Poly(ADP-ribosyl) glycohydrolase prevents the accumulation of unusual replication structures during unperturbed S phase

Molecular and Cellular Biology

Volumn 35, Issue 5, 2015, Pages 856-865

  Chaudhuri, Arnab Ray ^a,b   Ahuja, Akshay Kumar ^a   Herrador, Raquel ^a   Lopes, Massimo ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

53BP1 PROTEIN; ATM PROTEIN; ATR PROTEIN; GLYCOSIDASE; HISTONE H2AX; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLY(ADP RIBOSYL) GLYCOHYDROLASE; PROTEIN; PROTEIN P53; RAD51 PROTEIN; SINGLE STRANDED DNA; SMALL INTERFERING RNA; TANNIN; UNCLASSIFIED DRUG; ARHGAP29 PROTEIN, HUMAN; ATM PROTEIN, HUMAN; ATR PROTEIN, HUMAN; CHROMATIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; POLY ADP-RIBOSE GLYCOHYDROLASE; RAD51 PROTEIN, HUMAN; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN;

ARTICLE; BIOACCUMULATION; CANCER CHEMOTHERAPY; CELL CYCLE S PHASE; CELL PROLIFERATION; CHROMATIN; CHROMOSOME BREAKAGE; CHROMOSOME REPLICATION; CHROMOSOME STRUCTURE; DNA REPLICATION; DNA SYNTHESIS; DOUBLE STRANDED DNA BREAK; ELECTRON MICROSCOPY; ENZYME INHIBITION; FEMALE; GENE IDENTIFICATION; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN CHROMOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; CONFOCAL MICROSCOPY; DNA DAMAGE; DNA REPAIR; HELA CELL LINE; METABOLISM; PHENOTYPE;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL PROLIFERATION; CHROMATIN; DNA DAMAGE; DNA REPAIR; DNA, SINGLE-STRANDED; GLYCOSIDE HYDROLASES; GTPASE-ACTIVATING PROTEINS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; PHENOTYPE; RAD51 RECOMBINASE; S PHASE;

EID: 84922196613     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01077-14     Document Type: Article

References (45)

1. Gibson BA, Kraus WL. 2012. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13:411- 424. http://dx.doi.org/10.1038/nrm3376.
2. Bouchard VJ, Rouleau M, Poirier GG. 2003. PARP-1, a determinant of cell survival in response to DNA damage. Exp Hematol 31:446-454. http: //dx.doi.org/10.1016/S0301-472X(03)00083-3.
3. Woodhouse BC, Dianov GL. 2008. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair (Amst) 7:1077-1086. http://dx.doi.org/10.1016/j.dnarep.2008.03.009.
4. de Murcia JM, Niedergang C, Trucco C, Ricoul M, Dutrillaux B, Mark M, Oliver FJ, Masson M, Dierich A, LeMeur M, Walztinger C, Chambon P, de Murcia G. 1997. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc Natl Acad Sci U S A 94:7303-7307. http://dx.doi.org/10.1073/pnas.94.14.7303.
5. Ménissier de Murcia J, Ricoul M, Tartier L, Niedergang C, Huber A, Dantzer F, Schreiber V, Ame JC, Dierich A, LeMeur M, Sabatier L, Chambon P, de Murcia G. 2003. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J 22:2255-2263. http://dx.doi.org/10.1093/emboj/cdg206.
6. Wang ZQ, Stingl L, Morrison C, Jantsch M, Los M, Schulze-Osthoff K, Wagner EF. 1997. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev 11:2347-2358. http://dx.doi.org/10.1101 /gad.11.18.2347.
7. Anders CK, Winer EP, Ford JM, Dent R, Silver DP, Sledge GW, Carey LA. 2010. Poly(ADP-ribose) polymerase inhibition: "targeted" therapy for triple-negative breast cancer. Clin Cancer Res 16:4702-4710. http://dx.doi.org/10.1158/1078-0432.CCR-10-0939.
8. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T. 2005. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434:913-917. http://dx.doi.org/10.1038/nature03443.
9. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, Martin NM, Jackson SP, Smith GC, Ashworth A. 2005. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:917-921. http://dx.doi.org/10.1038/nature03445.
10. 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. Mol Cell 37:492-502. http://dx.doi.org/10.1016/j.molcel.2010.01.021.
11. Ray Chaudhuri A, Hashimoto Y, Herrador R, Neelsen KJ, 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. http://dx.doi.org/10.1038/nsmb.2258.
12. Berti M, Ray Chaudhuri A, Thangavel S, Gomathinayagam S, Kenig S, Vujanovic M, Odreman F, Glatter T, Graziano S, Mendoza-Maldonado R, Marino F, Lucic B, Biasin V, Gstaiger M, Aebersold R, Sidorova JM, Monnat RJ, Jr, Lopes M, Vindigni A. 2013. Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nat Struct Mol Biol 20:347-354. http://dx.doi.org/10.1038/nsmb.2501.
13. Gagné JP, Hendzel MJ, Droit A, Poirier GG. 2006. The expanding role of poly(ADP-ribose) metabolism: current challenges and new perspectives. Curr Opin Cell Biol 18:145-151. http://dx.doi.org/10.1016/j.ceb.2006.02.013.
14. Min W, Wang ZQ. 2009. Poly (ADP-ribose) glycohydrolase (PARG) and its therapeutic potential. Front Biosci 14:1619-1626. http://dx.doi.org/10.2741/3329.
15. Meyer-Ficca ML, Meyer RG, Coyle DL, Jacobson EL, Jacobson MK. 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. http://dx.doi.org/10.1016/j.yexcr.2004.03.050.
16. 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. http://dx.doi.org/10.1096/fj.09-133264.
17. Feng X, Zhou Y, Proctor AM, Hopkins MM, Liu M, Koh DW. 2012. Silencing of apoptosis-inducing factor and poly(ADP-ribose) glycohydrolase reveals novel roles in breast cancer cell death after chemotherapy. Mol Cancer 11:48. http://dx.doi.org/10.1186/1476-4598-11-48.
18. Koh DW, Lawler AM, Poitras MF, Sasaki M, Wattler S, Nehls MC, Stoger T, Poirier GG, Dawson VL, Dawson TM. 2004. Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad SciUSA101:17699-17704. http://dx.doi.org/10.1073/pnas.0406182101.
19. Cortes U, Tong WM, Coyle DL, Meyer-Ficca ML, Meyer RG, Petrilli V, Herceg Z, Jacobson EL, Jacobson MK, Wang ZQ. 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. http://dx.doi.org/10.1128/MCB.24.16.7163-7178.2004.
20. Fisher AE, Hochegger H, Takeda S, Caldecott KW. 2007. Poly(ADPribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol Cell Biol 27:5597-5605. http://dx.doi.org/10.1128/MCB.02248-06.
21. Mortusewicz O, Fouquerel E, Ame JC, 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. http: //dx.doi.org/10.1093/nar/gkr099.
22. Amé JC, Fouquerel E, Gauthier LR, Biard D, Boussin FD, Dantzer F, de Murcia G, Schreiber V. 2009. Radiation-induced mitotic catastrophe in PARG-deficient cells. J Cell Sci 122:1990-2002. http://dx.doi.org/10.1242 /jcs.039115.
23. Fathers C, Drayton RM, Solovieva S, Bryant HE. 2012. Inhibition of poly(ADP-ribose) glycohydrolase (PARG) specifically kills BRCA2- deficient tumor cells. Cell Cycle 11:990-997. http://dx.doi.org/10.4161/cc.11.5.19482.
