E. coli Fis Protein Insulates the cbpA Gene from Uncontrolled Transcription

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Chintakayala, Kiran ^a   Singh, Shivani S ^a   Rossiter, Amanda E ^a   Shahapure, Rajesh ^b   Dame, Remus T ^b   Grainger, David C ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CURVED DNA; CURVED DNA BINDING PROTEIN A; DNA BINDING PROTEIN; FACTOR FOR INVERSION STIMULATION; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; CBPA GENE; CELL GROWTH; CHEMICAL ANALYSIS; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA STRUCTURE; ESCHERICHIA COLI; GENE CONTROL; GENE DISRUPTION; GENE TARGETING; GENETIC ANALYSIS; GENOMICS; NONHUMAN; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION; STEADY STATE; TRANSCRIPTION REGULATION;

CARRIER PROTEINS; CHROMOSOMES, BACTERIAL; DNA, BACTERIAL; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FACTOR FOR INVERSION STIMULATION PROTEIN; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR CHAPERONES; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84873492223     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003152     Document Type: Article

References (43)

1. Dillon SC, Dorman CJ, (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8: 185-195.
2. Dorman CJ, Barr GC, Ni Bhriain N, Higgins CF, (1988) DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol 6: 2816-2826.
3. Sobetzko P, Travers A, Muskhelishvili G, (2012) Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc Natl Acad Sci 109: E42-E50.
4. Azam TA, Iwata A, Nishimura A, Ueda S, Ishihama A, (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181: 6361-6370.
5. Almirón M, Link AJ, Furlong D, Kolter R, (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6: 2646-2654.
6. Wolf SG, Frenkiel D, Arad T, Finkel SE, Kolter R, et al. (1999) DNA protection by stress-induced biocrystallization. Nature 400: 83-85.
7. Calhoun LN, Kwon YM, (2011) Structure, function and regulation of the DNA-binding protein Dps and its role in acid and oxidative stress resistance in Escherichia coli: a review. J Appl Microbiol 110: 375-386.
8. 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.
9. Ueguchi C, Kakeda M, Yamada H, Mizuno T, (1994) An analogue of the DnaJ molecular chaperone in Escherichia coli. Proc Natl Acad Sci 91: 1054-1058.
10. Azam TA, Ishihama A, (1999) Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem 274: 33105-33113.
11. Bird JG, Sharma S, Roshwalb SC, Hoskins JR, Wickner S, (2006) Functional analysis of CbpA, a DnaJ homolog and nucleoid-associated DNA-binding protein. J Biol Chem 281: 34349-34356.
12. Chintakayala K, Grainger DC, (2011) A conserved acidic amino acid mediates the interaction between modulators and co-chaperones in enterobacteria. J Mol Biol 411: 313-320.
13. Chae C, Sharma S, Hoskins JR, Wickner S, (2004) CbpA, a DnaJ homolog, is a DnaK co-chaperone, and its activity is modulated by CbpM. J Biol Chem 279: 33147-33153.
14. Sarraf NS, Baardsnes J, Cheng J, O'Connor-McCourt M, Cygler M, et al. (2010) Structural basis of the regulation of the CbpA co-chaperone by its specific modulator CbpM. J Mol Biol 398: 111-121.
15. Cosgriff S, Chintakayala K, Chim YT, Chen X, Allen S, et al. (2010) Dimerization and DNA-dependent aggregation of the Escherichia coli nucleoid protein and chaperone CbpA. Mol Microbiol 77: 1289-1300.
16. Singh SS, Typas A, Hengge R, Grainger DC, (2011) Escherichia coli σ70 senses sequence and conformation of the promoter spacer region. Nucleic Acids Res 39: 5109-5118.
17. 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.
18. 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.
19. Hengen PN, Bartram SL, Stewart LE, Schneider TD, (1997) Information analysis of Fis binding sites. Nucleic Acids Res 25: 4994-5002.
