Abstract
Escherichia coli ribosomal protein L1 (0.5 micro M) was found to inhibit the synthesis of both proteins of the L11 operon, L11 and L1, but not the synthesis of other proteins directed by lambda rifd 18 DNA. Similarly, S4 (1 micro M) selectively inhibited the synthesis of three proteins of the alpha operon, S13, S11, and S4, directed by lambda spcI DNA or a restriction enzyme fragment obtained from this DNA. S8 (3.6 micro M) also showed preferential inhibitory effects on the synthesis of some proteins encoded in the spc operon, L24 and L5 (and probably S14 and S8), directed by lambda spcl DNA or a restriction enzyme fragment carrying the genes for these proteins. The inhibitory effect of L1 was observed only with L1 and not with other proteins examined, including S4 and S8. Similarly, the effect of S4 was not observed with L1 or S8, and that of S8 was not seen with L1 or S4. Inhibition was shown to take place at the level of translation rather than transcription. Thus, at least some ribosomal proteins (L1 S4, and S8) have the ability to cause selective translational inhibition of the synthesis of certain ribosomal proteins whose genes are in the same operon as their own. These results support the hypothesis that certain free ribosomal proteins not assembled into ribosomes act as "autogenous" feedback inhibitors to regulate the synthesis of ribosomal proteins.
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- Branlant C., Krol A., Sriwdada J., Ebel J. P., Sloof P., Garrett R. A. The binding site of protein L1 ON 23-S ribosomal RNA of Escherichia coli. 2. Identification of the rna region contained in the L1 ribonucleoproteins and determination of the order of the RNA subfragments within this region. Eur J Biochem. 1976 Nov 15;70(2):457–469. doi: 10.1111/j.1432-1033.1976.tb11037.x. [DOI] [PubMed] [Google Scholar]
- Dennis P. P., Fill N. P. Transcriptional and post-transcriptional control of RNA polymerase and ribosomal protein genes cloned on composite ColE1 plasmids in the bacterium Escherichia coli. J Biol Chem. 1979 Aug 25;254(16):7540–7547. [PubMed] [Google Scholar]
- 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]
- Fallon A. M., Jinks C. S., Yamamoto M., Nomura M. Expression of ribosomal protein genes cloned in a hybrid plasmid in Escherichia coli: gene dosage effects on synthesis of ribosomal proteins and ribosomal protein messenger ribonucleic acid. J Bacteriol. 1979 May;138(2):383–396. doi: 10.1128/jb.138.2.383-396.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fiil N. P., Bendiak D., Collins J., Friesen J. D. Expression of Escherichia coli ribosomal protein and RNA polymerase genes cloned on plasmids. Mol Gen Genet. 1979 May 23;173(1):39–50. doi: 10.1007/BF00267689. [DOI] [PubMed] [Google Scholar]
- Gausing K. Ribosomal protein in E. coli: rate of synthesis and pool size at different growth rates. Mol Gen Genet. 1974 Mar 6;129(1):61–75. doi: 10.1007/BF00269266. [DOI] [PubMed] [Google Scholar]
- Gold L., O'Farrell P. Z., Russel M. Regulation of gene 32 expression during bacteriophage T4 infection of Escherichia coli. J Biol Chem. 1976 Nov 25;251(22):7251–7262. [PubMed] [Google Scholar]
- Held W. A., Mizushima S., Nomura M. Reconstitution of Escherichia coli 30 S ribosomal subunits from purified molecular components. J Biol Chem. 1973 Aug 25;248(16):5720–5730. [PubMed] [Google Scholar]
- Jaskunas S. R., Burgess R. R., Nomura M. Identification of a gene for the alpha-subunit of RNA polymerase at the str-spc region of the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5036–5040. doi: 10.1073/pnas.72.12.5036. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Jaskunas S. R., Nomura M. Organization of ribosomal protein genes of Escherichia coli as analyzed by polar insertion mutations. J Biol Chem. 1977 Oct 25;252(20):7337–7343. [PubMed] [Google Scholar]
