Autophagy-related cell death by pan-histone deacetylase inhibition in liver cancer

Oncotarget

Volumn 7, Issue 20, 2016, Pages 28998-29010

  Di Fazio, Pietro ^a   Waldegger, Petra ^b   Jabari, Samir ^c   Lingelbach, Susanne ^a   Montalbano, Roberta ^a   Ocker, Matthias ^a,e   Slater, Emily P ^a   Bartsch, Detlef K ^a   Illig, Romana ^d   Neureiter, Daniel ^d   Wissniowski, Thaddeus T ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d PARACELSUS MEDICAL UNIVERSITY   (Austria)

^e BAYER PHARMA AG   (Germany)

Author keywords

Autophagic cell death; Autophagosomes; Cancer therapy; Liver cancer; Pan deacetylase inhibitor

Indexed keywords

BECLIN 1; DRAM1 PROTEIN; HISTONE DEACETYLASE INHIBITOR; MAP1LC3B PROTEIN; MARKER; MICROTUBULE ASSOCIATED PROTEIN 1; PANOBINOSTAT; PROTEIN P53; PROTEIN P73; TAMOXIFEN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; HYDROXAMIC ACID; INDOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DRUG CYTOTOXICITY; HEPATOCELLULAR CARCINOMA CELL LINE; HEPG2 CELL LINE; HUMAN; HUMAN CELL; LIVER CANCER; MOUSE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; CELL DEATH; DRUG EFFECTS; DRUG SCREENING; HEP-G2 CELL LINE; LIVER CELL CARCINOMA; LIVER TUMOR; NUDE MOUSE; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; AUTOPHAGY; CARCINOMA, HEPATOCELLULAR; CELL DEATH; HEP G2 CELLS; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; INDOLES; LIVER NEOPLASMS; MICE; MICE, NUDE; TAMOXIFEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84969884831     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8585     Document Type: Article

References (53)

