Pathways of mammalian replication fork restart

Nature Reviews Molecular Cell Biology

Volumn 11, Issue 10, 2010, Pages 683-687

  Petermann, Eva ^a   Helleday, Thomas ^b,c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

APHIDICOLIN; BLOOM SYNDROME HELICASE; DEOXYRIBONUCLEASE; HELICASE; HYDROXYUREA; WERNER SYNDROME PROTEIN; CRUCIFORM DNA; DNA; DNA HELICASE;

CHROMOSOME; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; MAMMAL; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; BIOLOGICAL MODEL; BLOOM SYNDROME; DNA DAMAGE; GENETICS; HUMAN; METABOLISM;

ANIMALS; BLOOM SYNDROME; DNA; DNA DAMAGE; DNA HELICASES; DNA REPLICATION; DNA, CRUCIFORM; HUMANS; MAMMALS; MODELS, GENETIC;

MAMMALIA;

EID: 77957123627     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2974     Document Type: Review

References (47)

1. Hanada, K. et al. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nature Struct. Mol. Biol. 14, 1096-1104 (2007).
2. Heller, R. C. & Marians, K. J. Replisome assembly and the direct restart of stalled replication forks. Nature Rev. Mol. Cell Biol. 7, 932-943 (2006).
3. Ibarra, A., Schwob, E. & Mendez, J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl Acad. Sci. USA 105, 8956-8961 (2008).
4. Ge, X. Q., Jackson, D. A. & Blow, J. J. Dormant origins licensed by excess MCM2-7 are required for human cells to survive replicative stress. Genes Dev. 21, 3331-3341 (2007).
5. Lundin, C. et al. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 22, 5869-5878 (2002).
6. Saintigny, Y. et al. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20, 3861-3870 (2001).
7. Tuduri, S., Tourriere, H. & Pasero, P. Defining replication origin efficiency using DNA fiber assays. Chromosome Res. 18, 91-102 (2010).
8. Davies, S. L., North, P. S. & Hickson, I. D. Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nature Struct. Mol. Biol. 14, 677-679 (2007).
9. Franchitto, A. et al. Replication fork stalling in WRN-deficient cells is overcome by prompt activation of a MUS81-dependent pathway. J. Cell Biol. 183, 241-252 (2008).
10. Sidorova, J. M., Li, N., Folch, A. & Monnat, R. J. Jr. The RecQ helicase WRN is required for normal replication fork progression after DNA damage or replication fork arrest. Cell Cycle 7, 796-807 (2008).
11. Bryant, H. E. et al. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 28, 2601-2615 (2009).
12. Ciccia, A. et al. The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Genes Dev. 23, 2415-2425 (2009).
13. Petermann, E., Orta, M. L., Issaeva, N., Schultz, N. & Helleday, T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 37, 492-502 (2010).
14. Liu, J., Xu, L., Sandler, S. J. & Marians, K. J. Replication fork assembly at recombination intermediates is required for bacterial growth. Proc. Natl Acad. Sci. USA 96, 3552-3555 (1999).
15. Llorente, B., Smith, C. E. & Symington, L. S. Break-induced replication: what is it and what is it for? Cell Cycle 7, 859-864 (2008).
16. Karow, J. K., Constantinou, A., Li, J. L., West, S. C. & Hickson, I. D. The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc. Natl Acad. Sci. USA 97, 6504-6508 (2000).
17. Ralf, C., Hickson, I. D. & Wu, L. The Bloom's syndrome helicase can promote the regression of a model replication fork. J. Biol. Chem. 281, 22839-22846 (2006).
18. Bugreev, D. V., Yu, X., Egelman, E. H. & Mazin, A. V. Novel pro-and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 21, 3085-3094 (2007).
19. Rassool, F. V., North, P. S., Mufti, G. J. & Hickson, I. D. Constitutive DNA damage is linked to DNA replication abnormalities in Bloom's syndrome cells. Oncogene 22, 8749-8757 (2003).
20. Constantinou, A. et al. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 1, 80-84 (2000).
21. Machwe, A., Xiao, L., Groden, J. & Orren, D. K. The Werner and Bloom syndrome proteins catalyze regression of a model replication fork. Biochemistry 45, 13939-13946 (2006).
