An architectural role of the Escherichia coli chromatin protein FIS in organising DNA.

The Escherichia coli chromatin protein FIS modulates the topology of DNA in a growth phase-dependent manner. In this study we have investigated the global effect of FIS binding on DNA architecture in vitro. We show that in supercoiled DNA molecules FIS binds at multiple sites in a non-random fashion and increases DNA branching. This global DNA reshaping effect is independent of the helical phasing of FIS binding sites. We propose, in addition to the previously inferred stabilisation of tightly bent DNA microloops in the upstream regions of certain promoters, that FIS may perform the distinct architectural function of organising branched plectonemes in the E.coli nucleoid.

[1]  K Rippe,et al.  Action at a distance: DNA-looping and initiation of transcription. , 1995, Trends in biochemical sciences.

[2]  M Frank-Kamenetskii,et al.  Conformational and thermodynamic properties of supercoiled DNA. , 1992, Journal of molecular biology.

[3]  J. Dubochet,et al.  The apical localization of transcribing RNA polymerases on supercoiled DNA prevents their rotation around the template. , 1992, The EMBO journal.

[4]  J. Griffith,et al.  Curved helix segments can uniquely orient the topology of supertwisted DNA , 1988, Cell.

[5]  M. Waring,et al.  Effects of base substitutions on the binding of a DNA-bending protein. , 1995, Journal of molecular biology.

[6]  E. Kellenberger,et al.  The bacterial nucleoid revisited. , 1994, Microbiological reviews.

[7]  A. Minsky,et al.  Liquid-crystalline mesophases of plasmid DNA in bacteria. , 1994, Science.

[8]  E. Bremer,et al.  Synthesis of the Escherichia coli K‐12 nucleoid‐associated DNA‐binding protein H‐NS is subjected to growth‐phase control and autoregulation , 1993, Molecular microbiology.

[9]  A. Travers,et al.  FIS and RNA polymerase holoenzyme form a specific nucleoprotein complex at a stable RNA promoter. , 1995, The EMBO journal.

[10]  A. Travers,et al.  The acidic tail of the high mobility group protein HMG-D modulates the structural selectivity of DNA binding. , 1997, Journal of molecular biology.

[11]  W. Arber,et al.  Mutational analysis of a prokaryotic recombinational enhancer element with two functions. , 1989, The EMBO journal.

[12]  L. Claret,et al.  Regulation of HUα and HUβ by CRP and FIS inEscherichia coli , 1996 .

[13]  R Kahmann,et al.  The E.coli fis promoter is subject to stringent control and autoregulation. , 1992, The EMBO journal.

[14]  B. J. Hinnebusch,et al.  The bacterial nucleoid visualized by fluorescence microscopy of cells lysed within agarose: comparison of Escherichia coli and spirochetes of the genus Borrelia , 1997, Journal of bacteriology.

[15]  N R Cozzarelli,et al.  Structure of plectonemically supercoiled DNA. , 1990, Journal of molecular biology.

[16]  D. Ussery,et al.  The chromatin-associated protein H-NS. , 1994, Biochimie.

[17]  E. Kellenberger,et al.  Coralline shape of the bacterial nucleoid after cryofixation , 1991, Journal of bacteriology.

[18]  D. Ussery,et al.  The chromatin‐associated protein H‐NS alters DNA topology in vitro. , 1994, The EMBO journal.

[19]  T Schlick,et al.  Internal motion of supercoiled DNA: brownian dynamics simulations of site juxtaposition. , 1998, Journal of molecular biology.

[20]  A. Worcel,et al.  On the structure of the folded chromosome of Escherichia coli. , 1972, Journal of molecular biology.

[21]  R. Sinden,et al.  Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Molly B. Schmid,et al.  More than just “Histone-like” proteins , 1990, Cell.

[23]  D. Perkins-Balding,et al.  Location, degree, and direction of DNA bending associated with the Hin recombinational enhancer sequence and Fis-enhancer complex , 1997, Journal of bacteriology.

