Top1- and Top2-mediated topological transitions at replication forks ensure fork progression and stability and prevent DNA damage checkpoint activation

Genes and Development

Volumn 21, Issue 15, 2007, Pages 1921-1936

  Bermejo, Rodrigo ^a   Doksani, Ylli ^a   Capra, Thelma ^a   Katou, Yuki Mori ^b   Tanaka, Hirokazu ^b   Shirahige, Katsuhiko ^b   Foiani, Marco ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b Tokyo Institute of Technology ^*  (Japan)

Author keywords

Chromosome replication; DNA damage checkpoint; DNA topoisomerases; Replication forks

Indexed keywords

CHECKPOINT KINASE 2; EXONUCLEASE; MUTANT PROTEIN; PROTEIN TOP1; PROTEIN TOP2; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CHROMATIN; CHROMOSOME; CHROMOSOME BREAKAGE; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; GENE LOCUS; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; STRESS; TORSION;

CELL CYCLE; CELL CYCLE PROTEINS; CHROMOSOMES, FUNGAL; CONSENSUS SEQUENCE; DNA DAMAGE; DNA REPLICATION; DNA TOPOISOMERASES, TYPE I, EUKARYOTIC; DNA TOPOISOMERASES, TYPE II; DNA, FUNGAL; GENES, FUNGAL; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 34547626213     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.432107     Document Type: Article

References (70)