24. Illuzzi G, Fouquerel E, Ame JC, Noll A, Rehmet K, Nasheuer HP, Dantzer F, Schreiber V. 2014. 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 Res 42:7776-7792. http://dx.doi.org/10.1093/nar/gku505.
25. Jackson DA, Pombo A. 1998. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140:1285-1295. http://dx.doi.org/10.1083/jcb.140.6.1285.
26. Neelsen KJ, Chaudhuri AR, Follonier C, Herrador R, Lopes M. 2014. Visualization and interpretation of eukaryotic DNA replication intermediates in vivo by electron microscopy. Methods Mol Biol 1094:177-208. http://dx.doi.org/10.1007/978-1-62703-706-8_15.
27. Formentini L, Arapistas P, Pittelli M, Jacomelli M, Pitozzi V, Menichetti S, Romani A, Giovannelli L, Moroni F, Chiarugi A. 2008. Mono-galloyl glucose derivatives are potent poly(ADP-ribose) glycohydrolase (PARG) inhibitors and partially reduce PARP-1-dependent cell death. Br J Pharmacol 155:1235-1249. http://dx.doi.org/10.1038/bjp.2008.370.
28. Oakley GG, Patrick SM. 2010. Replication protein A: directing traffic at the intersection of replication and repair. Front Biosci (Landmark ed) 15:883-900. http://dx.doi.org/10.2741/3652.
29. Follonier C, Oehler J, Herrador R, Lopes M. 3 March 2013, posting date. Friedreich's ataxia-associated GAA repeats induce replication-fork reversal and unusual molecular junctions. Nat Struct Mol Biol http://dx.doi.org/10.1038/nsmb.2520.
30. Akbari M, Krokan HE. 2008. Cytotoxicity and mutagenicity of endoge- nous DNA base lesions as potential cause of human aging. Mech Ageing Dev 129:353-365. http://dx.doi.org/10.1016/j.mad.2008.01.007.
31. Mirkin SM. 2007. Expandable DNA repeats and human disease. Nature 447:932-940. http://dx.doi.org/10.1038/nature05977.
32. Neelsen KJ, Lopes M. Replication fork reversal in eukaryotes: from dead end to dynamic response. Nat Rev Mol Cell Biol, in press.
33. Neelsen KJ, Zanini IM, Herrador R, Lopes M. 2013. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J Cell Biol 200:699-708. http://dx.doi.org/10.1083/jcb.201212058.
34. Zellweger R, Dalcher D, Mutreja K, Berti M, Schmid J, Herrador R, Vindigni A, Lopes M. Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells. J Cell Biol, in press.
35. Min W, Bruhn C, Grigaravicius P, Zhou ZW, Li F, Kruger A, Siddeek B, Greulich KO, Popp O, Meisezahl C, Calkhoven CF, Burkle A, Xu X, Wang ZQ. 2013. Poly(ADP-ribose) binding to Chk1 at stalled replication forks is required for S-phase checkpoint activation. Nat Commun 4:2993. http://dx.doi.org/10.1038/ncomms3993.
36. Heller RC, Marians KJ. 2006. Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439:557-562. http://dx.doi.org/10.1038/nature04329.
37. Lopes M, Foiani M, Sogo JM. 2006. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell 21:15-27. http://dx.doi.org/10.1016/j.molcel.2005.11.015.
38. Cotta-Ramusino C, Fachinetti D, Lucca C, Doksani Y, Lopes M, Sogo J, Foiani M. 2005. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol Cell 17:153-159. http://dx.doi.org/10.1016/j.molcel.2004.11.032.
39. Hu J, Sun L, Shen F, Chen Y, Hua Y, Liu Y, Zhang M, Hu Y, Wang Q, Xu W, Sun F, Ji J, Murray JM, Carr AM, Kong D. 2012. The intra-S phase checkpoint targets Dna2 to prevent stalled replication forks from reversing. Cell 149:1221-1232. http://dx.doi.org/10.1016/j.cell.2012.04.030.
40. Hashimoto Y, Ray Chaudhuri A, Lopes M, Costanzo V. 2010. Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nat Struct Mol Biol 17:1305-1311. http://dx.doi.org/10.1038/nsmb.1927.
41. Schlacher K, Christ N, Siaud N, Egashira A, Wu H, Jasin M. 2011. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145:529-542. http: //dx.doi.org/10.1016/j.cell.2011.03.041.
42. Schlacher K, Wu H, Jasin M. 2012. A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51- BRCA1/2. Cancer Cell 22:106-116. http://dx.doi.org/10.1016/j.ccr.2012.05.015.
43. Tentori L, Leonetti C, Scarsella M, Muzi A, Vergati M, Forini O, Lacal PM, Ruffini F, Gold B, Li W, Zhang J, Graziani G. 2005. Poly(ADPribose) glycohydrolase inhibitor as chemosensitiser of malignant melanoma for temozolomide. Eur J Cancer 41:2948-2957. http://dx.doi.org /10.1016/j.ejca.2005.08.027.
44. Slade D, Dunstan MS, Barkauskaite E, Weston R, Lafite P, Dixon N, Ahel M, Leys D, Ahel I. 2011. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 477:616-620. http://dx.doi.org/10.1038/nature10404.
45. Sharifi R, Morra R, Appel CD, Tallis M, Chioza B, Jankevicius G, Simpson MA, Matic I, Ozkan E, Golia B, Schellenberg MJ, Weston R, Williams JG, Rossi MN, Galehdari H, Krahn J, Wan A, Trembath RC, Crosby AH, Ahel D, Hay R, Ladurner AG, Timinszky G, Williams RS, Ahel I. 2013. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J 32:1225-1237. http://dx.doi.org/10.1038/emboj.2013.51.