Histone deacetylase regulation of ATM-mediated DNA damage signaling

Molecular Cancer Therapeutics

Volumn 12, Issue 10, 2013, Pages 2078-2087

  Thurn, K Ted ^a   Thomas, Scott ^a   Raha, Paromita ^a   Qureshi, Ian ^a   Munster, Pamela N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ENTINOSTAT; EPIRUBICIN; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; PROTEIN P53; VALPROIC ACID; VORINOSTAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME INHIBITION; ENZYME REGULATION; FEMALE; GADD45A GENE; GENE; GENE INDUCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RRM2B GENE; SIGNAL TRANSDUCTION;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; BRCA1 PROTEIN; CHECKPOINT KINASE 2; DNA DAMAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HUMANS; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84885663744     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-1242     Document Type: Article

References (50)

1. Lee JH, Paull TT. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 2004;304: 93-6.
2. Gatei M, Scott SP, Filippovitch I, Soronika N, Lavin MF, Weber B, et al. Role for ATM in DNA damage-induced phosphorylation of BRCA1. Cancer Res 2000;60: 3299-304.
3. Kurz EU, Douglas P, Lees-Miller SP. Doxorubicin activates ATMdependent phosphorylation of multiple downstream targets in part through the generation of reactive oxygen species. J Biol Chem 2004; 279: 53272-81.
4. Hittelman WN, Pandita TK. Possible role of chromatin alteration in the radiosensitivity of ataxia-telangiectasia. Int J Radiat Biol 1994;66: S109-13.
5. Lavin MF, Shiloh Y. The genetic defect in ataxia-telangiectasia. Annu Rev Immunol 1997;15: 177-202.
6. Eot-Houllier G, Fulcrand G, Magnaghi-Jaulin L, Jaulin C. Histone deacetylase inhibitors and genomic instability. Cancer Lett 2009;274: 169-76.
7. Munshi A, Kurland JF, Nishikawa T, Tanaka T, Hobbs ML, Tucker SL, et al. Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 2005;11: 4912-22.
8. Marchion DC, Bicaku E, Daud AI, Sullivan DM, Munster PN. Valproic acid alters chromatin structure by regulation of chromatin modulation proteins. Cancer Res 2005;65: 3815-22.
9. Ji P, Yeh V, Ramirez T, Murata-Hori M, Lodish HF. Histone deacetylase 2 is required for chromatin condensation and subsequent enucleation of cultured mouse fetal erythroblasts. Haematologica 2010;95: 2013-21.
10. Kim GD, Choi YH, Dimtchev A, Jeong SJ, Dritschilo A, Jung M. Sensing of ionizing radiation-inducedDNA damage by ATM through interaction with histone deacetylase. J Biol Chem 1999;274: 31127-30.
11. Marchion DC, Bicaku E, Turner JG, Schmitt ML, Morelli DR, Munster PN. HDAC2 regulates chromatin plasticity and enhances DNA vulnerability. Mol Cancer Ther 2009;8: 794-801.
12. Kitagawa R, Bakkenist CJ,McKinnon PJ, Kastan MB. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 2004;18: 1423-38.
13. Thurn KT, Thomas S, Moore A, Munster PN. Rational therapeutic combinations with histone deacetylase inhibitors for the treatment of cancer. Future Oncol 2011;7: 263-83.
14. Osada H, Tatematsu Y, Saito H, Yatabe Y, Mitsudomi T, Takahashi T. Reduced expression of class II histone deacetylase genes is associated with poor prognosis in lung cancer patients. Int J Cancer 2004;112: 26-32.
15. Weichert W, Roske A, Gekeler V, Beckers T, Stephan C, Jung K, et al. Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy. Br J Cancer 2008;98: 604-10.
16. Kachhap SK, Rosmus N, Collis SJ, Kortenhorst MS, Wissing MD, Hedayati M, et al. Downregulation of homologous recombination DNA repair genes byHDACinhibition in prostate cancer ismediated through the E2F1 transcription factor. PLoS One 2010;5:e11208.
17. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM, Buggy JJ. HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc Natl Acad Sci U S A 2007;104: 19482-7.
18. Marchion DC, Bicaku E, Daud AI, Sullivan DM, Munster PN. In vivo synergy between topoisomerase II and histone deacetylase inhibitors: predictive correlates. Mol Cancer Ther 2005;4: 1993-2000.
19. Miller KM, Tjeertes JV, Coates J, Legube G, Polo SE, Britton S, et al. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 2010;17: 1144-51.
20. Chen CS, Wang YC, Yang HC, Huang PH, Kulp SK, Yang CC, et al. Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res 2007;67: 5318-27.
21. Li D, Marchenko ND, Moll UM. SAHA shows preferential cytotoxicity in mutant p53 cancer cells by destabilizing mutant p53 through inhibition of the HDAC6-Hsp90 chaperone axis. Cell Death Differ 2011;18: 1904-13.
22. Harms KL, Chen X. Histone deacetylase 2 modulates p53 transcriptional activities through regulation of p53-DNA binding activity. Cancer Res 2007;67: 3145-52.
23. Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R, et al. HDACs link the DNA damage response, processing of doublestrand breaks and autophagy. Nature 2011;471: 74-9.
