Skip to main content

FIS and Nucleoid Dynamics upon Exit from Lag Phase

  • Chapter
Bacterial Chromatin

Abstract

FIS is perhaps one of the most spectacular members of the small class of bacterial nucleoid-associated proteins. The transient pattern of FIS expression is unique and for no other protein of this class has been the spatial arrangement of multiple DNA binding sites so conspicuously related to function. The importance of the helical arrangement of FIS binding sites is especially obvious in synaptic complexes of DNA invertases and the transcription initiation complexes of stable RNA promoters. It is now apparent, that FIS can bind DNA cooperatively and that variable arrangements of DNA sites in conjunction with a wide range of binding site discrimination underlie the versatility and dynamics of the FIS nucleoprotein complexes. Furthermore, as an integral component of the homeostatic network regulating cellular DNA topology, FIS is so far the only highly abundant nucleoid-associated protein directly implicated in the control of genes coding for major cellular DNA topoisomerases. Nevertheless, the influence of FIS on global nucleoid architecture remains largely unknown. In this article we argue that modulation of DNA supercoil dynamics by FIS upon exit from lag phase facilitates conformational transitions of the nucleoprotein structures organized at two different - local and global - levels of complexity. At each level, the regulatory device involving FIS converts the analog information provided by supercoil dynamics of DNA into digital information uniquely encoded in the regulated gene(s). On this view, the mechanism of transcriptional regulation by topological transitions in the DNA molecule manifests a fractal character.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aiyar SE, McLeod SM, Ross W, Hirvonen CA, Thomas MS, Johnson RC, Gourse RL (2002) Architecture of Fis-activated transcription complexes at the Escherichia coli rrnB P1 and rrnE P1 promoters. J Mol Biol 316:501-516

    Article  CAS  PubMed  Google Scholar 

  • Auner H, Buckle M, Deufel A, Kutateladze T, Lazarus L, Mavathur R, Muskhelishvili G, Pemberton I, Schneider R, Travers A (2003) Mechanism of transcriptional activation by FIS: role of core promoter structure and DNA topology. J Mol Biol 331:331-344

    Article  CAS  PubMed  Google Scholar 

  • Azam TA, Hiraga S, Ishihama A (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5:613-626

    Article  CAS  PubMed  Google Scholar 

  • Bahloul A, Boubrik F, Rouviére-Yaniv J (2001) Roles of Escherichia coli histone-like protein HU in DNA replication: HU-beta suppresses the thermosensitivity of dnaA46ts. Biochimie 83:219-229

    Article  CAS  PubMed  Google Scholar 

  • Balke VL, Gralla JD (1987) Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J Bacteriol 169:4499-4506

    CAS  PubMed  Google Scholar 

  • Ball CA, Johnson RC (1991) Efficient excision of phage lambda from the Escherichia coli chromosome requires the Fis protein. J Bacteriol 173:4027-4031

    CAS  PubMed  Google Scholar 

  • Ball CA, Osuna R, Ferguson KC, Johnson RC (1992) Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol 174:8043-8056

    CAS  PubMed  Google Scholar 

  • Baxter MA, Jones BD (2005) The fimYZ genes regulate Salmonella enterica serovar Typhimurium invasion in addition to type 1 fimbrial expression and bacterial motility. Infect Immun 73:1377-1385

    Article  CAS  PubMed  Google Scholar 

  • Benjamin KR, Abola AP, Kanaar R, Cozzarelli NR (1996) Contributions of supercoiling to Tn3 resolvase and phage Mu Gin site-specific recombination. J Mol Biol 256:50-65

    Article  CAS  PubMed  Google Scholar 

  • Bensaid A, Almeida A, Drlica K, Rouviere-Yaniv J (1996) Cross-talk between topoisomerase I and HU in Escherichia coli. J Mol Biol 256:292-300

    Article  CAS  PubMed  Google Scholar 

  • Bétermier M, Poquet I, Alazard R, Chandler M (1993) Involvement of Escherichia coli FIS protein in maintenance of bacteriophage Mu lysogeny by the repressor: control of early transcription and inhibition of transposition. J Bacteriol 175:3798-3811

    Google Scholar 

  • Bétermier M, Galas DJ, Chandler M (1994) Interaction of Fis protein with DNA: bending and specificity of binding. Biochimie 76:958-967

    Article  PubMed  Google Scholar 

  • Blot N, Mavathur R, Geertz M, Travers A, Muskhelishvili G (2006) Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome. EMBO Rep 7:710-715

    Article  CAS  PubMed  Google Scholar 

  • Bokal AJ 4th, Ross W, Gourse RL (1995) The transcriptional activator protein FIS: DNA interactions and cooperative interactions with RNA polymerase at the Escherichia coli rrnB P1 promoter. J Mol Biol 245:197-207