1. Abdurashidova, G., Radulescu, S., Sandoval, O., Zahariev, S., Danailov, M.B., Demidovich, A., Santamaria, L., Biamonti, G., Riva, S., and Falaschi, A. 2007. Functional interactions of DNA topoisomerases with a human replication origin. EMBO J. 26: 998-1009.
2. Aguilera, A. 2002. The connection between transcription and genomic instability. EMBO J. 21: 195-201.
3. Alcasabas, A.A., Osborn, A.J., Bachant, J., Hu, F., Werler, P.J., Bousset, K., Furuya, K., Diffley, J.F., Carr, A.M., and Elledge, S.J. 2001. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3: 958-965.
4. Andrews, C.A., Vas, A.C., Meier, B., Gimenez-Abian, J.F., Diaz-Martinez, L.A., Green, J., Erickson, S.L., Vanderwaal, K.E., Hsu, W.S., and Clarke, D.J. 2006. A mitotic topoisomerase II checkpoint in budding yeast is required for genome stability but acts independently of Pds1/securin. Genes & Dev. 20: 1162-1174.
5. Benard, M., Maric, C., and Pierron, G. 2001. DNA replicationdependent formation of joint DNA molecules in Physarum polycephalum. Mol. Cell 7: 971-980.
6. Branzei, D. and Foiani, M. 2005. The DNA damage response during DNA replication. Curr. Opin. Cell Biol. 17: 568-575.
7. Brewer, B.J. and Fangman, W.L. 1988. A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell 55: 637-643.
8. Brill, S.J., DiNardo, S., Voelkel-Meinman, K., and Sternglanz, R. 1987. Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature 326: 414-416.
9. Chambeyron, S. and Bickmore, W.A. 2004. Does looping and clustering in the nucleus regulate gene expression? Curr. Opin. Cell Biol. 16: 256-262.
10. Champoux, J.J. 2001. DNA topoisomerases: Structure, function, and mechanism. Annu. Rev. Biochem. 70: 369-413.
11. Champoux, J. and Been, M. 1980. Topoisomerases and the swivel problem. In Mechanistic studies of DNA replication and genetic recombination: ICN-UCLA symposia on molecular and cellular biology (ed. B. Alberts), pp. 809-815. Academic Press, New York.
12. Collins, I., Weber, A., and Levens, D. 2001. Transcriptional consequences of topoisomerase inhibition. Mol. Cell. Biol. 21: 8437-8451.
13. Cotta-Ramusino, C., Fachinetti, D., Lucca, C., Doksani, Y., Lopes, M., Sogo, J., and Foiani, M. 2005. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17: 153-159.
14. DiNardo, S., Voelkel, K., and Sternglanz, R. 1984. DNA topoisomerase II mutant of Saccharomyces cerevisiae: Topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc. Natl. Acad. Sci. 81: 2616-2620.
15. Downes, C.S., Clarke, D.J., Mullinger, A.M., Gimenez-Abian, J.F., Creighton, A.M., and Johnson, R.T. 1994. A topoisomerase II-dependent G2 cycle checkpoint in mammalian cells. Nature 372: 467-470.
16. Feng, W., Collingwood, D., Boeck, M.E., Fox, L.A., Alvino, G.M., Fangman, W.L., Raghuraman, M.K., and Brewer, B.J. 2006. Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat. Cell Biol. 8: 148-155.
17. Friedman, K.L. and Brewer, B.J. 1995. Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol. 262: 613-627.
18. Friedman, K.L., Brewer, B.J., and Fangman, W.L. 1997. Replication profile of Saccharomyces cerevisiae chromosome VI. Genes Cells 2: 667-678.
19. Gambus, A., Jones, R.C., Sanchez-Diaz, A., Kanemaki, M., van Deursen, F., Edmondson, R.D., and Labib, K. 2006. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 8: 358-366.
20. Gasser, S.M., Laroche, T., Falquet, J., Boy de la Tour, E., and Laemmli, U.K. 1986. Metaphase chromosome structure. Involvement of topoisomerase II. J. Mol. Biol. 188: 613-629.
21. Goldman, M.A., Holmquist, G.P., Gray, M.C., Caston, L.A., and Nag, A. 1984. Replication timing of genes and middle repetitive sequences. Science 224: 686-692.
22. Goto, T. and Wang, J.C. 1985. Cloning of yeast TOP1, the gene encoding DNA topoisomerase I, and construction of mutants defective in both DNA topoisomerase I and DNA topoisomerase II. Proc. Natl. Acad. Sci. 82: 7178-7182.
23. Hartwell, L.H. and Weinert, T.A. 1989. Checkpoints: Controls that ensure the order of cell cycle events. Science 246: 629-634.
24. Holm, C., Goto, T., Wang, J.C., and Botstein, D. 1985. DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41: 553-563.
25. Holm, C., Stearns, T., and Botstein, D. 1989. DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol. Cell. Biol. 9: 159-168.
26. Jelinsky, S.A., Estep, P., Church, G.M., and Samson, L.D. 2000. Regulatory networks revealed by transcriptional profiling of damaged Saccharomyces cerevisiae cells: Rpn4 links base excision repair with proteasomes. Mol. Cell. Biol. 20: 8157-8167.
27. Ju, B.G., Lunyak, V.V., Perissi, V., Garcia-Bassets, I., Rose, D.W., Glass, C.K., and Rosenfeld, M.G. 2006. A topoisomerase IIβ-mediated dsDNA break required for regulated transcription. Science 312: 1798-1802.
28. Katou, Y., Kanoh, Y., Bando, M., Noguchi, H., Tanaka, H., Ashikari, T., Sugimoto, K., and Shirahige, K. 2003. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078-1083.
29. Katou, Y., Kaneshiro, K., Aburatani, H., and Shirahige, K. 2006. Genomic approach for the understanding of dynamic aspect of chromosome behavior. Methods Enzymol. 409: 389-410.
30. Kim, R.A. and Wang, J.C. 1989. Function of DNA topoisomerases as replication swivels in Saccharomyces cerevisiae. J. Mol. Biol. 208: 257-267.
31. Kuzminov, A. 1995. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16: 373-384.
32. Lemaitre, J.M., Danis, E., Pasero, P., Vassetzky, Y., and Mechali, M. 2005. Mitotic remodeling of the replicon and chromosome structure. Cell 123: 787-801.
33. Lengronne, A., Katou, Y., Mori, S., Yokobayashi, S., Kelly, G.P., Itoh, T., Watanabe, Y., Shirahige, K., and Uhlmann, F. 2004. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430: 573-578.
34. Li, T.K., Chen, A.Y., Yu, C., Mao, Y., Wang, H., and Liu, L.F. 1999. Activation of topoisomerase II-mediated excision of chromosomal DNA loops during oxidative stress. Genes & Dev. 13: 1553-1560.
