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. 1991 Aug 11;19(15):4167–4172. doi: 10.1093/nar/19.15.4167

The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli.

H Gille 1, J B Egan 1, A Roth 1, W Messer 1
PMCID: PMC328557  PMID: 1870971

Abstract

The FIS protein (factor for inversion stimulation) is known to stimulate site-specific recombination processes, such as the inversion of the G segment of bacteriophage Mu, by binding to specific enhancer sequences. It has also been shown to activate transcription from rRNA promoters both in vitro and in vivo. We have identified a specific binding site for FIS in the center of the origin of chromosomal DNA replication, oriC. The DNA bends upon FIS binding. Occupation of the FIS site and binding of DnaA, the initiator protein, to its adjacent binding site (R3) are mutually exclusive. A fis mutant strain can not be efficiently transformed with plasmids which carry and replicate from oriC, suggesting that FIS is required for minichromosome replication.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bramhill D., Kornberg A. Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell. 1988 Mar 11;52(5):743–755. doi: 10.1016/0092-8674(88)90412-6. [DOI] [PubMed] [Google Scholar]
  2. Bruist M. F., Glasgow A. C., Johnson R. C., Simon M. I. Fis binding to the recombinational enhancer of the Hin DNA inversion system. Genes Dev. 1987 Oct;1(8):762–772. doi: 10.1101/gad.1.8.762. [DOI] [PubMed] [Google Scholar]
  3. Donachie W. D. Relationship between cell size and time of initiation of DNA replication. Nature. 1968 Sep 7;219(5158):1077–1079. doi: 10.1038/2191077a0. [DOI] [PubMed] [Google Scholar]
  4. Filutowicz M., Roll J. The requirement of IHF protein for extrachromosomal replication of the Escherichia coli oriC in a mutant deficient in DNA polymerase I activity. New Biol. 1990 Sep;2(9):818–827. [PubMed] [Google Scholar]
  5. Fuller R. S., Kaguni J. M., Kornberg A. Enzymatic replication of the origin of the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7370–7374. doi: 10.1073/pnas.78.12.7370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Galas D. J., Schmitz A. DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 1978 Sep;5(9):3157–3170. doi: 10.1093/nar/5.9.3157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gille H., Messer W. Localized DNA melting and structural pertubations in the origin of replication, oriC, of Escherichia coli in vitro and in vivo. EMBO J. 1991 Jun;10(6):1579–1584. doi: 10.1002/j.1460-2075.1991.tb07678.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hughes P., Squali-Houssaini F., Forterre P., Kohiyama M. In vitro replication of a dam methylated and non-methylated ori-C plasmid. J Mol Biol. 1984 Jun 15;176(1):155–159. doi: 10.1016/0022-2836(84)90386-3. [DOI] [PubMed] [Google Scholar]
  9. Hwang D. S., Kornberg A. A novel protein binds a key origin sequence to block replication of an E. coli minichromosome. Cell. 1990 Oct 19;63(2):325–331. doi: 10.1016/0092-8674(90)90165-b. [DOI] [PubMed] [Google Scholar]
  10. Hübner P., Arber W. Mutational analysis of a prokaryotic recombinational enhancer element with two functions. EMBO J. 1989 Feb;8(2):577–585. doi: 10.1002/j.1460-2075.1989.tb03412.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hübner P., Haffter P., Iida S., Arber W. Bent DNA is needed for recombinational enhancer activity in the site-specific recombination system Cin of bacteriophage P1. The role of FIS protein. J Mol Biol. 1989 Feb 5;205(3):493–500. doi: 10.1016/0022-2836(89)90220-9. [DOI] [PubMed] [Google Scholar]
  12. Johnson R. C., Simon M. I. Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp recombinational enhancer. Cell. 1985 Jul;41(3):781–791. doi: 10.1016/s0092-8674(85)80059-3. [DOI] [PubMed] [Google Scholar]
  13. Kahmann R., Rudt F., Koch C., Mertens G. G inversion in bacteriophage Mu DNA is stimulated by a site within the invertase gene and a host factor. Cell. 1985 Jul;41(3):771–780. doi: 10.1016/s0092-8674(85)80058-1. [DOI] [PubMed] [Google Scholar]
  14. Kanaar R., van de Putte P., Cozzarelli N. R. Gin-mediated DNA inversion: product structure and the mechanism of strand exchange. Proc Natl Acad Sci U S A. 1988 Feb;85(3):752–756. doi: 10.1073/pnas.85.3.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kim J., Zwieb C., Wu C., Adhya S. Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector. Gene. 1989 Dec 21;85(1):15–23. doi: 10.1016/0378-1119(89)90459-9. [DOI] [PubMed] [Google Scholar]
  16. Kimura T., Asai T., Imai M., Takanami M. Methylation strongly enhances DNA bending in the replication origin region of the Escherichia coli chromosome. Mol Gen Genet. 1989 Oct;219(1-2):69–74. doi: 10.1007/BF00261159. [DOI] [PubMed] [Google Scholar]
  17. Koch C., Kahmann R. Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. J Biol Chem. 1986 Nov 25;261(33):15673–15678. [PubMed] [Google Scholar]