    Article  CAS  PubMed  Google Scholar 

  • Bokal AJ, Ross W, Gaal T, Johnson RC, Gourse RL (1997) Molecular anatomy of a transcription activation patch: FIS-RNA polymerase interactions at the Escherichia coli rrnB P1 promoter. EMBO J 16:154-162

    Article  CAS  PubMed  Google Scholar 

  • Bowater RP, Chen D, Lilley DM (1994) Modulation of tyrT promoter activity by template supercoiling in vivo. EMBO J 13:5647-5655

    CAS  PubMed  Google Scholar 

  • Bradley MD, Beach MB, de Koning AP, Pratt TS, Osuna R (2007) Effects of Fis on Escherichia coli gene expression during different growth stages. Microbiology 153:2922-2940

    Article  CAS  PubMed  Google Scholar 

  • Browning DF, Cole JA, Busby SJ (2000) Suppression of FNR-dependent transcription activation at the Escherichia coli nir promoter by Fis, IHF and H-NS: modulation of transcription initiation by a complex nucleo-protein assembly. Mol Microbiol 37:1258-1269

    Article  CAS  PubMed  Google Scholar 

  • Browning DF, Cole JA, Busby SJ (2004) Transcription activation by remodelling of a nucleoprotein assembly: the role of NarL at the FNR-dependent Escherichia coli nir promoter. Mol Microbiol 53:203-215

    Article  CAS  PubMed  Google Scholar 

  • Browning DF, Grainger DC, Beatty CM, Wolfe AJ, Cole JA, Busby SJ (2005) Integration of three signals at the Escherichia coli nrf promoter: a role for Fis protein in catabolite repression. Mol Microbiol 57:496-510

    Article  CAS  PubMed  Google Scholar 

  • Browning DF, Cole JA, Busby SJ (2008) Regulation by nucleoid-associated proteins at the Escherichia coli nir operon promoter. J Bacteriol 190:7258-7267

    Article  CAS  PubMed  Google Scholar 

  • Cabrera JE, Jin DJ (2003) The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues. Mol Microbiol 50:1493-1505

    Article  CAS  PubMed  Google Scholar 

  • Chalmers R, Guhathakurta A, Benjamin H, Kleckner N (1998) IHF modulation of Tn10 transposition: sensory transduction of supercoiling status via a proposed protein/DNA molecular spring. Cell 93:897-908

    Article  CAS  PubMed  Google Scholar 

  • Cheung KJ, Badarinarayana V, Selinger DW, Janse D, Church GM (2003) A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res 13:206-215

    Article  CAS  PubMed  Google Scholar 

  • Chodavarapu S, Felczak MM, Yaniv JR, Kaguni JM (2008) Escherichia coli DnaA interacts with HU in initiation at the E. coli replication origin. Mol Microbiol 67:781-792

    Article  CAS  PubMed  Google Scholar 

  • Crisona NJ, Kanaar R, Gonzalez TN, Zechiedrich EL, Klippel A, Cozzarelli NR (1994) Processive recombination by wild-type gin and an enhancer-independent mutant. Insight into the mechanisms of recombination selectivity and strand exchange. J Mol Biol 243:437-457

    Article  CAS  PubMed  Google Scholar 

  • Dame RT (2005) The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol Microbiol 56:858-870

    Article  CAS  PubMed  Google Scholar 

  • Dame RT, Wyman C, Goosen N (2000) H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res 28:3504-3510

    Google Scholar 

  • Deng S, Stein RA, Higgins NP (2005) Organization of supercoil domains and their reorganization by transcription. Mol Microbiol 57:1511-1521

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ (1996) Flexible response: DNA supercoiling, transcription and bacterial adaptation to environmental stress. Trends Microbiol 4:214-216

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ (2004) H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2:391-400

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ, Deighan P (2003) Regulation of gene expression by histone-like proteins in bacteria. Curr Opin Gen Dev 13:179-184

    Article  CAS  Google Scholar 

  • Drew HR, Travers AA (1984) DNA structural variations in the E. coli tyrT promoter. Cell 37:491-502

    Article  CAS  PubMed  Google Scholar 

  • Drlica K (1992) Control of DNA supercoiling. Mol Microbiol 6:425-433

    Article  CAS  PubMed  Google Scholar 

  • Erzberger JP, Mott ML, Berger JM (2006) Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat Struct Mol Biol 13:676-683

    Google Scholar 

  • Espeli O, Mercier R, Boccard F (2008) DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol 68:1418-1427

    Article  CAS  PubMed  Google Scholar 

  • Filutowicz M, Ross W, Wild J, Gourse RL (1992) Involvement of Fis protein in replication of the Escherichia coli chromosome. J Bacteriol 174:398-407

    CAS  PubMed  Google Scholar 

  • Finkel SE, Johnson RC (1993) The Fis protein: its not just for DNA inversion anymore. Mol Microbiol 7:1023-1026

