Survival of the Replication Checkpoint Deficient Cells Requires MUS81-RAD52 Function

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Murfuni, Ivana ^a   Basile, Giorgia ^a   Subramanyam, Shyamal ^b,c   Malacaria, Eva ^a   Bignami, Margherita ^a   Spies, Maria ^c   Franchitto, Annapaola ^a   Pichierri, Pietro ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; ENDONUCLEASE; HISTONE H2AX; PROTEIN MUS81; RAD52 PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; MUS81 PROTEIN, HUMAN; RAD51 PROTEIN; RAD52 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE S PHASE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CHROMOSOME ABERRATION; CHROMOSOME DAMAGE; CONTROLLED STUDY; DNA STRAND BREAKAGE; DOWN REGULATION; ENZYME INHIBITION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; BIOSYNTHESIS; CELL CYCLE CHECKPOINT; CHROMOSOMAL INSTABILITY; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETICS; HEK293 CELL LINE; HUMAN GENOME;

CELL CYCLE CHECKPOINTS; CELL SURVIVAL; CHROMOSOMAL INSTABILITY; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DNA-BINDING PROTEINS; ENDONUCLEASES; GENE EXPRESSION REGULATION; GENOME, HUMAN; HEK293 CELLS; HUMANS; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; S PHASE;

EID: 84887283315     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003910     Document Type: Article

References (67)

