Histone deacetylase inhibitors selectively target homology dependent DNA repair defective cells and elevate non-homologous endjoining activity

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Smith, Stephanie ^a   Fox, Jennifer ^a   Mejia, Marco ^b   Ruangpradit, Wanvipa ^b   Saberi, Alihossein ^c   Kim, Sunmi ^a,c,d   Choi, Yongjun ^a   Oh, Sehyun ^g   Wang, Yucai ^e,f   Choi, Kyungho ^d   Li, Lei ^e   Hendrickson, Eric A ^g   Takeda, Shunichi ^c   Muller, Mark ^b   Myung, Kyungjae ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d Seoul National University   (South Korea)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f UNIVERSITY OF TEXAS   (United States)

^g UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; PROTEIN ATAD5; RAD54 PROTEIN; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; HIGH THROUGHPUT SCREENING; HOMOLOGY DEPENDENT DNA REPAIR; HUMAN; HUMAN CELL; NONHUMAN; SENSITIVITY ANALYSIS;

ANIMALS; ANTIGENS, NUCLEAR; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CHICKENS; DNA DAMAGE; DNA END-JOINING REPAIR; DNA REPAIR; DNA-BINDING PROTEINS; ELECTROPHORESIS, GEL, PULSED-FIELD; FLUORESCENT ANTIBODY TECHNIQUE; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; LUCIFERASES; MUTATION; NEOPLASMS; RAD51 RECOMBINASE; RECQ HELICASES; RNA, SMALL INTERFERING;

EID: 84899847162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087203     Document Type: Article

References (54)

