Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria.

The sequence of a promoter determines not only the efficiency with which it forms a complex with RNA polymerase, but also the concentration of nucleoside triphosphate (NTP) required for initiating transcription. Escherichia coli ribosomal RNA (rrn P1) promoters require high initiating NTP concentrations for efficient transcription because they form unusually short-lived complexes with RNA polymerase; high initiating NTP concentrations [adenosine or guanosine triphosphate (ATP or GTP), depending on the rrn P1 promoter] are needed to bind to and stabilize the open complex. ATP and GTP concentrations, and therefore rrn P1 promoter activity, increase with growth rate. Because ribosomal RNA transcription determines the rate of ribosome synthesis, the control of ribosomal RNA transcription by NTP concentration provides a molecular explanation for the growth rate-dependent control and homeostatic regulation of ribosome synthesis.

[1]  R. Sousa,et al.  Role of open complex instability in kinetic promoter selection by bacteriophage T7 RNA polymerase. , 1997, Journal of molecular biology.

[2]  C. Turnbough,et al.  Regulation of upp expression in Escherichia coli by UTP-sensitive selection of transcriptional start sites coupled with UTP-dependent reiterative transcription , 1997, Journal of bacteriology.

[3]  R. Losick,et al.  Role of adenosine nucleotides in the regulation of a stress-response transcription factor in Bacillus subtilis. , 1996, Journal of molecular biology.

[4]  R. Gourse,et al.  rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. , 1996, Annual review of microbiology.

[5]  R. Ebright,et al.  DNA-binding determinants of the alpha subunit of RNA polymerase: novel DNA-binding domain architecture. , 1996, Genes & development.

[6]  C. Turnbough,et al.  Regulation of codBA operon expression in Escherichia coli by UTP-dependent reiterative transcription and UTP-sensitive transcriptional start site switching. , 1995, Journal of molecular biology.

[7]  C. Condon,et al.  Control of rRNA transcription in Escherichia coli. , 1995, Microbiological reviews.

[8]  C. Turnbough,et al.  Regulation of pyrBI operon expression in Escherichia coli by UTP-sensitive reiterative RNA synthesis during transcriptional initiation. , 1994, Genes & development.

[9]  S. Cohen,et al.  Isolated P2 rRNA promoters of Escherichia coli are strong promoters that are subject to stringent control. , 1994, Journal of molecular biology.

[10]  R. Ebright,et al.  Domain organization of RNA polymerase α subunit: C-terminal 85 amino acids constitute a domain capable of dimerization and DNA binding , 1994, Cell.

[11]  R. Gourse,et al.  Growth rate-dependent control of the rrnB P1 core promoter in Escherichia coli , 1994, Journal of bacteriology.

[12]  C. Turnbough,et al.  Nucleotide-specific transcriptional pausing in the pyrBI leader region of Escherichia coli K-12. , 1994, The Journal of biological chemistry.

[13]  C. Turnbough,et al.  Effects of transcriptional start site sequence and position on nucleotide-sensitive selection of alternative start sites at the pyrC promoter in Escherichia coli , 1994, Journal of bacteriology.

[14]  V. Emilsson,et al.  Factor for inversion stimulation-dependent growth rate regulation of individual tRNA species in Escherichia coli. , 1994, The Journal of biological chemistry.

[15]  R. Gourse,et al.  Factor independent activation of rrnB P1. An "extended" promoter with an upstream element that dramatically increases promoter strength. , 1994, Journal of molecular biology.

[16]  L. Lindahl,et al.  Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. , 1994, Progress in nucleic acid research and molecular biology.

[17]  R. Gourse,et al.  A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. , 1993, Science.

[18]  C. Condon,et al.  Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. , 1993, The EMBO journal.

[19]  K. Jensen The Escherichia coli K-12 "wild types" W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels , 1993, Journal of bacteriology.

[20]  W. M. Holmes,et al.  In vivo regulatory responses of four Escherichia coli operons which encode leucyl-tRNAs , 1993, Journal of bacteriology.

[21]  J. Greenblatt,et al.  Ribosomal RNA antitermination in vitro: requirement for Nus factors and one or more unidentified cellular components. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Ball,et al.  Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli , 1992, Journal of bacteriology.

[23]  J. Gralla,et al.  Interrelated effects of DNA supercoiling, ppGpp, and low salt on melting within the Escherichia coli ribosomal RNA rrnB P1 promoter , 1992, Molecular microbiology.

[24]  C. Turnbough,et al.  Translational control of pyrC expression mediated by nucleotide-sensitive selection of transcriptional start sites in Escherichia coli , 1992, Journal of bacteriology.

[25]  M. Record,et al.  Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity. Implications for protein-DNA interactions in vivo. , 1991, Journal of molecular biology.

[26]  R. Gourse,et al.  Factor-independent activation of Escherichia coli rRNA transcription. I. Kinetic analysis of the roles of the upstream activator region and supercoiling on transcription of the rrnB P1 promoter in vitro. , 1991, Journal of molecular biology.

[27]  K. Jensen,et al.  An unusual correlation between ppGpp pool size and rate of ribosome synthesis during partial pyrimidine starvation of Escherichia coli , 1991, Journal of bacteriology.

[28]  C. Turnbough,et al.  Characterization of transcriptional initiation from promoters P1 and P2 of the pyrBI operon of Escherichia coli K12. , 1990, The Journal of biological chemistry.

