Endoplasmic reticulum stress plays a pivotal role in cell death mediated by the pan-deacetylase inhibitor panobinostat in human hepatocellular cancer cells

Translational Oncology

Volumn 6, Issue 2, 2013, Pages 143-157

  Montalbano, Roberta ^a   Waldegger, Petra ^a   Quint, Karl ^a   Jabari, Samir ^b   Neureiter, Daniel ^c   Illig, Romana ^c   Ocker, Matthias ^a   Di Fazio, Pietro ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ANTHRA [1, 9 CD] PYRAZOL 6 (2H) ONE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE 12; CASPASE 3; CASPASE 4; CASPASE 7; CASPASE 8; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; PANOBINOSTAT; PROTEIN C JUN; THAPSIGARGIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; LIVER CELL CARCINOMA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WESTERN BLOTTING;

EID: 84875762280     PISSN: None     EISSN: 19365233     Source Type: Journal    
DOI: 10.1593/tlo.12271     Document Type: Article

References (67)

1. Schattenberg JM, Schuchmann M, and Galle PR (2011). Cell death and hepatocarcinogenesis: dysregulation of apoptosis signaling pathways. J Gastroenterol Hepatol 26(suppl 1), 213-219.
2. Tan J, Cang S, Ma Y, Petrillo RL, and Liu D (2010). Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J Hematol Oncol 3, 5.
3. Atadja P (2009). Development of the pan-DAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett 280, 233-241.
4. Di Fazio P, Ocker M, and Montalbano R (2011). New drugs, old fashioned ways: ER stress induced cell death. Curr Pharm Biotechnol 13, 2228-2234.
5. Rao R, Nalluri S, Kolhe R, Yang Y, Fiskus W, Chen J, Ha K, Buckley KM, Balusu R, Coothankandaswamy V, et al. (2010). Treatment with panobinostat induces glucose-regulated protein 78 acetylation and endoplasmic reticulum stress in breast cancer cells. Mol Cancer Ther 9, 942-952.
6. Suzuki M, Endo M, Shinohara F, Echigo S, and Rikiishi H (2009). Enhancement of cisplatin cytotoxicity by SAHA involves endoplasmic reticulum stressmediated apoptosis in oral squamous cell carcinoma cells. Cancer Chemother Pharmacol 64, 1115-1122.
7. Kahali S, Sarcar B, Fang B, Williams ES, Koomen JM, Tofilon PJ, and Chinnaiyan P (2010). Activation of the unfolded protein response contributes toward the antitumor activity of vorinostat. Neoplasia 12, 80-86.
8. Gahr S, Wissniowski T, Zopf S, Strobel D, Pustowka A, and Ocker M (2012). Combination of the deacetylase inhibitor panobinostat and the multi-kinase inhibitor sorafenib for the treatment of metastatic hepatocellular carcinoma-review of the underlying molecular mechanisms and first case report. J Cancer 3, 158-165.
9. Stewart AK (2012). Novel therapeutics in multiple myeloma. Hematology 17(suppl 1), 105-108.
10. Di Fazio P, Schneider-Stock R, Neureiter D, Okamoto K, Wissniowski T, Gahr S, Quint K, Meissnitzer M, Alinger B, Montalbano R, et al. (2010). The pandeacetylase inhibitor panobinostat inhibits growth of hepatocellular carcinoma models by alternative pathways of apoptosis. Cell Oncol 32, 285-300.
11. Walter P and Ron D (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086.
12. Wang HC, Huang W, LaiMD, and Su IJ (2006). Hepatitis B virus pre-S mutants, endoplasmic reticulum stress and hepatocarcinogenesis. Cancer Sci 97, 683-688.
13. Ron D and Walter P (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8, 519-529.
14. Hetz C and Glimcher LH (2009). Fine-tuning of the unfolded protein response: assembling the IRE1α interactome. Mol Cell 35, 551-561.
15. Malhi H and Kaufman RJ (2011). Endoplasmic reticulum stress in liver disease. J Hepatol 54, 795-809.
16. Rutkowski DT and Kaufman RJ (2004). A trip to the ER: coping with stress. Trends Cell Biol 14, 20-28.
17. Gorman AM, Healy SJ, Jager R, and Samali A (2012). Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacol Ther 134, 306-316.
18. Tabas I and Ron D (2011). Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13, 184-190.
19. Engin F and Hotamisligil GS (2010). Restoring endoplasmic reticulum function by chemical chaperones: an emerging therapeutic approach for metabolic diseases. Diabetes Obes Metab 12(suppl 2), 108-115.
