Bacterial DNA topology and infectious disease

The Gram-negative bacterium Escherichia coli and its close relative Salmonella enterica have made important contributions historically to our understanding of how bacteria control DNA supercoiling and of how supercoiling influences gene expression and vice versa. Now they are contributing again by providing examples where changes in DNA supercoiling affect the expression of virulence traits that are important for infectious disease. Available examples encompass both the earliest stages of pathogen–host interactions and the more intimate relationships in which the bacteria invade and proliferate within host cells. A key insight concerns the link between the physiological state of the bacterium and the activity of DNA gyrase, with downstream effects on the expression of genes with promoters that sense changes in DNA supercoiling. Thus the expression of virulence traits by a pathogen can be interpreted partly as a response to its own changing physiology. Knowledge of the molecular connections between physiology, DNA topology and gene expression offers new opportunities to fight infection.

[1]  C. Dorman,et al.  A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. , 2004, Microbiology.

[2]  C. Dorman.  DNA supercoiling and environmental regulation of gene expression in pathogenic bacteria , 1991, Infection and immunity.

[3]  C. Brinton.  Non-Flagellar Appendages of Bacteria , 1959, Nature.

[4]  J. Pinkner,et al.  LeuX tRNA‐dependent and ‐independent mechanisms of Escherichia coli pathogenesis in acute cystitis , 2007, Molecular microbiology.

[5]  Thijs J. G. Ettema,et al.  The Lrp family of transcriptional regulators , 2003, Molecular microbiology.

[6]  A. Travers,et al.  DNA supercoiling and transcription in Escherichia coli: The FIS connection. , 2001, Biochimie.

[7]  J. Galán,et al.  Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling , 1990, Infection and immunity.

[8]  J. Wain,et al.  An H-NS-like Stealth Protein Aids Horizontal DNA Transmission in Bacteria , 2007, Science.

[9]  C. Dorman,et al.  DNA Supercoiling and the Lrp Protein Determine the Directionality of fim Switch DNA Inversion in Escherichia coli K-12 , 2006, Journal of bacteriology.

[10]  M. Porter,et al.  The Shigella virulence gene regulatory cascade: a paradigm of bacterial gene control mechanisms , 1998, Molecular microbiology.

[11]  A. Klier,et al.  Protein A gene expression is regulated by DNA supercoiling which is modified by the ArlS-ArlR two-component system of Staphylococcus aureus. , 2004, Microbiology.

[12]  Ulrich Dobrindt,et al.  Genomic islands in pathogenic and environmental microorganisms , 2004, Nature Reviews Microbiology.

[13]  K. Drlica,et al.  Escherichia coli DNA topoisomerase I mutants: Increased supercoiling is corrected by mutations near gyrase genes , 1982, Cell.

[14]  N. Cozzarelli,et al.  Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. , 1987, Journal of molecular biology.

[15]  J. Abraham,et al.  An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[16]  C. Dorman,et al.  DNA sequence heterogeneity in Fim tyrosine‐integrase recombinase‐binding elements and functional motif asymmetries determine the directionality of the fim genetic switch in Escherichia coli K‐12 , 2007, Molecular microbiology.

[17]  P. Forterre,et al.  Effects of salt and temperature on plasmid topology in the halophilic archaeon Haloferax volcanii , 1994, Journal of bacteriology.

[18]  L. M. Schechter,et al.  The Small Nucleoid-Binding Proteins H-NS, HU, and Fis Affect hilA Expression in Salmonella enterica Serovar Typhimurium , 2003, Infection and Immunity.

[19]  Michael S. Cohen,et al.  Molecular Basis for the Enterocyte Tropism Exhibited bySalmonella typhimurium Type 1 Fimbriae* , 1999, The Journal of Biological Chemistry.

[20]  Mark Rochman,et al.  Promoter protection by a transcription factor acting as a local topological homeostat , 2002, EMBO reports.

[21]  J. Wang,et al.  Interaction between DNA and an Escherichia coli protein omega. , 1971, Journal of molecular biology.

[22]  A. Kolb,et al.  DNA supercoiling contributes to disconnect sigmaS accumulation from sigmaS-dependent transcription in Escherichia coli. , 2003, Molecular microbiology.

[23]  M. Gellert,et al.  Regulation of the genes for E. coli DNA gyrase: Homeostatic control of DNA supercoiling , 1983, Cell.

[24]  M. S. McClain,et al.  Type 1 fimbriation and fimE mutants of Escherichia coli K-12 , 1991, Journal of bacteriology.

[25]  S. McLeod,et al.  The C-terminal domains of the RNA polymerase alpha subunits: contact site with Fis and localization during co-activation with CRP at the Escherichia coli proP P2 promoter. , 2002, Journal of molecular biology.

[26]  H. Ochman,et al.  How Salmonella became a pathogen. , 1997, Trends in microbiology.

[27]  C. Dorman,et al.  Roles for DNA supercoiling and the Fis protein in modulating expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium , 2006, Molecular microbiology.

[28]  C. Dorman,et al.  Hierarchical gene regulators adapt Salmonella enterica to its host milieus. , 2005, International journal of medical microbiology : IJMM.

[29]  J. Galán,et al.  Salmonella interactions with host cells: type III secretion at work. , 2001, Annual review of cell and developmental biology.

[30]  C. Dorman,et al.  The Leucine-Responsive Regulatory Protein, Lrp, Activates Transcription of the fim Operon in Salmonella enterica Serovar Typhimurium via the fimZ Regulatory Gene , 2007, Journal of bacteriology.

[31]  C. Higgins,et al.  DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression , 1988, Journal of bacteriology.

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

[33]  S. Chevalier,et al.  Effects of DNA gyrase inhibitors in Escherichia coli topoisomerase I mutants , 1986, Journal of bacteriology.