1. Branzei D, Foiani M, (2009) The checkpoint response to replication stress. DNA Repair 8: 1038-1046.
2. Cimprich KA, Cortez D, (2008) ATR: an essential regulator of genome integrity. Nature reviews Molecular cell biology 9: 616-627.
3. Friedel AM, Pike BL, Gasser SM, (2009) ATR/Mec1: coordinating fork stability and repair. Current Opinion in Cell Biology 21: 237-244.
4. López-Contreras AJ, Fernandez-Capetillo O, (2010) The ATR barrier to replication-born DNA damage. DNA Repair 9: 1249-1255.
5. Cotta-Ramusino C, Fachinetti D, Lucca C, Doksani Y, Lopes M, et al. (2005) Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Molecular Cell 17: 153-159.
6. Sogo JM, Lopes M, Foiani M, (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science (New York, NY) 297: 599-602.
7. Osman F, Whitby MC, (2007) Exploring the roles of Mus81-Eme1/Mms4 at perturbed replication forks. DNA Repair 6: 1004-1017.
8. Ciccia A, Constantinou A, West SC, (2003) Identification and characterization of the human mus81-eme1 endonuclease. The Journal of biological chemistry 278: 25172-25178.
9. Haber J, Heyer WD, (2001) The Fuss about Mus81. Genetics 107: 551-554.
10. Whitby MC, Osman F, Dixon J, (2003) Cleavage of model replication forks by fission yeast Mus81-Eme1 and budding yeast Mus81-Mms4. J Biol Chem 278: 6928-6935.
11. Froget B, Lambert S, Baldacci G, (2008) Cleavage of Stalled Forks by Fission Yeast Mus81/Eme1 in Absence of DNA Replication Checkpoint. Molecular Biology of the Cell 19: 445-456.
12. Doe CL, Osman F, Dixon J, Whitby MC, (2004) DNA repair by a Rad22-Mus81-dependent pathway that is independent of Rhp51. Nucleic Acids Research 32: 5570-5581.
13. Doe CL, Ahn JS, Dixon J, Whitby MC, (2002) Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. The Journal of biological chemistry 277: 32753-32759.
14. Franchitto A, Pirzio LM, Prosperi E, Sapora O, Bignami M, et al. (2008) Replication fork stalling in WRN-deficient cells is overcome by prompt activation of a MUS81-dependent pathway. The Journal of Cell Biology 183: 241-252.
15. Fabre F, Chan A, Heyer WD, Gangloff S, (2002) Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc Natl Acad Sci U S A 99: 16887-16892.
16. Kaliraman V, Mullen JR, Fricke WM, Bastin-shanower SA, Brill SJ, (2001) Functional overlap between Sgs1 - Top3 and the Mms4 - Mus81 endonuclease. Genes & Development pp. 2730-2740.
17. Sørensen CS, Hansen LT, Dziegielewski J, Syljuäsen R, Lundin C, et al. (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nature Cell Biology 7: 195-201.
18. Murfuni I, Nicolai S, Baldari S, Crescenzi M, Bignami M, et al. (2012) The WRN and MUS81 proteins limit cell death and genome instability following oncogene activation. Oncogene pp. 1-11.
19. Toledo LI, Murga M, Zur R, Soria R, Rodriguez A, et al. (2011) A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations. Nature Structural & Molecular Biology 18: 721-727.
20. Zhao HUI, Piwnica-worms H, (2001) ATR-Mediated Checkpoint Pathways Regulate Phosphorylation and Activation of Human Chk1. Mol Cell Biol 21: 4129-4139.
21. Murfuni I, De Santis A, Federico M, Bignami M, Pichierri P, et al. (2012) Perturbed replication induced genome-wide or at common fragile sites is differently managed in the absence of WRN. Carcinogenesis 33 (9) (): 1655-63.
22. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T, (2010) Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Molecular Cell 37: 492-502.
23. Schwartz EK, Heyer WD, (2011) Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120: 109-127.
24. Hickson ID, Mankouri HW, (2011) Processing of homologous recombination repair intermediates by the Sgs1-Top3-Rmi1 and Mus81-Mms4 complexes. Cell Cycle 10: 3078-3085.
25. Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, et al. (2007) The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nature Structural & Molecular Biology 14: 1096-1104.
26. Wray J, Liu J, Nickoloff Ja, Shen Z, (2008) Distinct RAD51 associations with RAD52 and BCCIP in response to DNA damage and replication stress. Cancer Research 68: 2699-2707.
27. Cobb JA, Schleker T, Rojas V, Bjergbaek L, Tercero JA, et al. (2005) Replisome instability, fork collapse, and gross chromosomal rearrangements arise synergistically from Mec1 kinase and RecQ helicase mutations. Genes & Development 19: 3055-3069.
28. Cobb JA, Bjergbaek L, Shimada K, Frei C, Gasser SM, (2003) DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. The EMBO Journal 22: 4325-4336.
29. Lucca C, Vanoli F, Cotta-Ramusino C, Pellicioli A, Liberi G, et al. (2004) Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23: 1206-1213.
30. Syljuäsen R, Sørensen CS, Hansen LT, Fugger K, Lundin C, et al. (2005) Inhibition of Human Chk1 Causes Increased Initiation of DNA Replication, Phosphorylation of ATR Targets, and DNA Breakage. Molecular and cellular biology 25: 3553-3562.
31. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, et al. (2000) Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 14: 1448-1459.
32. Cliby Wa, Roberts CJ, Cimprich Ka, Stringer CM, Lamb JR, et al. (1998) Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. The EMBO Journal 17: 159-169.
33. Regairaz M, Zhang Y-W, Fu H, Agama KK, Tata N, et al. (2011) Mus81-mediated DNA cleavage resolves replication forks stalled by topoisomerase I-DNA complexes. The Journal of Cell Biology 195: 739-749.
34. Delacroix S, Wagner JM, Kobayashi M, Yamamoto K-i, Karnitz LM, (2007) The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes & Development 21: 1472-1477.
