Histone deacetylase inhibitors promote glioma cell death by G2 checkpoint abrogation leading to mitotic catastrophe

Cell Death and Disease

Volumn 5, Issue 10, 2014, Pages

  Cornago, M ^a   Garcia Alberich, C ^a   Blasco Angulo, N ^a   Vall llaura, N ^a   Nager, M ^a   Herreros, J ^a   Comella, J X ^b   Sanchis, D ^a   Llovera, M ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; DNA; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID DERIVATIVE; MEMBRANE PROTEIN; RAD51 PROTEIN; REACTIVE OXYGEN METABOLITE; SUBERANILOHYDROXAMIC ACID; SURVIVIN; TPX2 PROTEIN; UNCLASSIFIED DRUG; VALPROIC ACID; WEE1 PROTEIN; CELL CYCLE PROTEIN; HYDROXAMIC ACID; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; PROTEIN KINASE; TPX2 PROTEIN, HUMAN; VORINOSTAT;

ARTICLE; CELL CYCLE PROGRESSION; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CHROMOSOME SEGREGATION; CLONOGENESIS; DNA DAMAGE; DNA FRAGMENTATION; DNA REPAIR; G2 PHASE CELL CYCLE CHECKPOINT; GLIOBLASTOMA; GLIOMA CELL; GLIOMA CELL LINE; IN VITRO STUDY; MITOSIS; MITOSIS SPINDLE; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; APOPTOSIS; CELL SURVIVAL; DRUG EFFECTS; GENETICS; GLIOMA; HUMAN; METABOLISM; PATHOPHYSIOLOGY;

APOPTOSIS; CELL CYCLE PROTEINS; CELL DEATH; CELL SURVIVAL; G2 PHASE CELL CYCLE CHECKPOINTS; GLIOMA; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; NUCLEAR PROTEINS; PROTEIN KINASES; RAD51 RECOMBINASE; VALPROIC ACID;

EID: 84923048337     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.412     Document Type: Article

References (46)

1. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21: 2683-2710.
2. Wen PYKesari S.. Malignant gliomas in adults. N Engl J Med 2008; 359: 492-507.
3. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTCNCIC trial. Lancet Oncol 2009; 10: 459-466.
4. Di Marcotullio L, Canettieri G, Infante P, Greco A, Gulino A. Protected from the inside: endogenous histone deacetylase inhibitors and the road to cancer. Biochim Biophys Acta 2011; 1815: 241-252.
5. Weichert W. HDAC expression and clinical prognosis in human malignancies. Cancer Lett 2009; 280: 168-176.
6. Lucio-Eterovic AK, Cortez MA, Valera ET, Motta FJ, Queiroz RG, Machado HR et al. Differential expression of 12 histone deacetylase (HDAC) genes in astrocytomas and normal brain tissue: class II and IV are hypoexpressed in glioblastomas. BMC Cancer 2008; 8: 243.
7. Witt O, Deubzer HE, Milde T, Oehme I. HDAC family: What are the cancer relevant targets?. Cancer Lett 2009; 277: 8-21.
8. Bose P, Dai Y, Grant S. Histone deacetylase inhibitor (HDACI) mechanisms of action: Emerging insights. Pharmacol Ther 2014; 143: 323-336.
9. Carew JS, Giles FJ, Nawrocki ST. Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 2008; 269: 7-17.
10. Lee J-H, Choy ML, Ngo L, Foster SS, Marks PA. Histone deacetylase inhibitor induces DNA damage, which normal but not transformed cells can repair. Proc Natl Acad Sci USA 2010; 107: 14639-14644.
11. Liu X, Li P, Widlak P, Zou H, Luo X, Garrard WT et al. The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc Natl Acad Sci USA 1998; 95: 8461-8466.
12. Butler LM, Zhou X, Xu WS, Scher HI, Rifkind RA, Marks PA et al. The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxin-binding protein-2, and down-regulates thioredoxin. Proc Natl Acad Sci USA 2002; 99: 11700-11705.
13. Mateen S, Raina K, Jain AK, Agarwal C, Chan D, Agarwal R. Epigenetic modifications and p21-cyclin B1 nexus in anticancer effect of histone deacetylase inhibitors in combination with silibinin on non-small cell lung cancer cells. Epigenetics 2012; 7: 1161-1172.
14. Shen T, Huang S. The role of Cdc25A in the regulation of cell proliferation and apoptosis. Anticancer Agents Med Chem 2012; 12: 631-639.
15. Beck H, Nahse-Kumpf V, Larsen MS, O'Hanlon KA, Patzke S, Holmberg C et al. Cyclindependent kinase suppression by WEE1 kinase protects the genome through control of replication initiation and nucleotide consumption. Mol Cell Biol 2012; 32: 4226-4236.
16. Dominguez-Kelly R, Martin Y, Koundrioukoff S, Tanenbaum ME, Smits VAJ, Medema RH et al. Wee1 controls genomic stability during replication by regulating the Mus81-Eme1 endonuclease. J Cell Biol 2011; 194: 567-579.
17. Del Nagro CJ, Choi J, Xiao Y, Rangell L, Mohan S, Pandita A et al. Chk1 inhibition in p53- deficient cell lines drives rapid chromosome fragmentation followed by caspase-independent cell death. Cell Cycle 2014; 13: 303-314.
18. Mir SE, De Witt Hamer PC, Krawczyk PM, Balaj L, Claes A, Niers JM et al. In silico analysis of kinase expression identifies WEE1 as a gatekeeper against mitotic catastrophe in glioblastoma. Cancer Cell 2010; 18: 244-257.
19. Robert C, Rassool FV. HDAC inhibitors: roles of DNA damage and repair. Advances in cancer research 2012; 116: 87-129.
20. Castedo M, Perfettini J-L, Roumier T, Valent A, Raslova H, Yakushijin K et al. Mitotic catastrophe constitutes a special case of apoptosis whose suppression entails aneuploidy. Oncogene 2004; 23: 4362-4370.
21. Russell MR, Levin K, Rader J, Belcastro L, Li Y, Martinez D et al. Combination therapy targeting the Chk1 and Wee1 kinases shows therapeutic efficacy in neuroblastoma. Cancer Res 2013; 73: 776-784.
22. Guertin AD, Martin MM, Roberts B, Hurd M, Qu X, Miselis NR et al. Unique functions of CHK1 and WEE1 underlie synergistic anti-tumor activity upon pharmacologic inhibition. Cancer Cell Int 2012; 12: 45.
23. Huang X, Tran T, Zhang L, Hatcher R, Zhang P. DNA damage-induced mitotic catastrophe is mediated by the Chk1-dependent mitotic exit DNA damage checkpoint. Proc Natl Acad Sci USA 2005; 102: 1065-1070.
24. Brazelle W, Kreahling JM, Gemmer J, Ma Y, Cress WD, Haura E et al. Histone deacetylase inhibitors downregulate checkpoint kinase 1 expression to induce cell death in non-small cell lung cancer cells. PLoS One 2010; 5: e14335.
25. Ruefli AA, Ausserlechner MJ, Bernhard D, Sutton VR, Tainton KM, Kofler R et al. The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc Natl Acad Sci USA 2001; 98: 10833-10838.
26. Ungerstedt JS, Sowa Y, Xu WS, Shao Y, Dokmanovic M, Perez G et al. Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc Natl Acad Sci USA 2005; 102: 673-678.
27. Kao GD, McKenna WG, Guenther MG, Muschel RJ, Lazar MA, Yen TJ. Histone deacetylase 4 interacts with 53BP1 to mediate the DNA damage response. J Cell Biol 2003; 160: 1017-1027.
28. Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, Sun Z-WW et al. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 2008; 30: 61-72.
29. Forment JV, Blasius M, Guerini I, Jackson SP. Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation. PLoS One 2011; 6: e23517.
30. Stevens FE, Beamish H, Warrener R, Gabrielli B. Histone deacetylase inhibitors induce mitotic slippage. Oncogene 2008; 27: 1345-1354.
31. Noh EJ, Lim D-S, Jeong GLee J-S. An HDAC inhibitor, trichostatin A, induces a delay at G2/M transition, slippage of spindle checkpoint, and cell death in a transcriptiondependent manner. Biochem Biophys Res Commun 2009; 378: 326-331.
32. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008; 15: 1153-1162.
33. 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 USA 2007; 104: 19482-19487.
34. 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: 4912-4922.
35. Kachhap SK, Rosmus N, Collis SJ, Kortenhorst MSQ, Wissing MD, Hedayati M et al. Downregulation of homologous recombination DNA repair genes by HDAC inhibition in prostate cancer is mediated through the E2F1 transcription factor. PLoS One 2010;5: e11208.
36. Lens SM a, Vader G, Medema RH. The case for Survivin as mitotic regulator. Curr Opin Cell Biol 2006; 18: 616-622.
37. Duffy MJ, O'Donovan N, Brennan DJ, Gallagher WM, Ryan BM. Survivin: a promising tumor biomarker. Cancer Lett 2007; 249: 49-60.
38. Tu SP, Cui JT, Liston P, Huajiang X, Xu R, Lin MCMM et al. Gene therapy for colon cancer by adeno-associated viral vector-mediated transfer of survivin Cys84Ala mutant. Gastroenterology 2005; 128: 361-375.
39. Carvalho A. Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 2003; 116: 2987-2998.
40. Guvenc H, Pavlyukov MS, Joshi K, Kurt H, Banasavadi-Siddegowda YK, Mao P et al. Impairment of glioma stem cell survival and growth by a novel inhibitor for Survivin-Ran protein complex. Clin Cancer Res 2013; 19: 631-642.
41. Bruna A, Darken RS, Rojo F, Ocaña A, Peñuelas S, Arias A et al. High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 2007; 11: 147-160.
42. Zhang J, Ye J, Altafaj A, Cardona M, Bahi N, Llovera M et al. EndoG links Bnip3-induced mitochondrial damage and caspase-independent DNA fragmentation in ischemic cardiomyocytes. PLoS One 2011; 6: e17998.
43. Iglesias-Guimarais V, Gil-Guiñon E, Gabernet G, García-Belinchón M, Sánchez-Osuna M, Casanelles E et al. Apoptotic DNA degradation into oligonucleosomal fragments, but not apoptotic nuclear morphology, relies on a cytosolic pool of DFF40/CAD endonuclease. J Biol Chem 2012; 287: 7766-7779.
44. Bahi N, Zhang J, Llovera M, Ballester M, Comella JX, Sanchis D. Switch from Caspasedependent to caspase-independent death during heart development: essential role of endonuclease g in ischemia-induced dna processing of differentiated cardiomyocytes. J Biol Chem 2006; 281: 22943-22952.
45. Ye J, Llorian M, Cardona M, Rongvaux A, Moubarak RS, Comella JX et al. A pathway involving HDAC5, cFLIP and caspases regulates expression of the splicing regulator polypyrimidine tract binding protein in the heart. J Cell Sci 2013; 126: 1682-1691.
46. Sanchis D, Mayorga M, Ballester M, Comella JX. Lack of Apaf-1 expression confers resistance to cytochrome c-driven apoptosis in cardiomyocytes. Cell Death Differ 2003; 10: 977-986.