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. 1992 Jan;174(2):398–407. doi: 10.1128/jb.174.2.398-407.1992

Involvement of Fis protein in replication of the Escherichia coli chromosome.

M Filutowicz 1, W Ross 1, J Wild 1, R L Gourse 1
PMCID: PMC205730  PMID: 1309527

Abstract

We report evidence indicating that Fis protein plays a role in initiation of replication at oriC in vivo. At high temperatures, fis null mutants form filamentous cells, show aberrant nucleoid segregation, and are unable to form single colonies. DNA synthesis is inhibited in these fis mutant strains following upshift to 44 degrees C. The pattern of DNA synthesis inhibition upon temperature upshift and the requirement for RNA synthesis, but not protein synthesis, for resumed DNA synthesis upon downshift to 32 degrees C indicate that synthesis is affected in the initiation phase. fis mutations act synergistically with gyrB alleles known to affect initiation. oriC-dependent plasmids are poorly established and maintained in fis mutant strains. Finally, purified Fis protein interacts in vitro with sites in oriC. These interactions could be involved in mediating the effect of Fis on DNA synthesis in vivo.

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Selected References

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  1. Baker T. A., Kornberg A. Transcriptional activation of initiation of replication from the E. coli chromosomal origin: an RNA-DNA hybrid near oriC. Cell. 1988 Oct 7;55(1):113–123. doi: 10.1016/0092-8674(88)90014-1. [DOI] [PubMed] [Google Scholar]
  2. Balke V. L., Gralla J. D. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J Bacteriol. 1987 Oct;169(10):4499–4506. doi: 10.1128/jb.169.10.4499-4506.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernander R., Dasgupta S., Nordström K. The E. coli cell cycle and the plasmid R1 replication cycle in the absence of the DnaA protein. Cell. 1991 Mar 22;64(6):1145–1153. doi: 10.1016/0092-8674(91)90269-5. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Dixon N. E., Kornberg A. Protein HU in the enzymatic replication of the chromosomal origin of Escherichia coli. Proc Natl Acad Sci U S A. 1984 Jan;81(2):424–428. doi: 10.1073/pnas.81.2.424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dorman C. J., Barr G. C., Ni Bhriain N., Higgins C. F. DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol. 1988 Jun;170(6):2816–2826. doi: 10.1128/jb.170.6.2816-2826.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Drlica K., Rouviere-Yaniv J. Histonelike proteins of bacteria. Microbiol Rev. 1987 Sep;51(3):301–319. doi: 10.1128/mr.51.3.301-319.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fayet O., Louarn J. M., Georgopoulos C. Suppression of the Escherichia coli dnaA46 mutation by amplification of the groES and groEL genes. Mol Gen Genet. 1986 Mar;202(3):435–445. doi: 10.1007/BF00333274. [DOI] [PubMed] [Google Scholar]
  10. Filutowicz M., Jonczyk P. Essential role of the gyrB gene product in the transcriptional event coupled to dnaA-dependent initiation of Escherichia coli chromosome replication. Mol Gen Genet. 1981;183(1):134–138. doi: 10.1007/BF00270151. [DOI] [PubMed] [Google Scholar]
  11. Filutowicz M. Requirement of DNA gyrase for the initiation of chromosome replication in Escherichia coli K-12. Mol Gen Genet. 1980 Jan;177(2):301–309. doi: 10.1007/BF00267443. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Friedman D. I. Integration host factor: a protein for all reasons. Cell. 1988 Nov 18;55(4):545–554. doi: 10.1016/0092-8674(88)90213-9. [DOI] [PubMed] [Google Scholar]
  14. Fuller R. S., Funnell B. E., Kornberg A. The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell. 1984 Oct;38(3):889–900. doi: 10.1016/0092-8674(84)90284-8. [DOI] [PubMed] [Google Scholar]