    Article  CAS  PubMed  Google Scholar 

  • Free A, Dorman CJ (1994) Escherichia coli tyrT gene transcription is sensitive to DNA supercoiling in its native chromosomal context: effect of DNA topoisomerase IV overexpression on tyrT promoter function. Mol Microbiol 14:151-161

    Article  CAS  PubMed  Google Scholar 

  • French SL, Miller JR (1989) Transcription mapping of the Escherichia coli chromosome by electron microscopy. J Bacteriol 171:4207-4216

    CAS  PubMed  Google Scholar 

  • Galán B, Manso I, Kolb A, García JL, Prieto MA (2008) The role of FIS protein in the physiological control of the expression of the Escherichia coli meta-hpa operon. Microbiology 154:2151-2160

    Article  PubMed  CAS  Google Scholar 

  • Geertz M, Travers A, Janga SC, Mehandziska S, Shimamoto N, Muskhelishvili G (2009) Coordination of genomic transcription by bacterial RNA polymerase: role of the omega subunit (submitted)

    Google Scholar 

  • Gille H, Egan JB, Roth A, Messer W (1991) The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli. Nucleic Acids Res 19:4167-4172

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Gil G, Kahmann R, Muskhelishvili G (1998) Regulation of crp transcription by oscillation between distinct nucleoprotein complexes. EMBO J 17:2877-2885

    Article  CAS  PubMed  Google Scholar 

  • González-Gil G, Bringmann P, Kahmann R (1996) FIS is a regulator of metabolism in Escherichia coli. Mol Microbiol 22:21-29

    Article  PubMed  Google Scholar 

  • Gosink KK, Ross W, Leirmo S, Osuna R, Finkel SE, Johnson RC, Gourse RL (1993) DNA binding and bending are necessary but not sufficient for Fis-dependent activation of rrnB P1. J Bacteriol 175:1580-1589

    CAS  PubMed  Google Scholar 

  • Grainger DC, Hurd D, Goldberg MD, Busby S (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34:4642-4652

    Article  CAS  PubMed  Google Scholar 

  • Grainger DC, Goldberg MD, Lee DJ, Busby SJ (2008) Selective repression by Fis and H-NS at the Escherichia coli dps promoter. Mol Microbiol 68:1366-1377

    Article  CAS  PubMed  Google Scholar 

  • Green J, Anjum MF, Guest JR (1996) The ndh-binding protein (Nbp) regulates the ndh gene of Escherichia coli in response to growth phase and is identical to Fis. Mol Microbiol 20:1043-1055

    Article  CAS  PubMed  Google Scholar 

  • Haffter P, Bickle TA (1987) Purification and DNA-binding properties of FIS and Cin, two proteins required for the bacteriophage P1 site-specific recombination system, cin. J Mol Biol 198:579-587

    Article  CAS  PubMed  Google Scholar 

  • Hardy CD, Cozzarelli NR (2005) A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol Microbiol 57:1636-1652

    Article  CAS  PubMed  Google Scholar 

  • Hatfield GW, Benham CJ (2002) DNA topology-mediated control of global gene expression in Escherichia coli. Annu Rev Genet 36:175-203

    Article  CAS  PubMed  Google Scholar 

  • Haykinson MJ, Johnson LM, Soong J, Johnson RC (1996) The Hin dimer interface is critical for Fis-mediated activation of the catalytic steps of site-specific DNA inversion. Curr Biol 6:163-177

    Article  CAS  PubMed  Google Scholar 

  • Heichman KA, Johnson RC (1990) The Hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science 249:511-517

    Article  CAS  PubMed  Google Scholar 

  • Hirsch M, Elliott T (2005) Fis regulates transcriptional induction of RpoS in Salmonella enterica. J Bacteriol 187:1568-1580

    Article  CAS  PubMed  Google Scholar 

  • Hsieh LS, Burger RM, Drlica K (1991) Bacterial DNA supercoiling and [ATP]/[ADP]. Changes associated with a transition to anaerobic growth. J Mol Biol 219:443-450

    Article  CAS  PubMed  Google Scholar 

  • Hwang DS, Kornberg A (1992) Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHF. J Biol Chem 267:23083-23086

    CAS  PubMed  Google Scholar 

  • Jackson L, Blake T, Green J (2004) Regulation of ndh expression in Escherichia coli by Fis. Microbiology 150:407-413

    Article  CAS  PubMed  Google Scholar 

  • Jeong KS, Ahn J, Khodursky AB (2004) Spatial patterns of transcriptional activity in the chromosome of Escherichia coli. Genome Biol 5:R86

    Article  PubMed  Google Scholar 

  • Johnson RC, Bruist MF, Simon MI (1986) Host protein requirements for in vitro site-specific DNA inversion. Cell 46:531-539

    Article  CAS  PubMed  Google Scholar 

  • Johnson RC, Glasgow AC, Simon MI (1987) Spatial relationship of the Fis binding sites for Hin recombinational enhancer activity. Nature 329:462-465

