Activation of transcription initiation from a stable RNA promoter by a Fis protein‐mediated DNA structural transmission mechanism

The leuV operon of Escherichia coli encodes three of the four genes for the tRNA1Leu isoacceptors. Transcription from this and other stable RNA promoters is known to be affected by a cis‐acting UP element and by Fis protein interactions with the carboxyl‐terminal domain of the α‐subunits of RNA polymerase. In this report, we suggest that transcription from the leuV promoter also is activated by a Fis‐mediated, DNA supercoiling‐dependent mechanism similar to the IHF‐mediated mechanism described previously for the ilvPG promoter (S. D. Sheridan et al., 1998, J Biol Chem 273: 21298–21308). We present evidence that Fis binding results in the translocation of superhelical energy from the promoter‐distal portion of a supercoiling‐induced DNA duplex destabilized (SIDD) region to the promoter‐proximal portion of the leuV promoter that is unwound within the open complex. A mutant Fis protein, which is defective in contacting the carboxyl‐terminal domain of the α‐subunits of RNA polymerase, remains competent for stimulating open complex formation, suggesting that this DNA supercoiling‐dependent component of Fis‐mediated activation occurs in the absence of specific protein interactions between Fis and RNA polymerase. Fis‐mediated translocation of superhelical energy from upstream binding sites to the promoter region may be a general feature of Fis‐mediated activation of transcription at stable RNA promoters, which often contain A+T‐rich upstream sequences.

[1]  P. Sander,et al.  Mechanisms of upstream activation of the rrnD promoter P1 of Escherichia coli. , 1993, The Journal of biological chemistry.

[2]  R. Gourse,et al.  The transcriptional activator protein FIS: DNA interactions and cooperative interactions with RNA polymerase at the Escherichia coli rrnB P1 promoter. , 1995, Journal of molecular biology.

[3]  A. Travers,et al.  DNA microloops and microdomains: a general mechanism for transcription activation by torsional transmission. , 1998, Journal of molecular biology.

[4]  C. Squires,et al.  Antitermination of E. coli rRNA transcription is caused by a control region segment containing lambda nut-like sequences , 1984, Cell.

[5]  W. Keller.  Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. W. Hatfield,et al.  Effects of Integration Host Factor and DNA Supercoiling on Transcription from the ilvPG Promoter of Escherichia coli* , 1996, The Journal of Biological Chemistry.

[7]  G W Hatfield,et al.  DNA supercoiling‐dependent transcriptional coupling between the divergently transcribed promoters of the ilvYC operon of Escherichia coli is proportional to promoter strengths and transcript lengths , 2001, Molecular microbiology.

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

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

[10]  Malcolm Buckle,et al.  Mechanism of transcriptional activation by FIS: role of core promoter structure and DNA topology. , 2003, Journal of molecular biology.

[11]  R. Gourse,et al.  Identification of an UP element consensus sequence for bacterial promoters. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  M. Cashel,et al.  The stringent response , 1996 .

[13]  M. Buckle,et al.  The G+C-rich discriminator region of the tyrT promoter antagonises the formation of stable preinitiation complexes. , 2000, Journal of molecular biology.

[14]  L. Chao,et al.  OF ESCHERICHIA COLI , 1983 .

[15]  M. Zacharias,et al.  Analysis of the Fis-dependent and Fis-independent transcription activation mechanisms of the Escherichia coli ribosomal RNA P1 promoter. , 1992, Biochemistry.

[16]  Dmitry Pokholok,et al.  Multiple Mechanisms Are Used for Growth Rate and Stringent Control of leuV Transcriptional Initiation inEscherichia coli , 1999, Journal of bacteriology.

[17]  R. Planta.  Regulation of ribosome synthesis in yeast , 1997, Yeast.

[18]  L. Bosch,et al.  FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions , 1992, Journal of bacteriology.

[19]  R. C. Johnson,et al.  Localization of amino acids required for Fis to function as a class II transcriptional activator at the RpoS-dependent proP P2 promoter. , 1999, Journal of molecular biology.