  15. Gille H., Egan J. B., Roth A., Messer W. The FIS protein binds and bends the origin of chromosomal DNA replication, oriC, of Escherichia coli. Nucleic Acids Res. 1991 Aug 11;19(15):4167–4172. doi: 10.1093/nar/19.15.4167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goldstein E., Drlica K. Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4046–4050. doi: 10.1073/pnas.81.13.4046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Haffter P., Bickle T. A. Purification and DNA-binding properties of FIS and Cin, two proteins required for the bacteriophage P1 site-specific recombination system, cin. J Mol Biol. 1987 Dec 20;198(4):579–587. doi: 10.1016/0022-2836(87)90201-4. [DOI] [PubMed] [Google Scholar]
  18. Heichman K. A., Johnson R. C. The Hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science. 1990 Aug 3;249(4968):511–517. doi: 10.1126/science.2166334. [DOI] [PubMed] [Google Scholar]
  19. Higgins C. F., Dorman C. J., Stirling D. A., Waddell L., Booth I. R., May G., Bremer E. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell. 1988 Feb 26;52(4):569–584. doi: 10.1016/0092-8674(88)90470-9. [DOI] [PubMed] [Google Scholar]
  20. Hiraga S., Niki H., Ogura T., Ichinose C., Mori H., Ezaki B., Jaffé A. Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. J Bacteriol. 1989 Mar;171(3):1496–1505. doi: 10.1128/jb.171.3.1496-1505.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hirose S., Hiraga S., Okazaki T. Initiation site of deoxyribonucleotide polymerization at the replication origin of the Escherichia coli chromosome. Mol Gen Genet. 1983;189(3):422–431. doi: 10.1007/BF00325904. [DOI] [PubMed] [Google Scholar]
  22. Hirota Y., Mordoh J., Jacob F. On the process of cellular division in Escherichia coli. 3. Thermosensitive mutants of Escherichia coli altered in the process of DNA initiation. J Mol Biol. 1970 Nov 14;53(3):369–387. doi: 10.1016/0022-2836(70)90072-0. [DOI] [PubMed] [Google Scholar]
  23. Hodges-Garcia Y., Hagerman P. J., Pettijohn D. E. DNA ring closure mediated by protein HU. J Biol Chem. 1989 Sep 5;264(25):14621–14623. [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Jenkins A. J., March J. B., Oliver I. R., Masters M. A DNA fragment containing the groE genes can suppress mutations in the Escherichia coli dnaA gene. Mol Gen Genet. 1986 Mar;202(3):446–454. doi: 10.1007/BF00333275. [DOI] [PubMed] [Google Scholar]
  27. Johnson R. C., Ball C. A., Pfeffer D., Simon M. I. Isolation of the gene encoding the Hin recombinational enhancer binding protein. Proc Natl Acad Sci U S A. 1988 May;85(10):3484–3488. doi: 10.1073/pnas.85.10.3484. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Kaguni J. M., Fuller R. S., Kornberg A. Enzymatic replication of E. coli chromosomal origin is bidirectional. Nature. 1982 Apr 15;296(5858):623–627. doi: 10.1038/296623a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. LARK K. G., REPKO T., HOFFMAN E. J. THE EFFECT OF AMINO ACID DEPRIVATION ON SUBSEQUENT DEOXYRIBONUCLEIC ACID REPLICATION. Biochim Biophys Acta. 1963 Sep 17;76:9–24. [PubMed] [Google Scholar]
  34. MAALOE O., HANAWALT P. C. Thymine deficiency and the normal DNA replication cycle. I. J Mol Biol. 1961 Apr;3:144–155. doi: 10.1016/s0022-2836(61)80041-7. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Numrych T. E., Gumport R. I., Gardner J. F. A genetic analysis of Xis and FIS interactions with their binding sites in bacteriophage lambda. J Bacteriol. 1991 Oct;173(19):5954–5963. doi: 10.1128/jb.173.19.5954-5963.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Ogawa T., Baker T. A., van der Ende A., Kornberg A. Initiation of enzymatic replication at the origin of the Escherichia coli chromosome: contributions of RNA polymerase and primase. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3562–3566. doi: 10.1073/pnas.82.11.3562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ogden G. B., Pratt M. J., Schaechter M. The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell. 1988 Jul 1;54(1):127–135. doi: 10.1016/0092-8674(88)90186-9. [DOI] [PubMed] [Google Scholar]
  40. Orr E., Fairweather N. F., Holland I. B., Pritchard R. H. Isolation and characterisation of a strain carrying a conditional lethal mutation in the cou gene of Escherichia coli K12. Mol Gen Genet. 1979;177(1):103–112. doi: 10.1007/BF00267259. [DOI] [PubMed] [Google Scholar]