35. Sorensen CS, Syljuasen RG, Lukas J, Bartek J, (2004) ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 3: 941-945.
36. Kumagai A, Lee J, Yoo HY, Dunphy WG, (2006) TopBP1 activates the ATR-ATRIP complex. Cell 124: 943-955.
37. Forment JV, Blasius M, Guerini I, Jackson SP, (2011) Structure-specific DNA endonuclease mus81/eme1 generates DNA damage caused by chk1 inactivation. PLoS One 6: e23517.
38. Liu S, Bekker-Jensen S, Mailand N, Lukas C, Bartek J, et al. (2006) Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Molecular and cellular biology 26: 6056-6064.
39. Chou DM, Elledge SJ, (2006) Tipin and Timeless form a mutually protective complex required for genotoxic stress resistance and checkpoint function. Proceedings of the National Academy of Sciences of the United States of America 103: 18143-18147.
40. Smith KD, Fu Ma, Brown EJ, (2009) Tim-Tipin dysfunction creates an indispensible reliance on the ATR-Chk1 pathway for continued DNA synthesis. The Journal of Cell Biology 187: 15-23.
41. Ying S, Minocherhomji S, Chan KL, Palmai-Pallag T, Chu WK, et al. (2013) MUS81 promotes common fragile site expression. Nat Cell Biol 15: 1001-1007.
42. Hashimoto Y, Chaudhuri AR, Lopes M, Costanzo V, (2010) Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nature Structural & Molecular Biology 17: 1305-1311.
43. Sonoda E, Sasaki MS, Buerstedde JM, Bezzubova O, Shinohara A, et al. (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 17: 598-608.
44. Kai M, Boddy MN, Russell P, Wang TS-F, (2005) Replication checkpoint kinase Cds1 regulates Mus81 to preserve genome integrity during replication stress. Genes & Development 19: 919-932.
45. Willis N, Rhind N, (2009) Mus81, Rhp51(Rad51), and Rqh1 form an epistatic pathway required for the S-phase DNA damage checkpoint. Mol Biol Cell 20: 819-833.
46. Taylor ER, McGowan CH, (2008) Cleavage mechanism of human Mus81-Eme1 acting on Holliday-junction structures. Proceedings of the National Academy of Sciences of the United States of America 105: 3757-3762.
47. Blais V, Gao H, Elwell CA, Boddy MN, Gaillard P-hL, et al. (2004) RNA Interference Inhibition of Mus81 Reduces Mitotic Recombination in Human Cells. Molecular Biology of the Cell 15: 552-562.
48. Matos J, Blanco MG, Maslen S, Skehel JM, West SC, (2011) Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 147: 158-172.
49. Altmannova V, Eckert-Boulet N, Arneric M, Kolesar P, Chaloupkova R, et al. (2010) Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Research 38: 4708-4721.
50. Ohuchi T, Seki M, Branzei D, Maeda D, Ui A, et al. (2008) Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. DNA Repair 7: 879-889.
51. Llorente B, Smith CE, Symington LS, (2008) Break-induced replication: what is it and what is it for? Cell Cycle 7: 859-864.
52. Haber JE, (1999) DNA recombination: the replication connection. Trends Biochem Sci 24: 271-275.
53. Feng Z, Scott SP, Bussen W, Sharma GG, Guo G, et al. (2011) Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proceedings of the National Academy of Sciences of the United States of America 108: 686-691.
54. Schlacher K, Christ N, Siaud N, Egashira A, Wu H, et al. (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145: 529-542.
55. Munoz-Galvan S, Tous C, Blanco MG, Schwartz EK, Ehmsen KT, et al. (2012) Distinct roles of Mus81, Yen1, Slx1-Slx4, and Rad1 nucleases in the repair of replication-born double-strand breaks by sister chromatid exchange. Mol Cell Biol 32: 1592-1603.
56. Schwartz EK, Heyer WD, (2011) Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma pp. 109-127.
57. Naim V, Wilhelm T, Debatisse M, Rosselli F, (2013) ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat Cell Biol 15: 1008-1015.
58. Malkova A, Naylor ML, Yamaguchi M, Ira G, Haber JE, (2005) RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol Cell Biol 25: 933-944.
59. Davis AP, Symington LS, (2004) RAD51-dependent break-induced replication in yeast. Mol Cell Biol 24: 2344-2351.
60. Huang F, Motlekar NA, Burgwin CM, Napper AD, Diamond SL, et al. (2011) Identification of specific inhibitors of human RAD51 recombinase using high-throughput screening. ACS Chem Biol 6: 628-635.
61. Ammazzalorso F, Pirzio LM, Bignami M, Franchitto A, Pichierri P, (2010) ATR and ATM differently regulate WRN to prevent DSBs at stalled replication forks and promote replication fork recovery. The EMBO Journal pp. 1-14.
62. Rothenberg E, Grimme JM, Spies M, Ha T, (2008) Human Rad52-mediated homology search and annealing occurs by continuous interactions between overlapping nucleoprotein complexes. Proceedings of the National Academy of Sciences 105: 20274-20279.
63. Tombline G, Fishel R, (2002) Biochemical characterization of the human RAD51 protein. I. ATP hydrolysis. J Biol Chem 277: 14417-14425.
64. Masuda-Ozawa T, Hoang T, Seo YS, Chen LF, Spies M, (2013) Single-molecule sorting reveals how ubiquitylation affects substrate recognition and activities of FBH1 helicase. Nucleic Acids Res 41 (6) (): 3576-87.
65. Kagawa W, Kurumizaka H, Ikawa S, Yokoyama S, Shibata T, (2001) Homologous pairing promoted by the human Rad52 protein. J Biol Chem 276: 35201-35208.
66. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9: 671-675.
67. Pirzio LM, Pichierri P, Bignami M, Franchitto A, (2008) Werner syndrome helicase activity is essential in maintaining fragile site stability. The Journal of Cell Biology 180: 305-314.