Sumoylation regulates EXO1 stability and processing of DNA damage

Cell Cycle

Volumn 14, Issue 15, 2015, Pages 2439-2450

  Bologna, Serena ^a   Altmannova, Veronika ^b   Valtorta, Emanuele ^c   Koenig, Christiane ^a   Liberali, Prisca ^a   Gentili, Christian ^a   Anrather, Dorothea ^d   Ammerer, Gustav ^d   Pelkmans, Lucas ^a   Krejci, Lumir ^b,e   Ferrari, Stefano ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MASARYK UNIVERSITY   (Czech Republic)

^c Niguarda Cancer Center   (Italy)

^d UNIVERSITY OF VIENNA   (Austria)

^e ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

Author keywords

Chromosome aberrations; DNA resection; Exonuclease 1; Sumoylation; Ubiquitylation

Indexed keywords

CAMPTOTHECIN; EXO1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CYSTEINE PROTEINASE; DNA LIGASE; EXO1 PROTEIN, HUMAN; EXODEOXYRIBONUCLEASE; PIAS1 PROTEIN, HUMAN; PIAS4 PROTEIN, HUMAN; PROTEIN INHIBITOR OF ACTIVATED STAT; SACCHAROMYCES CEREVISIAE PROTEIN; SENP6 PROTEIN, HUMAN; SIZ1 PROTEIN, S CEREVISIAE; SIZ2 PROTEIN, S CEREVISIAE; SUMO 1 PROTEIN; SUMO PROTEIN; SUMO1 PROTEIN, HUMAN; SUMO2 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE; UBIQUITIN-CONJUGATING ENZYME UBC9;

ARTICLE; CELL CYCLE PHASE; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STABILITY; SUMOYLATION; U2OS CELL LINE; UBIQUITINATION; CELL LINE; DOUBLE STRANDED DNA BREAK; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CAMPTOTHECIN; CELL LINE; CYSTEINE ENDOPEPTIDASES; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPAIR ENZYMES; EXODEOXYRIBONUCLEASES; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMO-1 PROTEIN; SUMOYLATION; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84943777973     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.1080/15384101.2015.1060381     Document Type: Article

References (49)

