PMC free article] [PubMed]
  • Harlocker SL, Rampersaud A, Yang WP, Inouye M. Phenotypic revertant mutations of a new OmpR2 mutant (V203Q) of Escherichia coli lie in the envZ gene, which encodes the OmpR kinase. J Bacteriol. 1993 Apr;175(7):1956–1960. [PMC free article] [PubMed]
  • Higgins CF, Hinton JC, Hulton CS, Owen-Hughes T, Pavitt GD, Seirafi A. Protein H1: a role for chromatin structure in the regulation of bacterial gene expression and virulence? Mol Microbiol. 1990 Dec;4(12):2007–2012. [PubMed]
  • Jiang W, Hou Y, Inouye M. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem. 1997 Jan 3;272(1):196–202. [PubMed]
  • Jones PG, Inouye M. The cold-shock response--a hot topic. Mol Microbiol. 1994 Mar;11(5):811–818. [PubMed]
  • Jones PG, VanBogelen RA, Neidhardt FC. Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol. 1987 May;169(5):2092–2095. [PMC free article] [PubMed]
  • Lee SJ, Xie A, Jiang W, Etchegaray JP, Jones PG, Inouye M. Family of the major cold-shock protein, CspA (CS7.4), of Escherichia coli, whose members show a high sequence similarity with the eukaryotic Y-box binding proteins. Mol Microbiol. 1994 Mar;11(5):833–839. [PubMed]
  • Loewen PC, Hengge-Aronis R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol. 1994;48:53–80. [PubMed]
  • Nakashima K, Kanamaru K, Mizuno T, Horikoshi K. A novel member of the cspA family of genes that is induced by cold shock in Escherichia coli. J Bacteriol. 1996 May;178(10):2994–2997. [PMC free article] [PubMed]
  • Newkirk K, Feng W, Jiang W, Tejero R, Emerson SD, Inouye M, Montelione GT. Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: identification of a binding epitope for DNA. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5114–5118. [PMC free article] [PubMed]
  • Oshima T, Aiba H, Baba T, Fujita K, Hayashi K, Honjo A, Ikemoto K, Inada T, Itoh T, Kajihara M, et al. A 718-kb DNA sequence of the Escherichia coli K-12 genome corresponding to the 12.7-28.0 min region on the linkage map. DNA Res. 1996 Jun 30;3(3):137–155. [PubMed]
  • Ozaki M, Fujita N, Wada A, Ishihama A. Promoter selectivity of the stationary-phase forms of Escherichia coli RNA polymerase and conversion in vitro of the S1 form enzyme into a log-phase enzyme-like form. Nucleic Acids Res. 1992 Jan 25;20(2):257–261. [PMC free article] [PubMed]
  • Ozaki M, Wada A, Fujita N, Ishihama A. Growth phase-dependent modification of RNA polymerase in Escherichia coli. Mol Gen Genet. 1991 Nov;230(1-2):17–23. [PubMed]
  • Ryals J, Little R, Bremer H. Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate. J Bacteriol. 1982 Sep;151(3):1261–1268. [PMC free article] [PubMed]
  • Schindelin H, Jiang W, Inouye M, Heinemann U. Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5119–5123. [PMC free article] [PubMed]
  • Sledjeski DD, Gupta A, Gottesman S. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J. 1996 Aug 1;15(15):3993–4000. [PMC free article] [PubMed]
  • Sonden B, Uhlin BE. Coordinated and differential expression of histone-like proteins in Escherichia coli: regulation and function of the H-NS analog StpA. EMBO J. 1996 Sep 16;15(18):4970–4980. [PMC free article] [PubMed]
  • Tanabe H, Goldstein J, Yang M, Inouye M. Identification of the promoter region of the Escherichia coli major cold shock gene, cspA. J Bacteriol. 1992 Jun;174(12):3867–3873. [PMC free article] [PubMed]
  • Ueguchi C, Kakeda M, Mizuno T. Autoregulatory expression of the Escherichia coli hns gene encoding a nucleoid protein: H-NS functions as a repressor of its own transcription. Mol Gen Genet. 1993 Jan;236(2-3):171–178. [PubMed]
  • Williams MD, Ouyang TX, Flickinger MC. Starvation-induced expression of SspA and SspB: the effects of a null mutation in sspA on Escherichia coli protein synthesis and survival during growth and prolonged starvation. Mol Microbiol. 1994 Mar;11(6):1029–1043. [PubMed]
  • Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, Cashel M. Residual guanosine 3',5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J Biol Chem. 1991 Mar 25;266(9):5980–5990. [PubMed]
  • Yamada H, Yoshida T, Tanaka K, Sasakawa C, Mizuno T. Molecular analysis of the Escherichia coli hns gene encoding a DNA-binding protein, which preferentially recognizes curved DNA sequences. Mol Gen Genet. 1991 Nov;230(1-2):332–336. [PubMed]
  • Yamagishi M, Matsushima H, Wada A, Sakagami M, Fujita N, Ishihama A. Regulation of the Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase- and growth rate-dependent control. EMBO J. 1993 Feb;12(2):625–630. [PMC free article] [PubMed]
  • Yamanaka K, Mitani T, Ogura T, Niki H, Hiraga S. Cloning, sequencing, and characterization of multicopy suppressors of a mukB mutation in Escherichia coli. Mol Microbiol. 1994 Jul;13(2):301–312. [PubMed]
  • Yamashino T, Ueguchi C, Mizuno T. Quantitative control of the stationary phase-specific sigma factor, sigma S, in Escherichia coli: involvement of the nucleoid protein H-NS. EMBO J. 1995 Feb 1;14(3):594–602. [PMC free article] [PubMed]
  • Zhang A, Rimsky S, Reaban ME, Buc H, Belfort M. Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J. 1996 Mar 15;15(6):1340–1349. [PMC free article] [PubMed]

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