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PMID: 7685276 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The Escherichia coli FIS protein is not required for the activation of tyrT transcription on entry into exponential growth.

The EMBO journal ·Vol. 12 ·No. 6 ·1993-06-00 ·Pages 2483-94

Lazarus LR, Travers AA

Abstract

The Escherichia coli DNA bending protein factor for inversion stimulation (FIS), is neither necessary nor responsible for the stimulation of transcription from the wild type promoter for the tyrT operon (encoding a species of tyrosine tRNA) that occurs upon resumption of exponential growth. This conclusion is unexpected given that the regulatory element required for optimal transcription of tyrT contains three binding sites for FIS protein. In addition, it is in apparent conflict with reports from other laboratories which have described FIS-dependent activation of the stable RNA promoters rrnB P1 and thrU(tufB) in vivo. However, tyrT transcription is stimulated in a FIS-dependent manner both in vivo and in vitro when promoter function is impaired by mutation of the promoter itself or by the addition of the polymerase effector guanosine 5'-diphosphate 3'-diphosphate. These conditions, which expose a requirement for activation of stable RNA synthesis by FIS, suggest that FIS serves an adaptive role permitting high levels of stable RNA transcription on nutritional shift-up when RNA polymerase levels are depleted. In principle such a mechanism could confer a significant selective advantage thus accounting for the conservation of FIS binding sites in the regulatory regions of stable RNA promoters.