22. Sidorova, J. M. Roles of the Werner syndrome RecQ helicase in DNA replication. DNA Repair (Amst.) 7, 1776-1786 (2008).
23. Yusufzai, T. & Kadonaga, J. T. HARP is an ATP-driven annealing helicase. Science 322, 748-750 (2008).
24. Bansbach, C. E., Betous, R., Lovejoy, C. A., Glick, G. G. & Cortez, D. The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks. Genes Dev. 23, 2405-2414 (2009).
25. Baumann, P., Benson, F. E. & West, S. C. Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87, 757-766 (1996).
26. Seigneur, M., Ehrlich, S. D. & Michel, B. RuvABC-dependent double-strand breaks in DnaBts mutants require RecA. Mol. Microbiol. 38, 565-574 (2000).
27. Robu, M. E., Inman, R. B. & Cox, M. M. RecA protein promotes the regression of stalled replication forks in vitro. Proc. Natl Acad. Sci. USA 98, 8211-8218 (2001).
28. Yoon, D., Wang, Y., Stapleford, K., Wiesmuller, L. &Chen, J. p53 inhibits strand exchange and replication fork regression promoted by human Rad51. J. Mol. Biol. 336, 639-654 (2004).
29. Buis, J. et al. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135, 85-96 (2008).
30. Sartori, A. A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007).
31. Franchitto, A. & Pichierri, P. Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBS1 complex after replication fork arrest. J. Cell Biol. 157, 19-30 (2002).
32. Franchitto, A. & Pichierri, P. Werner syndrome protein and the MRE11 complex are involved in a common pathway of replication fork recovery. Cell Cycle 3, 1331-1339 (2004).
33. Tittel-Elmer, M., Alabert, C., Pasero, P. & Cobb, J. A. The MRX complex stabilizes the replisome independently of the S phase checkpoint during replication stress. EMBO J. 28, 1142-1156 (2009).
34. Terret, M. E., Sherwood, R., Rahman, S., Qin, J. & Jallepalli, P. V. Cohesin acetylation speeds the replication fork. Nature 462, 231-234 (2009).
35. Bishop, D. K. et al. Xrcc3 is required for assembly of Rad51 complexes in vivo. J. Biol. Chem. 273, 21482-21488 (1998).
36. Raynard, S., Bussen, W. & Sung, P. A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIα, and BLAP75. J. Biol. Chem. 281, 13861-13864 (2006).
37. Singh, T. R. et al. BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes Dev. 22, 2856-2868 (2008).
38. Wu, L. & Hickson, I. D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874 (2003).
39. Shimura, T. et al. Bloom's syndrome helicase and Mus81 are required to induce transient double-strand DNA breaks in response to DNA replication stress. J. Mol. Biol. 375, 1152-1164 (2008).
40. Malkova, A., Naylor, M. L., Yamaguchi, M., Ira, G. & Haber, J. E. RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell Biol. 25, 933-944 (2005).
41. Lee, S. H. et al. The SET domain protein Metnase mediates foreign DNA integration and links integration to nonhomologous end-joining repair. Proc. Natl Acad. Sci. USA 102, 18075-18080 (2005).
42. De Haro, L. P. et al. Metnase promotes restart and repair of stalled and collapsed replication forks. Nucleic Acids Res. 10 May 2010 (doi:10.1093/nar/ gkq339).
43. Feijoo, C. et al. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J. Cell Biol. 154, 913-923 (2001).
44. Zachos, G., Rainey, M. D. & Gillespie, D. A. Chk1-dependent S-M checkpoint delay in vertebrate cells is linked to maintenance of viable replication structures. Mol. Cell Biol. 25, 563-574 (2005).
45. Scorah, J. & McGowan, C. H. Claspin and Chk1 regulate replication fork stability by different mechanisms. Cell Cycle 8, 1036-1043 (2009).
46. Leman, A. R., Noguchi, C., Lee, C. Y. & Noguchi, E. Human Timeless and Tipin stabilize replication forks and facilitate sister-chromatid cohesion. J. Cell Sci. 123, 660-670 (2010).
47. Tanaka, H. et al. Replisome progression complex links DNA replication to sister chromatid cohesion in Xenopus egg extracts. Genes Cells 14, 949-963 (2009).