    Article  CAS  PubMed  Google Scholar 

  • Kahmann R, Rudt F, Koch C, Mertens G (1985) G inversion in bacteriophage Mu DNA is stimulated by a site within the invertase gene and a host factor. Cell 41:771-780

    Article  CAS  PubMed  Google Scholar 

  • Kanaar R, Klippel A, Shekhtman E, Dungan JM, Kahmann R, Cozzarelli NR (1990) Processive recombination by the phage Mu Gin system: implications for the mechanisms of DNA strand exchange, DNA site alignment, and enhancer action. Cell 62:353-366

    Article  CAS  PubMed  Google Scholar 

  • Karsenti E (2008) Self-organization in cell biology: a brief history. Nat Rev Mol Cell Biol 9:255-262

    Article  CAS  PubMed  Google Scholar 

  • Keane OM, Dorman CJ (2003) The gyr genes of Salmonella enterica serovar Typhimurium are repressed by the factor for inversion stimulation, Fis. Mol Gen Genet 270:56-65

    CAS  Google Scholar 

  • Kelly A, Goldberg MD, Carroll RK, Danino V, Hinton JC, Dorman CJ (2004) A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150:2037-2053

    Article  CAS  PubMed  Google Scholar 

  • Khodursky AB, Zechiedrich EL, Cozzarelli NR (1995) Topoisomerase IV is a target of quinolones in Escherichia coli. Proc Natl Acad Sci USA 92:11801-11805

    Article  CAS  PubMed  Google Scholar 

  • Klippel A, Cloppenborg K, Kahmann R (1988) Isolation and characterization of unusual gin mutants. EMBO J 7:3983-3989

    CAS  PubMed  Google Scholar 

  • Klippel A, Kanaar R, Kahmann R, Cozzarelli NR (1993) Analysis of strand exchange and DNA binding of enhancer-independent Gin recombinase mutants. EMBO J 12:1047-1057

    CAS  PubMed  Google Scholar 

  • Koch C, Kahmann R (1986) Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. J Biol Chem 261:15673-15678

    CAS  PubMed  Google Scholar 

  • Koch C, Ninnemann O, Fuss H, Kahmann R (1991) The N-terminal part of the E.coli DNA binding protein FIS is essential for stimulating site-specific DNA inversion but is not required for specific DNA binding. Nucleic Acids Res 19:5915-5922

    Article  CAS  PubMed  Google Scholar 

  • Kondo T, Mima S, Fukuma N, Sekimizu K, Tsuchiya T, Mizushima T (2000) Suppression of temperature-sensitivity of a dnaA46 mutant by excessive DNA supercoiling. Biochem J 348:375-379

    Article  CAS  PubMed  Google Scholar 

  • Kostrewa D, Granzin J, Koch C, Choe HW, Raghunathan S, Wolf W, Labahn J, Kahmann R, Saenger W (1991) Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature 349:178-180

    Google Scholar 

  • Lang B, Blot N, Bouffartigues E, Buckle M, Geertz M, Gualerzi CO, Mavathur R, Muskhelishvili G, Pon CL, Rimsky S, Stella S, Babu MM, Travers A (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35:6330-6337

    Article  CAS  PubMed  Google Scholar 

  • Lau IF, Filipe SR, Søballe B, Økstad OA, Barre FX, Sherratt DJ (2003) Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol Microbiol 49:731-743

    Article  CAS  PubMed  Google Scholar 

  • Lautier T, Blot N, Muskhelishvili G, Nasser W (2007) Roles for Fis in the growth phase regulation of pectate lyases, essential virulence factors in the phytopathogenic bacterium Erwinia chrysanthemi. Mol Microbiol 66:1491-1505

    CAS  PubMed  Google Scholar 

  • Lavigne M, Kolb A, Buc H (1992) Transcription activation by cAMP receptor protein (CRP) at the Escherichia coli galP1 promoter. Crucial role for the spacing between the CRP binding site and the -10 region. Biochemistry 31:9647-9656

    Article  CAS  PubMed  Google Scholar 

  • Lazarus LR, Travers AA (1993) The Escherichia coli FIS protein is not required for the activation of tyrT transcription on entry into exponential growth. EMBO J 12:2483-2494

    CAS  PubMed  Google Scholar 

  • Lee HJ, Lee SY, Lee H, Lim HM (2001) Effects of dimer interface mutations in Hin recombinase on DNA binding and recombination. Mol Genet Genomics 266:598-607

    Article  CAS  PubMed  Google Scholar 

  • Lim HM, Simon MI (1992) The role of negative supercoiling in Hin-mediated site-specific recombination. J Biol Chem 267:11176-11182

    CAS  PubMed  Google Scholar 

  • Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84:7024-7027

    Article  CAS  PubMed  Google Scholar 

  • Mallik P, Paul BJ, Rutherford ST, Gourse RL, Osuna R (2006) DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli. J Bacteriol 188:5775-5782