[34]  I. Smith,et al.  Non-flagellar filamentous appendages (fimbriae) and haemagglutinating activity in Bacterium coli. , 1955, The Journal of pathology and bacteriology.

[35]  L. Hsieh,et al.  Bacterial DNA supercoiling and [ATP]/[ADP]. Changes associated with a transition to anaerobic growth. , 1991, Journal of molecular biology.

[36]  M. Gellert,et al.  DNA gyrase: an enzyme that introduces superhelical turns into DNA. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[37]  J. Collado-Vides,et al.  Identifying global regulators in transcriptional regulatory networks in bacteria. , 2003, Current opinion in microbiology.

[38]  A. D. de Koning,et al.  Effects of Fis on Escherichia coli gene expression during different growth stages. , 2007, Microbiology.

[39]  C. Dorman,et al.  Regulation of gene expression by histone-like proteins in bacteria. , 2003, Current opinion in genetics & development.

[40]  S. Altuvia,et al.  Differential regulation of Escherichia coli topoisomerase I by Fis , 2007, Molecular microbiology.

[41]  Marcel Geertz,et al.  Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome , 2006, EMBO reports.

[42]  C. Beuzón,et al.  The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system. , 2003, Microbiology.

[43]  J. Oliveros,et al.  Modulation of Horizontally Acquired Genes by the Hha-YdgT Proteins in Salmonella enterica Serovar Typhimurium , 2007, Journal of bacteriology.

[44]  Ian R. Booth,et al.  A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli , 1988, Cell.

[45]  M. Gellert,et al.  Modulation of transcription by DNA supercoiling: a deletion analysis of the Escherichia coli gyrA and gyrB promoters. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[46]  C. Dorman,et al.  The site‐specific recombination system regulating expression of the Type 1 fimbrial subunit gene of Escherichia coli is sensitive to changes in DNA supercoiling , 1994, Molecular microbiology.

[47]  L. Hsieh,et al.  Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock , 1991, Journal of bacteriology.

[48]  Kelly J. Wright,et al.  Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili , 2007, Cellular microbiology.

[49]  C. Dorman,et al.  Characterization of the Detachable Rho-Dependent Transcription Terminator of the fimE Gene in Escherichia coli K-12 , 2005, Journal of bacteriology.

[50]  R. Gourse,et al.  Control of rRNA expression in Escherichia coli. , 2003, Current opinion in microbiology.

[51]  Andrew Travers,et al.  DNA supercoiling — a global transcriptional regulator for enterobacterial growth? , 2005, Nature Reviews Microbiology.

[52]  C. Josenhans,et al.  Flagellar and global gene regulation in Helicobacter pylori modulated by changes in DNA supercoiling. , 2007, International journal of medical microbiology : IJMM.

[53]  K. Drlica,et al.  DNA supercoiling and prokaryotic transcription , 1989, Cell.

[54]  Peter Ruhdal Jensen,et al.  DNA supercoiling in Escherichia coli is under tight and subtle homeostatic control, involving gene-expression and metabolic regulation of both topoisomerase I and DNA gyrase. , 2002, European journal of biochemistry.

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

[56]  J. Rohde,et al.  The Yersinia enterocolitica pYV Virulence Plasmid Contains Multiple Intrinsic DNA Bends Which Melt at 37°C , 1999, Journal of bacteriology.

[57]  R. Sternglanz,et al.  Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes , 1982, Cell.

[58]  C. Dorman.  Dna Supercoiling and Bacterial Gene Expression , 2006, Science progress.

[59]  M. Hensel,et al.  Salmonella Pathogenicity Island 2 , 2000, Molecular microbiology.

[60]  The gyr genes of Salmonella enterica serovar Typhimurium are repressed by the factor for inversion stimulation, Fis , 2003, Molecular Genetics and Genomics.

[61]  C. Dorman,et al.  Expression of the Fis protein is sustained in late‐exponential‐ and stationary‐phase cultures of Salmonella enterica serovar Typhimurium grown in the absence of aeration , 2007, Molecular microbiology.

[62]  J. Gralla,et al.  General stress response signalling: unwrapping transcription complexes by DNA relaxation via the sigma38 C‐terminal domain , 2008, Molecular microbiology.

[63]  Yongping Shao,et al.  Biochemical identification of base and phosphate contacts between Fis and a high-affinity DNA binding site. , 2008, Journal of molecular biology.

[64]  M. S. McClain,et al.  Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli , 1991, Journal of bacteriology.

[65]  C. Dorman,et al.  A Rho‐dependent phase‐variable transcription terminator controls expression of the FimE recombinase in Escherichia coli , 2002, Molecular microbiology.

[66]  J. Wang,et al.  The Escherichia coli supX locus is topA, the structural gene for DNA topoisomerase I. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[67]  S. Falkow,et al.  The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[68]  M. Gellert,et al.  Fusions of the Escherichia coli gyrA and gyrB control regions to the galactokinase gene are inducible by coumermycin treatment , 1987, Journal of bacteriology.

[69]  N. Yamamoto,et al.  Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

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

[71]  J. Pinkner,et al.  Utilization of an Intracellular Bacterial Community Pathway in Klebsiella pneumoniae Urinary Tract Infection and the Effects of FimK on Type 1 Pilus Expression , 2008, Infection and Immunity.

[72]  R. C. Johnson,et al.  The Fis protein: it's not just for DNA inversion anymore , 1992, Molecular microbiology.

[73]  R. Sinden.  DNA Structure and Function , 1994 .

[74]  A. Kolb,et al.  DNA supercoiling contributes to disconnect σS accumulation from σS‐dependent transcription in Escherichia coli , 2003 .