Home LiteratureArticle Details
PMID: 7003354 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Autogenous and post-transcriptional regulation of RNA polymerase synthesis.

Molecular and cellular biochemistry ·Vol. 31 ·No. 3 ·1980-08-16 ·Pages 177-96

Ishihama A, Fukuda R

Abstract

The regulation of gene expression was studied, for the Escherichia coli rpoBC operon, which includes the genes, rpoB and rpoC, for the beta and beta subunits of RNA polymerase, and rplJ and rplL, for the two proteins, L10 and L7/12, of the 50S ribosome. The gene organization agrees well with the accumulated observations indicating the coordinate synthesis of RNA polymerase and ribosomes under various growth conditions for wild-type E. coli cells. On the other hand, the differential regulation of the two essential components observed under restrictive growth conditions, after addition of various drugs or with certain mutants, in particular those carrying mutations in the RNA polymerase genes, was found to take place through two novel regulation systems: The transcriptional termination at an internal attenuation site and the two autogenous and posttranscriptional controls, being specific for the two ribosomal protein genes and the two RNA polymerase subunit genes, respectively. The majority of the transcription initiated from the promoter rpoP beta terminates at an attenuator site between the promoter-proximal rplJL and the promoter-distal rpoBC genes. The frequency of the attenuation seems to control the relative level of RNA polymerase synthesis to that of ribosomes. The expression of rpoBC genes is subject to an autogenous regulation, in which both RNA polymerase holoenzyme and alpha 2 beta complex function as regulatory molecules with repressor activity. The autogenous regulation was found to operate at post-transcriptional step(s), probably at the level of translation. During the study on the regulation of RNA polymerase synthesis, we noticed that the rpoBC operon contained another autogenous regulation circuit, in which the synthesis of L10 and L7/12 was specifically repressed by the L10-L7/12 complex. Molecular mechanisms and physiological meanings of the novel regulations are discussed.

