Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1994 Feb 11;22(3):397–403. doi: 10.1093/nar/22.3.397

Polynucleotide phosphorylase of Escherichia coli induces the degradation of its RNase III processed messenger by preventing its translation.

M R Meur 1, C Portier 1
PMCID: PMC523595  PMID: 7510392

Abstract

Polynucleotide phosphorylase, a 3' to 5' processive exoribonuclease is post-transcriptionally autocontrolled and it was previously shown that this control is dependent on a 5' processing by RNase III. In this paper, the mechanism of regulation is analyzed by studying the properties of a pnp-lacZ translational gene fusion. It is shown that this message is stable, even when processed by RNase III, and that the degradation rate is directly linked to the intracellular concentration of polynucleotide phosphorylase or to the pnp-lacZ messenger translation rate. Mutations able to decrease the level of repression are all located in the ribosome loading site. Taken together, these results suggest that polynucleotide phosphorylase is able to recognize specifically the processed messenger and to prevent its translation, thus allowing degradation of the message.

Full text

PDF
397

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Balbás P., Soberón X., Merino E., Zurita M., Lomeli H., Valle F., Flores N., Bolivar F. Plasmid vector pBR322 and its special-purpose derivatives--a review. Gene. 1986;50(1-3):3–40. doi: 10.1016/0378-1119(86)90307-0. [DOI] [PubMed] [Google Scholar]
  2. Case C. C., Simons E. L., Simons R. W. The IS10 transposase mRNA is destabilized during antisense RNA control. EMBO J. 1990 Apr;9(4):1259–1266. doi: 10.1002/j.1460-2075.1990.tb08234.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Lindahl L., Zengel J. M. Ribosomal genes in Escherichia coli. Annu Rev Genet. 1986;20:297–326. doi: 10.1146/annurev.ge.20.120186.001501. [DOI] [PubMed] [Google Scholar]
  4. Nakamaye K. L., Eckstein F. Inhibition of restriction endonuclease Nci I cleavage by phosphorothioate groups and its application to oligonucleotide-directed mutagenesis. Nucleic Acids Res. 1986 Dec 22;14(24):9679–9698. doi: 10.1093/nar/14.24.9679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Nomura M., Yates J. L., Dean D., Post L. E. Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein MRNA. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7084–7088. doi: 10.1073/pnas.77.12.7084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Plumbridge J. A., Dondon J., Nakamura Y., Grunberg-Manago M. Effect of NusA protein on expression of the nusA,infB operon in E. coli. Nucleic Acids Res. 1985 May 10;13(9):3371–3388. doi: 10.1093/nar/13.9.3371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Plumbridge J. A. Repression and induction of the nag regulon of Escherichia coli K-12: the roles of nagC and nagA in maintenance of the uninduced state. Mol Microbiol. 1991 Aug;5(8):2053–2062. doi: 10.1111/j.1365-2958.1991.tb00828.x. [DOI] [PubMed] [Google Scholar]
  8. Portier C., Dondon L., Grunberg-Manago M., Régnier P. The first step in the functional inactivation of the Escherichia coli polynucleotide phosphorylase messenger is a ribonuclease III processing at the 5' end. EMBO J. 1987 Jul;6(7):2165–2170. doi: 10.1002/j.1460-2075.1987.tb02484.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Portier C., Migot C., Grumberg-Manago M. Cloning of E. coli pnp gene from an episome. Mol Gen Genet. 1981;183(2):298–305. doi: 10.1007/BF00270632. [DOI] [PubMed] [Google Scholar]
  10. Poulsen L. K., Refn A., Molin S., Andersson P. The gef gene from Escherichia coli is regulated at the level of translation. Mol Microbiol. 1991 Jul;5(7):1639–1648. doi: 10.1111/j.1365-2958.1991.tb01911.x. [DOI] [PubMed] [Google Scholar]
  11. Robert-Le Meur M., Portier C. E.coli polynucleotide phosphorylase expression is autoregulated through an RNase III-dependent mechanism. EMBO J. 1992 Jul;11(7):2633–2641. doi: 10.1002/j.1460-2075.1992.tb05329.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Régnier P., Grunberg-Manago M., Portier C. Nucleotide sequence of the pnp gene of Escherichia coli encoding polynucleotide phosphorylase. Homology of the primary structure of the protein with the RNA-binding domain of ribosomal protein S1. J Biol Chem. 1987 Jan 5;262(1):63–68. [PubMed] [Google Scholar]
  13. Régnier P., Portier C. Initiation, attenuation and RNase III processing of transcripts from the Escherichia coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J Mol Biol. 1986 Jan 5;187(1):23–32. doi: 10.1016/0022-2836(86)90403-1. [DOI] [PubMed] [Google Scholar]
  14. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sulewski M., Marchese-Ragona S. P., Johnson K. A., Benkovic S. J. Mechanism of polynucleotide phosphorylase. Biochemistry. 1989 Jul 11;28(14):5855–5864. doi: 10.1021/bi00440a023. [DOI] [PubMed] [Google Scholar]
  16. Takata R., Izuhara M., Hori K. Differential degradation of the Escherichia coli polynucleotide phosphorylase mRNA. Nucleic Acids Res. 1989 Sep 25;17(18):7441–7451. doi: 10.1093/nar/17.18.7441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Uzan M., Favre R., Brody E. A nuclease that cuts specifically in the ribosome binding site of some T4 mRNAs. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8895–8899. doi: 10.1073/pnas.85.23.8895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  19. Yarchuk O., Jacques N., Guillerez J., Dreyfus M. Interdependence of translation, transcription and mRNA degradation in the lacZ gene. J Mol Biol. 1992 Aug 5;226(3):581–596. doi: 10.1016/0022-2836(92)90617-s. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES