Vorinostat induces reactive oxygen species and dna damage in acute myeloid leukemia cells

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Petruccelli, Luca A ^a   Dupéré Richer, Daphné ^a   Pettersson, Filippa ^a   Retrouvey, Hélène ^a   Skoulikas, Sophia ^a   Miller, Wilson H ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; REACTIVE OXYGEN METABOLITE; VORINOSTAT; ANTINEOPLASTIC AGENT; ANTIOXIDANT; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID;

ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL VIABILITY; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; DRUG CYTOTOXICITY; ENZYME ACTIVITY; GROWTH DISORDER; HUMAN; HUMAN CELL; LEUKEMIA CELL; OXIDATIVE STRESS; CELL DIVISION; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; DNA REPLICATION; DOSE RESPONSE; DRUG EFFECT; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; APOPTOSIS; CELL DIVISION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; DNA REPLICATION; DOSE-RESPONSE RELATIONSHIP, DRUG; G2 PHASE; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; LEUKEMIA, MYELOID, ACUTE; REACTIVE OXYGEN SPECIES;

EID: 79958695612     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020987     Document Type: Article

References (50)

1. Martens JH, Stunnenberg HG, (2010) The molecular signature of oncofusion proteins in acute myeloid leukemia. FEBS Lett 584: 2662-2669.
2. Pan LN, Lu J, Huang B, (2007) HDAC inhibitors: a potential new category of anti-tumor agents. Cell Mol Immunol 4: 337-343.
3. Carew JS, Giles FJ, Nawrocki ST, (2008) Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 269: 7-17.
4. Inoue T, Hiratsuka M, Osaki M, Oshimura M, (2007) The molecular biology of mammalian SIRT proteins: SIRT2 in cell cycle regulation. Cell Cycle 6: 1011-1018.
5. Cote S, Rosenauer A, Bianchini A, Seiter K, Vandewiele J, et al. (2002) Response to histone deacetylase inhibition of novel PML/RARalpha mutants detected in retinoic acid-resistant APL cells. Blood 100: 2586-2596.
6. Pandolfi PP, (2001) Transcription therapy for cancer. Oncogene 20: 3116-3127.
7. Mitsiades CS, Mitsiades NS, McMullan CJ, Poulaki V, Shringarpure R, et al. (2004) Transcriptional signature of histone deacetylase inhibition in multiple myeloma: biological and clinical implications. Proc Natl Acad Sci U S A 101: 540-545.
8. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, et al. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325: 834-840.
9. Marks PA, Richon VM, Rifkind RA, (2000) Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J Natl Cancer Inst 92: 1210-1216.
10. Richon VM, Emiliani S, Verdin E, Webb Y, Breslow R, et al. (1998) A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases. Proc Natl Acad Sci U S A 95: 3003-3007.
11. Hrzenjak A, Moinfar F, Kremser ML, Strohmeier B, Petru E, et al. (2010) Histone deacetylase inhibitor vorinostat suppresses the growth of uterine sarcomas in vitro and in vivo. Mol Cancer 9: 49.
12. Sargeant AM, Rengel RC, Kulp SK, Klein RD, Clinton SK, et al. (2008) OSU-HDAC42, a histone deacetylase inhibitor, blocks prostate tumor progression in the transgenic adenocarcinoma of the mouse prostate model. Cancer Res 68: 3999-4009.
13. Eot-Houllier G, Fulcrand G, Magnaghi-Jaulin L, Jaulin C, (2009) Histone deacetylase inhibitors and genomic instability. Cancer Lett 274: 169-176.
14. Chen CS, Wang YC, Yang HC, Huang PH, Kulp SK, et al. (2007) Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res 67: 5318-5327.
15. Zhang Y, Carr T, Dimtchev A, Zaer N, Dritschilo A, et al. (2007) Attenuated DNA damage repair by trichostatin A through BRCA1 suppression. Radiat Res 168: 115-124.
16. Gaymes TJ, Padua RA, Pla M, Orr S, Omidvar N, et al. (2006) Histone deacetylase inhibitors (HDI) cause DNA damage in leukemia cells: a mechanism for leukemia-specific HDI-dependent apoptosis? Mol Cancer Res 4: 563-573.
17. Glaser KB, (2007) HDAC inhibitors: clinical update and mechanism-based potential. Biochem Pharmacol 74: 659-671.
18. Rahmani M, Reese E, Dai Y, Bauer C, Payne SG, et al. (2005) Coadministration of histone deacetylase inhibitors and perifosine synergistically induces apoptosis in human leukemia cells through Akt and ERK1/2 inactivation and the generation of ceramide and reactive oxygen species. Cancer Res 65: 2422-2432.
19. Ruefli AA, Bernhard D, Tainton KM, Kofler R, Smyth MJ, et al. (2002) Suberoylanilide hydroxamic acid (SAHA) overcomes multidrug resistance and induces cell death in P-glycoprotein-expressing cells. Int J Cancer 99: 292-298.
20. Vrana JA, Decker RH, Johnson CR, Wang Z, Jarvis WD, et al. (1999) Induction of apoptosis in U937 human leukemia cells by suberoylanilide hydroxamic acid (SAHA) proceeds through pathways that are regulated by Bcl-2/Bcl-XL, c-Jun, and p21CIP1, but independent of p53. Oncogene 18: 7016-7025.
21. He LZ, Tolentino T, Grayson P, Zhong S, Warrell RP Jr, et al. (2001) Histone deacetylase inhibitors induce remission in transgenic models of therapy-resistant acute promyelocytic leukemia. J Clin Invest 108: 1321-1330.