Related Genes
MeSH Terms
Bacterial Proteins/genetics,metabolism Base Sequence Binding Sites Carrier Proteins/metabolism DNA, Bacterial DNA-Binding Proteins/metabolism Escherichia coli/genetics,growth & development,metabolism Escherichia coli Proteins Factor For Inversion Stimulation Protein Guanosine Tetraphosphate/metabolism Integration Host Factors Molecular Sequence Data Mutation Promoter Regions, Genetic RNA, Bacterial/genetics RNA, Transfer, Amino Acyl/genetics Transcription, Genetic Transcriptional Activation
Chemicals
Bacterial Proteins Carrier Proteins DNA, Bacterial DNA-Binding Proteins Escherichia coli Proteins Factor For Inversion Stimulation Protein Integration Host Factors RNA, Bacterial RNA, Transfer, Amino Acyl integration host factor, E coli Guanosine Tetraphosphate
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lazarus L R
MRC Laboratory of Molecular Biology, Cambridge, UK.
Travers A A
References (72)
72 references, click to expand
  1. Promoter-dependent transcription of tRNAITyr genes using DNA fragments produced by restriction enzymes.
    Proc Natl Acad Sci U S A. 1975 Dec;72(12):4754-8 PMID: 1107999
  2. Two compounds implicated in the function of the RC gene of Escherichia coli.
    Nature. 1969 Mar 1;221(5183):838-41 PMID: 4885263
  3. Stringent control of bacterial transcription.
    Cell. 1985 May;41(1):6-8 PMID: 2581696
  4. Curved helix segments can uniquely orient the topology of supertwisted DNA.
    Cell. 1988 Feb 26;52(4):545-9 PMID: 2830027
  5. Supercoiling response of a bacterial tRNA gene.
    EMBO J. 1985 Feb;4(2):501-7 PMID: 3894008
  6. The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli.
    Nucleic Acids Res. 1991 Aug 11;19(15):4167-72 PMID: 1870971
  7. Both fis-dependent and factor-independent upstream activation of the rrnB P1 promoter are face of the helix dependent.
    Nucleic Acids Res. 1992 Feb 25;20(4):719-26 PMID: 1542568
  8. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo.
    EMBO J. 1990 Nov;9(11):3733-42 PMID: 2209559
  9. Sequence distributions associated with DNA curvature are found upstream of strong E. coli promoters.
    Nucleic Acids Res. 1987 Jan 26;15(2):785-96 PMID: 3547329
  10. Cation transport in Escherichia coli. I. Intracellular Na and K concentrations and net cation movement.
    J Gen Physiol. 1961 Nov;45:355-69 PMID: 13909521
  11. Regulation of the synthesis of ribosomes and ribosomal components.
    Annu Rev Biochem. 1984;53:75-117 PMID: 6206783
  12. In vivo DNA loops in araCBAD: size limits and helical repeat.
    Proc Natl Acad Sci U S A. 1989 Jan;86(2):476-80 PMID: 2643114
  13. Characterization of the guanosine-3'-diphosphate-5'-diphosphate binding site on E. coli RNA polymerase using a photoprobe, 8-azidoguanosine-3'-5'-bisphosphate.
    Biochem Biophys Res Commun. 1987 Feb 13;142(3):964-71 PMID: 3548721
  14. A synthetic tyrosine suppressor tRNA gene with an altered promoter sequence. Its cloning and relative expression in vivo.
    J Biol Chem. 1979 Nov 10;254(21):10803-10 PMID: 387755
  15. Analysis of E. coli promoter sequences.
    Nucleic Acids Res. 1987 Mar 11;15(5):2343-61 PMID: 3550697
  16. A gel electrophoresis method for quantifying the binding of proteins to specific DNA regions: application to components of the Escherichia coli lactose operon regulatory system.
    Nucleic Acids Res. 1981 Jul 10;9(13):3047-60 PMID: 6269071
  17. xerB, an Escherichia coli gene required for plasmid ColE1 site-specific recombination, is identical to pepA, encoding aminopeptidase A, a protein with substantial similarity to bovine lens leucine aminopeptidase.
    EMBO J. 1989 May;8(5):1623-7 PMID: 2670557
  18. The Fis protein: it's not just for DNA inversion anymore.
    Mol Microbiol. 1992 Nov;6(22):3257-65 PMID: 1484481
  19. Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes.
    Nucleic Acids Res. 1988 Oct 25;16(20):9687-705 PMID: 2972993
  20. Guanosine 3'-diphosphate 5'-diphosphate is not required for growth rate-dependent control of rRNA synthesis in Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Jul;87(14):5533-7 PMID: 2196571
  21. Sequence determinants for promoter strength in the leuV operon of Escherichia coli.
    Gene. 1988;63(1):123-34 PMID: 2454871
  22. Sequences upstream of the-35 hexamer of rrnB P1 affect promoter strength and upstream activation.
    Biochim Biophys Acta. 1990 Aug 27;1050(1-3):307-11 PMID: 2119814
  23. The apical localization of transcribing RNA polymerases on supercoiled DNA prevents their rotation around the template.
    EMBO J. 1992 Feb;11(2):667-72 PMID: 1537341
  24. FIS-dependent trans-activation of tRNA and rRNA operons of Escherichia coli.
    Biochim Biophys Acta. 1990 Aug 27;1050(1-3):293-301 PMID: 2145039
  25. Promoter sequence for stringent control of bacterial ribonucleic acid synthesis.
    J Bacteriol. 1980 Feb;141(2):973-6 PMID: 6154042
  26. Modulation of RNA polymerase specificity by ppGpp.
    Mol Gen Genet. 1976 Aug 19;147(2):225-32 PMID: 787760
  27. Conserved features of coordinately regulated E. coli promoters.
    Nucleic Acids Res. 1984 Mar 26;12(6):2605-18 PMID: 6369249
  28. A system to study promoter and terminator signals recognized by Escherichia coli RNA polymerase.
    Gene Amplif Anal. 1981;2:383-415 PMID: 6101056
  29. Potential binding sites of the trans-activator FIS are present upstream of all rRNA operons and of many but not all tRNA operons.
    Biochim Biophys Acta. 1990 Aug 27;1050(1-3):302-6 PMID: 2207159
  30. Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate.
    J Bacteriol. 1982 Sep;151(3):1261-8 PMID: 6179924
  31. Control of bacterial DNA supercoiling.
    Mol Microbiol. 1992 Feb;6(4):425-33 PMID: 1313943
  32. Superhelical torsion in cellular DNA responds directly to environmental and genetic factors.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8373-7 PMID: 2172986
  33. The mechanism of trans-activation of the Escherichia coli operon thrU(tufB) by the protein FIS. A model.