1. Curtin NJ. DNA repair dysregulation from cancer driver to therapeutic target. Nat Rev Cancer 2012; 12: 801-17; PMID: 23175119; http://dx. doi. org/10. 1038/nrc3399.
2. Whitby MC. Making crossovers during meiosis. Biochem Soc Trans 2005; 33: 1451-5; PMID: 16246144; http://dx. doi. org/10. 1042/BST20051451.
3. Bassing CH, Swat W, Alt FW. The mechanism and regulation of chromosomal V(D)J recombination. Cell 2002; 109: S45-55; PMID: 11983152; http://dx. doi. org/10. 1016/S0092-8674(02)00675-X.
4. Errico A, Costanzo V. Mechanisms of replication fork protection: a safeguard for genome stability. Critical Rev Biochem Mol Biol 2012; 47: 222-35; PMID: 22324461; http://dx. doi. org/10. 3109/10409238. 2012. 655374.
5. Eid W, Steger M, El-Shemerly M, Ferretti LP, Pena-Diaz J, Konig C, Valtorta E, Sartori AA, Ferrari S. DNA end resection by CtIP and exonuclease 1 prevents genomic instability. EMBO Rep 2010; 11: 962-8; PMID: 21052091; http://dx. doi. org/10. 1038/embor. 2010. 157.
6. Thompson LH. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutation Res 2012; 751: 158-246; PMID: 22743550; http://dx. doi. org/10. 1016/j. mrrev. 2012. 06. 002.
7. Nimonkar AV, Genschel J, Kinoshita E, Polaczek P, Campbell JL, Wyman C, Modrich P, Kowalczykowski SC. BLM-DNA2-RPA-MRN and EXO1-BLM-RPAMRN constitute two DNA end resection machineries for human DNA break repair. Genes Devel 2011; 25: 350-62; PMID: 21325134; http://dx. doi. org/10. 1101/gad. 2003811.
8. Karanja KK, Cox SW, Duxin JP, Stewart SA, Campbell JL. DNA2 and EXO1 in replication-coupled, homology-directed repair and in the interplay between HDR and the FA/BRCA network. Cell Cycle 2012; 11: 3983-96; PMID: 22987153; http://dx. doi. org/10. 4161/cc. 22215.
9. Szankasi P, Smith GR. A DNA exonuclease induced during meiosis of Schizosaccharomyces pombe. J Biol Chem 1992; 267: 3014-23; PMID: 1737756.
10. Tishkoff DX, Amin NS, Viars CS, Arden KC, Kolodner RD. Identification of a human gene encoding a homologue of Saccharomyces cerevisiae EXO1, an exonuclease implicated in mismatch repair and recombination. Cancer Res 1998; 58: 5027-31; PMID: 9823303.
11. Lee BI, Wilson DM 3rd. The RAD2 domain of human exonuclease 1 exhibits 50 to 30 exonuclease and flap structure-specific endonuclease activities. J Biol Chem 1999; 274: 37763-9; PMID: 10608837; http://dx. doi. org/10. 1074/jbc. 274. 53. 37763.
12. Szankasi P, Smith GR. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 1995; 267: 1166-9; PMID: 7855597; http://dx. doi. org/10. 1126/science. 7855597.
13. Fiorentini P, Huang KN, Tishkoff DX, Kolodner RD, Symington LS. Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol 1997; 17: 2764-73; PMID: 9111347.
14. Kirkpatrick DT, Ferguson JR, Petes TD, Symington LS. Decreased meiotic intergenic recombination and increased meiosis I nondisjunction in exo1 mutants of Saccharomyces cerevisiae. Genetics 2000; 156: 1549-57; PMID: 11102356.
15. Tsubouchi H, Ogawa H. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol Biol Cell 2000; 11: 2221-33; PMID: 10888664; http://dx. doi. org/10. 1091/mbc. 11. 7. 2221.
16. Mimitou EP, Symington LS. DNA end resection: many nucleases make light work. DNA Repair (Amst) 2009; 8: 983-95; PMID: 19473888; http://dx. doi. org/10. 1016/j. dnarep. 2009. 04. 017.
17. Qiu J, Qian Y, Chen V, Guan MX, Shen B. Human exonuclease 1 functionally complements its yeast homologues in DNA recombination, RNA primer removal, and mutation avoidance. J Biol Chem 1999; 274: 17893-900; PMID: 10364235; http://dx. doi. org/10. 1074/jbc. 274. 25. 17893.
18. Cotta-Ramusino C, Fachinetti D, Lucca C, Doksani Y, Lopes M, Sogo J, Foiani M. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol Cell 2005; 17: 153-9; PMID: 15629726; http://dx. doi. org/10. 1016/j. molcel. 2004. 11. 032.
19. Bologna S, Ferrari S. It takes two to tango: Ubiquitin and SUMO in the DNA damage response. Front Genet 2013; 4: 106; PMID: 23781231; http://dx. doi. org/10. 3389/fgene. 2013. 00106.
20. Bennetzen MV, Larsen DH, Dinant C, Watanabe S, Bartek J, Lukas J, Andersen JS. Acetylation dynamics of human nuclear proteins during the ionizing radiationinduced DNA damage response. Cell Cycle 2013; 12: 1688-95; PMID: 23656789; http://dx. doi. org/10. 4161/cc. 24758.
21. Jackson SP, Durocher D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol Cell 2013; 49: 795-807; PMID: 23416108; http://dx. doi. org/10. 1016/j. molcel. 2013. 01. 017.
22. Engels K, Giannattasio M, Muzi-Falconi M, Lopes M, Ferrari S. Fourteen-3-3 proteins regulate exonuclease 1-dependent processing of stalled replication forks. PLoS Genet 2011; 7: e1001367; PMID: 21533173; http://dx. doi. org/10. 1371/journal. pgen. 1001367.
23. El-Shemerly M, Janscak P, Hess D, Jiricny J, Ferrari S. Degradation of human exonuclease 1b upon DNA synthesis inhibition. Cancer Res 2005; 65: 3604-9; PMID: 15867354; http://dx. doi. org/10. 1158/0008-5472. CAN-04-4069.
24. El-Shemerly M, Hess D, Pyakurel AK, Moselhy S, Ferrari S. ATR-dependent pathways control hEXO1 stability in response to stalled forks. Nucleic Acids Res 2008; 36: 511-9; PMID: 18048416; http://dx. doi. org/10. 1093/nar/gkm1052.