20. Di Fazio P, Montalbano R, Neureiter D, Alinger B, Schmidt A, Merkel AL, Quint K, and Ocker M (2012). Downregulation of HMGA2 by the pandeacetylase inhibitor panobinostat is dependent on hsa-let-7b expression in liver cancer cell lines. Exp Cell Res 318, 1832-1843.
21. Kirkeby S and Thomsen CE (2005). Quantitative immunohistochemistry of fluorescence labelled probes using low-cost software. J Immunol Methods 301, 102-113.
22. Karnovsky M (1971). Use of ferrocyanide reduced osmium in electron microscopy. Proc 14th Annu Meet Am Soc Cell Biol 146a.
23. Small J (1968). Measurement of section thickness. Abstr 4th Eur Reg Conf Electron Microsc 1, 609-610.
24. Peachey LD (1958). Thin sections. I. A study of section thickness and physical distortion produced during microtomy. J Biophys Biochem Cytol 4, 233-242.
25. Oyadomari S and Mori M (2004). Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11, 381-389.
26. Yoshida H (2007). Unconventional splicing of XBP-1 mRNA in the unfolded protein response. Antioxid Redox Signal 9, 2323-2333.
27. Meister S, Schubert U, Neubert K, Herrmann K, Burger R, Gramatzki M, Hahn S, Schreiber S, Wilhelm S, Herrmann M, et al. (2007). Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Res 67, 1783-1792.
28. Cao H, Phan H, and Yang LX (2012). Improved chemotherapy for hepatocellular carcinoma. Anticancer Res 32, 1379-1386.
29. Frenette C and Gish R (2012). Targeted systemic therapies for hepatocellular carcinoma: clinical perspectives, challenges and implications. World J Gastroenterol 18, 498-506.
30. Coradini D and Speranza A (2005). Histone deacetylase inhibitors for treatment of hepatocellular carcinoma. Acta Pharmacol Sin 26, 1025-1033.
31. Khan O and La Thangue NB (2012). HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol 90, 85-94.
32. Miller CP, Singh MM, Rivera-Del Valle N, Manton CA, and Chandra J (2011). Therapeutic strategies to enhance the anticancer efficacy of histone deacetylase inhibitors. J Biomed Biotechnol 2011, 514261.
33. Prince HM, Bishton MJ, and Johnstone RW (2009). Panobinostat (LBH589): a potent pan-deacetylase inhibitor with promising activity against hematologic and solid tumors. Future Oncol 5, 601-612.
34. Ocker M and Schneider-Stock R (2007). Histone deacetylase inhibitors: signalling towards p21cip1/waf1. Int J Biochem Cell Biol 39, 1367-1374.
35. OckerM(2010). Deacetylase inhibitors-focus on non-histone targets and effects. World J Biol Chem 1, 55-61.
36. Rao R, Balusu R, Fiskus W, Mudunuru U, Venkannagari S, Chauhan L, Smith JE, Hembruff SL, Ha K, Atadja P, et al. (2012). Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther 11, 973-983.
37. Liu YL, Yang PM, Shun CT, Wu MS, Weng JR, and Chen CC (2010). Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy 6, 1057-1065.
38. Ni M and Lee AS (2007). ER chaperones in mammalian development and human diseases. FEBS Lett 581, 3641-3651.
39. Lee AS (2007). GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res 67, 3496-3499.
40. Kamiya T, Obara A, Hara H, Inagaki N, and Adachi T (2011). ER stress inducer, thapsigargin, decreases extracellular-superoxide dismutase through MEK/ERK signalling cascades in COS7 cells. Free Radic Res 45, 692-698.
41. Lee AH and Glimcher LH (2009). Intersection of the unfolded protein response and hepatic lipid metabolism. Cell Mol Life Sci 66, 2835-2850.
42. Parmar VM and Schroder M (2012). Sensing endoplasmic reticulum stress. Adv Exp Med Biol 738, 153-168.
43. Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, Arias C, Lennon CJ, Kluger Y, and DynlachtBD(2007). XBP1 controls diverse cell type-and conditionspecific transcriptional regulatory networks. Mol Cell 27, 53-66.
44. Yokouchi M, Hiramatsu N, Hayakawa K, Kasai A, Takano Y, Yao J, and Kitamura M (2007). Atypical, bidirectional regulation of cadmium-induced apoptosis via distinct signaling of unfolded protein response. Cell Death Differ 14, 1467-1474.
45. Chakrabarti A, Chen AW, and Varner JD (2011). A review of the mammalian unfolded protein response. Biotechnol Bioeng 108, 2777-2793.
46. Hetz C (2012). The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13, 89-102.
