During the last few years, several genes, such as pap, bgl and flhDC, have been shown to be coregulated by the histone-like nucleoid-structuring (H-NS) protein and the cyclic AMP-catabolite activator protein (cAMP/CAP) complex, suggesting an interaction between both systems in the control of some cellular functions. In this study, the possible effect of H-NS on the cAMP level was investigated. In a CAP-deficient strain, the presence of an hns mutation results in a strong reduction in the amount of cAMP, due to a decrease in adenylate cyclase activity. This is caused by the reduced expression of crr, which encodes the Enzyme IIAGlc of the phosphoenolpyruvate:carbohydrate phosphotransferase system (PTS), from its specific P2 promoter. This leads to a twofold reduction in the global amount of Enzyme IIAGlc, the adenylate cyclase activator, responsible for the decrease in adenylate cyclase activity observed in the hns crp strain.
AibaH.1985; Transcription of the Escherichia coli adenylate cyclase gene is negatively regulated by cAMP-cAMP receptor protein. J Biol Chem 260:3063–3070
BalsalobreC., JohanssonJ., UhlinB. E., JuarezA.,
MunoaF. J.1999; Alterations in protein expression caused by the hha mutation in Escherichia coli : influence of growth medium osmolarity. J Bacteriol 181:3018–3024
BertinP., TeraoE., LeeE. H., LejeuneP., ColsonC., DanchinA.,
CollatzE.1994; The H-NS protein is involved in the biogenesis of flagella in Escherichia coli . J Bacteriol 176:5537–5540
BertinP., HommaisF., KrinE., SoutourinaO., TendengC., DerzelleS.,
DanchinA.2001; H-NS and H-NS-like proteins in Gram-negative bacteria and their multiple role in the regulation of bacterial metabolism. Biochimie 83:235–241[CrossRef]
BusbyS.,
KolbA.1996; The CAP modulon. In Regulation of Gene Expression in Escherichia coli pp 255–279 Edited by
LinE. C. C.LynchA. S.
Austin, TX: R. G. Landes;
CollJ. L., HeydeM.,
PortalierR.1994; Expression of the nmpC gene of Escherichia coli K-12 is modulated by external pH. Identification of cis -acting regulatory sequences involved in this regulation. Mol Microbiol 12:83–93[CrossRef]
CrasnierM., DumayV.,
DanchinA.1994; The catalytic domain of Escherichia coli K-12 adenylate cyclase as revealed by deletion analysis of the cya gene. Mol Gen Genet 243:409–416[CrossRef]
Den BlaauwenJ. L.,
PostmaP. W.1985; Regulation of cyclic AMP synthesis by enzyme IIIGlc of the phosphoenolpyruvate: sugar phosphotransferase system in crp strains of Salmonella typhimurium . J Bacteriol 164:477–478
De ReuseH.,
DanchinA.1988; The ptsH , ptsI , and crr genes of the Escherichia coli phosphoenolpyruvate-dependent phosphotransferase system: a complex operon with several modes of transcription. J Bacteriol 170:3827–3837
De ReuseH., TouatiE., GlaserP.,
DanchinA.1986; Low copy number plasmid vectors for gene cloning and for monitoring gene expression. FEMS Microbiol Lett 37:193–197[CrossRef]
De ReuseH., KolbA.,
DanchinA.1992; Positive regulation of the expression of the Escherichia coli pts operon. Identification of the regulatory regions. J Mol Biol 226:623–635[CrossRef]
ForsmanK., UhlinB. E., SondénB.,
GöranssonM.1992; Antirepression function in Escherichia coli for the cAMP–cAMP receptor protein transcriptional activator. Proc Natl Acad Sci USA 89:9880–9884[CrossRef]
Gonzalez-PastorJ. E., San MillanJ. L., CastillaM. A.,
MorenoF.1995; Structure and organization of plasmid genes required to produce the translation inhibitor microcin C7. J Bacteriol 177:7131–7140
Guidi-RontaniC., DanchinA.,
UllmannA.1981; Isolation and characterization of an Escherichia coli mutant affected in the regulation of adenylate cyclase. J Bacteriol 148:753–761
InadaT., TakahashiH., MizunoT.,
AibaH.1996; Down regulation of cAMP production by cAMP receptor protein in Escherichia coli : an assessment of the contributions of transcriptional and posttranscriptional control of adenylate cyclase. Mol Gen Genet 253:198–204[CrossRef]
