Tus-Ter As a Tool to Study Site-specific DNA Replication Perturbation in Eukaryotes

Overview

Journal Cell Cycle

Specialty Cell Biology

Date 2014 Dec 9

PMID 25486560

Citations 10

Authors

Nicolai B Larsen

Ian D Hickson

Hocine W Mankouri

Affiliations

Soon will be listed here.

Abstract

The high-affinity binding of the Tus protein to specific 21-bp sequences, called Ter, causes site-specific, and polar, DNA replication fork arrest in E coli. The Tus-Ter complex serves to coordinate DNA replication with chromosome segregation in this organism. A number of recent and ongoing studies have demonstrated that Tus-Ter can be used as a heterologous tool to generate site-specific perturbation of DNA replication when reconstituted in eukaryotes. Here, we review these recent findings and explore the molecular mechanism by which Tus-Ter mediates replication fork (RF) arrest in the budding yeast, S. cerevisiae. We propose that Tus-Ter is a versatile, genetically tractable, and regulatable RF blocking system that can be utilized for disrupting DNA replication in a diverse range of host cells.

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References

Calzada A, Hodgson B, Kanemaki M, Bueno A, Labib K . Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev. 2005; 19(16):1905-19. PMC: 1186190. DOI: 10.1101/gad.337205. View

Nickoloff J, Chen E, Heffron F . A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc Natl Acad Sci U S A. 1986; 83(20):7831-5. PMC: 386816. DOI: 10.1073/pnas.83.20.7831. View

Plessis A, PERRIN A, Haber J, Dujon B . Site-specific recombination determined by I-SceI, a mitochondrial group I intron-encoded endonuclease expressed in the yeast nucleus. Genetics. 1992; 130(3):451-60. PMC: 1204864. DOI: 10.1093/genetics/130.3.451. View

Mulcair M, Schaeffer P, Oakley A, Cross H, Neylon C, Hill T . A molecular mousetrap determines polarity of termination of DNA replication in E. coli. Cell. 2006; 125(7):1309-19. DOI: 10.1016/j.cell.2006.04.040. View

Ahn J, Osman F, Whitby M . Replication fork blockage by RTS1 at an ectopic site promotes recombination in fission yeast. EMBO J. 2005; 24(11):2011-23. PMC: 1142605. DOI: 10.1038/sj.emboj.7600670. View

Mankouri H, Huttner D, Hickson I . How unfinished business from S-phase affects mitosis and beyond. EMBO J. 2013; 32(20):2661-71. PMC: 3801442. DOI: 10.1038/emboj.2013.211. View

Liberi G, Maffioletti G, Lucca C, Chiolo I, Baryshnikova A, Cotta-Ramusino C . Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 2005; 19(3):339-50. PMC: 546512. DOI: 10.1101/gad.322605. View

Leipe D, Aravind L, Grishin N, Koonin E . The bacterial replicative helicase DnaB evolved from a RecA duplication. Genome Res. 2000; 10(1):5-16. View

Ivessa A, Lenzmeier B, Bessler J, Goudsouzian L, Schnakenberg S, Zakian V . The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell. 2003; 12(6):1525-36. DOI: 10.1016/s1097-2765(03)00456-8. View

10.

Kaplan D, Davey M, ODonnell M . Mcm4,6,7 uses a "pump in ring" mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. J Biol Chem. 2003; 278(49):49171-82. DOI: 10.1074/jbc.M308074200. View

11.

Liberi G, Cotta-Ramusino C, Lopes M, Sogo J, Conti C, Bensimon A . Methods to study replication fork collapse in budding yeast. Methods Enzymol. 2006; 409:442-62. DOI: 10.1016/S0076-6879(05)09026-9. View

12.

Hill T, Henson J, KUEMPEL P . The terminus region of the Escherichia coli chromosome contains two separate loci that exhibit polar inhibition of replication. Proc Natl Acad Sci U S A. 1987; 84(7):1754-8. PMC: 304519. DOI: 10.1073/pnas.84.7.1754. View

13.

Henderson T, Nilles A, Valjavec-Gratian M, Hill T . Site-directed mutagenesis and phylogenetic comparisons of the Escherichia coli Tus protein: DNA-protein interactions alone can not account for Tus activity. Mol Genet Genomics. 2001; 265(6):941-53. DOI: 10.1007/s004380100501. View

14.

Lopes M, Foiani M, Sogo J . Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell. 2006; 21(1):15-27. DOI: 10.1016/j.molcel.2005.11.015. View

15.

Willis N, Chandramouly G, Huang B, Kwok A, Follonier C, Deng C . BRCA1 controls homologous recombination at Tus/Ter-stalled mammalian replication forks. Nature. 2014; 510(7506):556-9. PMC: 4118467. DOI: 10.1038/nature13295. View

16.

Bizard A, Hickson I . The dissolution of double Holliday junctions. Cold Spring Harb Perspect Biol. 2014; 6(7):a016477. PMC: 4067992. DOI: 10.1101/cshperspect.a016477. View

17.

Valjavec-Gratian M, Henderson T, Hill T . Tus-mediated arrest of DNA replication in Escherichia coli is modulated by DNA supercoiling. Mol Microbiol. 2005; 58(3):758-73. DOI: 10.1111/j.1365-2958.2005.04860.x. View

18.

Mankouri H, Ashton T, Hickson I . Holliday junction-containing DNA structures persist in cells lacking Sgs1 or Top3 following exposure to DNA damage. Proc Natl Acad Sci U S A. 2011; 108(12):4944-9. PMC: 3064375. DOI: 10.1073/pnas.1014240108. View

19.

Lambert S, Mizuno K, Blaisonneau J, Martineau S, Chanet R, Freon K . Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol Cell. 2010; 39(3):346-59. DOI: 10.1016/j.molcel.2010.07.015. View

20.

Hashimoto Y, Ray Chaudhuri A, Lopes M, Costanzo V . Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nat Struct Mol Biol. 2010; 17(11):1305-11. PMC: 4306207. DOI: 10.1038/nsmb.1927. View