[20]  C. Turnbough,et al.  Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. , 1997, Science.

[21]  R. C. Johnson,et al.  DNA binding and bending are necessary but not sufficient for Fis-dependent activation of rrnB P1 , 1993, Journal of bacteriology.

[22]  S. Ueda,et al.  Growth Phase-Dependent Variation in Protein Composition of the Escherichia coli Nucleoid , 1999, Journal of bacteriology.

[23]  D. Natale,et al.  Stable DNA unwinding, not "breathing," accounts for single-strand-specific nuclease hypersensitivity of specific A+T-rich sequences. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Gourse,et al.  Molecular anatomy of a transcription activation patch: FIS–RNA polymerase interactions at the Escherichia coli rrnB P1 promoter , 1997, The EMBO journal.

[25]  R. Wells,et al.  The facile generation of covalently closed, circular DNAs with defined negative superhelical densities. , 1982, Analytical biochemistry.

[26]  C. Benham,et al.  Sites of predicted stress-induced DNA duplex destabilization occur preferentially at regulatory loci. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J. Gralla,et al.  Melting during steady-state transcription of the rrnB P1 promoter in vivo and in vitro , 1992, Journal of bacteriology.

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

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

[30]  A. Ishihama,et al.  Promoter selectivity of Escherichia coli RNA polymerase. Differential stringent control of the multiple promoters from ribosomal RNA and protein operons. , 1984, The Journal of biological chemistry.

[31]  Craig J. Benham,et al.  Activation of Gene Expression by a Novel DNA Structural Transmission Mechanism That Requires Supercoiling-induced DNA Duplex Destabilization in an Upstream Activating Sequence* , 1998, The Journal of Biological Chemistry.

[32]  R. Gourse,et al.  Activation of Escherichia coli rRNA Transcription by FIS during a Growth Cycle , 1998, Journal of bacteriology.

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

[34]  G. W. Hatfield,et al.  DNA topology-mediated control of global gene expression in Escherichia coli. , 2002, Annual review of genetics.

[35]  C. Benham,et al.  Energetics of the strand separation transition in superhelical DNA. , 1992, Journal of molecular biology.

[36]  M. Buckle,et al.  FIS activates sequential steps during transcription initiation at a stable RNA promoter , 1997, The EMBO journal.

[37]  R. Gourse,et al.  Regulation of rRNA Transcription Is Remarkably Robust: FIS Compensates for Altered Nucleoside Triphosphate Sensing by Mutant RNA Polymerases at Escherichia coli rrn P1 Promoters , 2000, Journal of bacteriology.

[38]  A. Travers,et al.  Transcription factor as a topological homeostat. , 2003, Frontiers in bioscience : a journal and virtual library.

[39]  M. Zacharias,et al.  Analysis of sequence elements important for the synthesis and control of ribosomal RNA in E coli. , 1991, Biochimie.

[40]  G. W. Hatfield,et al.  Transcriptional activation by protein-induced DNA bending: evidence for a DNA structural transmission model. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. Gourse,et al.  Activation of Escherichia coli leuVTranscription by FIS , 1999, Journal of bacteriology.

[42]  R. Gourse,et al.  Both fis-dependent and factor-independent upstream activation of the rrnB P1 promoter are face of the helix dependent. , 1992, Nucleic acids research.

[43]  G W Hatfield,et al.  Inhibition of DNA Supercoiling-dependent Transcriptional Activation by a Distant B-DNA to Z-DNA Transition* , 1999, The Journal of Biological Chemistry.

[44]  R. Gourse,et al.  Regulation of rRNA Transcription Correlates with Nucleoside Triphosphate Sensing , 2001, Journal of bacteriology.

[45]  Reid C. Johnson,et al.  Fis Stabilizes the Interaction between RNA Polymerase and the Ribosomal Promoter rrnB P1, Leading to Transcriptional Activation* , 2003, Journal of Biological Chemistry.