22. Amin HM, Saeed S, Alkan S, (2001) Histone deacetylase inhibitors induce caspase-dependent apoptosis and downregulation of daxx in acute promyelocytic leukaemia with t(15;17). Br J Haematol 115: 287-297.
23. Olive PL, Banath JP, (2006) The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 1: 23-29.
24. Conti C, Leo E, Eichler GS, Sordet O, Martin MM, et al. (2010) Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res 70: 4470-4480.
25. Hamer G, Roepers-Gajadien HL, van Duyn-Goedhart A, Gademan IS, Kal HB, et al. (2003) DNA double-strand breaks and gamma-H2AX signaling in the testis. Biol Reprod 68: 628-634.
26. Ibrado AM, Kim CN, Bhalla K, (1998) Temporal relationship of CDK1 activation and mitotic arrest to cytosolic accumulation of cytochrome C and caspase-3 activity during Taxol-induced apoptosis of human AML HL-60 cells. Leukemia 12: 1930-1936.
27. Bolden JE, Peart MJ, Johnstone RW, (2006) Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-784.
28. Campas-Moya C, (2009) Romidepsin for the treatment of cutaneous T-cell lymphoma. Drugs Today (Barc) 45: 787-795.
29. Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R, (2007) FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12: 1247-1252.
30. Ramalingam SS, Parise RA, Ramanathan RK, Lagattuta TF, Musguire LA, et al. (2007) Phase I and pharmacokinetic study of vorinostat, a histone deacetylase inhibitor, in combination with carboplatin and paclitaxel for advanced solid malignancies. Clin Cancer Res 13: 3605-3610.
31. Dickson MA, Rathkopf DE, Carvajal RD, Grant S, Roberts JD, et al. (2010) A phase I pharmacokinetic study of pulse-dose vorinostat with flavopiridol in solid tumors. Invest New Drugs.
32. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM, et al. (2007) HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc Natl Acad Sci U S A 104: 19482-19487.
33. Munshi A, Kurland JF, Nishikawa T, Tanaka T, Hobbs ML, et al. (2005) Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 11: 4912-4922.
34. Jazayeri A, McAinsh AD, Jackson SP, (2004) Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc Natl Acad Sci U S A 101: 1644-1649.
35. Murga M, Jaco I, Fan Y, Soria R, Martinez-Pastor B, et al. (2007) Global chromatin compaction limits the strength of the DNA damage response. J Cell Biol 178: 1101-1108.
36. Tamburini BA, Tyler JK, (2005) Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 25: 4903-4913.
37. Boyle GM, Martyn AC, Parsons PG, (2005) Histone deacetylase inhibitors and malignant melanoma. Pigment Cell Res 18: 160-166.
38. Dokmanovic M, Marks PA, (2005) Prospects: histone deacetylase inhibitors. J Cell Biochem 96: 293-304.
39. Yi X, Wei W, Wang SY, Du ZY, Xu YJ, et al. (2008) Histone deacetylase inhibitor SAHA induces ERalpha degradation in breast cancer MCF-7 cells by CHIP-mediated ubiquitin pathway and inhibits survival signaling. Biochem Pharmacol 75: 1697-1705.
40. Kramer OH, Knauer SK, Zimmermann D, Stauber RH, Heinzel T, (2008) Histone deacetylase inhibitors and hydroxyurea modulate the cell cycle and cooperatively induce apoptosis. Oncogene 27: 732-740.
41. Moon DO, Park C, Heo MS, Park YM, Choi YH, et al. (2007) PD98059 triggers G1 arrest and apoptosis in human leukemic U937 cells through downregulation of Akt signal pathway. Int Immunopharmacol 7: 36-45.
42. Ruefli AA, Ausserlechner MJ, Bernhard D, Sutton VR, Tainton KM, et al. (2001) 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 U S A 98: 10833-10838.
43. Martirosyan A, Leonard S, Shi X, Griffith B, Gannett P, et al. (2006) Actions of a histone deacetylase inhibitor NSC3852 (5-nitroso-8-quinolinol) link reactive oxygen species to cell differentiation and apoptosis in MCF-7 human mammary tumor cells. J Pharmacol Exp Ther 317: 546-552.
44. Xu W, Ngo L, Perez G, Dokmanovic M, Marks PA, (2006) Intrinsic apoptotic and thioredoxin pathways in human prostate cancer cell response to histone deacetylase inhibitor. Proc Natl Acad Sci U S A 103: 15540-15545.
45. Demple B, DeMott MS, (2002) Dynamics and diversions in base excision DNA repair of oxidized abasic lesions. Oncogene 21: 8926-8934.
46. Garcia-Manero G, Yang H, Bueso-Ramos C, Ferrajoli A, Cortes J, et al. (2008) Phase 1 study of the histone deacetylase inhibitor vorinostat (suberoylanilide hydroxamic acid [SAHA]) in patients with advanced leukemias and myelodysplastic syndromes. Blood 111: 1060-1066.
47. Schaefer EW, Loaiza-Bonilla A, Juckett M, DiPersio JF, Roy V, et al. (2009) A phase 2 study of vorinostat in acute myeloid leukemia. Haematologica 94: 1375-1382.
48. Kim MS, Blake M, Baek JH, Kohlhagen G, Pommier Y, et al. (2003) Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res 63: 7291-7300.
49. Ozaki K, Kishikawa F, Tanaka M, Sakamoto T, Tanimura S, et al. (2008) Histone deacetylase inhibitors enhance the chemosensitivity of tumor cells with cross-resistance to a wide range of DNA-damaging drugs. Cancer Sci 99: 376-384.
50. Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, et al. (2008) Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 30: 61-72.