PARG is dispensable for recovery from transient replicative stress but required to prevent detrimental accumulation of poly(ADP-ribose) upon prolonged replicative stress

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 7776-7792

  Illuzzi, Giuditta ^a   Fouquerel, Elise ^a,c   Amé, Jean Christophe ^a   Noll, Aurélia ^a   Rehmet, Kristina ^b,d   Nasheuer, Heinz Peter ^b   Dantzer, Françoise ^a   Schreiber, Valérie ^a  

^a Institut de Recherche de l'Ecole de Biotechnologie de Strasbourg   (France)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d Boehringer Ingelheim Veterinary Research Center GmbH and Co KG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; HYDROXYUREA; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLY(ADENOSINE DIPHOSPHATE RIBOSE) GLYCOHYDROLASE; UNCLASSIFIED DRUG;

ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL;

CELL LINE; CHROMATIN; DNA REPAIR; DNA REPLICATION; DNA, SINGLE-STRANDED; GLYCOSIDE HYDROLASES; HELA CELLS; HISTONES; HUMANS; HYDROXYUREA; PHOSPHORYLATION; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; RECOMBINATIONAL DNA REPAIR; REPLICATION PROTEIN A; S PHASE; S PHASE CELL CYCLE CHECKPOINTS; STRESS, PHYSIOLOGICAL;

EID: 84903954677     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku505     Document Type: Article

References (64)

1. Luo, X., Kraus, W.L. (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev., 26, 417-432.
2. Kalisch, T., Ame, J.C., Dantzer, F., Schreiber, V. (2012) New readers and interpretations of poly(ADP-ribosyl)ation. Trends Biochem. Sci., 37, 381-390.
3. Meyer-Ficca, M.L., Meyer, R.G., Coyle, D.L., Jacobson, E.L., Jacobson, M.K. (2004) Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp. Cell Res., 297, 521-532.
4. Feng, X., Koh, D.W. (2013) Roles of poly(ADP-ribose) glycohydrolase in DNA damage and apoptosis. Int. Rev. Cell Mol. Biol., 304, 227-281.
5. Koh, D.W., Lawler, A.M., Poitras, M.F., Sasaki, M., Wattler, S., Nehls, M.C., Stoger, T., Poirier, G.G., Dawson, V.L., Dawson, T.M. (2004) Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc. Natl. Acad. Sci. U.S.A., 101, 17699-17704.
6. Ame, J.C., Fouquerel, E., Gauthier, L.R., Biard, D., Boussin, F.D., Dantzer, F., de Murcia, G., Schreiber, V. (2009) Radiation-induced mitotic catastrophe in PARG-deficient cells. J. Cell Sci., 122, 1990-2002.
7. Fisher, A.E., Hochegger, H., Takeda, S., Caldecott, K.W. (2007) Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol. Cell Biol., 27, 5597-5605.
8. Erdelyi, K., Bai, P., Kovacs, I., Szabo, E., Mocsar, G., Kakuk, A., Szabo, C., Gergely, P., Virag, L. (2009) Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. Faseb J., 23, 3553-3563.
9. Petermann, E., Helleday, T. (2010) Pathways of mammalian replication fork restart.Nat. Rev. Mol. Cell Biol., 11, 683-687.
10. Petermann, E., Orta, M.L., 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. Mol. Cell, 37, 492-502.
11. Yang, Y.G., Cortes, U., Patnaik, S., Jasin, M., Wang, Z.Q. (2004) Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene, 23, 3872-3882.
12. Bryant, H.E., Petermann, E., Schultz, N., Jemth, A.S., Loseva, O., Issaeva, N., Johansson, F., Fernandez, S., McGlynn, P., Helleday, T. (2009) PARP is activated at stalled forks to mediateMre11-dependent replication restart and recombination. EMBO J., 28, 2601-2615.
13. Min, W., Bruhn, C., Grigaravicius, P., Zhou, Z.W., Li, F., Kruger, A., Siddeek, B., Greulich, K.O., Popp, O., Meisezahl, C. et al. (2013) Poly(ADP-ribose) binding to Chk1 at stalled replication forks is required for S-phase checkpoint activation. Nat. Commun., 4, 2993.
14. Fujihara, H., Ogino, H., Maeda, D., Shirai, H., Nozaki, T., Kamada, N., Jishage, K., Tanuma, S., Takato, T., Ochiya, T. et al. (2009) Poly(ADP-ribose) Glycohydrolase deficiency sensitizes mouse ES cells to DNA damaging agents. Curr. Cancer Drug Targets, 9, 953-962.
15. Lin, Z.P., Ratner, E.S., Whicker, M.E., Lee, Y., Sartorelli, A.C. (2014) Triapine disrupts CtIP-mediated homologous recombination repair and sensitizes ovarian cancer cells to PARP and topoisomerase inhibitors. Mol. Cancer Res., 12, 381-393.
16. Schultz, N., Lopez, E., Saleh-Gohari, N., Helleday, T. (2003) Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res., 31, 4959-4964.
17. Ying, S., Hamdy, F.C., Helleday, T. (2012) Mre11-dependent degradation of stalled DNA replication forks is prevented by BRCA2 and PARP1. Cancer Res., 72, 2814-2821.
18. Sugimura, K., Takebayashi, S., Taguchi, H., Takeda, S., Okumura, K. (2008) PARP-1 ensures regulation of replication fork progression by homologous recombination on damaged DNA. J. Cell Biol., 183, 1203-1212.
19. Berti, M., Ray Chaudhuri, A., Thangavel, S., Gomathinayagam, S., Kenig, S., Vujanovic, M., Odreman, F., Glatter, T., Graziano, S., Mendoza-Maldonado, R. et al. (2013) Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nat. Struct. Mol. Biol., 20, 347-354.
20. Ray Chaudhuri, A., Hashimoto, Y., Herrador, R., Neelsen, K.J., Fachinetti, D., Bermejo, R., Cocito, A., Costanzo, V., Lopes, M. (2012) Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat. Struct. Mol. Biol., 19, 417-423.
21. Mortusewicz, O., Fouquerel, E., Ame, J.C., Leonhardt, H., Schreiber, V. (2011) PARG is recruited to DNA damage sites through poly(ADP-ribose)- and PCNA-dependent mechanisms. Nucleic Acids Res., 39, 5045-5056.
22. Shirai, H., Poetsch, A.R., Gunji, A., Maeda, D., Fujimori, H., Fujihara, H., Yoshida, T., Ogino, H., Masutani, M. (2013) PARG dysfunction enhances DNA double strand break formation in S-phase after alkylation DNA damage and augments different cell death pathways. Cell Death Dis., 4, e656.
23. Min, W., Cortes, U., Herceg, Z., Tong, W.M., Wang, Z.Q. (2010) Deletion of the nuclear isoform of poly(ADP-ribose) glycohydrolase (PARG) reveals its function in DNA repair, genomic stability and tumorigenesis. Carcinogenesis, 31, 2058-2065.
