Disruption of autophagy by the histone deacetylase inhibitor MGCD0103 and its therapeutic implication in B-cell chronic lymphocytic leukemia

Leukemia

Volumn 28, Issue 8, 2014, Pages 1636-1646

  El Khoury, V ^a   Pierson, S ^a   Szwarcbart, E ^a   Brons, N H C ^a   Roland, O ^a   Cherrier De Wilde, S ^b   Plawny, L ^b   Van Dyck, E ^a   Berchem, G ^a,b  

^a LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^b CENTRE HOSPITALIER DE LUXEMBOURG   (Luxembourg)

Author keywords

autophagy; B cell chronic lymphocytic leukemia; calpains; caspases; histone deacetylase inhibitor; MGCD0103

Indexed keywords

AGED; AGED, 80 AND OVER; AUTOPHAGY; BENZAMIDES; CALPAIN; CELL SURVIVAL; FEMALE; FLAVONOIDS; HISTONE DEACETYLASE INHIBITORS; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; PHOSPHATIDYLINOSITOL 3-KINASES; PIPERIDINES; PROTO-ONCOGENE PROTEINS C-AKT; PYRIMIDINES; TOR SERINE-THREONINE KINASES; TRANSCRIPTION, GENETIC;

EID: 84905679330     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2014.19     Document Type: Article

References (61)

