A novel mechanism of ribonuclease regulation: GcvB and Hfq stabilize the mRNA that encodes RNase BN/Z during exponential phase

J Biol Chem. 2019 Dec 27;294(52):19997-20008. doi: 10.1074/jbc.RA119.011367. Epub 2019 Nov 19.

Abstract

RNase BN, the Escherichia coli RNase Z family member, plays a limited role in tRNA metabolism, in contrast to most other organisms. However, RNase BN does act on 6S RNA, the global transcription regulator, degrading it in exponential-phase cells and maintaining it at low levels during this phase of growth. RNase BN levels decrease in stationary-phase cells, leading to elevation of 6S RNA and subsequent regulation of RNA polymerase. These findings were the first indication that RNase BN itself is growth phase-regulated. Here, we analyze the mechanism of this regulation of RNase BN. We find that RNase BN decreases in stationary phase because its mRNA becomes unstable, due primarily to its degradation by RNase E. However, in exponential-phase cells rbn mRNA is stabilized due to binding by the sRNA, GcvB, and the protein, Hfq, which reduce cleavage by RNase E. Because the amount of GcvB decreases in stationary phase, rbn mRNA is less protected and becomes increasingly unstable resulting in reduction in the amount of RNase BN. The small RNA-dependent, positive regulation of RNase BN in exponential-phase cells is the first example of this novel mechanism for RNase regulation.

Keywords: RNA; bacteria; growth-phase regulation; mRNA decay; mRNA stability; post-transcriptional regulation; regulatory RNA; ribonuclease.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Base Sequence
  • Endoribonucleases / metabolism
  • Escherichia coli / growth & development
  • Escherichia coli / metabolism*
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Exoribonucleases / genetics
  • Exoribonucleases / metabolism*
  • Host Factor 1 Protein / metabolism*
  • Protein Binding
  • RNA Stability
  • RNA, Messenger / chemistry
  • RNA, Messenger / metabolism*
  • RNA, Small Untranslated / genetics
  • RNA, Small Untranslated / metabolism*
  • Transcription Initiation Site

Substances

  • Escherichia coli Proteins
  • Hfq protein, E coli
  • Host Factor 1 Protein
  • RNA, Messenger
  • RNA, Small Untranslated
  • Endoribonucleases
  • Exoribonucleases
  • ribonuclease BN
  • ribonuclease E