1. Bosch FX, Ribes J, Diaz M, Cleries R. Primary liver cancer: worldwide incidence and trends. Gastroenterology. 2004; 127:S5-S16.
2. Simonetti RG, Liberati A, Angiolini C, Pagliaro L. Treatment of hepatocellular carcinoma: a systematic review of randomized controlled trials. Ann Oncol. 1997; 8:117-36.
3. Denton D, Xu T, Kumar S. Autophagy as a pro-death pathway. Immunol Cell Biol. 2015; 93:35-42. doi: 10.1038/icb.2014.85.
4. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008; 132:27-42.
5. Gray JV, Petsko GA, Johnston GC, Ringe D, Singer RA, Werner-Washburne M. "Sleeping beauty": quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 2004; 68:187-206.
6. Liang C, Jung JU. Autophagy genes as tumor suppressors. Curr Opin Cell Biol. 2010; 22:226-33.
7. Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008; 9:1004-10.
8. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, Cattoretti G, Levine B. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest. 2003; 112:1809-20.
9. Fischer TD, Wang JH, Vlada A, Kim JS, Behrns KE. Role of autophagy in differential sensitivity of hepatocarcinoma cells to sorafenib. World J Hepatol. 2014; 6:752-8.
10. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH, Jung JU. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol. 2006; 8:688-99.
11. Ruivo R, Anne C, Sagne C, Gasnier B. Molecular and cellular basis of lysosomal transmembrane protein dysfunction. Biochim Biophys Acta. 2009; 1793:636-49.
12. Laurin N, Brown JP, Morissette J, Raymond V. Recurrent mutation of the gene encoding sequestosome 1 (SQSTM1/ p62) in Paget disease of bone. Am J Hum Genet. 2002; 70:1582-8.
13. Hale AN, Ledbetter DJ, Gawriluk TR, Rucker EB, 3rd. Autophagy: regulation and role in development. Autophagy. 2013; 9:951-72.
14. Loos B, Engelbrecht AM, Lockshin RA, Klionsky DJ, Zakeri Z. The variability of autophagy and cell death susceptibility: Unanswered questions. Autophagy. 2013; 9:1270-85.
15. Mah LY, Ryan KM. Autophagy and cancer. Cold Spring Harb Perspect Biol. 2012; 4:a008821.
16. Gryder BE, Sodji QH, Oyelere AK. Targeted cancer therapy: giving histone deacetylase inhibitors all they need to succeed. Future Med Chem. 2012; 4:505-24.
17. Anne M, Sammartino D, Barginear MF, Budman D. Profile of panobinostat and its potential for treatment in solid tumors: an update. Onco Targets Ther. 2013; 6:1613-24.
18. Di Fazio P, Schneider-Stock R, Neureiter D, Okamoto K, Wissniowski T, Gahr S, Quint K, Meissnitzer M, Alinger B, Montalbano R, Sass G, Hohenstein B, Hahn EG, et al. The pan-deacetylase inhibitor panobinostat inhibits growth of hepatocellular carcinoma models by alternative pathways of apoptosis. Cell Oncol. 2010; 32:285-300.
19. Montalbano R, Waldegger P, Quint K, Jabari S, Neureiter D, Illig R, Ocker M, Di Fazio P. Endoplasmic reticulum stress plays a pivotal role in cell death mediated by the pandeacetylase inhibitor panobinostat in human hepatocellular cancer cells. Transl Oncol. 2013; 6:143-57.
20. Di Fazio P, Montalbano R, Neureiter D, Alinger B, Schmidt A, Merkel AL, Quint K, Ocker M. Downregulation of HMGA2 by the pan-deacetylase inhibitor panobinostat is dependent on hsa-let-7b expression in liver cancer cell lines. Exp Cell Res. 2012; 318:1832-43.
21. Henrici A, Montalbano R, Neureiter D, Krause M, Stiewe T, Slater EP, Quint K, Ocker M, Di Fazio P. The pan-deacetylase inhibitor panobinostat suppresses the expression of oncogenic miRNAs in hepatocellular carcinoma cell lines. Mol Carcinog. 2015; 54:585-97. doi: 10.1002/mc.22122.
22. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012; 8:445-544.
23. Ryan KM. p53 and autophagy in cancer: guardian of the genome meets guardian of the proteome. Eur J Cancer. 2011; 47:44-50.
24. Levine B, Abrams J. p53: The Janus of autophagy? Nat Cell Biol. 2008; 10:637-9.
25. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007; 3:452-60.
26. Mitou G, Frentzel J, Desquesnes A, Le Gonidec S, AlSaati T, Beau I, Lamant L, Meggetto F, Espinos E, Codogno P, Brousset P, Giuriato S. Targeting autophagy enhances the anti-tumoral action of crizotinib in ALK-positive anaplastic large cell lymphoma. Oncotarget. 2015; 6:30149-64. doi: 10.18632/oncotarget.4999.
27. Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol. 2010; 221:117-24.
28. Di Fazio P, Montalbano R, Quint K, Alinger B, Kemmerling R, Kiesslich T, Ocker M, Neureiter D. The pan-deacetylase inhibitor panobinostat modulates the expression of epithelialmesenchymal transition markers in hepatocellular carcinoma models. Oncol Lett. 2013; 5:127-34.
29. Murata S, Mine T, Sugihara F, Yasui D, Yamaguchi H, Ueda T, Onozawa S, Kumita SI. Interventional treatment for unresectable hepatocellular carcinoma. World J Gastroenterol. 2014; 20:13453-65.