MeSH Terms
Acridine Orange/pharmacology DNA-Directed RNA Polymerases/biosynthesis,genetics Escherichia coli/genetics,growth & development Ethidium/pharmacology Gene Expression Regulation/drug effects Mutation Operon Plasmids Protein Biosynthesis Ribosomes/metabolism Rifampin/pharmacology Transcription, Genetic
Chemicals
DNA-Directed RNA Polymerases Ethidium Acridine Orange Rifampin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ishihama A
Fukuda R
References (65)
65 references, click to expand
  1. Regulation of ribosomal and transfer ribonucleic acid synthesis in Escherichia coli B-r.
    J Biol Chem. 1972 May 10;247(9):2842-5 PMID: 4337104
  2. Control of ribosomal RNA synthesis in Escherichia coli. IV. Frequency of transcription of ribosomal RNA genes as a function of growth rate.
    Mol Gen Genet. 1978 Aug 4;164(1):39-44 PMID: 360039
  3. Localization of the structural gene for the ' subunit of RNA polymerase in Escherichia coli.
    Biochem Biophys Res Commun. 1973 Jul 17;53(2):645-52 PMID: 4577588
  4. Biosynthesis of RNA polymerase in Escherichia coli. II. control of RNA polymerase synthesis during nutritional shift up and down.
    Mol Gen Genet. 1975 Dec 23;142(1):67-84 PMID: 765737
  5. Regulation of RNA polymerase synthesis in Escherichia coli: a mutant unable to synthesize the enzyme at 43 degrees.
    Proc Natl Acad Sci U S A. 1975 Mar;72(3):911-5 PMID: 1093173
  6. Effects of rifampicin on synthesis and functional activity of DNA-dependent RNA polymerase in Escherichia coli.
    Mol Gen Genet. 1976 Jun 15;145(3):227-37 PMID: 781514
  7. Regulation of ribonucleic acid synthesis in Escherichia coli B-r: an analysis of a shift-up. II. Fraction of RNA polymerase engaged in the synthesis of stable RNA at different steady-state growth rates.
    J Mol Biol. 1973 Mar 25;75(1):161-79 PMID: 4197337
  8. Genetic regulatory mechanisms in the synthesis of proteins.
    J Mol Biol. 1961 Jun;3:318-56 PMID: 13718526
  9. 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):5036-40 PMID: 1108010
  10. Evidence for a positive regulation of RNA polymerase synthesis in Escherichia coli.
    J Mol Biol. 1975 Oct 5;97(4):621-42 PMID: 1102717
  11. Regulation of ribonucleic acid synthesis in growing bacterial cells. I. Control over the total rate of RNA synthesis.
    J Mol Biol. 1972 Dec 30;72(3):751-64 PMID: 4573847
  12. The influence of mutations upon the synthesis of RNA polymerase subunits in Escherichia coli cells.
    Mol Gen Genet. 1976 Jun 15;145(3):317-26 PMID: 781519
  13. Regulation of RNA polymerase subunit synthesis in Escherichia coli: utilization of DNA-Intercalating drugs as a probe.
    Arch Biochem Biophys. 1977 Sep;183(1):242-9 PMID: 334079
  14. Evidence for a lambda transducing phage carrying the genes for the beta and beta' subunits of Escherichia coli RNA polymerase.
    Mol Gen Genet. 1974;132(3):193-201 PMID: 4607989
  15. Biosynthesis of RNA polymerase in Escherichia coli. III. Identification of intermediates in the assembly of RNA polymerase.
    J Mol Biol. 1975 Aug 5;96(2):257-71 PMID: 1100844
  16. Different effects of rifampicin and streptolydigin on the control of RNA polymerase subunit synthesis in Escherichia coli.
    Mol Gen Genet. 1974;134(2):181-6 PMID: 4617163
  17. Biosynthesis of RNA polymerase in Escherichia coli. IX. Growth-dependent variations in the synthesis rate, content and distribution of RNA polymerase.
    Mol Gen Genet. 1979 Jul 13;174(2):107-16 PMID: 386039
  18. Sequential biosynthesis of the and ' subunits of the DNA-dependent RNA polymerase from Escherichia coli.
    J Mol Biol. 1971 Jul 14;59(1):17-25 PMID: 4934314
  19. Coordination of levels of elongation factors Tu, Ts, and G, and ribosomal protein SI in Escherichia coli.
    J Biochem. 1978 Feb;83(2):453-62 PMID: 344309
  20. Expression of RNA polymerase and ribosome component genes in Escherichia coli mutants having conditionally defective RNA polymerases.
    J Bacteriol. 1979 Jan;137(1):115-23 PMID: 368011
  21. Evidence for a cryptic RNA polymerase activity in DNA-free minicells of Escherichia coli.
    Biochem Biophys Res Commun. 1975 Sep 16;66(2):665-70 PMID: 1101890
  22. Genetic and physical studies of lambda transducing bacteriophage carrying the beta subunit gene of the Escherichia coli ribonucleic acid polymerase.
    J Bacteriol. 1975 Jun;122(3):1247-56 PMID: 1097397
  23. Autorepressor model for control of DNA replication.
    Nat New Biol. 1973 Jan 31;241(109):133-5 PMID: 4573387
  24. Azotobacter vinelandii RNA polymerase. VII. Enzyme transitions during unprimed r[I-C] synthesis.
    Proc Natl Acad Sci U S A. 1969 Feb;62(2):432-7 PMID: 5256222
  25. Nature and self-regulated synthesis of the repressor of the hut operons in Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1971 Jul;68(7):1493-7 PMID: 4934521
  26. Regulation of subunit synthesis of Escherichia coli RNA polymerase.
    Proc Natl Acad Sci U S A. 1973 Sep;70(9):2651-5 PMID: 4126266
  27. Evidence for specific control of RNA polymerase synthesis in Escherichia coli.
    Nat New Biol. 1973 May 2;243(122):6-9 PMID: 17319069
  28. In vivo transcription of E. coli genes coding for rRNA, ribosomal proteins and subunits of RNA polymerase: influence of the stringent control system.
    Mol Gen Genet. 1977 Oct 20;155(2):203-11 PMID: 337129
  29. On the bacterial life sequence.
    Cold Spring Harb Symp Quant Biol. 1968;33:809-22 PMID: 4892010
  30. Regulation of synthesis and activity of a mutant RNA polymerase in Escherichia coli.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5416-20 PMID: 341156