1. Smith S, Sikdar N, Liaw H, Lee K, Myung K (2009) Pathways for suppressing and promoting gross chromosomal rearrangements in Saccharomyces cerevesiae. In: Witt SN, editor. Yeast as a Model for Human Disease. Kerala, India: Transworld Research Network. pp. 249-276.
2. Krejci L, Altmannova V, Spirek M, Zhao X (2012) Homologous recombination and its regulation. Nucleic Acids Research 40: 5795-5818.
3. Chapman JR, Taylor MRG, Boulton SJ (2012) Playing the End Game: DNA Double-Strand Break Repair Pathway Choice. Molecular Cell 47: 497-510.
4. Roy R, Chun J, Powell SN (2012) BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat Rev Cancer 12: 68-78.
5. Chu WK, Hickson ID (2009) RecQ helicases: multifunctional genome caretakers. Nat Rev Cancer 9: 644-654.
6. Hu Y, Raynard S, Sehorn MG, Lu X, Bussen W, et al. (2007) RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes & Development 21: 3073-3084. (Pubitemid 350223525)
7. Sommers JA, Rawtani N, Gupta R, Bugreev DV, Mazin AV, et al. (2009) FANCJ Uses Its Motor ATPase to Destabilize Protein-DNA Complexes, Unwind Triplexes, and Inhibit RAD51 Strand Exchange. Journal of Biological Chemistry 284: 7505-7517.
8. Moldovan G-L, Dejsuphong D, Petalcorin MIR, Hofmann K, Takeda S, et al. (2012) Inhibition of Homologous Recombination by the PCNA-Interacting Protein PARI. Molecular Cell 45: 75-86.
9. Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O'Neil NJ, et al. (2008) RTEL1 Maintains Genomic Stability by Suppressing Homologous Recombination. Cell 135: 261-271.
10. Mathew CG (2006) Fanconi anaemia genes and susceptibility to cancer. Oncogene 25: 5875-5884.
11. Douglas P, Gupta S, Morrice N, Meek K, Lees-Miller SP (2005) DNA-PK-dependent phosphorylation of Ku70/80 is not required for non-homologous end joining. DNA Repair 4: 1006-1018. (Pubitemid 40966971)
12. Wang Y-G, Nnakwe C, Lane WS, Modesti M, Frank KM (2004) Phosphorylation and Regulation of DNA Ligase IV Stability by DNA-dependent Protein Kinase. Journal of Biological Chemistry 279: 37282-37290. (Pubitemid 39195434)
13. Yu Y, Wang W, Ding Q, Ye R, Chen D, et al. (2003) DNA-PK phosphorylation sites in XRCC4 are not required for survival after radiation or for V(D)J recombination. DNA Repair 2: 1239-1252. (Pubitemid 37340180)
14. Goodarzi AA, Yu Y, Riballo E, Douglas P, Walker SA, et al. (2006) DNA-PK autophosphorylation facilitates Artemis endonuclease activity.
15. Lieber MR (2010) The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway. Annual Review of Biochemistry 79: 181-211.
16. Kasparek TR, Humphrey TC (2011) DNA double-strand break repair pathways, chromosomal rearrangements and cancer. Seminars in Cell & Developmental Biology 22: 886-897.
17. Kirchgessner C, Patil C, Evans J, Cuomo C, Fried L, et al. (1995) DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 24: 1178-1183.
18. Blunt T, Finnie NJ, Taccioli GE, Smith GCM, Demengeot J, et al. (1995) Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80: 813-823.
19. Peterson SR, Kurimasa A, Oshimura M, Dynan WS, Bradbury EM, et al. (1995) Loss of the catalytic subunit of the DNA-dependent protein kinase in DNA double-strand-break-repair mutant mammalian cells. Proceedings of the National Academy of Sciences 92: 3171-3174.
20. Miller RD, Hogg J, Ozaki JH, Gell D, Jackson SP, et al. (1995) Gene for the catalytic subunit of mouse DNA-dependent protein kinase maps to the scid locus. Proceedings of the National Academy of Sciences 92: 10792-10795.
21. Lee GE, Kim JH, Taylor M, Muller MT (2010) DNA Methyltransferase 1-associated Protein (DMAP1) Is a Co-repressor That Stimulates DNA Methylation Globally and Locally at Sites of Double Strand Break Repair. Journal of Biological Chemistry 285: 37630-37640.
22. Lee B, Morano A, Porcellini A, Muller MT (2012) GADD45alpha inhibition of DNMT1 dependent DNA methylation during homology directed DNA repair. Nucleic Acids Research 40: 2481-2493.
23. Cuozzo C, Porcellini A, Angrisano T, Morano A, Lee B, et al. (2007) DNA Damage, Homology-Directed Repair, and DNA Methylation. PLoS Genet 3: e110.
24. Sikdar N, Banerjee S, Lee K-y, Wincovitch S, Pak E, et al. (2009) DNA damage responses by human ELG1 in S phase are important to maintain genomic integrity. Cell Cycle 8: 3199-3207.
25. Fox JT, Sakamuru S, Huang R, Teneva N, Simmons SO, et al. (2012) High-throughput genotoxicity assay identifies antioxidants as inducers of DNA damage response and cell death. Proceedings of the National Academy of Sciences 109: 5423-5428.
26. Ho AS, Turcan S, Chan TA (2013) Epigenetic therapy: use of agents targeting deacetylation and methylation in cancer management.
27. Ai T, Cui H, Chen L (2012) Multi-targeted histone deacetylase inhibitors in cancer therapy. Curr Med Chem 19: 475-487.
28. Li D, Marchenko ND, Moll UM (2011) SAHA shows preferential cytotoxicity in mutant p53 cancer cells by destabilizing mutant p53 through inhibition of the HDAC6-Hsp90 chaperone axis. Cell Death Differ 18: 1904-1913.