  18. Koch C., Vandekerckhove J., Kahmann R. Escherichia coli host factor for site-specific DNA inversion: cloning and characterization of the fis gene. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4237–4241. doi: 10.1073/pnas.85.12.4237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kostrewa D., Granzin J., Koch C., Choe H. W., Raghunathan S., Wolf W., Labahn J., Kahmann R., Saenger W. Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature. 1991 Jan 10;349(6305):178–180. doi: 10.1038/349178a0. [DOI] [PubMed] [Google Scholar]
  20. Landy A. Dynamic, structural, and regulatory aspects of lambda site-specific recombination. Annu Rev Biochem. 1989;58:913–949. doi: 10.1146/annurev.bi.58.070189.004405. [DOI] [PubMed] [Google Scholar]
  21. Lother H., Kölling R., Kücherer C., Schauzu M. dnaA protein-regulated transcription: effects on the in vitro replication of Escherichia coli minichromosomes. EMBO J. 1985 Feb;4(2):555–560. doi: 10.1002/j.1460-2075.1985.tb03664.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Løbner-Olesen A., Skarstad K., Hansen F. G., von Meyenburg K., Boye E. The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell. 1989 Jun 2;57(5):881–889. doi: 10.1016/0092-8674(89)90802-7. [DOI] [PubMed] [Google Scholar]
  23. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  24. Messer W., Bellekes U., Lother H. Effect of dam methylation on the activity of the E. coli replication origin, oriC. EMBO J. 1985 May;4(5):1327–1332. doi: 10.1002/j.1460-2075.1985.tb03780.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Messer W., Egan B., Gille H., Holz A., Schaefer C., Woelker B. The complex of oriC DNA with the DnaA initiator protein. Res Microbiol. 1991 Feb-Apr;142(2-3):119–125. doi: 10.1016/0923-2508(91)90018-6. [DOI] [PubMed] [Google Scholar]
  26. Messer W., Meijer M., Bergmans H. E., Hansen F. G., von Meyenburg K., Beck E., Schaller H. Origin of replication, oriC, of the Escherichia coli K12 chromosome: nucleotide sequence. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):139–145. doi: 10.1101/sqb.1979.043.01.020. [DOI] [PubMed] [Google Scholar]
  27. Nilsson L., Vanet A., Vijgenboom E., Bosch L. The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J. 1990 Mar;9(3):727–734. doi: 10.1002/j.1460-2075.1990.tb08166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Polaczek P. Bending of the origin of replication of E. coli by binding of IHF at a specific site. New Biol. 1990 Mar;2(3):265–271. [PubMed] [Google Scholar]
  29. Quiñones A., Jüterbock W. R., Messer W. Expression of the dnaA gene of Escherichia coli is inducible by DNA damage. Mol Gen Genet. 1991 May;227(1):9–16. doi: 10.1007/BF00260699. [DOI] [PubMed] [Google Scholar]
  30. Ramstein J., Lavery R. Energetic coupling between DNA bending and base pair opening. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7231–7235. doi: 10.1073/pnas.85.19.7231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ross W., Thompson J. F., Newlands J. T., Gourse R. L. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J. 1990 Nov;9(11):3733–3742. doi: 10.1002/j.1460-2075.1990.tb07586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Russell D. W., Zinder N. D. Hemimethylation prevents DNA replication in E. coli. Cell. 1987 Sep 25;50(7):1071–1079. doi: 10.1016/0092-8674(87)90173-5. [DOI] [PubMed] [Google Scholar]
  33. Samitt C. E., Hansen F. G., Miller J. F., Schaechter M. In vivo studies of DnaA binding to the origin of replication of Escherichia coli. EMBO J. 1989 Mar;8(3):989–993. doi: 10.1002/j.1460-2075.1989.tb03462.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schmid M. B. More than just "histone-like" proteins. Cell. 1990 Nov 2;63(3):451–453. doi: 10.1016/0092-8674(90)90438-k. [DOI] [PubMed] [Google Scholar]
  35. Sekimizu K., Yung B. Y., Kornberg A. The dnaA protein of Escherichia coli. Abundance, improved purification, and membrane binding. J Biol Chem. 1988 May 25;263(15):7136–7140. [PubMed] [Google Scholar]
  36. Smith D. W., Garland A. M., Herman G., Enns R. E., Baker T. A., Zyskind J. W. Importance of state of methylation of oriC GATC sites in initiation of DNA replication in Escherichia coli. EMBO J. 1985 May;4(5):1319–1326. doi: 10.1002/j.1460-2075.1985.tb03779.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thompson J. F., Landy A. Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes. Nucleic Acids Res. 1988 Oct 25;16(20):9687–9705. doi: 10.1093/nar/16.20.9687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thompson J. F., Moitoso de Vargas L., Koch C., Kahmann R., Landy A. Cellular factors couple recombination with growth phase: characterization of a new component in the lambda site-specific recombination pathway. Cell. 1987 Sep 11;50(6):901–908. doi: 10.1016/0092-8674(87)90516-2. [DOI] [PubMed] [Google Scholar]
  39. Wu H. M., Crothers D. M. The locus of sequence-directed and protein-induced DNA bending. Nature. 1984 Apr 5;308(5959):509–513. doi: 10.1038/308509a0. [DOI] [PubMed] [Google Scholar]

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