[29]  R. Gourse,et al.  E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. , 1990, The EMBO journal.

[30]  H. Bremer,et al.  Guanosine tetraphosphate (ppGpp) dependence of the growth rate control of rrnB P1 promoter activity in Escherichia coli. , 1990, The Journal of biological chemistry.

[31]  R. Gourse,et al.  Guanosine 3'-diphosphate 5'-diphosphate is not required for growth rate-dependent control of rRNA synthesis in Escherichia coli. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[32]  K. Jensen,et al.  Metabolic growth rate control in Escherichia coli may be a consequence of subsaturation of the macromolecular biosynthetic apparatus with substrates and catalytic components. , 1990, Microbiological reviews.

[33]  R. Gourse Visualization and quantitative analysis of complex formation between E. coli RNA polymerase and an rRNA promoter in vitro. , 1988, Nucleic acids research.

[34]  J R Cole,et al.  Feedback regulation of rRNA synthesis in Escherichia coli. Requirement for initiation factor IF2. , 1987, Journal of molecular biology.

[35]  J. Gralla,et al.  Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli , 1987, Journal of bacteriology.

[36]  F. Neidhardt,et al.  Escherichia Coli and Salmonella: Typhimurium Cellular and Molecular Biology , 1987 .

[37]  R. Gourse,et al.  DNA determinants of rRNA synthesis in E. coli: Growth rate dependent regulation, feedback inhibition, upstream activation, antitermination , 1986, Cell.

[38]  R. Gourse,et al.  Defective antitermination of rRNA transcription and derepression of rRNA and tRNA synthesis in the nusB5 mutant of Escherichia coli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Brosius,et al.  Characterization in vitro of the effect of spacer length on the activity of Escherichia coli RNA polymerase at the TAC promoter. , 1985, The Journal of biological chemistry.

[40]  R. Gourse,et al.  Regulation of the synthesis of ribosomes and ribosomal components. , 1984, Annual review of biochemistry.

[41]  R. Gourse,et al.  Expression of rRNA and tRNA genes in Escherichia coli: Evidence for feedback regulation by products of rRNA operons , 1983, Cell.

[42]  C. Turnbough,et al.  Attenuation control of pyrBI operon expression in Escherichia coli K-12. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[43]  H. Bremer,et al.  Quantitation of guanosine 5',3'-bisdiphosphate in extracts from bacterial cells by ion-pair reverse-phase high-performance liquid chromatography. , 1982, Analytical biochemistry.

[44]  H. Bremer,et al.  Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate , 1982, Journal of bacteriology.

[45]  E. Lund,et al.  Initiation of Escherichia coli ribosomal RNA synthesis in vivo. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. Nomura,et al.  In vivo transcription of rRNA operons in Escherichia coli initiates with purine nucleoside triphosphates at the first promoter and with CTP at the second promoter. , 1979, The Journal of biological chemistry.

[47]  D. E. Johnston,et al.  A steady state assay for the RNA polymerase initiation reaction. , 1978, The Journal of biological chemistry.

[48]  B. Ames,et al.  Transport of antibiotics and metabolite analogs by systems under cyclic AMP control: positive selection of Salmonella typhimurium cya and crp mutants , 1978, Journal of bacteriology.

[49]  H. Bremer,et al.  Rate of ribosomal ribonucleic acid chain elongation in Escherichia coli B/r during chloramphenicol treatment , 1977, Journal of bacteriology.

[50]  A. Travers RNA polymerase specificity and the control of growth , 1976, Nature.

[51]  F. Grummt,et al.  Control of nucleolar RNA synthesis by the intracellular pool sizes of ATP and GTP , 1976, Cell.

[52]  L. R. Finch,et al.  Relationships between intracellular contents of nucleotides and 5-phosphoribosyl 1-pyrophosphate in Escherichia coli. , 1973, European journal of biochemistry.

[53]  E. Lund,et al.  Metabolism of guanosine tetraphosphate in Escherichia coli. , 1972, European journal of biochemistry.

[54]  J. Gallant,et al.  Control of RNA synthesis in Escherichia coli. I. Amino acid dependence of the synthesis of the substrates of RNA polymerase. , 1968, Journal of molecular biology.

[55]  F. Neidhardt,et al.  Properties of a Mutant of Escherichia coli with a Temperature-sensitive Fructose-1,6-Diphosphate Aldolase , 1966, Journal of bacteriology.

[56]  O. Maaløe,et al.  Control of macromolecular synthesis : a study of DNA, RNA, and protein synthesis in bacteria , 1966 .

[57]  O. Maaløe,et al.  EFFECT OF GROWTH RATE ON THE ACID-SOLUBLE NUCLEOTIDE COMPOSITION OF SALMONELLA TYPHIMURIUM. , 1964, Biochimica et biophysica acta.

[58]  J. Franzen,et al.  Comparison of the acid-soluble nucleotides in Escherichia coli at different growth rates. , 1961, The Journal of biological chemistry.

[59]  F. Neidhardt,et al.  Metabolic regulation of RNA synthesis in bacteria. , 1961, Cold Spring Harbor symposia on quantitative biology.

[60]  O. Maaløe,et al.  Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. , 1958, Journal of general microbiology.