1. Zenz T, Mertens D, Kuppers R, Dohner H, Stilgenbauer S. From pathogenesis to treatment of chronic lymphocytic leukaemia. Nat Rev Cancer 2010; 10: 37-50.
2. Burger JA. Targeting the microenvironment in chronic lymphocytic leukemia is changing the therapeutic landscape. Curr Opin Oncol 2012; 24: 643-649.
3. Rikiishi H. Autophagic and apoptotic effects of HDAC inhibitors on cancer cells. J Biomed Biotechnol 2011; 2011: 830260.
4. True O, Matthias P. Interplay between histone deacetylases and autophagy-from cancer therapy to neurodegeneration. Immunol Cell Biol 2012; 90: 78-84.
5. Gammoh N, Lam D, Puente C, Ganley I, Marks PA, Jiang X. Role of autophagy in histone deacetylase inhibitor-induced apoptotic and nonapoptotic cell death. Proc Natl Acad Sci USA 2012; 109: 6561-6565.
6. Shao Y, Gao Z, Marks PA, Jiang X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci USA 2004; 101: 18030-18035.
7. Liu YL, Yang PM, Shun CT, Wu MS, Weng JR, Chen CC. Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy 2010; 6: 1057-1065.
8. Gordy C, He YW. The crosstalk between autophagy and apoptosis: where does this lead? Protein Cell 2012; 3: 17-27.
9. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
10. Carew JS, Medina EC, Esquivel 2nd JA, Mahalingam D, Swords R, Kelly K et al. Autophagy inhibition enhances vorinostat-induced apoptosis via ubiquitinated protein accumulation. J Cell Mol Med 2010; 14: 2448-2459.
11. Townsend KN, Hughson LR, Schlie K, Poon VI, Westerback A, Lum JJ. Autophagy inhibition in cancer therapy: metabolic considerations for antitumor immunity. Immunol Rev 2012; 249: 176-194.
12. Kovaleva V, Mora R, Park YJ, Plass C, Chiramel AI, Bartenschlager R et al. miRNA- 130a targets ATG2B and DICER1 to inhibit autophagy and trigger killing of chronic lymphocytic leukemia cells. Cancer Res 2012; 72: 1763-1772.
13. Laane E, Tamm KP, Buentke E, Ito K, Kharaziha P, Oscarsson J et al. Cell death induced by dexamethasone in lymphoid leukemia is mediated through initiation of autophagy. Cell Death Differ 2009; 16: 1018-1029.
14. El-Khoury V, Moussay E, Janji B, Palissot V, Aouali N, Brons NH et al. The histone deacetylase inhibitor MGCD0103 induces apoptosis in B-cell chronic lymphocytic leukemia cells through a mitochondria-mediated caspase activation cascade. Mol Cancer Ther 2010; 9: 1349-1360.
15. Atmaca A, Al-Batran SE, Maurer A, Neumann A, Heinzel T, Hentsch B et al. Valproic acid (VPA) in patients with refractory advanced cancer: a dose escalating phase I clinical trial. Br J Cancer 2007; 97: 177-182.
16. Sung V, Richard N, Brady H, Maier A, Kelter G, Heise C. Histone deacetylase inhibitor MGCD0103 synergizes with gemcitabine in human pancreatic cells. Cancer Sci 2011; 102: 1201-1207.
17. Di Trani L, Savarino A, Campitelli L, Norelli S, Puzelli S, D'Ostilio D et al. Different pH requirements are associated with divergent inhibitory effects of chloroquine on human and avian influenza A viruses. Virol J 2007; 4: 39.
18. Byrd JC, Lin TS, Dalton JT, Wu D, Phelps MA, Fischer B et al. Flavopiridol administered using a pharmacologically derived schedule is associated with marked clinical efficacy in refractory, genetically high-risk chronic lymphocytic leukemia. Blood 2007; 109: 399-404.
19. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006; 58: 621-681.
20. Ichimura Y, Komatsu M. Selective degradation of p62 by autophagy. Semin Immunopathol 2010; 32: 431-436.
21. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010; 90: 1383-1435.
22. Norman JM, Cohen GM, Bampton ET. The in vitro cleavage of the hAtg proteins by cell death proteases. Autophagy 2010; 6: 1042-1056.
23. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119: 753-766.
24. Akar U, Ozpolat B, Mehta K, Fok J, Kondo Y, Lopez-Berestein G. Tissue transglutaminase inhibits autophagy in pancreatic cancer cells. Mol Cancer Res 2007; 5: 241-249.
25. D'Eletto M, Farrace MG, Rossin F, Strappazzon F, Giacomo GD, Cecconi F et al. Type 2 transglutaminase is involved in the autophagy-dependent clearance of ubiquitinated proteins. Cell Death Differ 2012; 19: 1228-1238.
26. Xia HG, Zhang L, Chen G, Zhang T, Liu J, Jin M et al. Control of basal autophagy by calpain1 mediated cleavage of ATG5. Autophagy 2010; 6: 61-66.
27. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L et al. Calpainmediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8: 1124-1132.
28. Van Bockstaele F, Pede V, Naessens E, Van Coppernolle S, Van Tendeloo V, Verhasselt B et al. Efficient gene transfer in CLL by mRNA electroporation. Leukemia 2008; 22: 323-329.
29. Serafini M, Naldini L, Introna M. Molecular evidence of inefficient transduction of proliferating human B lymphocytes by VSV-pseudotyped HIV-1-derived lentivectors. Virology 2004; 325: 413-424.
30. Mahoney E, Lucas DM, Gupta SV, Wagner AJ, Herman SE, Smith LL et al. ER stress and autophagy: new discoveries in the mechanism of action and drug resistance of the cyclin-dependent kinase inhibitor flavopiridol. Blood 2012; 120: 1262-1273.
31. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122: 927-939.
