Regulation of Ribosomal Protein Synthesis in Escherichia Coli by Selective MRNA Inactivation

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1979 Jul 1

PMID 158759

Citations 59

Authors

A M Fallon

C S Jinks

G D Strycharz

M Nomura

Affiliations

Soon will be listed here.

Abstract

In an Escherichia coli strain lysogenic for lambda spc2 transducing phage, an extra copy of ribosomal protein (r-protein) genes in the spc and alpha operons are carried on the phage chromosome. Expression of genes in the spc operon in this merodiploid strain was compared with that in a control "haploid" strain carrying lambda trkA phage. It was found that the synthesis rate of spc mRNA, relative to other reference mRNA in the merodiploid strain, is about 2-fold higher than that in the control strain; yet, no dosage effect was observed in the synthesis rate of r-proteins in the spc or alpha operon. The spc mRNA was found to be more rapidly degraded in the merodiploid strain than in the control strain, and its steady-state amount, relative to reference mRNA, was only slightly higher in the merodiploid strain than in the control strain. Thus, E. coli cells have the ability to regulate the rate of r-protein synthesis regardless of the rate of transcription of r-protein genes, presumably by inactivation of the mRNA followed by its degradation. A model is proposed which involves selective inactivation of r-protein mRNA by a feedback mechanism. The model can explain coordinated synthesis of r-proteins and other observations related to selective expression of certain alleles in diploid strains.

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References

Isono K, Kitakawa M . Cluster of ribosomal protein genes in Escherichia coli containing genes for proteins S6, S18, and L9. Proc Natl Acad Sci U S A. 1978; 75(12):6163-7. PMC: 393139. DOI: 10.1073/pnas.75.12.6163. View

Jaskunas S, Fallon A, Nomura M . Identification and organization of ribosomal protein genes of Escherichia coli carried by lambdafus2 transducing phage. J Biol Chem. 1977; 252(20):7323-36. View

Post L, Arfsten A, Reusser F, Nomura M . DNA sequences of promoter regions for the str and spc ribosomal protein operons in E. coli. Cell. 1978; 15(1):215-29. DOI: 10.1016/0092-8674(78)90096-x. View

Bowman C, Sidikaro J, Nomura M . Specific inactivation of ribosomes by colicin E3 in vitro and mechanism of immunity in colicinogenic cells. Nat New Biol. 1971; 234(48):133-7. DOI: 10.1038/newbio234133a0. View

Geyl D, Bock A . Synthesis of ribosomal proteins in merodiploid strains and in minicells of Escherichia coli. Mol Gen Genet. 1977; 154(3):327-34. DOI: 10.1007/BF00571290. View

Hardy S . The stoichiometry of the ribosomal proteins of Escherichia coli. Mol Gen Genet. 1975; 140(3):253-74. DOI: 10.1007/BF00334270. View

Nomura M, Morgan E . Genetics of bacterial ribosomes. Annu Rev Genet. 1977; 11:297-347. DOI: 10.1146/annurev.ge.11.120177.001501. View

Lindahl L, Post L, Zengel J, Gilbert S, Strycharz W, Nomura M . Mapping of ribosomal protein genes by in vitro protein synthesis using DNA fragments of lambdafus3 transducing phage DNA as templates. J Biol Chem. 1977; 252(20):7365-83. View

Dennis P, Nomura M . Regulation of the expression of ribosomal protein genes in Escherichia coli. J Mol Biol. 1975; 97(1):61-76. DOI: 10.1016/s0022-2836(75)80022-2. View

10.

Dennis P, Nomura M . Stringent control of the transcriptional activities of ribosomal protein genes in E. coli. Nature. 1975; 255(5508):460-5. DOI: 10.1038/255460a0. View

11.

Glass R . Identification of an amber fragment of the beta subunit of Escherichia coli RNA polymerase: a yardstick for measuring controls on RNA polymerase subunit synthesis. Mol Gen Genet. 1977; 151(1):83-8. DOI: 10.1007/BF00446916. View

12.

Dennis P . In vivo stability, maturation and relative differential synthesis rates of individual ribosomal proteins in Escherichia coli B/r. J Mol Biol. 1974; 88(1):25-41. DOI: 10.1016/0022-2836(74)90293-9. View

13.

Chang F, Wang Y, Fetterolf C, Flaks J . Letter: Unequal contribution to ribosomal assembly of both str alleles in Escherichia coli merodiploids and its relationship to the dominance phenomenon. J Mol Biol. 1974; 82(2):273-7. DOI: 10.1016/0022-2836(74)90345-3. View

14.

Post L, Strycharz G, Nomura M, Lewis H, Dennis P . Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. Proc Natl Acad Sci U S A. 1979; 76(4):1697-701. PMC: 383457. DOI: 10.1073/pnas.76.4.1697. View

15.

Boon T . Inactivation of ribosomes in vitro by colicin E 3 . Proc Natl Acad Sci U S A. 1971; 68(10):2421-5. PMC: 389435. DOI: 10.1073/pnas.68.10.2421. View

16.

Yamamoto M, Nomura M . Contranscription of genes for RNA polymerase subunits beta and beta' with genes for ribosomal proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1978; 75(8):3891-5. PMC: 392894. DOI: 10.1073/pnas.75.8.3891. View

17.

Glass R, Goman M, Errington L, Scaife J . Induction of RNA polymerase synthesis in Escherichia coli. Mol Gen Genet. 1975; 143(1):79-83. DOI: 10.1007/BF00269423. View

18.

Sidikaro J, Nomura M . Colicin E3-induced in vitro inactivation of ribosomes from colicin-insensitive bacterial species. FEBS Lett. 1973; 29(1):15-19. DOI: 10.1016/0014-5793(73)80005-5. View

19.

Jaskunas S, Lindahl L, Nomura M . Specialized transducing phages for ribosomal protein genes of Escherichia coli. Proc Natl Acad Sci U S A. 1975; 72(1):6-10. PMC: 432228. DOI: 10.1073/pnas.72.1.6. View

20.

Linn T, Scaife J . Identification of a single promoter in E. coli for rplJ, rplL and rpoBC. Nature. 1978; 276(5683):33-7. DOI: 10.1038/276033a0. View