Histone deacetylase inhibitors augment doxorubicin-induced DNA damage in cardiomyocytes

Cellular and Molecular Life Sciences

Volumn 68, Issue 24, 2011, Pages 4101-4114

  Ververis, Katherine ^a,b   Rodd, Annabelle L ^a,b   Tang, Michelle M ^a   El Osta, Assam ^a,b,c   Karagiannis, Tom C ^a,b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

H2AX; Cardiomyocyte; Cardiotoxicity; DNA double strand break; Doxorubicin; Histone deacetylase inhibitor; Sodium butyrate; Trichostatin A; Valproic acid

Indexed keywords

BUTYRIC ACID; DOXORUBICIN; HISTONE DEACETYLASE INHIBITOR; TRICHOSTATIN A; VALPROIC ACID;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DNA STRAND BREAKAGE; EMBRYO; HEART HYPERTROPHY; HEART MUSCLE CELL; NONHUMAN; RAT;

ANIMALS; ANTINEOPLASTIC AGENTS; DNA DAMAGE; DOXORUBICIN; HISTONE DEACETYLASE INHIBITORS; HYDROXAMIC ACIDS; MYOCYTES, CARDIAC; RATS;

EID: 82255163057     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0727-1     Document Type: Article

References (61)

1. Marks PA (2010) The clinical development of histone deacetylase inhibitors as targeted anticancer drugs. Expert Opin Investig Drugs 19(9):1049-1066. doi:10.1517/13543784.2010.510514
2. Grant C, Rahman F, Piekarz R, Peer C, Frye R, Robey RW, Gardner ER, Figg WD, Bates SE (2010) Romidepsin: a new therapy for cutaneous T-cell lymphoma and a potential therapy for solid tumors. Expert Rev Anticancer Ther 10(7):997-1008. doi:10.1586/era.10.88
3. Marks PA, Xu WS (2009) Histone deacetylase inhibitors: potential in cancer therapy. J Cell Biochem 107(4):600-608. doi: 10.1002/jcb.22185
4. Minucci S, Pelicci PG (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6(1):38-51. doi:10.1038/nrc1779 (Pubitemid 43054973)
5. Dokmanovic M, Clarke C, Marks PA (2007) Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5(10):981-989. doi:10.1158/1541-7786. MCR-07-0324 (Pubitemid 350080267)
6. Frew AJ, Johnstone RW, Bolden JE (2009) Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Lett 280(2):125-133. doi:10.1016/j.canlet.2009.02.042
7. Rasheed W, Bishton M, Johnstone RW, Prince HM (2008) Histone deacetylase inhibitors in lymphoma and solid malignancies. Expert Rev Anticancer Ther 8(3):413-432. doi:10.1586/14737 140.8.3.413 (Pubitemid 351836289)
8. Singh BN, Zhang G, Hwa YL, Li J, Dowdy SC, Jiang SW (2010) Nonhistone protein acetylation as cancer therapy targets. Expert Rev Anticancer Ther 10(6):935-954. doi:10.1586/era.10.62
9. Bots M, Johnstone RW (2009) Rational combinations using HDAC inhibitors. Clin Cancer Res 15(12):3970-3977. doi:10.1158/1078-0432. CCR-08-2786
10. Richon VM, Garcia-Vargas J, Hardwick JS (2009) Development of vorinostat: current applications and future perspectives for cancer therapy. Cancer Lett 280(2):201-210. doi:10.1016/j. canlet.2009.01.002
11. Chen CS, Wang YC, Yang HC, Huang PH, Kulp SK, Yang CC, Lu YS, Matsuyama S, Chen CY (2007) Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res 67(11):5318-5327. doi:10.1158/0008-5472. CAN-06-3996 (Pubitemid 46997271)
12. Harikrishnan KN, Karagiannis TC, Chow MZ, El-Osta A (2008) Effect of valproic acid on radiation-induced DNA damage in euchromatic and heterochromatic compartments. Cell Cycle 7(4):468-476 (Pubitemid 351366475)
13. Karagiannis TC, Harikrishnan KN, El-Osta A (2005) The histone deacetylase inhibitor, Trichostatin A, enhances radiation sensitivity and accumulation of gammaH2A. X. Cancer Biol Ther 4(7):787-793 (Pubitemid 41351181)