47. Nagai H, Noguchi T, Takeda K, and Ichijo H (2007). Pathophysiological roles of ASK1-MAP kinase signaling pathways. J Biochem Mol Biol 40, 1-6.
48. Szegezdi E, Fitzgerald U, and Samali A (2003). Caspase-12 and ER-stressmediated apoptosis: the story so far. Ann N Y Acad Sci 1010, 186-194.
49. Jing G, Wang JJ, and Zhang SX (2012). ER stress and apoptosis: a new mechanism for retinal cell death. Exp Diabetes Res 2012, 589589.
50. Momoi T (2004). Caspases involved in ER stress-mediated cell death. J Chem Neuroanat 28, 101-105.
51. Lamkanfi M, Festjens N, Declercq W, Vanden Berghe T, and Vandenabeele P (2007). Caspases in cell survival, proliferation and differentiation. Cell Death Differ 14, 44-55.
52. Asselah T, Bieche I, Mansouri A, Laurendeau I, Cazals-Hatem D, Feldmann G, Bedossa P, Paradis V, Martinot-Peignoux M, Lebrec D, et al. (2010). In vivo hepatic endoplasmic reticulum stress in patients with chronic hepatitis C. J Pathol 221, 264-274.
53. Yang G, Sun Q, Teng Y, Li F, Weng T, and Yang X (2008). PTEN deficiency causes dyschondroplasia in mice by enhanced hypoxia-inducible factor 1α signaling and endoplasmic reticulum stress. Development 135, 3587-3597.
54. Vijayalakshmi K, Alladi PA, Ghosh S, Prasanna VK, Sagar BC, Nalini A, Sathyaprabha TN, and Raju TR (2011). Evidence of endoplasmic reticular stress in the spinal motor neurons exposed to CSF from sporadic amyotrophic lateral sclerosis patients. Neurobiol Dis 41, 695-705.
55. Zocchi L, Bourdon JC, Codispoti A, Knight R, Lane DP, Melino G, and Terrinoni A (2008). Scotin: a new p63 target gene expressed during epidermal differentiation. Biochem Biophys Res Commun 367, 271-276.
56. Pyati UJ, Gjini E, Carbonneau S, Lee JS, Guo F, Jette CA, Kelsell DP, and Look AT (2011). p63 mediates an apoptotic response to pharmacological and disease-related ER stress in the developing epidermis. Dev Cell 21, 492-505.
57. Jia W, Pua HH, Li QJ, and He YW (2011). Autophagy regulates endoplasmic reticulum homeostasis and calcium mobilization in T lymphocytes. J Immunol 186, 1564-1574.
58. Benbrook DM and Long A (2012). Integration of autophagy, proteasomal degradation, unfolded protein response and apoptosis. Exp Oncol 34, 286-297.
59. Deegan S, Saveljeva S, Gorman AM, and Samali A (2012). Stress-induced selfcannibalism: on the regulation of autophagy by endoplasmic reticulum stress. Cell Mol Life Sci.
60. Woehlbier U and Hetz C (2011). Modulating stress responses by the UPRosome: a matter of life and death. Trends Biochem Sci 36, 329-337.
61. Gandesiri M, Chakilam S, Ivanovska J, Benderska N, Ocker M, Di Fazio P, Feoktistova M, Gali-Muhtasib H, Rave-Frank M, Prante O, et al. (2012). DAPK plays an important role in panobinostat-induced autophagy and commits cells to apoptosis under autophagy deficient conditions. Apoptosis 17, 1300-1315.
62. Bartoszewski R, Brewer JW, Rab A, Crossman DK, Bartoszewska S, Kapoor N, Fuller C, Collawn JF, and Bebok Z (2011). The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J Biol Chem 286, 41862-41870.
63. Behrman S, Acosta-Alvear D, and Walter P (2011). A CHOP-regulated micro-RNA controls rhodopsin expression. J Cell Biol 192, 919-927.
64. Duan Q, Wang X, Gong W, Ni L, Chen C, He X, Chen F, Yang L, Wang P, and Wang DW (2012). ER stress negatively modulates the expression of the miR-199a/214 cluster to regulates tumor survival and progression in human hepatocellular cancer. PLoS One 7, e31518.
65. Sampath D, Liu C, Vasan K, Sulda M, Puduvalli VK, Wierda WG, and Keating MJ (2012). Histone deacetylases mediate the silencing of miR-15a, miR-16, and miR-29b in chronic lymphocytic leukemia. Blood 119, 1162-1172.
66. Rhodes LV, Nitschke AM, Segar HC, Martin EC, Driver JL, Elliott S, Nam SY, Li M, Nephew KP, Burow ME, et al. (2012). The histone deacetylase inhibitor trichostatin A alters microRNA expression profiles in apoptosis-resistant breast cancer cells. Oncol Rep 27, 10-16.
67. Lee EM, Shin S, Cha HJ, Yoon Y, Bae S, Jung JH, Lee SM, Lee SJ, Park IC, Jin YW, et al. (2009). Suberoylanilide hydroxamic acid (SAHA) changes micro-RNA expression profiles in A549 human non-small cell lung cancer cells. Int J Mol Med 24, 45-50.