The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenylation in Escherichia coli

Nucleic Acids Res. 2008 May;36(8):2570-80. doi: 10.1093/nar/gkn091. Epub 2008 Mar 11.

Abstract

In Escherichia coli the glmS gene encoding glucosamine 6-phosphate (GlcN-6-P) synthase GlmS is feedback regulated by GlcN-6-P in a pathway that involves the small RNA GlmZ. Expression of glmS is activated by the unprocessed form of GlmZ, which accumulates when the intracellular GlcN-6-P concentration decreases. GlmZ stabilizes a glmS transcript that derives from processing. Overexpression of a second sRNA, GlmY, also activates glmS expression in an unknown way. Furthermore, mutations in two genes, yhbJ and pcnB, cause accumulation of full-length GlmZ and thereby activate glmS expression. The function of yhbJ is unknown and pcnB encodes poly(A) polymerase PAP-I known to polyadenylate and destabilize RNAs. Here we show that GlmY acts indirectly in a way that depends on GlmZ. When the intracellular GlcN-6-P concentration decreases, GlmY accumulates and causes in turn accumulation of full-length GlmZ, which finally activates glmS expression. In glmZ mutants, GlmY has no effect on glmS, whereas artificially expressed GlmZ can activate glmS expression also in the absence of GlmY. Furthermore, we show that PAP-I acts at the top of this regulatory pathway by polyadenylating and destabilizing GlmY. In pcnB mutants, GlmY accumulates and induces glmS expression by stabilizing full-length GlmZ. Hence, the data reveal a regulatory cascade composed of two sRNAs, which responds to GlcN-6-P and is controlled by polyadenylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / biosynthesis
  • Escherichia coli Proteins / genetics*
  • Escherichia coli Proteins / metabolism
  • Gene Expression Regulation, Bacterial*
  • Glucosamine / analogs & derivatives
  • Glucosamine / metabolism
  • Glucose-6-Phosphate / analogs & derivatives
  • Glucose-6-Phosphate / metabolism
  • Glutamine-Fructose-6-Phosphate Transaminase (Isomerizing) / biosynthesis
  • Glutamine-Fructose-6-Phosphate Transaminase (Isomerizing) / genetics*
  • Mutation
  • Polyadenylation*
  • Polynucleotide Adenylyltransferase / genetics
  • RNA Stability
  • RNA, Messenger / metabolism
  • RNA, Untranslated / metabolism*
  • RNA-Binding Proteins

Substances

  • Escherichia coli Proteins
  • RNA, Messenger
  • RNA, Untranslated
  • RNA-Binding Proteins
  • YhbJ protein, E coli
  • glucosamine 6-phosphate
  • Glucose-6-Phosphate
  • Glutamine-Fructose-6-Phosphate Transaminase (Isomerizing)
  • Polynucleotide Adenylyltransferase
  • Glucosamine