35. Liberi, G., Maffioletti, G., Lucca, C., Chiolo, I., Baryshnikova, A., Cotta-Ramusino, C., Lopes, M., Pellicioli, A., Haber, J.E., and Foiani, M. 2005. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes & Dev. 19: 339-350.
36. Lindroos, H.B., Strom, L., Itoh, T., Katou, Y., Shirahige, K., and Sjogren, C. 2006. Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways. Mol. Cell 22: 755-767.
37. Lisby, M., Barlow, J.H., Burgess, R.C., and Rothstein, R. 2004. Choreography of the DNA damage response: Spatiotemporal relationships among checkpoint and repair proteins. Cell 118: 699-713.
38. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C.S., and Foiani, M. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
39. Lopes, M., Cotta-Ramusino, C., Liberi, G., and Foiani, M. 2003. Branch migrating sister chromatid junctions form at replication origins through Rad51/Rad52-independent mechanisms. Mol. Cell 12: 1499-1510.
40. Lucas, I., Germe, T., Chevrier-Miller, M., and Hyrien, O. 2001. Topoisomerase II can unlink replicating DNA by precatenane removal. EMBO J. 20: 6509-6519.
41. Lucca, C., Vanoli, F., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Haber, J., and Foiani, M. 2004. Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23: 1206-1213.
42. Lupo, R., Breiling, A., Bianchi, M.E., and Orlando, V. 2001. Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing. Mol. Cell 7: 127-136.
43. Lydall, D. and Whitehall, S. 2005. Chromatin and the DNA damage response. DNA Repair (Amst.) 4: 1195-1207.
44. Nakada, D., Hirano, Y., and Sugimoto, K. 2004. Requirement of the Mre11 complex and exonuclease 1 for activation of the Mec1 signaling pathway. Mol. Cell. Biol. 24: 10016-10025.
45. Pan, X., Ye, P., Yuan, D.S., Wang, X., Bader, J.S., and Boeke, J.D. 2006. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
46. Paulovich, A.G., Margulies, R.U., Garvik, B.M., and Hartwell, L.H. 1997. RAD9, RAD17, and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics 145: 45-62.
47. Pellicioli, A., Lucca, C., Liberi, G., Marini, F., Lopes, M., Plevani, P., Romano, A., Di Fiore, P.P., and Foiani, M. 1999. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18: 6561-6572.
48. Pellicioli, A., Lee, S.E., Lucca, C., Foiani, M., and Haber, J.E. 2001. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol. Cell 7: 293-300.
49. Poirier, M.G. and Marko, J.F. 2002. Mitotic chromosomes are chromatin networks without a mechanically contiguous protein scaffold. Proc. Natl. Acad. Sci. 99: 15393-15397.
50. Poloumienko, A., Dershowitz, A., De, J., and Newlon, C.S. 2001. Completion of replication map of Saccharomyces cerevisiae chromosome III. Mol. Biol. Cell 12: 3317-3327.
51. Postow, L., Crisona, N.J., Peter, B.J., Hardy, C.D., and Cozzarelli, N.R. 2001. Topological challenges to DNA replication: Conformations at the fork. Proc. Natl. Acad. Sci. 98: 8219-8226.
52. Postow, L., Hardy, C.D., Arsuaga, J., and Cozzarelli, N.R. 2004. Topological domain structure of the Escherichia coli chromosome. Genes & Dev. 18: 1766-1779.
53. Raghuraman, M.K., Winzeler, E.A., Collingwood, D., Hunt, S., Wodicka, L., Conway, A., Lockhart, D.J., Davis, R.W., Brewer, B.J., and Fangman, W.L. 2001. Replication dynamics of the yeast genome. Science 294: 115-121.
54. Robinson, N.P., Blood, K.A., McCallum, S.A., Edwards, P.A., and Bell, S.D. 2007. Sister chromatid junctions in the hyperthermophilic archaeon Sulfolobus solfataricus. EMBO J. 26: 816-824.
55. Schvartzman, J.B. and Stasiak, A. 2004. A topological view of the replicon. EMBO Rep. 5: 256-261.
56. Schwacha, A. and Kleckner, N. 1994. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51-63.
57. Segurado, M., Gomez, M., and Antequera, F. 2002. Increased recombination intermediates and homologous integration hot spots at DNA replication origins. Mol. Cell 10: 907-916.
58. Shirahige, K., Iwasaki, T., Rashid, M.B., Ogasawara, N., and Yoshikawa, H. 1993. Location and characterization of autonomously replicating sequences from chromosome VI of Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 5043-5056.
59. Tercero, J.A. and Diffley, J.F. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412: 553-557.
60. Uemura, T., Ohkura, H., Adachi, Y., Morino, K., Shiozaki, K., and Yanagida, M. 1987. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50: 917-925.
61. Varga-Weisz, P.D., Wilm, M., Bonte, E., Dumas, K., Mann, M., and Becker, P.B. 1997. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388: 598-602.
62. Vidanes, G.M., Bonilla, C.Y., and Toczyski, D.P. 2005. Complicated tails: Histone modifications and the DNA damage response. Cell 121: 973-976.
63. Wallis, J.W., Chrebet, G., Brodsky, G., Rolfe, M., and Rothstein, R. 1989. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409-419.
64. Wang, J.C. 1996. DNA topoisomerases. Annu. Rev. Biochem. 65: 635-692.
65. Wang, J.C. 2002. Cellular roles of DNA topoisomerases: A molecular perspective. Nat. Rev. Mol. Cell Biol. 3: 430-440.
66. Wyrick, J.J., Aparicio, J.G., Chen, T., Barnett, J.D., Jennings, E.G., Young, R.A., Bell, S.P., and Aparicio, O.M. 2001. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: High-resolution mapping of replication origins. Science 294: 2357-2360.
67. Yamashita, M., Hori, Y., Shinomiya, T., Obuse, C., Tsurimoto, T., Yoshikawa, H., and Shirahige, K. 1997. The efficiency and timing of initiation of replication of multiple replicons of Saccharomyces cerevisiae chromosome VI. Genes Cells 2: 655-665.
68. Zhu, Q., Pongpech, P., and DiGate, R.J. 2001. Type I topoisomerase activity is required for proper chromosomal segregation in Escherichia coli. Proc. Natl. Acad. Sci. 98: 9766-9771.
69. Zou, L. and Elledge, S.J. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
70. Zou, H. and Rothstein, R. 1997. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 90: 87-96.