24. Munster P, Marchion D, Bicaku E, Schmitt M, Lee JH, DeConti R, et al. Phase I trial of histone deacetylase inhibition by valproic acid followed by the topoisomerase II inhibitor epirubicin in advanced solid tumors: a clinical and translational study. J Clin Oncol 2007;25: 1979-85.
25. Marchion DC, Bicaku E, Daud AI, Richon V, Sullivan DM, Munster PN. Sequence-specific potentiation of topoisomerase II inhibitors by the histone deacetylase inhibitor suberoylanilide hydroxamic acid. J Cell Biochem 2004;92: 223-37.
26. Singh S, Le H, Shih SJ, Ho B, Vaughan AT. Suberoylanilide hydroxyamic acid modification of chromatin architecture affects DNA break formation and repair. Int J Radiat Oncol Biol Phys 2010;76: 566-73.
27. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nat Protoc 2006;1: 2315-9.
28. Dumaz N, Meek DW. Serine15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. EMBO J 1999;18: 7002-10.
29. Devlin HL, Mack PC, Burich RA, Gumerlock PH, Kung HJ, Mudryj M, et al. Impairment of the DNA repair and growth arrest pathways by p53R2 silencing enhances DNA damage-induced apoptosis in a p53- dependent manner in prostate cancer cells. Mol Cancer Res 2008;6: 808-18.
30. Sato J, Kimura T, Saito T, Anazawa T, Kenjo A, Sato Y, et al. Gene expression analysis for predicting gemcitabine resistance in human cholangiocarcinoma. J Hepatobiliary Pancreat Sci 2011;18: 700-11.
31. Munster PN, Marchion D, Thomas S, Egorin M, Minton S, Springett G, et al. Phase I trial of vorinostat and doxorubicin in solid tumours: histone deacetylase 2 expression as a predictive marker. Br J Cancer 2009;101: 1044-50.
32. Khan SN, Danishuddin M, Varshney B, Lal SK, Khan AU. Inhibition of Nterminal lysines acetylation and transcription factor assembly by epirubicin induced deranged cell homeostasis. PLoS One 2012;7: e51850.
33. Conti C, Leo E, Eichler GS, Sordet O, Martin MM, Fan A, et al. Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res 2010;70: 4470-80.
34. Di Micco R, Sulli G, Dobreva M, Liontos M, Botrugno OA, Gargiulo G, et al. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat Cell Biol 2011;13: 292-302.
35. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA.ATMand DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004;64: 2390-6.
36. Khan N, Jeffers M, Kumar S, Hackett C, Boldog F, Khramtsov N, et al. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 2008;409: 581-9.
37. Jurkin J, Zupkovitz G, Lagger S, Grausenburger R, Hagelkruys A, Kenner L, et al. Distinct and redundant functions of histone deacetylases HDAC1 and HDAC2 in proliferation and tumorigenesis. Cell Cycle 2011;10: 406-12.
38. Lee JH, Choy ML, Ngo L, Foster SS, Marks PA. Histone deacetylase inhibitor inducesDNA damage, which normal but not transformed cells can repair. Proc Natl Acad Sci U S A 2010;107: 14639-44.
39. Lopez G, Liu J, Ren W, Wei W, Wang S, Lahat G, et al. Combining PCI- 24781, a novel histone deacetylase inhibitor, with chemotherapy for the treatment of soft tissue sarcoma. Clin Cancer Res 2009;15: 3472-83.
40. Berkovich E, Ginsberg D.ATMis a target for positive regulation by E2F-1. Oncogene 2003;22: 161-7.
41. Gui CY, Ngo L, Xu WS, Richon VM, Marks PA. Histone deacetylase (HDAC) inhibitor activation of p21WAF1 involves changes in promoterassociated proteins, including HDAC1. Proc Natl Acad Sci U S A 2004;101: 1241-6.
42. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 2009;361: 123-34.
43. Ashwell S, Zabludoff S. DNA damage detection and repair pathways- recent advances with inhibitors of checkpoint kinases in cancer therapy. Clin Cancer Res 2008;14: 4032-7.
44. Nome RV, Bratland A, Harman G, Fodstad O, Andersson Y, Ree AH. Cell cycle checkpoint signaling involved in histone deacetylase inhibition and radiation-induced cell death. Mol Cancer Ther 2005;4: 1231-8.
45. Siliciano JD, Canman CE, Taya Y, Sakaguchi K, Appella E, Kastan MB. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev 1997;11: 3471-81.
46. Kimura T, Takeda S, Sagiya Y, Gotoh M, Nakamura Y, Arakawa H. Impaired function of p53R2 in Rrm2b-null mice causes severe renal failure through attenuation of dNTP pools. Nat Genet 2003;34: 440-5.
47. Blumenschein GR Jr, Kies MS, Papadimitrakopoulou VA, Lu C, Kumar AJ, Ricker JL, et al. Phase II trial of the histone deacetylase inhibitor vorinostat (Zolinza, suberoylanilide hydroxamic acid, SAHA) in patients with recurrent and/or metastatic head and neck cancer. Invest New Drugs 2008;26: 81-7.
48. Luu TH, Morgan RJ, Leong L, Lim D, McNamara M, Portnow J, et al. A phase II trial of vorinostat (suberoylanilide hydroxamic acid) in metastatic breast cancer: a California Cancer Consortium study. Clin Cancer Res 2008;14: 7138-42.
49. Zhang Y, Carr T, Dimtchev A, Zaer N, Dritschilo A, Jung M. Attenuated DNA damage repair by trichostatin A through BRCA1 suppression. Radiat Res 2007;168: 115-24.
50. Lee JS. Functional link between DNA damage responses and transcriptional regulation by ATM in response to a histone deacetylase inhibitor TSA. Cancer Res Treat 2007;39: 116-24.