14. Karagiannis TC, Harikrishnan KN, El-Osta A (2007) Disparity of histone deacetylase inhibition on repair of radiation-induced DNA damage on euchromatin and constitutive heterochromatin compartments. Oncogene 26(27):3963-3971. doi:10.1038/sj.onc. 1210174 (Pubitemid 46884300)
15. Karagiannis TC, Kn H, El-Osta A (2006) The epigenetic modifier, valproic acid, enhances radiation sensitivity. Epigenetics 1(3):131-137
16. Munshi A, Kurland JF, Nishikawa T, Tanaka T, Hobbs ML, Tucker SL, Ismail S, Stevens C, Meyn RE (2005) Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 11(13):4912-4922. doi:10.1158/1078-0432. CCR-04-2088 (Pubitemid 41557212)
17. Munster P, Marchion D, Bicaku E, Lacevic M, Kim J, Centeno B, Daud A, Neuger A, Minton S, Sullivan D (2009) Clinical and biological effects of valproic acid as a histone deacetylase inhibitor on tumor and surrogate tissues: phase I/II trial of valproic acid and epirubicin/FEC. Clin Cancer Res 15(7):2488-2496. doi:10.1158/1078-0432. CCR-08-1930
18. Schuchmann M, Schulze-Bergkamen H, Fleischer B, Schattenberg JM, Siebler J, Weinmann A, Teufel A, Worns M, Fischer T, Strand S, Lohse AW, Galle PR (2006) Histone deacetylase inhibition by valproic acid down-regulates c-FLIP/CASH and sensitizes hepatoma cells towards CD95-and TRAIL receptor-mediated apoptosis and chemotherapy. Oncol Rep 15(1):227-230
19. Namdar M, Perez G, Ngo L, Marks PA (2010) Selective inhibition of histone deacetylase 6(HDAC6) induces DNA damage and sensitizes transformed cells to anticancer agents. Proc Natl Acad Sci USA 107 (46):20003-20008. doi:10.1073/pnas.1013754107
20. Lee JH, Choy ML, Ngo L, Foster SS, Marks PA (2010) Histone deacetylase inhibitor induces DNA damage, which normal but not transformed cells can repair. Proc Natl Acad Sci USA 107(33):14639-14644. doi:10.1073/pnas.1008522107
21. Karagiannis TC, Lin AJ, Ververis K, Chang L, Tang MM, Okabe J, El-Osta A (2010) Trichostatin A accentuates doxorubicininduced hypertrophy in cardiac myocytes. Aging (Albany NY) 2(10):659-668
22. Hortobagyi GN (1997) Anthracyclines in the treatment of cancer. An overview. Drugs 54(Suppl 4):1-7 (Pubitemid 27487789)
23. Young RC, Ozols RF, Myers CE (1981) The anthracycline antineoplastic drugs. N Engl J Med 305(3):139-153. doi: 10.1056/NEJM198107163050305 (Pubitemid 11073081)
24. Mordente A, Meucci E, Martorana GE, Giardina B, Minotti G (2001) Human heart cytosolic reductases and anthracycline cardiotoxicity. IUBMB Life 52(1-2):83-88. doi:10.1080/1521654 0252774829 (Pubitemid 33769675)
25. Olson RD, Mushlin PS (1990) Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J 4(13):3076-3086
26. Swain SM, Whaley FS, Ewer MS (2003) Congestive heart failure in patients treated with doxorubicin: a retrospective analysis of three trials. Cancer 97(11):2869-2879. doi:10.1002/cncr.11407 (Pubitemid 36605157)
27. Weiss RB (1992) The anthracyclines: will we ever find a better doxorubicin? Semin Oncol 19(6):670-686 (Pubitemid 23004844)
28. Zordoky BN, El-Kadi AO (2008) Induction of several cytochrome P450 genes by doxorubicin in H9c2 cells. Vascul Pharmacol 49(4-6):166-172. doi:10.1016/j.vph.2008.07.004
29. Vasireddy RS, Tang MM, Mah LJ, Georgiadis GT, El-Osta A, Karagiannis TC (2010) Evaluation of the spatial distribution of gammaH2AX following ionizing radiation. J Vis Exp (42). doi: 10.3791/2203
30. Mah LJ, Vasireddy RS, Tang MM, Georgiadis GT, El-Osta A, Karagiannis TC (2010) Quantification of gammaH2AX foci in response to ionising radiation. J Vis Exp (38). doi:10.3791/1957
31. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, Pommier Y (2008) GammaH2AX and cancer. Nat Rev Cancer 8(12):957-967. doi:10.1038/nrc2523
32. Mah LJ, El-Osta A, Karagiannis TC (2010) gammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 24(4):679-686. doi:10.1038/leu.2010.6
33. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273(10):5858-5868 (Pubitemid 28124064)
34. Kimes BW, Brandt BL (1976) Properties of a clonal muscle cell line from rat heart. Exp Cell Res 98(2):367-381
35. Menard C, Pupier S, Mornet D, Kitzmann M, Nargeot J, Lory P (1999) Modulation of L-type calcium channel expression during retinoic acid-induced differentiation of H9C2 cardiac cells. J Biol Chem 274(41):29063-29070
36. Chien KR, Knowlton KU, Zhu H, Chien S (1991) Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. FASEB J 5(15):3037-3046 (Pubitemid 21892863)
37. Merten KE, Jiang Y, Feng W, Kang YJ (2006) Calcineurin activation is not necessary for Doxorubicin-induced hypertrophy in H9c2 embryonic rat cardiac cells: involvement of the phosphoinositide 3-kinase-Akt pathway. J Pharmacol Exp Ther 319(2):934-940. doi:10.1124/jpet.106.108845
38. McMullen JR, Jennings GL (2007) Differences between pathological and physiological cardiac hypertrophy: novel therapeutic strategies to treat heart failure. Clin Exp Pharmacol Physiol 34(4):255-262. doi:10.1111/j.1440-1681.2007. 04585.x
39. Frey N, Olson EN (2003) Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol 65:45-79. doi:10.1146/annurev. physiol.65.092101 (Pubitemid 38249147)
40. Ho KK, Pinsky JL, Kannel WB, Levy D (1993) The epidemiology of heart failure: the Framingham Study. J Am Coll Cardiol 22(4 Suppl A):6A-13A (Pubitemid 23285789)
41. Lloyd-Jones DM, Larson MG, Leip EP, Beiser A, D'Agostino RB, Kannel WB, Murabito JM, Vasan RS, Benjamin EJ, Levy D (2002) Lifetime risk for developing congestive heart failure: the Framingham Heart Study. Circulation 106(24):3068-3072 (Pubitemid 35440290)
42. Salvatorelli E, Guarnieri S, Menna P, Liberi G, Calafiore AM, Mariggio MA, Mordente A, Gianni L, Minotti G (2006) Defective one-or two-electron reduction of the anticancer anthracycline epirubicin in human heart. Relative importance of vesicular sequestration and impaired efficiency of electron addition. J Biol Chem 281(16):10990-11001 (Pubitemid 43855522)
43. Ikegami E, Fukazawa R, Kanbe M, Watanabe M, Abe M, Kamisago M, Hajikano M, Katsube Y, Ogawa S (2007) Edaravone, a potent free radical scavenger, prevents anthracyclineinduced myocardial cell death. Circ J 71(11):1815-1820. doi: JST. JSTAGE/circj/71.1815 (Pubitemid 350240109)
44. Kim DS, Kim HR, Woo ER, Hong ST, Chae HJ, Chae SW (2005) Inhibitory effects of rosmarinic acid on adriamycin-induced apoptosis in H9c2 cardiac muscle cells by inhibiting reactive oxygen species and the activations of c-Jun. N-terminal kinase and extracellular signal-regulated kinase. Biochem Pharmacol 70(7):1066-1078. doi:10.1016/j.bcp. 2005.06.026
45. Kim DS, Woo ER, Chae SW, Ha KC, Lee GH, Hong ST, Kwon DY, Kim MS, Jung YK, Kim HM, Kim HK, Kim HR, Chae HJ (2007) Plantainoside D protects adriamycin-induced apoptosis in H9c2 cardiac muscle cells via the inhibition of ROS generation and NF-kappaB activation. Life Sci 80(4):314-323. doi: 10.1016/j.lfs.2006.09.019 (Pubitemid 44958709)