    Article  CAS  PubMed  Google Scholar 

  • Margulies C, Kaguni JM (1998) The FIS protein fails to block the binding of DnaA protein to oriC, the Escherichia coli chromosomal origin. Nucleic Acids Res 26:5170-5175

    Google Scholar 

  • Marr C, Geertz M, Hütt MT, Muskhelishvili G (2008) Dissecting the logical types of network control in gene expression profiles. BMC Syst Biol 2:18

    Article  PubMed  CAS  Google Scholar 

  • Maurer S, Fritz J, Muskhelishvili G, Travers A (2006) RNA polymerase and an activator form discrete subcomplexes in a transcription initiation complex. EMBO J 25:3784-3790

    Article  CAS  PubMed  Google Scholar 

  • Maurer S, Fritz J, Muskhelishvili G (2009) A systematic in vitro study of nucleoprotein complexes formed by bacterial nucleoid associated proteins revealing novel types of DNA organization. J Mol Biol 387:1261-1276

    Article  CAS  PubMed  Google Scholar 

  • McClellan JA, Boublíková P, Palecek E, Lilley DMJ (1990) Superhelical torsion in cellular DNA responds directly to environmental and genetic factors. Proc Natl Acad Sci USA 87:8373-8377

    Article  CAS  PubMed  Google Scholar 

  • McLeod SM, Johnson RC (2001) Control of transcription by nucleoid proteins. Curr Opin Microbiol 4:152-159

    Article  CAS  PubMed  Google Scholar 

  • McLeod SM, Xu J, Cramton SE, Gaal T, Gourse RL, Johnson RC (1999) Localization of amino acids required for Fis to function as a class II transcriptional activator at the RpoS-dependent proP P2 promoter. J Mol Biol 294:333-346

    Article  CAS  PubMed  Google Scholar 

  • McLeod SM, Xu J, Johnson RC (2000) Coactivation of the RpoS-dependent proP P2 promoter by fis and cyclic AMP receptor protein. J Bacteriol 182:4180-4187

    Article  CAS  PubMed  Google Scholar 

  • Menzel R, Gellert M (1983) Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell 34:105-113

    Google Scholar 

  • Merickel SK, Johnson RC (2004) Topological analysis of Hin-catalysed DNA recombination in vivo and in vitro. Mol Microbiol 51:1143-1154

    Article  CAS  PubMed  Google Scholar 

  • Merickel SK, Haykinson MJ, Johnson RC (1998) Communication between Hin recombinase and Fis regulatory subunits during coordinate activation of Hin-catalyzed site-specific DNA inversion. Genes Dev 12:2803-2816

    Article  CAS  PubMed  Google Scholar 

  • Merickel SK, Sanders ER, Vazquez-Ibar JL, Johnson RC (2002) Subunit exchange and the role of dimer flexibility in DNA binding by the Fis protein. Biochemistry 41:5788-5798

    Article  CAS  PubMed  Google Scholar 

  • Muskhelishvili G, Travers AA (1997) The stabilization of DNA microloops by FIS - a mechanism for torsional transmission in transcription activation and DNA inversion. In: Eckstein F, Lilley DMJ (eds) Nucleic acids and molecular biology, Springer 11:179-190

    Google Scholar 

  • Muskhelishvili G, Travers A (2003) Transcription factor as a topological homeostat. Front Biosci 8:d279-d285

    Article  CAS  PubMed  Google Scholar 

  • Muskhelishvili G, Travers A (2009) Intrinsic in vivo modulators: negative supercoiling and the constituents of the bacterial nucleoid. In: RNA polymerases as molecular motors. R SC ­publishing, Cambridge, pp 69-95

    Google Scholar 

  • Muskhelishvili G, Travers AA, Heumann H, Kahmann R (1995) FIS and RNA polymerase form a specific nucleoprotein complex at a stable RNA promoter. EMBO J 14:1446-1452

    CAS  PubMed  Google Scholar 

  • Muskhelishvili G, Buckle M, Heumann H, Kahmann R, Travers AA (1997) FIS activates sequential steps during transcription initiation at a stable RNA promoter. EMBO J 16:3655-3665

    Article  CAS  PubMed  Google Scholar 

  • Nanassy OZ, Hughes KT (1998) In vivo identification of intermediate stages of the DNA inversion reaction catalyzed by the Salmonella Hin recombinase. Genetics 149:1649-1663

    CAS  PubMed  Google Scholar 

  • Nasser W, Schneider R, Travers A, Muskhelishvili G (2001) CRP modulates fis transcription by alternate formation of activating and repressing nucleoprotein complexes. J Biol Chem 276:17878-17886

    Article  CAS  PubMed  Google Scholar 

  • Nilsson L, Vanet A, Vijgenboom E, Bosch L (1990) The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J 9:727-734

    CAS  PubMed  Google Scholar 

  • Nilsson L, Verbeek H, Vijgenboom E, van Drunen C, Vanet A, Bosch L (1992a) FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J Bacteriol 174:921-929