- Kahan L., Held W. A., Nomura M. Effects of aminoethylation of cysteine residues on the structural and functional activities of the Escherichia coli 30 S ribosomal proteins. J Mol Biol. 1974 Oct 5;88(4):797–808. doi: 10.1016/0022-2836(74)90400-8. [DOI] [PubMed] [Google Scholar]
- Kaltschmidt E., Kahan L., Nomura M. In vitro synthesis of ribosomal proteins directed by Escherichia coli DNA. Proc Natl Acad Sci U S A. 1974 Feb;71(2):446–450. doi: 10.1073/pnas.71.2.446. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
- Krisch H. M., Bolle A., Epstein R. H. Regulation of the synthesis of bacteriophage T4 gene 32 protein. J Mol Biol. 1974 Sep 5;88(1):89–104. doi: 10.1016/0022-2836(74)90296-4. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lemaire G., Gold L., Yarus M. Autogenous translational repression of bacteriophage T4 gene 32 expression in vitro. J Mol Biol. 1978 Nov 25;126(1):73–90. doi: 10.1016/0022-2836(78)90280-2. [DOI] [PubMed] [Google Scholar]
- Lindahl L. Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J Mol Biol. 1975 Feb 15;92(1):15–37. doi: 10.1016/0022-2836(75)90089-3. [DOI] [PubMed] [Google Scholar]
- Lindahl L., Post L., Zengel J., Gilbert S. F., Strycharz W. A., 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 Oct 25;252(20):7365–7383. [PubMed] [Google Scholar]
- Lindahl L., Zengel J. M. Operon-specific regulation of ribosomal protein synthesis in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6542–6546. doi: 10.1073/pnas.76.12.6542. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindahl S., Yamamoto M., Nomura M. Mapping of a cluster of genes for components of the transcriptional and translational machineries of Escherichia coli. J Mol Biol. 1977 Jan 5;109(1):23–47. doi: 10.1016/s0022-2836(77)80044-2. [DOI] [PubMed] [Google Scholar]
- Linn T., Scaife J. Identification of a single promoter in E. coli for rplJ, rplL and rpoBC. Nature. 1978 Nov 2;276(5683):33–37. doi: 10.1038/276033a0. [DOI] [PubMed] [Google Scholar]
- Mizushima S., Nomura M. Assembly mapping of 30S ribosomal proteins from E. coli. Nature. 1970 Jun 27;226(5252):1214–1214. doi: 10.1038/2261214a0. [DOI] [PubMed] [Google Scholar]
- Nomura M., Morgan E. A. Genetics of bacterial ribosomes. Annu Rev Genet. 1977;11:297–347. doi: 10.1146/annurev.ge.11.120177.001501. [DOI] [PubMed] [Google Scholar]
- Olsson M. O., Isaksson L. A. Analysis of rpsD mutations in Escherichia coli. III. Effects of rpsD mutations on expression of some ribosomal protein genes. Mol Gen Genet. 1979 Feb 1;169(3):271–278. doi: 10.1007/BF00382273. [DOI] [PubMed] [Google Scholar]
- Post L. E., Nomura M. Nucleotide sequence of the intercistronic region preceding the gene for RNA polymerase subunit alpha in Escherichia coli. J Biol Chem. 1979 Nov 10;254(21):10604–10606. [PubMed] [Google Scholar]
- Post L. E., Strycharz G. D., Nomura M., Lewis H., Dennis P. 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 Apr;76(4):1697–1701. doi: 10.1073/pnas.76.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaup H. W., Sogin M. L., Kurland C. G., Woese C. R. Localization of a binding site for ribosomal protein S8 within the 16S ribosomal ribonucleic acid of Escherichia coli. J Bacteriol. 1973 Jul;115(1):82–87. doi: 10.1128/jb.115.1.82-87.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto M., Nomura M. Organization of genes for transcription and translation in the rif region of the Escherichia coli chromosome. J Bacteriol. 1979 Jan;137(1):584–594. doi: 10.1128/jb.137.1.584-594.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yates J. L., Gette W. R., Furth M. E., Nomura M. Effects of ribosomal mutations on the read-through of a chain termination signal: studies on the synthesis of bacteriophage lambda O gene protein in vitro. Proc Natl Acad Sci U S A. 1977 Feb;74(2):689–693. doi: 10.1073/pnas.74.2.689. [DOI] [PMC free article] [PubMed] [Google Scholar]