[24]  H. Hansma,et al.  DNA binding to mica correlates with cationic radius: assay by atomic force microscopy. , 1996, Biophysical journal.

[25]  Akira Ishihama,et al.  Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival , 1999, Genes to cells : devoted to molecular & cellular mechanisms.

[26]  D. Pettijohn.  Bacterial Chromosome Structure , 1990 .

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

[28]  R. C. Johnson,et al.  Variable structures of Fis-DNA complexes determined by flanking DNA-protein contacts. , 1996, Journal of molecular biology.

[29]  R. Kahmann,et al.  Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. , 1986, The Journal of biological chemistry.

[30]  R. Lurz,et al.  13 Electron Microscopic Analysis of Nucleic Acids and Nucleic Acid-Protein Complexes , 1988 .

[31]  Akira Ishihama,et al.  Two types of localization of the DNA‐binding proteins within the Escherichia coli nucleoid , 2000, Genes to cells : devoted to molecular & cellular mechanisms.

[32]  A. Travers,et al.  The Escherichia coli FIS protein is not required for the activation of tyrT transcription on entry into exponential growth. , 1993, The EMBO journal.

[33]  A. Travers,et al.  FIS modulates growth phase‐dependent topological transitions of DNA in Escherichia coli , 1997, Molecular microbiology.

[34]  Annick Spassky,et al.  H1a, an E. coli DNA-binding protein which accumulates in stationary phase, strongly compacts DNA in vitro , 1984, Nucleic Acids Res..

[35]  R. Sinden,et al.  Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: Analogous measurements in insect and human cells , 1980, Cell.

[36]  A. Travers,et al.  Stabilization of DNA Microloops by FIS — A Mechanism for Torsional Transmission in Transcription Activation and DNA Inversion , 1997 .

[37]  S. Halford,et al.  DNA cleavage at two recognition sites by the SfiI restriction endonuclease: salt dependence of cis and trans interactions between distant DNA sites. , 1995, Journal of molecular biology.

[38]  C. Wyman,et al.  H-NS mediated compaction of DNA visualised by atomic force microscopy. , 2000, Nucleic acids research.

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

[40]  D Roberts,et al.  Growth phase variation of integration host factor level in Escherichia coli , 1994, Journal of bacteriology.

[41]  M. Yaniv,et al.  E. coli DNA binding protein HU forms nucleosome-like structure with circular double-stranded DNA , 1979, Cell.

[42]  S. Iida,et al.  Bent DNA is needed for recombinational enhancer activity in the site-specific recombination system Cin of bacteriophage P1. The role of FIS protein. , 1989, Journal of molecular biology.

[43]  C. Siegerist,et al.  Reproducible Imaging and Dissection of Plasmid DNA Under Liquid with the Atomic Force Microscope , 1992, Science.

[44]  M. Bjornsti,et al.  Intracellular location of the histonelike protein HU in Escherichia coli , 1988, Journal of bacteriology.

[45]  P. Stączek,et al.  Gyrase and Topo IV modulate chromosome domain size in vivo , 1998, Molecular microbiology.

[46]  A. Travers,et al.  A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli , 1999, Molecular microbiology.

[47]  Roberto Spurio,et al.  Expression of the gene encoding the major bacterial nucleoid protein H‐NS is subject to transcriptional auto‐repression , 1993, Molecular microbiology.

[48]  R. Wagner,et al.  Conformational changes of the upstream DNA mediated by H-NS and FIS regulate E. coli RrnB P1 promoter activity. , 1999, Journal of molecular biology.

[49]  Paul K. Hansma,et al.  Tapping mode atomic force microscopy in liquids , 1994 .

[50]  D. Pettijohn,et al.  Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. , 1986, Journal of molecular biology.

[51]  S Brunak,et al.  Genome organisation and chromatin structure in Escherichia coli. , 2001, Biochimie.

[52]  A. Travers,et al.  The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA , 2000, Molecular microbiology.