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. 1989 Jan;86(2):448–452. doi: 10.1073/pnas.86.2.448

Retroregulation of the synthesis of ribosomal proteins L14 and L24 by feedback repressor S8 in Escherichia coli.

L Mattheakis 1, L Vu 1, F Sor 1, M Nomura 1
PMCID: PMC286487  PMID: 2643112

Abstract

Previous studies on regulation of the spc operon containing genes for ribosomal proteins have shown that S8, encoded by the fifth gene of the operon in Escherichia coli, is a translational repressor and regulates the synthesis of the third gene product (L5) and distal gene products by acting at a site near the L5 mRNA translation initiation site. We have now shown that S8 also regulates the synthesis of the first and second gene products (L14 and L24) of the operon by acting at the same mRNA target site--that is, the site located distal to sites coding for L14 and L24--and that mRNA degradation is involved in this retroregulation. It was shown that single base substitutions in the target site, which abolish repression of the synthesis of L5 and L5-distal gene products by S8, also cause derepression of L14-L24 synthesis. Inhibition of L14-L24 synthesis by S8 was also shown by overproducing S8 in trans from a plasmid carrying the S8 gene under lac promoter/operator control. A strain carrying temperature-sensitive mutations in genes for polynucleotide phosphorylase and RNase II was found upon shift to nonpermissive temperature to show higher differential synthesis rates of L14-L24 (and L5) relative to those of several L5-distal spc operon gene products. We suggest that repression of distal ribosomal protein synthesis by S8 triggers nucleolytic cleavage of spc operon mRNA, followed by mRNA degradation by these 3'- to 5'- exonucleases, which is then responsible for inhibition of L14-L24 synthesis.

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Selected References

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

  1. Arraiano C. M., Yancey S. D., Kushner S. R. Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutants of Escherichia coli K-12. J Bacteriol. 1988 Oct;170(10):4625–4633. doi: 10.1128/jb.170.10.4625-4633.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cole J. R., Nomura M. Changes in the half-life of ribosomal protein messenger RNA caused by translational repression. J Mol Biol. 1986 Apr 5;188(3):383–392. doi: 10.1016/0022-2836(86)90162-2. [DOI] [PubMed] [Google Scholar]
  3. Coulondre C., Miller J. H. Genetic studies of the lac repressor. III. Additional correlation of mutational sites with specific amino acid residues. J Mol Biol. 1977 Dec 15;117(3):525–567. doi: 10.1016/0022-2836(77)90056-0. [DOI] [PubMed] [Google Scholar]
  4. Dean D., Yates J. L., Nomura M. Escherichia coli ribosomal protein S8 feedback regulates part of spc operon. Nature. 1981 Jan 1;289(5793):89–91. doi: 10.1038/289089a0. [DOI] [PubMed] [Google Scholar]
  5. Donovan W. P., Kushner S. R. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1986 Jan;83(1):120–124. doi: 10.1073/pnas.83.1.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fallon A. M., Jinks C. S., Strycharz G. D., Nomura M. Regulation of ribosomal protein synthesis in Escherichia coli by selective mRNA inactivation. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3411–3415. doi: 10.1073/pnas.76.7.3411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Guarneros G., Galindo J. M. The regulation of integrative recombination by the b2 region and the cII gene of bacteriophage lambda. Virology. 1979 May;95(1):119–126. doi: 10.1016/0042-6822(79)90406-9. [DOI] [PubMed] [Google Scholar]
  8. Guarneros G., Montañez C., Hernandez T., Court D. Posttranscriptional control of bacteriophage lambda gene expression from a site distal to the gene. Proc Natl Acad Sci U S A. 1982 Jan;79(2):238–242. doi: 10.1073/pnas.79.2.238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jaskunas S. R., Fallon A. M., Nomura M. Identification and organization of ribosomal protein genes of Escherichia coli carried by lambdafus2 transducing phage. J Biol Chem. 1977 Oct 25;252(20):7323–7336. [PubMed] [Google Scholar]
  10. 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]
  11. Mattheakis L. C., Nomura M. Feedback regulation of the spc operon in Escherichia coli: translational coupling and mRNA processing. J Bacteriol. 1988 Oct;170(10):4484–4492. doi: 10.1128/jb.170.10.4484-4492.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Miura A., Krueger J. H., Itoh S., de Boer H. A., Nomura M. Growth-rate-dependent regulation of ribosome synthesis in E. coli: expression of the lacZ and galK genes fused to ribosomal promoters. Cell. 1981 Sep;25(3):773–782. doi: 10.1016/0092-8674(81)90185-9. [DOI] [PubMed] [Google Scholar]
  13. Neidhardt F. C., Bloch P. L., Smith D. F. Culture medium for enterobacteria. J Bacteriol. 1974 Sep;119(3):736–747. doi: 10.1128/jb.119.3.736-747.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nomura M., Gourse R., Baughman G. Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem. 1984;53:75–117. doi: 10.1146/annurev.bi.53.070184.000451. [DOI] [PubMed] [Google Scholar]
  15. Schindler D., Echols H. Retroregulation of the int gene of bacteriophage lambda: control of translation completion. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4475–4479. doi: 10.1073/pnas.78.7.4475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schmeissner U., McKenney K., Rosenberg M., Court D. Removal of a terminator structure by RNA processing regulates int gene expression. J Mol Biol. 1984 Jun 15;176(1):39–53. doi: 10.1016/0022-2836(84)90381-4. [DOI] [PubMed] [Google Scholar]
  17. Studier F. W. Genetic mapping of a mutation that causes ribonucleases III deficiency in Escherichia coli. J Bacteriol. 1975 Oct;124(1):307–316. doi: 10.1128/jb.124.1.307-316.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Takebe Y., Miura A., Bedwell D. M., Tam M., Nomura M. Increased expression of ribosomal genes during inhibition of ribosome assembly in Escherichia coli. J Mol Biol. 1985 Jul 5;184(1):23–30. doi: 10.1016/0022-2836(85)90040-3. [DOI] [PubMed] [Google Scholar]
  19. Yates J. L., Arfsten A. E., Nomura M. In vitro expression of Escherichia coli ribosomal protein genes: autogenous inhibition of translation. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1837–1841. doi: 10.1073/pnas.77.4.1837. [DOI] [PMC free article] [PubMed] [Google Scholar]

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