25. Bolderson E, Tomimatsu N, Richard DJ, Boucher D, Kumar R, Pandita TK, Burma S, Khanna KK. Phosphorylation of Exo1 modulates homologous recombination repair of DNA double-strand breaks. Nucleic Acids Res 2010; 38: 1821-31; PMID: 20019063; http://dx. doi. org/10. 1093/nar/gkp1164.
26. Morin I, Ngo HP, Greenall A, Zubko MK, Morrice N, Lydall D. Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J 2008; 27: 2400-10; PMID: 18756267; http://dx. doi. org/10. 1038/emboj. 2008. 171.
27. Tomimatsu N, Mukherjee B, Catherine Hardebeck M, Ilcheva M, Vanessa Camacho C, Louise Harris J, Porteus M, Llorente B, Khanna KK, Burma S. Phosphorylation of EXO1 by CDKs 1 and 2 regulates DNA end resection and repair pathway choice. Nature Commun 2014; 5: 3561; PMID: 24705021; http://dx. doi. org/10. 1038/ncomms4561.
28. Altmannova V, Eckert-Boulet N, Arneric M, Kolesar P, Chaloupkova R, Damborsky J, Sung P, Zhao X, Lisby M, Krejci L. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res 2010; 38: 4708-21; PMID: 20371517; http://dx. doi. org/10. 1093/nar/gkq195.
29. Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, Jackson SP. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009; 462: 935-9; PMID: 20016603; http://dx. doi. org/10. 1038/nature08657.
30. Forment JV, Walker RV, Jackson SP. A high-throughput, flow cytometry-based method to quantify DNAend resection in mammalian cells. Cytometry Part A 2012; 81: 922-8; PMID: 22893507; http://dx. doi. org/10. 1002/cyto. a. 22155.
31. Smits VA, Gillespie DA. Cancer therapy. Targeting the poison within. Cell Cycle 2014; 13: 2330-3; PMID: 25483183; http://dx. doi. org/10. 4161/cc. 29756.
32. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-74; PMID: 21376230; http://dx. doi. org/10. 1016/j. cell. 2011. 02. 013.
33. Lieber MR. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 2010; 79: 181-211; PMID: 20192759; http://dx. doi. org/10. 1146/annurev. biochem. 052308. 093131.
34. Wogan GN, Hecht SS, Felton JS, Conney AH, Loeb LA. Environmental and chemical carcinogenesis. Semin Cancer Biol 2004; 14: 473-86; PMID: 15489140; http://dx. doi. org/10. 1016/j. semcancer. 2004. 06. 010.
35. Altmannova V, Kolesar P, Krejci L. SUMO Wrestles with Recombination. Biomolecules 2012; 2: 350-75; PMID: 24970142; http://dx. doi. org/10. 3390/biom2030350.
36. Genschel J, Modrich P. Mechanism of 50-directed excision in human mismatch repair. Mol Cell 2003; 12: 1077-86; PMID: 14636568; http://dx. doi. org/10. 1016/S1097-2765(03)00428-3.
37. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008; 134: 981-94; PMID: 18805091; http://dx. doi. org/10. 1016/j. cell. 2008. 08. 037.
38. Mimitou EP, Symington LS. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 2008; 455: 770-4; PMID: 18806779; http://dx. doi. org/10. 1038/nature07312.
39. Gravel S, Chapman JR, Magill C, Jackson SP. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev 2008; 22: 2767-72; PMID: 18923075; http://dx. doi. org/10. 1101/gad. 503108.
40. Sertic S, Pizzi S, Cloney R, Lehmann AR, Marini F, Plevani P, Muzi-Falconi M. Human exonuclease 1 connects nucleotide excision repair (NER) processing with checkpoint activation in response to UV irradiation. Proc Natl Acad Sci U S A 2011; 108: 13647-52; PMID: 21808022; http://dx. doi. org/10. 1073/pnas. 1108547108.
41. Tatham MH, Matic I, Mann M, Hay RT. Comparative proteomic analysis identifies a role for SUMO in protein quality control. Science Signal 2011; 4: rs4; PMID: 21693764; http://dx. doi. org/10. 1126/scisignal. 2001484.
42. Hendriks IA, D'Souza RC, Yang B, Verlaan-de Vries M, Mann M, Vertegaal AC. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 2014; 21: 927-36; PMID: 25218447.
43. Galanty Y, Belotserkovskaya R, Coates J, Jackson SP. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev 2012; 26: 1179-95; PMID: 22661229; http://dx. doi. org/10. 1101/gad. 188284. 112.
44. Yin Y, Seifert A, Chua JS, Maure JF, Golebiowski F, Hay RT. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev 2012; 26: 1196-208; PMID: 22661230; http://dx. doi. org/10. 1101/gad. 189274. 112.
45. Guo Z, Kanjanapangka J, Liu N, Liu S, Liu C, Wu Z, Wang Y, Loh T, Kowolik C, Jamsen J, et al. Sequential posttranslational modifications program FEN1 degradation during cell-cycle progression. Molecular cell 2012; 47: 444-56; PMID: 22749529; http://dx. doi. org/10. 1016/j. molcel. 2012. 05. 042.
46. Doerfler Z, Schmidt KH. Exo1 phosphorylation status controls the hydroxyurea sensitivity of cells lacking the Pol32 subunit of DNA polymerases delta and zeta. DNA Repair (Amst) 2014; 24: 26-36; PMID: 25457771; http://dx. doi. org/10. 1016/j. dnarep. 2014. 10. 004.
47. Muthuswami M, Ramesh V, Banerjee S, Viveka Thangaraj S, Periasamy J, Bhaskar Rao D, Barnabas GD, Raghavan S, Ganesan K. Breast tumors with elevated expression of 1q candidate genes confer poor clinical outcome and sensitivity to Ras/PI3K inhibition. PloS one 2013; 8: e77553; PMID: 24147022; http://dx. doi. org/10. 1371/journal. pone. 0077553.
48. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006; 7: R100; PMID: 17076895; http://dx. doi. org/10. 1186/gb-2006-7-10-r100.
49. Liberali P, Snijder B, Pelkmans L. A hierarchical map of regulatory genetic interactions in membrane trafficking. Cell 2014; 157: 1473-87; PMID: 24906158; http://dx. doi. org/10. 1016/j. cell. 2014. 04. 029.