29. Jasek E, Lis GJ, Jasinska M, Jurkowska H, Litwin JA (2012) Effect of Histone Deacetylase Inhibitors Trichostatin A and Valproic Acid on Etoposide-induced Apoptosis in Leukemia Cells. Anticancer Research 32: 2791-2799 .
30. Evans TJ, Yamamoto KN, Hirota K, Takeda S (2010) Mutant cells defective in DNA repair pathways provide a sensitive high-throughput assay for genotoxicity. DNA Repair 9: 1292-1298.
31. Lee J-H, Choy ML, Ngo L, Foster SS, Marks PA (2010) Histone deacetylase inhibitor induces DNA damage, which normal but not transformed cells can repair. Proceedings of the National Academy of Sciences 107: 14639-14644.
32. Kass EM, Helgadottir HR, Chen C-C, Barbera M, Wang R, et al. (2013) Double-strand break repair by homologous recombination in primary mouse somatic cells requires BRCA1 but not the ATM kinase. Proceedings of the National Academy of Sciences 110: 5564-5569.
33. Tikoo S, Sengupta S (2010) Time to Bloom. Genome Integrity 1: 14.
34. Xia B, Sheng Q, Nakanishi K, Ohashi A, Wu J, et al. (2006) Control of BRCA2 Cellular and Clinical Functions by a Nuclear Partner, PALB2. Molecular Cell 22: 719-729.
35. Pierce AJ, Johnson RD, Thompson LH, Jasin M (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes & Development 13: 2633-2638. (Pubitemid 29508550)
36. Kotian S, Liyanarachchi S, Zelent A, Parvin JD (2011) Histone Deacetylases 9 and 10 Are Required for Homologous Recombination. Journal of Biological Chemistry 286: 7722-7726.
37. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM, et al. (2007) HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proceedings of the National Academy of Sciences 104: 19482-19487.
38. Bunting SF, Callen E, Wong N, Chen H-T, Polato F, et al. (2010) 53BP1 Inhibits Homologous Recombination in Brca1-Deficient Cells by Blocking Resection of DNA Breaks. Cell 141: 243-254.
39. Mao Z, Bozzella M, Seluanov A, Gorbunova V (2008) Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair 7: 1765-1771.
40. Gunn A, Stark JM (2012) I-SceI-Based Assays to Examine Distinct Repair Outcomes of Mammalian Chromosomal Double Strand Breaks. In: Bjergb!"k L, editor. DNA Repair Protocols: Humana Press. pp. 379-391.
41. Murr R, Loizou J, Yang Y, Cuenin C, Li H, et al. (2006) Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA doublestrand breaks.
42. Hsiao K-Y, Mizzen CA (2013) Histone H4 deacetylation facilitates 53BP1 DNA damage signaling and double-strand break repair. Journal of Molecular Cell Biology.
43. Fattah F, Lee EH, Weisensel N, Wang Y, Lichter N, et al. (2010) Ku Regulates the Non-Homologous End Joining Pathway Choice of DNA Double-Strand Break Repair in Human Somatic Cells. PLoS Genet 6: e1000855.
44. Oh S, Wang Y, Zimbric J, Hendrickson EA (2013) Human LIGIV is synthetically lethal with the loss of Rad54B-dependent recombination and is required for certain chromosome fusion events induced by telomere dysfunction. Nucleic Acids Research 41: 1734-1749.
45. Yu X, Fu S, Lai M, Baer R, Chen J (2006) BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes & Development 20: 1721-1726. (Pubitemid 43992880)
46. Wang Y, Leung JW, Jiang Y, Lowery MG, Do H, et al. (2013) FANCM and FAAP24 Maintain Genome Stability via Cooperative as Well as Unique Functions. Molecular Cell 49: 997-1009.
47. Nalabothula N, Carrier F (2011) Cancer cells' epigenetic composition and predisposition to histone deacetylase inhibitor sensitization. Epigenomics 3: 145-155.
48. Olaharski AJ, Ji Z, Woo J-Y, Lim S, Hubbard AE, et al. (2006) The Histone Deacetylase Inhibitor Trichostatin A Has Genotoxic Effects in Human Lymphoblasts In Vitro. Toxicological Sciences 93: 341-347. (Pubitemid 44400452)
49. Candotti F, Oakes SA, Johnston JA, Giliani S, Schumacher RF, et al. (1997) Structural and functional basis for JAK3-deficient severe combined immuno-deficiency. Blood 90: 3996-4003. (Pubitemid 27484053)
50. Krijger PHL, Lee K-Y, Wit N, van den Berk PCM, Wu X, et al. (2011) HLTF and SHPRH are not essential for PCNA polyubiquitination, survival and somatic hypermutation: Existence of an alternative E3 ligase. DNA Repair 10: 438-444.
51. Nakanishi K, Yang Y-G, Pierce AJ, Taniguchi T, Digweed M, et al. (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proceedings of the National Academy of Sciences of the United States of America 102: 1110-1115. (Pubitemid 40170734)
52. Lee K-y, Yang K, Cohn MA, Sikdar N, D'Andrea AD, et al. (2010) Human ELG1 Regulates the Level of Ubiquitinated Proliferating Cell Nuclear Antigen (PCNA) through Its Interactions with PCNA and USP1. Journal of Biological Chemistry 285: 10362-10369.
53. Kuchma M, Kim J, Muller M, Arlen P (2012) Prostate Cancer Cell Surface-Associated Keratin 8 and Its Implications for Enhanced Plasmin Activity. The Protein Journal 31: 195-205.
54. Merolla F, Luise C, Muller MT, Pacelli R, Fusco A, et al. (2012) Loss of CCDC6, the First Identified RET Partner Gene, Affects pH2AX S139 Levels and Accelerates Mitotic Entry upon DNA Damage. PLoS ONE 7: e36177.