46. Li K, Sung RY, Huang WZ, Yang M, Pong NH, Lee SM, Chan WY, Zhao H, To MY, Fok TF, Li CK, Wong YO, Ng PC (2006) Thrombopoietin protects against in vitro and in vivo cardiotoxicity induced by doxorubicin. Circulation 113(18):2211-2220. doi:10.1161/CIRCULATIONAHA.105.560250
47. Mohamed HE, Asker ME, Ali SI, el-Fattah TM (2004) Protection against doxorubicin cardiomyopathy in rats: role of phosphodiesterase inhibitors type 4. J Pharm Pharmacol 56(6):757-768. doi:10.1211/0022357023565 (Pubitemid 38801692)
48. Spallarossa P, Garibaldi S, Altieri P, Fabbi P, Manca V, Nasti S, Rossettin P, Ghigliotti G, Ballestrero A, Patrone F, Barsotti A, Brunelli C (2004) Carvedilol prevents doxorubicin-induced free radical release and apoptosis in cardiomyocytes in vitro. J Mol Cell Cardiol 37(4):837-846. doi:10.1016/j.yjmcc.2004.05.024 (Pubitemid 39222076)
49. Blagosklonny MV, Hall MN (2009) Growth and aging: a common molecular mechanism. Aging (Albany NY) 1(4):357-362
50. Demidenko ZN, Blagosklonny MV (2009) Quantifying pharmacologic suppression of cellular senescence: prevention of cellular hypertrophy versus preservation of proliferative potential. Aging (Albany NY) 1(12):1008-1016
51. Demidenko ZN, Zubova SG, Bukreeva EI, Pospelov VA, Pospelova TV, Blagosklonny MV (2009) Rapamycin decelerates cellular senescence. Cell Cycle 8(12):1888-1895. doi:8606[pii]
52. Dickey JS, Redon CE, Nakamura AJ, Baird BJ, Sedelnikova OA, Bonner WM (2009) H2AX: functional roles and potential applications. Chromosoma 118(6):683-692. doi:10.1007/s00412-009-0234-4
53. Chua CC, Liu X, Gao J, Hamdy RC, Chua BH (2006) Multiple actions of pifithrin-alpha on doxorubicin-induced apoptosis in rat myoblastic H9c2 cells. Am J Physiol Heart Circ Physiol 290(6):H2606-H2613. doi:10.1152/ajpheart.01138. 2005 (Pubitemid 43846092)
54. L'Ecuyer T, Sanjeev S, Thomas R, Novak R, Das L, Campbell W, Heide RV (2006) DNA damage is an early event in doxorubicin-induced cardiac myocyte death. Am J Physiol Heart Circ Physiol 291(3):H1273-H1280. doi:10.1152/ajpheart. 00738.2005 (Pubitemid 44343672)
55. Liu J, Mao W, Ding B, Liang CS (2008) ERKs/p53 signal transduction pathway is involved in doxorubicin-induced apoptosis in H9c2 cells and cardiomyocytes. Am J Physiol Heart Circ Physiol 295(5):H1956-H1965. doi:10.1152/ajpheart.00407.2008
56. Kim J, Park H, Im JY, Choi WS, Kim HS (2007) Sodium butyrate regulates androgen receptor expression and cell cycle arrest in human prostate cancer cells. Anticancer Res 27(5):3285-3292 (Pubitemid 47607553)
57. Antos CL, McKinsey TA, Dreitz M, Hollingsworth LM, Zhang CL, Schreiber K, Rindt H, Gorczynski RJ, Olson EN (2003) Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J Biol Chem 278(31):28930-28937. doi:10.1074/jbc. M303113200 (Pubitemid 36935803)
58. Sprigg L, Li A, Choy FY, Ausio J (2010) Interaction of daunomycin with acetylated chromatin. J Med Chem 53(17):6457-6465. doi:10.1021/jm1007853
59. Karagiannis TC, El-Osta A (2007) Will broad-spectrum histone deacetylase inhibitors be superseded by more specific compounds? Leukemia 21(1):61-65. doi:10.1038/sj.leu.2404464 (Pubitemid 44921835)
60. McKinsey TA (2010) Isoform-selective HDAC inhibitors: Closing in on translational medicine for the heart. J Mol Cell Cardiol. doi:10.1016/j.yjmcc. 2010.11.009
61. Su H, Altucci L, You Q (2008) Competitive or noncompetitive, that's the question: research toward histone deacetylase inhibitors. Mol Cancer Ther 7(5):1007-1012. doi:10.1158/1535-7163. MCT-07-2289