  41. Paek K. H., Walker G. C. Escherichia coli dnaK null mutants are inviable at high temperature. J Bacteriol. 1987 Jan;169(1):283–290. doi: 10.1128/jb.169.1.283-290.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Prentki P., Chandler M., Galas D. J. Escherichia coli integration host factor bends the DNA at the ends of IS1 and in an insertion hotspot with multiple IHF binding sites. EMBO J. 1987 Aug;6(8):2479–2487. doi: 10.1002/j.1460-2075.1987.tb02529.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pruss G. J., Manes S. H., Drlica K. Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell. 1982 Nov;31(1):35–42. doi: 10.1016/0092-8674(82)90402-0. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Rokeach L. A., Zyskind J. W. RNA terminating within the E. coli origin of replication: stringent regulation and control by DnaA protein. Cell. 1986 Aug 29;46(5):763–771. doi: 10.1016/0092-8674(86)90352-1. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  49. Ryan M. J. Coumermycin A1: A preferential inhibitor of replicative DNA synthesis in Escherichia coli. I. In vivo characterization. Biochemistry. 1976 Aug 24;15(17):3769–3777. doi: 10.1021/bi00662a020. [DOI] [PubMed] [Google Scholar]
  50. Sakakibara Y. The dnaK gene of Escherichia coli functions in initiation of chromosome replication. J Bacteriol. 1988 Feb;170(2):972–979. doi: 10.1128/jb.170.2.972-979.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. 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]
  53. Skarstad K., Baker T. A., Kornberg A. Strand separation required for initiation of replication at the chromosomal origin of E.coli is facilitated by a distant RNA--DNA hybrid. EMBO J. 1990 Jul;9(7):2341–2348. doi: 10.1002/j.1460-2075.1990.tb07406.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Smith D. H., Davis B. D. Mode of action of novobiocin in Escherichia coli. J Bacteriol. 1967 Jan;93(1):71–79. doi: 10.1128/jb.93.1.71-79.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. 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]
  56. Steck T. R., Pruss G. J., Manes S. H., Burg L., Drlica K. DNA supercoiling in gyrase mutants. J Bacteriol. 1984 May;158(2):397–403. doi: 10.1128/jb.158.2.397-403.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. 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]
  58. 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]
  59. Trun N. J., Gottesman S. On the bacterial cell cycle: Escherichia coli mutants with altered ploidy. Genes Dev. 1990 Dec;4(12A):2036–2047. doi: 10.1101/gad.4.12a.2036. [DOI] [PubMed] [Google Scholar]
  60. Wang J. C. Degree of superhelicity of covalently closed cyclic DNA's from Escherichia coli. J Mol Biol. 1969 Jul 28;43(2):263–272. doi: 10.1016/0022-2836(69)90266-6. [DOI] [PubMed] [Google Scholar]
  61. Yuan H. S., Finkel S. E., Feng J. A., Kaczor-Grzeskowiak M., Johnson R. C., Dickerson R. E. The molecular structure of wild-type and a mutant Fis protein: relationship between mutational changes and recombinational enhancer function or DNA binding. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9558–9562. doi: 10.1073/pnas.88.21.9558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Zyskind J. W., Deen L. T., Smith D. W. Temporal sequence of events during the initiation process in Escherichia coli deoxyribonucleic acid replication: roles of the dnaA and dnaC gene products and ribonucleic acid polymerase. J Bacteriol. 1977 Mar;129(3):1466–1475. doi: 10.1128/jb.129.3.1466-1475.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Zyskind J. W., Smith D. W. NOVEL Escherichia coli dnaB mutant: direct involvement of the dnaB252 gene product in the synthesis of an origin-ribonucleic acid species during initiaion of a round of deoxyribonucleic acid replication. J Bacteriol. 1977 Mar;129(3):1476–1486. doi: 10.1128/jb.129.3.1476-1486.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. von Meyenburg K., Hansen F. G., Riise E., Bergmans H. E., Meijer M., Messer W. Origin of replication, oriC, of the Escherichia coli K12 chromosome: genetic mapping and minichromosome replication. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):121–128. doi: 10.1101/sqb.1979.043.01.018. [DOI] [PubMed] [Google Scholar]

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