JosephE., BernsleyC., GuisoN.,
UllmannA.1982; Multiple regulation of the activity of adenylate cyclase in Escherichia coli . Mol Gen Genet 185:262–268[CrossRef]
Laurent-WinterC., NgoS., DanchinA.,
BertinP.1997; Role of Escherichia coli histone-like nucleoid structuring protein in bacterial metabolism and stress response: identification of targets by two-dimensional electrophoresis. Eur J Biochem 244:767–773[CrossRef]
LevinthalM., LejeuneP.,
DanchinA.1994; The H-NS protein modulates the activation of the ilvIH operon of Escherichia coli K12 by Lrp, the leucine regulatory protein. Mol Gen Genet 242:736–743
LevyS., ZengG.-Q.,
DanchinA.1990; Cyclic AMP synthesis in Escherichia coli strains bearing known deletions in the pts phosphotransferase operon. Gene 86:27–33[CrossRef]
MillerJ. H.1992A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
MitchellW. J., SaffenD. W.,
RosemanS.1987; Sugar transport by the bacterial phosphotransferase system: in vivo regulation of lactose transport in Escherichia coli by IIIGlc, a protein of the phosphoenolpyruvate: glucose phosphotransferase system. J Biol Chem 262:16254–16260
NietoJ. M., MadridC., PrenafetaA., MiquelayE., BalsalobreC., CarrascalM.,
JuarezA.2000; Expression of the hemolysin operon in Escherichia coli is modulated by a nucleoid-protein complex that includes the proteins Hha and H-NS. Mol Gen Genet 263:349–358[CrossRef]
OshimaT., ItoK., KabayamaH.,
NakamuraY.1995; Regulation of lrp gene expression by H-NS and Lrp proteins in Escherichia coli : dominant negative mutations in lrp . Mol Gen Genet 247:521–528[CrossRef]
PeterkofskyA., SeokY.-J., AminN.8 other authors1995; The Escherichia coli adenylyl cyclase complex: requirement of PTS proteins for stimulation by nucleotides. Biochem 34:8950–8959[CrossRef]
PotterK., Chaloner-LarssonG.,
YamazakiH.1974; Abnormally high rate of cyclic AMP excretion from an Escherichia coli mutant deficient in cyclic AMP receptor protein. Biochem Biophys Res Commun 57:379–385[CrossRef]
ReddyP.,
KamireddiM.1998; Modulation of Escherichia coli adenylyl cyclase activity by catalytic-site mutants of protein IIAGlc of the phosphoenolpyruvate: sugar phosphotransferase system. J Bacteriol 180:732–736
RephaeliA. W., SaierM. H.Jr1976; Effects of crp mutations on adenosine 3′,5′-monophosphate metabolism in Salmonella typhimurium . J Bacteriol 127:120–127
RoyA., HazizaC.,
DanchinA.1983; Regulation of adenylate cyclase synthesis in Escherichia coli : nucleotide sequence of the control region. EMBO J 2:791–797
RyuS., RamseierT. M., MichoteyV., GargesS., SaierM. H.Jr1995; Effect of the FruR regulator on transcription of the pts operon in Escherichia coli . J Biol Chem 270:2489–2496[CrossRef]
SaierM. H.Jr, RamseierT. M.,
ReizerJ.others1996; Regulation of carbon utilization. In Escherichia coli and Salmonella: Cellular and Molecular Biology . pp 1325–1343 Edited by
NeidhardtF. C.
Washington, DC: American Society for Microbiology;
SchnetzK.,
WangJ. C.1996; Silencing of the Escherichia coli bgl promoter: effects of template supercoiling and cell extracts on promoter activity in vitro . Nucleic Acids Res 24:2422–2428[CrossRef]
SoutourinaO., KolbA., KrinE., Laurent-WinterC., RimskyS., DanchinA.,
BertinP.1999; Multiple control of flagellum biosynthesis in Escherichia coli : role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181:7500–7508
TakahashiH., InadaT., PostmaP.,
AibaH.1998; CRP down-regulates adenylate cyclase activity by reducing the level of phosphorylated IIAGlc, the glucose-specific phosphotransferase protein, in Escherichia coli . Mol Gen Genet 259:317–326[CrossRef]
ZengG. Q., De ReuseH.,
DanchinA.1992; Mutational analysis of the enzyme IIIGlc of the phosphoenolpyruvate phosphotransferase system in Escherichia coli . Res Microbiol 143:251–261[CrossRef]