    CAS  PubMed  Google Scholar 

  • Nilsson L, Verbeek H, Hoffmann U, Haupt M, Bosch L (1992b) Inactivation of the fis gene leads to reduced growth rate. FEMS Microbiol Lett 78:85-88

    Article  CAS  PubMed  Google Scholar 

  • Ninnemann O, Koch C, Kahmann R (1992) The E.coli fis promoter is subject to stringent control and autoregulation. EMBO J 11:1075-1083

    CAS  PubMed  Google Scholar 

  • Ó Cróinín T, Dorman CJ (2007) 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. Mol Microbiol 66:237-251

    Article  CAS  Google Scholar 

  • Ó Cróinín T, Carroll RK, Kelly A, Dorman CJ (2006) Roles for DNA supercoiling and the Fis protein in modulating expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium. Mol Microbiol 62:869-882

    Article  CAS  Google Scholar 

  • Ohlsen KL, Gralla JD (1992) Interrelated effects of DNA supercoiling, ppGpp, and low salt on melting within the Escherichia coli ribosomal RNA rrnB P1 promoter. Mol Microbiol 6:2243-2251

    Article  CAS  PubMed  Google Scholar 

  • Ohniwa RL, Morikawa K, Kim J, Ohta T, Ishihama A, Wada C, Takeyasu K (2006) Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J 25:5591-5602

    Article  CAS  PubMed  Google Scholar 

  • Oostra BA, van Vliet AJ, Ab G, Gruber M (1981) Enhancement of ribosomal ribonucleic acid synthesis by deoxyribonucleic acid gyrase activity in Escherichia coli. J Bacteriol 148:782-787

    CAS  PubMed  Google Scholar 

  • Opel ML, Aeling KA, Holmes WM, Johnson RC, Benham CJ, Hatfield GW (2004) Activation of transcription initiation from a stable RNA promoter by a Fis protein-mediated DNA structural transmission mechanism. Mol Microbiol 53:665-674

    Article  CAS  PubMed  Google Scholar 

  • Osuna R, Finkel SE, Johnson RC (1991) Identification of two functional regions in Fis: the N-terminus is required to promote Hin-mediated DNA inversion but not lambda excision. EMBO J 10:1593-1603

    CAS  PubMed  Google Scholar 

  • Pan CQ, Finkel SE, Cramton SE, Feng JA, Sigman DS, Johnson RC (1996) Variable structures of Fis-DNA complexes determined by flanking DNA-protein contacts. J Mol Biol 264:675-695

    Article  CAS  PubMed  Google Scholar 

  • Paull TT, Haykinson MJ, Johnson RC (1994) HU and functional analogs in eukaryotes promote Hin invertasome assembly. Biochimie 76:992-1004

    Article  CAS  PubMed  Google Scholar 

  • Pemberton I, Muskhelishvili G, Travers A, Buckle M (2002) FIS modulates the kinetics of successive interactions of RNA polymerase with the core and upstream regions of the E. coli tyrT promoter. J Mol Biol 318:651-663

    Article  CAS  PubMed  Google Scholar 

  • Perkins-Balding D, Dias DP, Glasgow AC (1997) Location, degree and direction of DNA bending associated with the Hin recombinational enhancer sequence and Fis-enhancer complex. J Bacteriol 179:4747-4753

    CAS  PubMed  Google Scholar 

  • Peter BJ, Arsuaga J, Breier AM, Khodursky AB, Brown PO, Cozzarelli NR (2004) Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol 5:R87

    Article  PubMed  Google Scholar 

  • Postow L, Hardy CD, Arsuaga J, Cozzarelli NR (2004) Topological domain structure of the Escherichia coli chromosome. Genes Dev 18:1766-1779

    Article  CAS  PubMed  Google Scholar 

  • Pratt TS, Steiner T, Feldman LS, Walker KA, Osuna R (1997) Deletion analysis of the fis promoter region in Escherichia coli: antagonistic effects of integration host factor and Fis. J Bacteriol 179:6367-6377

    CAS  PubMed  Google Scholar 

  • Rochman M, Aviv M, Glaser G, Muskhelishvili G (2002) Promoter protection by a transcription factor acting as a local topological homeostat. EMBO Rep 3:355-360

    Article  CAS  PubMed  Google Scholar 

  • Rochman M, Blot N, Dyachenko M, Glaser G, Travers A, Muskhelishvili G (2004) Buffering of stable RNA promoter activity against DNA relaxation requires a far upstream sequence. Mol Microbiol 53:143-152

    Article  CAS  PubMed  Google Scholar 

  • Ross W, Thompson JF, Newlands JT, Gourse RL (1990) E. coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J 9:3733-3742

    CAS  PubMed  Google Scholar 

  • Roth A, Urmoneit B, Messer W (1994) Functions of histone-like proteins in the initiation of DNA replication at oriC of Escherichia coli. Biochimie 76:917-923