32. Pyo JO, Jang MH, Kwon YK, Lee HJ, Jun JI, Woo HN et al. Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death. J Biol Chem 2005; 280: 20722-20729.
33. Wirawan E, Vande Walle L, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I et al. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 2010; 1: e18.
34. Amrein L, Soulieres D, Johnston JB, Aloyz R. p53 and autophagy contribute to dasatinib resistance in primary CLL lymphocytes. Leuk Res 2011; 35: 99-102.
35. Lopez G, Torres K, Lev D. Autophagy blockade enhances HDAC inhibitors' pro-apoptotic effects: potential implications for the treatment of a therapeuticresistant malignancy. Autophagy 2011; 7: 440-441.
36. Kovacs JR, Li C, Yang Q, Li G, Garcia IG, Ju S et al. Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery. Cell Death Differ 2012; 19: 144-152.
37. Li C, Capan E, Zhao Y, Zhao J, Stolz D, Watkins SC et al. Autophagy is induced in CD4+ T cells and important for the growth factor-withdrawal cell death. J Immunol 2006; 177: 5163-5168.
38. Abarientos C, Sperber K, Shapiro DL, Aronow WS, Chao CP, Ash JY. Hydroxychloroquine in systemic lupus erythematosus and rheumatoid arthritis and its safety in pregnancy. Expert Opin Drug Saf 2011; 10: 705-714.
39. Lee SJ, Silverman E, Bargman JM. The role of antimalarial agents in the treatment of SLE and lupus nephritis. Nat Rev Nephrol 2011; 7: 718-729.
40. Choi KS. Autophagy and cancer. Exp Mol Med 2012; 44: 109-120.
41. Christian BA, Grever MR, Byrd JC, Lin TS. Flavopiridol in the treatment of chronic lymphocytic leukemia. Curr Opin Oncol 2007; 19: 573-578.
42. Lin TS, Ruppert AS, Johnson AJ, Fischer B, Heerema NA, Andritsos LA et al. Phase II study of flavopiridol in relapsed chronic lymphocytic leukemia demonstrating high response rates in genetically high-risk disease. J Clin Oncol 2009; 27: 6012-6018.
43. MacCallum SF, Groves MJ, James J, Murray K, Appleyard V, Prescott AR et al. Dysregulation of autophagy in chronic lymphocytic leukemia with the smallmolecule Sirtuin inhibitor Tenovin-6. Sci Rep 2013; 3: 1275.
44. Cao DJ, Wang ZV, Battiprolu PK, Jiang N, Morales CR, Kong Y et al. Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci USA 2011; 108: 4123-4128.
45. Stankov MV, El Khatib M, Kumar Thakur B, Heitmann K, Panayotova-Dimitrova D, Schoening J et al. Histone deacetylase inhibitors induce apoptosis in myeloid leukemia by suppressing autophagy. Leukemia 2014; 28: 577-588.
46. Cao Q, Yu C, Xue R, Hsueh W, Pan P, Chen Z et al. Autophagy induced by suberoylanilide hydroxamic acid in Hela S3 cells involves inhibition of protein kinase B and up-regulation of Beclin 1. Int J Biochem Cell Biol 2008; 40: 272-283.
47. Li J, Liu R, Lei Y, Wang K, Lau QC, Xie N et al. Proteomic analysis revealed association of aberrant ROS signaling with suberoylanilide hydroxamic acid-induced autophagy in Jurkat T-leukemia cells. Autophagy 2010; 6: 711-724.
48. Ben Sahra I, Laurent K, Giuliano S, Larbret F, Ponzio G, Gounon P et al. Targeting cancer cell metabolism: the combination of metformin and 2-deoxyglucose induces p53-dependent apoptosis in prostate cancer cells. Cancer Res 2010; 70: 2465-2475.
49. Dowling RJ, Zakikhani M, Fantus IG, Pollak M, Sonenberg N. Metformin inhibits mammalian target of rapamycin-dependent translation initiation in breast cancer cells. Cancer Res 2007; 67: 10804-10812.
50. van Staveren WC, Solis DY, Hebrant A, Detours V, Dumont JE, Maenhaut C. Human cancer cell lines: experimental models for cancer cells in situ? For cancer stem cells? Biochim Biophys Acta 2009; 1795: 92-103.
51. van Helden SF, van Leeuwen FN, Figdor CG. Human and murine model cell lines for dendritic cell biology evaluated. Immunol Lett 2008; 117: 191-197.
52. Huszthy PC, Daphu I, Niclou SP, Stieber D, Nigro JM, Sakariassen PO et al. In vivo models of primary brain tumors: pitfalls and perspectives. Neuro Oncol 2012; 14: 979-993.
53. Ahn MY, Ahn SG, Yoon JH. Apicidin, a histone deaceylase inhibitor, induces both apoptosis and autophagy in human oral squamous carcinoma cells. Oral Oncol 2011; 47: 1032-1038.
54. Yang XJ, Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 2008; 31: 449-461.
55. Lee JY, Yao TP. Quality control autophagy: a joint effort of ubiquitin, protein deacetylase and actin cytoskeleton. Autophagy 2010; 6: 555-557.
56. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003; 115: 727-738.
57. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140: 313-326.
58. Ichimura Y, Kominami E, Tanaka K, Komatsu M. Selective turnover of p62/A170/SQSTM1 by autophagy. Autophagy 2008; 4: 1063-1066.
59. Buchser WJ, Laskow TC, Pavlik PJ, Lin HM, Lotze MT. Cell-mediated autophagy promotes cancer cell survival. Cancer Res 2012; 72: 2970-2979.
60. Pham VC, Pitti R, Anania VG, Bakalarski CE, Bustos D, Jhunjhunwala S et al. Complementary proteomic tools for the dissection of apoptotic proteolysis events. J Proteome Res 2012; 11: 2947-2954.
61. Moscat J, Diaz-Meco MT. p62: a versatile multitasker takes on cancer. Trends Biochem Sci 2012; 37: 230-236.