  31. Coordinate and differential in vitro syntheses of two RNA polymerase subunits.
    Nature. 1974 Dec 13;252(5484):596-7 PMID: 4610425
  32. Chromosome replication and the division cycle of Escherichia coli B/r.
    J Mol Biol. 1968 Feb 14;31(3):519-40 PMID: 4866337
  33. The size of transcriptional units for ribosomal proteins in Escherichia coli.
    Mol Gen Genet. 1974 Mar 6;129(1):11-26 PMID: 4600012
  34. Relationships among deoxyribonucleic acid, ribonucleic acid, and specific transfer ribonucleic acids in Escherichia coli 15T - at various growth rates.
    J Bacteriol. 1973 Jul;115(1):177-87 PMID: 4577741
  35. Chromosomal location of a structural gene for the RNA polymerase sigma factor in Escherichia coli.
    Proc Natl Acad Sci U S A. 1977 May;74(5):1831-5 PMID: 325555
  36. Regulatory state of ribosomal genes and physiological changes in the concentration of free ribonucleic acid polymerase in Escherichia coli.
    Biochem J. 1975 Jul;150(1):9-12 PMID: 1106405
  37. Cyclic re-use of the RNA polymerase sigma factor.
    Nature. 1969 May 10;222(5193):537-40 PMID: 5781654
  38. 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):7540-7 PMID: 381287
  39. Cell division and DNA replication following a shift to a richer medium.
    J Mol Biol. 1969 Jul 14;43(1):1-11 PMID: 4897790
  40. Biosynthesis of RNA polymerase in Escherichia coli VI. Distribution of RNA polymerase subunits between nucleoid and cytoplasm.
    J Mol Biol. 1977 Sep 25;115(3):403-16 PMID: 338912
  41. Temperature-sensitive RNA polymerase mutants with altered subunit synthesis and degradation.
    Proc Natl Acad Sci U S A. 1975 Jun;72(6):2375-9 PMID: 1094466
  42. The size of transcriptional units for ribosomal proteins in Escherichia coli. Rates of synthesis of ribosomal proteins during a nuritional shift-up.
    Mol Gen Genet. 1974 May 31;130(3):271-4 PMID: 4602262
  43. Biosynthesis of the beta and beta' subunits of RNA polymerase in Escherichia coli.
    J Mol Biol. 1973 Feb 15;74(1):9-20 PMID: 4581288
  44. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system.
    Gene. 1977;2(2):95-113 PMID: 344137
  45. Translation of the genome of a ribonucleic acid bacteriophage.
    Bacteriol Rev. 1972 Mar;36(1):109-34 PMID: 4555183
  46. Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature.
    J Bacteriol. 1978 Jun;134(3):1133-40 PMID: 149109
  47. 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 Aug;75(8):3891-5 PMID: 358203
  48. Autogenous regulation of RNA polymerase beta subunit synthesis in vitro.
    J Biol Chem. 1978 Jul 10;253(13):4501-4 PMID: 350875
  49. Biosynthesis of RNA polymerase in Escherichia coli. I. Control of RNA polymerase content at various growth rates.
    Mol Gen Genet. 1974;133(1):1-23 PMID: 4214991
  50. Autogenous regulation of gene expression.
    Science. 1974 Mar 1;183(4127):810-6 PMID: 4589900
  51. Control of production of ribosomal protein.
    J Mol Biol. 1967 Jul 14;27(1):41-55 PMID: 5340469
  52. Biosynthesis of RNA polymerase in Escherichia coli. IV. Accumulation of intermediates in mutants defective in the subunit assembly.
    J Mol Biol. 1976 Apr 5;102(2):297-310 PMID: 775104
  53. Differential rate of ribosomal protein synthesis in Escherichia coli B/r.
    J Mol Biol. 1974 Apr 15;84(3):407-22 PMID: 4618855
  54. Biosynthesis of RNA polymerase in Escherichia coli. VII. Regulation of betabeta' operon on lambda transducing phage in assembly-defective mutants.
    Mol Gen Genet. 1978 Sep 20;165(1):7-14 PMID: 362166
  55. Over-synthesis and instability of sigma protein in a merodiploid strain of Escherichia coli.
    Mol Gen Genet. 1978 Feb 7;159(1):89-99 PMID: 345086
  56. Metabolic regulation of aminoacyl-tRNA synthetase formation in bacteria.
    Biochem Biophys Res Commun. 1972 Oct 17;49(2):495-501 PMID: 4565494
  57. Biosynthesis of RNA polymerase in Escherichia coli. V. Defects of the subunit assembly in a temperature-sensitive beta subunit mutant.
    J Mol Biol. 1977 May 5;112(1):65-74 PMID: 328895
  58. Synthesis of RNA polymerase in Escherichia coli B-r growing at different rates.
    J Mol Biol. 1973 Mar 25;75(1):181-4 PMID: 4576590
  59. The effect of gene dosage on the synthesis and stability of RNA polymerase subunits in Escherichia coli.
    Mol Gen Genet. 1974;131(2):173-80 PMID: 4607939
  60. Regulation of ribosomal protein synthesis in Escherichia coli by selective mRNA inactivation.
    Proc Natl Acad Sci U S A. 1979 Jul;76(7):3411-5 PMID: 158759
  61. 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 PMID: 320344
  62. Identification of a single promoter in E. coli for rplJ, rplL and rpoBC.
    Nature. 1978 Nov 2;276(5683):33-7 PMID: 368640
  63. Peptide analysis of RNA polymerase alpha subunit from Escherichia coli: comparison of free with assembled form.
    Mol Gen Genet. 1976 Jun 15;145(3):311-6 PMID: 781518
  64. Altered synthesis and stability of RNA polymerase holoenzyme subunits in mutants of Escherichia coli with mutations in the beta or beta' subunit genes.
    Mol Gen Genet. 1976 Aug 19;147(2):139-43 PMID: 787754
  65. The RNA binding properties of "native" protein-protein complexes isolated from the Escherichia coli ribosome.
    FEBS Lett. 1977 May 15;77(2):295-300 PMID: 324809
Article Info
Journal
Molecular and cellular biochemistry
Abbr.
Mol Cell Biochem
ISSN
0300-8177
Published
1980-08-16
Pages
177-96
Language
English
Region
Netherlands
NLM ID
0364456
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]