    Article  CAS  PubMed  Google Scholar 

  • Ryan VT, Grimwade JE, Camara JE, Crooke E, Leonard AC (2004) Escherichia coli prereplication complex assembly is regulated by dynamic interplay among Fis, IHF and DnaA. Mol Microbiol 51:1347-1359

    Article  CAS  PubMed  Google Scholar 

  • Salgado H, Gama-Castro S, Peralta-Gil M, Diaz-Peredo E, Sanchez-Solano F, Santos-Zavaleta A, Martinez-Flores I, Jimenez-Jacinto V, Bonavides-Martinez C, Segura-Salazar J et al (2006) RegulonDB (version 5.0): Escherichia coli K-12 transcriptional regulatory network, operon organization, and growth conditions. Nucleic Acids Res 34:D394-D397

    Article  CAS  PubMed  Google Scholar 

  • Schneider R, Travers AA, Muskhelishvili G (1997) FIS regulates the bacterial growth phase-dependent topological transitions in DNA. Mol Microbiol 26:519-530

    Article  CAS  PubMed  Google Scholar 

  • Schneider R, Travers A, Kutateladze T, Muskhelishvili G (1999) A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol Microbiol 34:953-964

    Article  CAS  PubMed  Google Scholar 

  • Schneider R, Travers A, Muskhelishvili G (2000) The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA. Mol Microbiol 38:167-175

    Article  CAS  PubMed  Google Scholar 

  • Schneider R, Lurz R, Lüder G, Tolksdorf C, Travers A, Muskhelishvili G (2001) An architectural role of the Escherichia coli protein FIS in organising DNA. Nucleic Acids Res 29:5107-5114

    Article  CAS  PubMed  Google Scholar 

  • Shanado Y, Kato JI, Ikeda H (1997) Fis is required for illegitimate recombination during formation of λ bio transducing phage. J Bacteriol 179:4239-4245

    CAS  PubMed  Google Scholar 

  • Shao Y, Feldman-Cohen LS, Osuna R (2008) Functional characterization of the Escherichia coli Fis-DNA binding sequence. J Mol Biol 376:771-785

    Article  CAS  PubMed  Google Scholar 

  • Skarstad K, Baker TA, Kornberg A (1990) Strand separation required for initiation of replication at the chromosomal origin of E.coli is facilitated by a distant RNA-DNA hybrid. EMBO J 9:2341-2348

    CAS  PubMed  Google Scholar 

  • Skoko D, Yoo D, Bai H, Schnurr B, Yan J, McLeod SM, Marko JF, Johnson RC (2006) Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis. J Mol Biol 364:777-798

    Article  CAS  PubMed  Google Scholar 

  • Snoep JL, van der Weijden CC, Andersen HW, Westerhoff HV, Jensen PR (2002) 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. Eur J Biochem 269:1662-1669

    Article  CAS  PubMed  Google Scholar 

  • Stuger R, Woldringh CL, van der Weijden CC, Vischer NO, Bakker BM, van Spanning RJ, Snoep JL, Westerhoff HV (2002) DNA supercoiling by gyrase is linked to nucleoid compaction. Mol Biol Rep 29:79-82

    Article  CAS  PubMed  Google Scholar 

  • Thompson JF, Landy A (1988) Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes. Nucleic Acids Res 16:9687-9705

    Article  CAS  PubMed  Google Scholar 

  • Thompson JF, Moitoso de Vargas L, Koch C, Kahmann R, Landy A (1987) Cellular factors couple recombination with growth phase: characterization of a new component in the lambda site-specific recombination pathway. Cell 50:901-908

    Article  CAS  PubMed  Google Scholar 

  • Travers AA, Muskhelishvili G (1998) DNA microloops and microdomains - a general mechanism for transcription activation by torsional transmission. J Mol Biol 279:1027-1043

    Article  CAS  PubMed  Google Scholar 

  • Travers A, Muskhelishvili G (2005a) DNA supercoiling - a global transcriptional regulator for enterobacterial growth? Nat Rev Microbiol 3:157-169

    Article  CAS  PubMed  Google Scholar 

  • Travers A, Muskhelishvili G (2005b) Bacterial chromatin. Curr Opin Genet Dev 15:507-514

    Article  CAS  PubMed  Google Scholar 

  • Travers A, Muskhelishvili G (2007) A common topology for bacterial and eukaryotic transcription initiation? EMBO Rep 8:147-151

    Article  CAS  PubMed  Google Scholar 

  • Travers A, Schneider R, Muskhelishvili G (2001) DNA supercoiling and transcription in Escherichia coli - the FIS connection. Biochimie 83:213-217

    Article  CAS  PubMed  Google Scholar 

  • Tse-Dinh YC, Qi H, Menzel R (1997) DNA supercoiling and bacterial adaptation: thermotolerance and thermoresistance. Trends Microbiol 5:323-326