    Nucleic Acids Res. 1992 Aug 11;20(15):4077-81 PMID: 1380692
  34. Mutational analysis of a prokaryotic recombinational enhancer element with two functions.
    EMBO J. 1989 Feb;8(2):577-85 PMID: 2656257
  35. Regulation of ribosome production in Escherichia coli: synthesis and stability of ribosomal RNA and of ribosomal protein messenger RNA at different growth rates.
    J Mol Biol. 1977 Sep 25;115(3):335-54 PMID: 338910
  36. Escherichia coli host factor for site-specific DNA inversion: cloning and characterization of the fis gene.
    Proc Natl Acad Sci U S A. 1988 Jun;85(12):4237-41 PMID: 2837762
  37. Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli.
    EMBO J. 1992 Nov;11(11):4175-85 PMID: 1396599
  38. Isolation of the gene encoding the Hin recombinational enhancer binding protein.
    Proc Natl Acad Sci U S A. 1988 May;85(10):3484-8 PMID: 2835774
  39. Interrelated effects of DNA supercoiling, ppGpp, and low salt on melting within the Escherichia coli ribosomal RNA rrnB P1 promoter.
    Mol Microbiol. 1992 Aug;6(16):2243-51 PMID: 1406265
  40. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees.
    Science. 1991 Aug 30;253(5023):1001-7 PMID: 1653449
  41. Analysis of local helix geometry in three B-DNA decamers and eight dodecamers.
    J Mol Biol. 1991 Jan 5;217(1):201-14 PMID: 1988678
  42. 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.
    J Mol Biol. 1991 Aug 5;220(3):555-68 PMID: 1870123
  43. DNA bending and its relation to nucleosome positioning.
    J Mol Biol. 1985 Dec 20;186(4):773-90 PMID: 3912515
  44. Structure of plectonemically supercoiled DNA.
    J Mol Biol. 1990 Jun 20;213(4):931-51 PMID: 2359128
  45. FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions.
    J Bacteriol. 1992 Feb;174(3):921-9 PMID: 1732224
  46. Bent DNA is needed for recombinational enhancer activity in the site-specific recombination system Cin of bacteriophage P1. The role of FIS protein.
    J Mol Biol. 1989 Feb 5;205(3):493-500 PMID: 2648006
  47. Crystal structure of the factor for inversion stimulation FIS at 2.0 A resolution.
    J Mol Biol. 1992 Jul 5;226(1):209-26 PMID: 1619650
  48. To bend or...?
    Curr Biol. 1991 Jun;1(3):171-3 PMID: 15336157
  49. The role of FIS in trans activation of stable RNA operons of E. coli.
    EMBO J. 1990 Mar;9(3):727-34 PMID: 1690124
  50. Cellular factors couple recombination with growth phase: characterization of a new component in the lambda site-specific recombination pathway.
    Cell. 1987 Sep 11;50(6):901-8 PMID: 2957063
  51. In vivo synthesis of tRNA Tyr 1 and tRNA Tyr 2 : differences in "early" and "late log" E. coli MRE 600.
    Biochem Biophys Res Commun. 1972 Mar 24;46(6):2006-11 PMID: 4553153
  52. Supercoiling response of the lac ps promoter in vitro.
    J Mol Biol. 1985 Aug 20;184(4):587-98 PMID: 3900418
  53. Regulation of bacterial growth, RNA, and protein synthesis.
    Annu Rev Microbiol. 1978;32:393-432 PMID: 360971
  54. Determination of synthesis rate and lifetime of bacterial mRNAs.
    Anal Biochem. 1987 Dec;167(2):245-60 PMID: 2450483
  55. Fis binding to the recombinational enhancer of the Hin DNA inversion system.
    Genes Dev. 1987 Oct;1(8):762-72 PMID: 2828170
  56. Requirement for an upstream element for optimal transcription of a bacterial tRNA gene.
    Nature. 1983 Sep 15-21;305(5931):248-50 PMID: 6350894
  57. Promoter mutations in the transfer RNA gene tyrT of Escherichia coli.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4303-7 PMID: 116232
  58. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli.
    J Bacteriol. 1992 Dec;174(24):8043-56 PMID: 1459953
  59. Visualization and quantitative analysis of complex formation between E. coli RNA polymerase and an rRNA promoter in vitro.
    Nucleic Acids Res. 1988 Oct 25;16(20):9789-809 PMID: 3054811
  60. G inversion in bacteriophage Mu DNA is stimulated by a site within the invertase gene and a host factor.
    Cell. 1985 Jul;41(3):771-80 PMID: 3159478
  61. All three elements of the lac ps promoter mediate its transcriptional response to DNA supercoiling.
    J Mol Biol. 1987 May 5;195(1):89-97 PMID: 3309333
  62. FIS-induced bending of a region upstream of the promoter activates transcription of the E coli thrU(tufB) operon.
    Biochimie. 1991 Jun;73(6):713-8 PMID: 1764517
  63. Transcription from efficient promoters can interfere with plasmid replication and diminish expression of plasmid specified genes.
    EMBO J. 1982;1(11):1399-404 PMID: 6327267
  64. Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp recombinational enhancer.
    Cell. 1985 Jul;41(3):781-91 PMID: 2988787
  65. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  66. Genetically separable functional elements mediate the optimal expression and stringent regulation of a bacterial tRNA gene.
    Cell. 1985 Feb;40(2):319-26 PMID: 3881184
  67. The E.coli fis promoter is subject to stringent control and autoregulation.
    EMBO J. 1992 Mar;11(3):1075-83 PMID: 1547773
  68. A tRNATyr promoter with an altered in vitro response to ppgpp.
    J Mol Biol. 1980 Jul 25;141(1):91-7 PMID: 6159476
  69. The nucleotide sequence of tufB and four nearby tRNA structural genes of Escherichia coli.
    Gene. 1980 Dec;12(1-2):33-9 PMID: 7011904
  70. Equilibria and kinetics of lac repressor-operator interactions by polyacrylamide gel electrophoresis.
    Nucleic Acids Res. 1981 Dec 11;9(23):6505-25 PMID: 6275366
  71. DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination.
    Cell. 1986 Jan 17;44(1):197-205 PMID: 2416474
  72. Transcription of the tRNA-tufB operon of Escherichia coli: activation, termination and antitermination.
    Nucleic Acids Res. 1987 Nov 25;15(22):9515-30 PMID: 3317280
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1993-06-00
Pages
2483-94
Language
English
Region
England
NLM ID
8208664
PMCID
PMC413486
Subset
IM
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