30. P DIF, Montalbano R, Quint K, Alinger B, Kemmerling R, Kiesslich T, Ocker M, Neureiter D. The pan-deacetylase inhibitor panobinostat modulates the expression of epithelial-mesenchymal transition markers in hepatocellular carcinoma models. Oncol Lett. 2013; 5:127-34.
31. Deter RL. Quantitative characterization of dense body, autophagic vacuole, and acid phosphatase-bearing particle populations during the early phases of glucagon-induced autophagy in rat liver. J Cell Biol. 1971; 48:473-89.
32. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol. 2010; 12:814-22.
33. Tian Y, Kuo C, Sir D, Wang L, Govindarajan S, Petrovic LM, Ou JJ. Autophagy inhibits oxidative stress and tumor suppressors to exert its dual effect on hepatocarcinogenesis. Cell Death Differ. 2015; 22:1025-34. doi: 10.1038/cdd.2014.201.
34. Rautou PE, Mansouri A, Lebrec D, Durand F, Valla D, Moreau R. Autophagy in liver diseases. J Hepatol. 2010; 53:1123-34.
35. Huang G, Jiang Q, Cai C, Qu M, Shen W. SCD1 negatively regulates autophagy-induced cell death in human hepatocellular carcinoma through inactivation of the AMPK signaling pathway. Cancer Lett. 2015; 358:180-90. doi: 10.1016/j.canlet.2014.12.036.
36. Peng YF, Shi YH, Ding ZB, Ke AW, Gu CY, Hui B, Zhou J, Qiu SJ, Dai Z, Fan J. Autophagy inhibition suppresses pulmonary metastasis of HCC in mice via impairing anoikis resistance and colonization of HCC cells. Autophagy. 2013; 9:2056-68.
37. Song W, Wang F, Lotfi P, Sardiello M, Segatori L. 2-Hydroxypropyl-beta-cyclodextrin promotes transcription factor EB-mediated activation of autophagy: implications for therapy. J Biol Chem. 2014; 289:10211-22.
38. Lachenmayer A, Toffanin S, Cabellos L, Alsinet C, Hoshida Y, Villanueva A, Minguez B, Tsai HW, Ward SC, Thung S, Friedman SL, Llovet JM. Combination therapy for hepatocellular carcinoma: additive preclinical efficacy of the HDAC inhibitor panobinostat with sorafenib. J Hepatol. 2012; 56:1343-50.
39. 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; 6:1057-65.
40. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011; 18:571-80.
41. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A. 2003; 100:15077-82.
42. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell. 2006; 126:121-34.
43. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri- Mergny M, D'Amelio M, Criollo A, Morselli E, Zhu C, Harper F, Nannmark U, Samara C, Pinton P, et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol. 2008; 10:676-87.
44. Zou M, Lu N, Hu C, Liu W, Sun Y, Wang X, You Q, Gu C, Xi T, Guo Q. Beclin 1-mediated autophagy in hepatocellular carcinoma cells: implication in anticancer efficiency of oroxylin A via inhibition of mTOR signaling. Cell Signal. 2012; 24:1722-32.
45. Wild P, McEwan DG, Dikic I. The LC3 interactome at a glance. J Cell Sci. 2014; 127:3-9.
46. Salhab M, Canelo R. An overview of evidence-based management of hepatocellular carcinoma: a meta-analysis. J Cancer Res Ther. 2011; 7:463-75.
47. Kohli L, Kaza N, Coric T, Byer SJ, Brossier NM, Klocke BJ, Bjornsti MA, Carroll SL, Roth KA. 4-Hydroxytamoxifen induces autophagic death through K-Ras degradation. Cancer Res. 2013; 73:4395-405.
48. Nagahara Y, Takeyoshi M, Sakemoto S, Shiina I, Nakata K, Fujimori K, Wang Y, Umeda E, Watanabe C, Uetake S, Yamori T, Dan S, Yoshimi Y, et al. Novel tamoxifen derivative Ridaifen-B induces Bcl-2 independent autophagy without estrogen receptor involvement. Biochem Biophys Res Commun. 2013; 435:657-63.
49. Tong Y, Huang H, Pan H. Inhibition of MEK/ERK activation attenuates autophagy and potentiates pemetrexedinduced activity against HepG2 hepatocellular carcinoma cells. Biochem Biophys Res Commun. 2015; 456:86-91.
50. Dragowska WH, Weppler SA, Wang JC, Wong LY, Kapanen AI, Rawji JS, Warburton C, Qadir MA, Donohue E, Roberge M, Gorski SM, Gelmon KA, Bally MB. Induction of autophagy is an early response to gefitinib and a potential therapeutic target in breast cancer. PLoS One. 2013; 8:e76503.
51. Wang YX, Xu SQ, Chen XH, Liu RS, Liang ZQ. Autophagy involvement in olanzapine-mediated cytotoxic effects in human glioma cells. Asian Pac J Cancer Prev. 2014; 15:8107-13.
52. Lan SH, Wu SY, Zuchini R, Lin XZ, Su IJ, Tsai TF, Lin YJ, Wu CT, Liu HS. Autophagy-preferential degradation of MIR224 participates in hepatocellular carcinoma tumorigenesis. Autophagy. 2014; 10:1687-9.
53. Kiesslich T, Alinger B, Wolkersdorfer GW, Ocker M, Neureiter D, Berr F. Active Wnt signalling is associated with low differentiation and high proliferation in human biliary tract cancer in vitro and in vivo and is sensitive to pharmacological inhibition. Int J Oncol. 2010; 36:49-58.