20. Hirvonen CA, Ross W, Wozniak CE, Marasco E, Anthony JR, et al. (2001) Contributions of UP elements and the transcription factor FIS to expression from the seven rrn P1 promoters in Escherichia coli. J Bacteriol 183: 6305-6314.
21. Shao Y, Feldman-Cohen LS, Osuna R, (2008) Functional characterisation of the Escherichia coli Fis-DNA binding sequence. J Mol Biol 376: 771-785.
22. Grainger DC, Hurd D, Goldberg MD, Busby SJ, (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34: 4642-4652.
23. Cho BK, Knight EM, Barrett CL, Palsson BØ, (2008) Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res 18: 900-910.
24. Kahramanoglou C, Seshasayee AS, Prieto AI, Ibberson D, Schmidt S, et al. (2011) Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res 39: 2073-2091.
25. Attey A, Belyaeva T, Savery N, Hoggett J, Fujita N, et al. (1994) Interactions between the cyclic AMP receptor protein and the alpha subunit of RNA polymerase at the Escherichia coli galactose operon P1 promoter. Nucleic Acids Res 22: 4375-4380.
26. Xu M, Busby SJ, Browning DF, (2009) Activation and repression at the Escherichia coli ynfEFGHI operon promoter. J Bacteriol 191: 3172-3176.
27. Squire DJ, Xu M, Cole JA, Busby SJ, Browning DF, (2009) Competition between NarL-dependent activation and Fis-dependent repression controls expression from the Escherichia coli yeaR and ogt promoters. Biochem J 420: 249-257.
28. Hollands K, Lee DJ, Lloyd GS, Busby SJ, (2010) Activation of sigma 28-dependent transcription in Escherichia coli by the cyclic AMP receptor protein requires an unusual promoter organization. Mol Microbiol 75: 1098-1111.
29. Pedersen AG, Jensen LJ, Brunak S, Staerfeldt HH, Ussery DW, (2000) A DNA structural atlas for Escherichia coli. J Mol Biol 299: 907-930.
30. Conter A, (2003) Plasmid DNA supercoiling and survival in long-term cultures of Escherichia coli: role of NaCl. J Bacteriol 185: 5324-5327.
31. Conter A, Menchon C, Gutierrez C, (1997) Role of DNA supercoiling and rpoS sigma factor in the osmotic and growth phase-dependent induction of the gene osmE of Escherichia coli K12. J Mol Biol 273: 75-83.
32. Yamashino T, Kakeda M, Ueguchi C, Mizuno T, (1994) An analogue of the DnaJ molecular chaperone whose expression is controlled by σS during the stationary phase and phosphate starvation in Escherichia coli. Mol Microbiol 13: 475-483.
33. Dornenburg JE, Devita AM, Palumbo MJ, Wade JT, (2010) Widespread antisense transcription in Escherichia coli. mBio 1 (1):: e00024-10 doi:10.1128/mBio.00024-10.
34. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
35. Kawano M, Storz G, Rao BS, Rosner JL, Martin RG, (2005) Detection of low-level promoter activity within open reading frame sequences of Escherichia coli. Nucleic Acids Res 33: 6268-6276.
36. Ohniwa RL, Morikawa K, Kim J, Ohta T, Ishihama A, et al. (2006) Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J 25: 5591-5602.
37. Miller J (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. Lloyd GS, Hollands K, Godfrey RE, Busby SJ, (2008) Transcription initiation in the Escherichia coli K-12 malI-malX intergenic region and the role of the cyclic AMP receptor protein. FEMS Microbiol Lett 288: 250-7.
39. Kolb A, Kotlarz D, Kusano S, Ishihama A, (1995) Selectivity of the Escherichia coli RNA polymerase E sigma 38 for overlapping promoters and ability to support CRP activation. Nucleic Acids Res 23: 819-826.
40. Grainger DC, Overton TW, Reppas N, Wade JT, Tamai E, et al. (2004) Genomic studies with Escherichia coli MelR protein: applications of chromatin immunoprecipitation and microarrays. J Bacteriol 186: 6938-6943.
41. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J, (2009) DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
42. Shpigelman ES, Trifonov EN, Bolshoy A, (1993) CURVATURE: software for the analysis of curved DNA. Comput Appl Biosci 9: 435-440.
43. 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.