    Article  CAS  PubMed  Google Scholar 

  • Ussery D, Larsen TS, Wilkes KT, Friis C, Worning P, Krogh A, Brunak S (2001) Genome organisation and chromatin structure in Escherichia coli. Biochimie 83:201-212

    Article  CAS  PubMed  Google Scholar 

  • Valens M, Penaud S, Rossignol M, Cornet F, Boccard F (2004) Macrodomain organization of the Escherichia coli chromosome. EMBO J 23:4330-4341

    Article  CAS  PubMed  Google Scholar 

  • van Drunen CM, van Zuylen CE, Mentjes J, Goosen, van de Putte P (1993) Inhibition of bacteriophage Mu transposition by Mu repressor and Fis. Mol Microbiol 10:293-298

    Google Scholar 

  • van Workum M, van Dooren SJM, Oldenburg N, Molenaar D, Jensen PR, Snoep JL, Westerhoff HV (1996) DNA supercoiling depends on the phosphorylation potential in Escherichia coli. Mol Microbiol 20:351-360

    Article  PubMed  Google Scholar 

  • Verbeek H, Nilsson L, Baliko G, Bosch L (1990) 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 1050:302-306

    CAS  PubMed  Google Scholar 

  • Verbeek H, Nilsson L, Bosch L (1992) The mechanism of trans-activation of the Escherichia coli operon thrU(tufB) by the protein FIS. A model. Nucleic Acids Res 20:4077-4081

    Article  CAS  PubMed  Google Scholar 

  • von Freiesleben U, Rasmussen KV (1992) The level of supercoiling affects the regulation of DNA replication in Escherichia coli. Res Microbiol 143:655-663

    Article  Google Scholar 

  • Wackwitz B, Bongaerts J, Goodman SD, Unden G (1999) Growth phase-dependent regulation of nuoA-N expression in Escherichia coli K-12 by the Fis protein: upstream binding sites and bioenergetic significance. Mol Gen Genet 262:876-883

    Article  CAS  PubMed  Google Scholar 

  • Walker KA, Mallik P, Pratt TS, Osuna R (2004) The Escherichia coli Fis promoter is regulated by changes in the levels of its transcription initiation nucleotide CTP. J Biol Chem 279:50818-50828

    Article  CAS  PubMed  Google Scholar 

  • Weinstein-Fischer D, Altuvia S (2007) Differential regulation of Escherichia coli topoisomerase I by Fis. Mol Microbiol 63:1131-1144

    Article  CAS  PubMed  Google Scholar 

  • Weinstein-Fischer D, Elgrably-Weiss M, Altuvia S (2000) Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol 35:1413-1420

    Article  CAS  PubMed  Google Scholar 

  • Wold S, Crooke E, Skarstad K (1996) The Escherichia coli Fis protein prevents initiation of DNA replication from oriC in vitro. Nucleic Acids Res 24:3527-3532

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Tyson KL, Cole JA, Busby SJ (1998) Regulation of transcription initiation at the Escherichia coli nir operon promoter: a new mechanism to account for co-dependence on two transcription factors. Mol Microbiol 27:493-505

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Johnson RC (1995a) Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J Bacteriol 177:938-947

    CAS  PubMed  Google Scholar 

  • Xu J, Johnson RC (1995b) Fis activates the RpoS-dependent stationary-phase expression of proP in Escherichia coli. J Bacteriol 177:5222-5231

    CAS  PubMed  Google Scholar 

  • Xu J, Johnson RC (1997) Activation of RpoS-dependent proP P2 transcription by the Fis protein in vitro. J Mol Biol 270:346-359

    Article  CAS  PubMed  Google Scholar 

  • Yuan HS, Finkel SE, Feng JA, Kacsor-Grzeskowiak M, Johnson RC, Dickerson RE (1991) The molecular structure of wild-type and mutant Fis protein: relationship between mutational changes and recombinational enhancer function or DNA binding. Proc Natl Acad Sci USA 88:9558-9562

    Article  CAS  PubMed  Google Scholar 

  • Zacharias M, Göringer HU, Wagner R (1992) Analysis of the Fis-dependent and Fis-independent transcription activation mechanisms of the Escherichia coli ribosomal RNA promoter. Biochemistry 31:2621-2628

    Article  CAS  PubMed  Google Scholar 

  • Zechiedrich EL, Khodursky AB, Cozzarelli NR (1997) Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. Genes Dev 11:2580-2592

    Article  CAS  PubMed  Google Scholar 

  • Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DMJ, Cozzarelli NR (2000) Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem 275:8103-8113

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Georgi Muskhelishvili .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Muskhelishvili, G., Travers, A. (2010). FIS and Nucleoid Dynamics upon Exit from Lag Phase. In: Dame, R.T., Dorman, C.J. (eds) Bacterial Chromatin. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3473-1_14

Download citation

Publish with us

Policies and ethics