24. Cortes, U., Tong, W.M., Coyle, D.L., Meyer-Ficca, M.L., Meyer, R.G., Petrilli, V., Herceg, Z., Jacobson, E.L., Jacobson, M.K., Wang, Z.Q. (2004) Depletion of the 110-kilodalton isoform of poly(ADP-ribose) glycohydrolase increases sensitivity to genotoxic and endotoxic stress in mice. Mol. Cell Biol., 24, 7163-7178.
25. Fathers, C., Drayton, R.M., Solovieva, S., Bryant, H.E. (2012) Inhibition of poly(ADP-ribose) glycohydrolase (PARG) specifically kills BRCA2-deficient tumor cells. Cell Cycle, 11, 990-997.
26. Falsig, J., Christiansen, S.H., Feuerhahn, S., Burkle, A., Oei, S.L., Keil, C., Leist, M. (2004) Poly(ADP-ribose) glycohydrolase as a target for neuroprotective intervention: assessment of currently available pharmacological tools. Eur. J. Pharmacol., 497, 7-16.
27. Le May, N., Iltis, I., Ame, J.C., Zhovmer, A., Biard, D., Egly, J.M., Schreiber, V., Coin, F. (2012) Poly (adp-ribose) glycohydrolase regulates retinoic Acid receptor-mediated gene expression. Mol. Cell, 48, 785-798.
28. Shahar, O.D., Raghu Ram, E.V., Shimshoni, E., Hareli, S., Meshorer, E., Goldberg, M. (2012) Live imaging of induced and controlled DNA double-strand break formation reveals extremely low repair by homologous recombination in human cells. Oncogene, 31, 3495-3504.
29. Farmer, H., McCabe, N., Lord, C.J., Tutt, A.N., Johnson, D.A., Richardson, T.B., Santarosa, M., Dillon, K.J., Hickson, I., Knights, C. et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 434, 917-921.
30. Raderschall, E., Golub, E.I., Haaf, T. (1999) Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. U.S.A., 96, 1921-1926.
31. Cheng, Q., Barboule, N., Frit, P., Gomez, D., Bombarde, O., Couderc, B., Ren, G.S., Salles, B., Calsou, P. (2011) Ku counteracts mobilization of PARP1 and MRN in chromatin damaged with DNA double-strand breaks. Nucleic Acids Res., 39, 9605-9619.
32. Mashimo, M., Kato, J., Moss, J. (2013) ADP-ribosyl-acceptor hydrolase 3 regulates poly (ADP-ribose) degradation and cell death during oxidative stress. Proc. Natl. Acad. Sci. U.S.A., 110, 18964-18969.
33. Vassin, V.M., Anantha, R.W., Sokolova, E., Kanner, S., Borowiec, J.A. (2009) Human RPA phosphorylation by ATR stimulates DNA synthesis and prevents ssDNA accumulation during DNA-replication stress. J. Cell Sci., 122, 4070-4080.
34. Anantha, R.W., Vassin, V.M., Borowiec, J.A. (2007) Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J. Biol. Chem., 282, 35910-35923.
35. Jones, R.M., Petermann, E. (2012) Replication fork dynamics and the DNA damage response. The Biochemical journal, 443, 13-26.
36. Sirbu, B.M., Couch, F.B., Feigerle, J.T., Bhaskara, S., Hiebert, S.W., Cortez, D. (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev, 25, 1320-1327.
37. Liaw, H., Lee, D., Myung, K. (2011) DNA-PK-dependent RPA2 hyperphosphorylation facilitates DNA repair and suppresses sister chromatid exchange. PLoS ONE, 6, e21424.
38. Serrano, M.A., Li, Z., Dangeti, M., Musich, P.R., Patrick, S., Roginskaya, M., Cartwright, B., Zou, Y. (2013) DNA-PK, ATM and ATR collaboratively regulate p53-RPA interaction to facilitate homologous recombination DNA repair. Oncogene, 32, 2452-2462.
39. Sartori, A.A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J., Jackson, S.P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
40. Huertas, P., Jackson, S.P. (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem., 284, 9558-9565.
41. Stephan, H., Concannon, C., Kremmer, E., Carty, M.P., Nasheuer, H.P. (2009) Ionizing radiation-dependent and independent phosphorylation of the 32-kDa subunit of replication protein A during mitosis. Nucleic Acids Res., 37, 6028-6041.
42. Ransburgh, D.J., Chiba, N., Ishioka, C., Toland, A.E., Parvin, J.D. (2010) Identification of breast tumor mutations in BRCA1 that abolish its function in homologous DNA recombination. Cancer Res., 70, 988-995.
43. Zhou, Y., Feng, X., Koh, D.W. (2010) Enhanced DNA accessibility and increased DNA damage induced by the absence of poly(ADP-ribose) hydrolysis. Biochemistry, 49, 7360-7366.
44. Haince, J.F., McDonald, D., Rodrigue, A., Dery, U., Masson, J.Y., Hendzel, M.J., Poirier, G.G. (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem., 283, 1197-1208.
45. Dupre, A., Boyer-Chatenet, L., Sattler, R.M., Modi, A.P., Lee, J.H., Nicolette, M.L., Kopelovich, L., Jasin, M., Baer, R., Paull, T.T. et al. (2008) A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nat. Chem. Biol., 4, 119-125.
46. Eki, T., Hurwitz, J. (1991) Influence of poly(ADP-ribose) polymerase on the enzymatic synthesis of SV40 DNA. J. Biol. Chem., 266, 3087-3100.
47. Jungmichel, S., Rosenthal, F., Altmeyer, M., Lukas, J., Hottiger, M.O., Nielsen, M.L. (2013) Proteome-wide identification of poly(ADP-ribosyl)ation targets in different genotoxic stress responses. Mol. Cell, 52, 272-285.
48. Pestryakov, P.E., Weisshart, K., Schlott, B., Khodyreva, S.N., Kremmer, E., Grosse, F., Lavrik, O.I., Nasheuer, H.P. (2003) Human replication protein A. The C-terminal RPA70 and the central RPA32 domains are involved in the interactions with the 3'-end of a primer-template DNA. J. Biol. Chem., 278, 17515-17524.
49. Shi, W., Feng, Z., Zhang, J., Gonzalez-Suarez, I., Vanderwaal, R.P., Wu, X., Powell, S.N., Roti Roti, J.L., Gonzalo, S. (2010) The role of RPA2 phosphorylation in homologous recombination in response to replication arrest. Carcinogenesis, 31, 994-1002.
50. Liu, S., Opiyo, S.O., Manthey, K., Glanzer, J.G., Ashley, A.K., Amerin, C., Troksa, K., Shrivastav, M., Nickoloff, J.A., Oakley, G.G. (2012) Distinct roles for DNA-PK, ATM and ATR in RPA phosphorylation and checkpoint activation in response to replication stress. Nucleic Acids Res., 40, 10780-10794.
51. Shao, R.G., Cao, C.X., Zhang, H., Kohn, K.W., Wold, M.S., Pommier, Y. (1999) Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA:DNA-PK complexes. EMBO J., 18, 1397-1406.
52. Ruscetti, T., Lehnert, B.E., Halbrook, J., Le Trong, H., Hoekstra, M.F., Chen, D.J., Peterson, S.R. (1998) Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J. Biol. Chem., 273, 14461-14467.
53. Sajish, M., Zhou, Q., Kishi, S., Valdez, D.M. Jr., Kapoor, M., Guo, M., Lee, S., Kim, S., Yang, X.L., Schimmel, P. (2012) Trp-tRNA synthetase bridges DNA-PKcs to PARP-1 to link IFN-gamma and p53 signaling. Nat. Chem. Biol., 8, 547-554.
54. Blackwell, L.J., Borowiec, J.A., Mastrangelo, I.A. (1996) Single-stranded-DNA binding alters human replication protein A structure and facilitates interaction with DNA-dependent protein kinase. Mol. Cell Biol., 16, 4798-4807.
55. Brosey, C.A., Chagot, M.E., Ehrhardt, M., Pretto, D.I., Weiner, B.E., Chazin, W.J. (2009) NMR analysis of the architecture and functional remodeling of a modular multidomain protein, RPA. J. Am. Chem. Soc., 131, 6346-6347.
56. Pleschke, J.M., Kleczkowska, H.E., Strohm, M., Althaus, F.R. (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem., 275, 40974-40980.
57. Gagne, J.P., Pic, E., Isabelle, M., Krietsch, J., Ethier, C., Paquet, E., Kelly, I., Boutin, M., Moon, K.M., Foster, L.J. et al. (2012) Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res., 40, 7788-7805.
58. Toledo, L.I., Altmeyer, M., Rask, M.B., Lukas, C., Larsen, D.H., Povlsen, L.K., Bekker-Jensen, S., Mailand, N., Bartek, J., Lukas, J. (2013) ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell, 155, 1088-1103.
59. Fernandez-Capetillo, O., Nussenzweig, A. (2013) Naked replication forks break apRPArt. Cell, 155, 979-980.
60. Sleeth, K.M., Sorensen, C.S., Issaeva, N., Dziegielewski, J., Bartek, J., Helleday, T. (2007) RPA mediates recombination repair during replication stress and is displaced from DNA by checkpoint signalling in human cells. J. Mol. Biol., 373, 38-47.
61. Metzger, M.J., Stoddard, B.L., Monnat, R.J. Jr. (2013) PARP-mediated repair, homologous recombination, and back-up non-homologous end joining-like repair of single-strand nicks. DNA Repair (Amst.), 12, 529-534.
62. Gunji, A., Fujihara, H., Kamada, N., Omura, K., Jishage, K.I., Nakagama, H., Sugimura, T., Masutani, M. (2003) Lack of altered frequency of sister-chromatid exchanges in poly(ADP-ribose) glycohydrolase-deficient mouse ES cells treated with methylmethanesulfonate. Proc. Japan Acad., 79, 305-307.
63. Shirai, H., Fujimori, H., Gunji, A., Maeda, D., Hirai, T., Poetsch, A.R., Harada, H., Yoshida, T., Sasai, K., Okayasu, R. et al. (2013) Parg deficiency confers radio-sensitization through enhanced cell death in mouse ES cells exposed to various forms of ionizing radiation. Biochem. Biophys. Res. Commun., 435, 100-106.
64. Feng, X., Koh, D.W. (2013) Inhibition of poly(ADP-ribose) polymerase-1 or poly(ADPribose) glycohydrolase individually, but not in combination, leads to improved chemotherapeutic efficacy in HeLa cells. Int. J. Oncol., 42, 749-756.