New Drugs, Old Fashioned Ways: ER Stress Induced Cell Death

Current Pharmaceutical Biotechnology

Volumn 13, Issue 11, 2012, Pages 2228-2234

  Di Fazio, Pietro ^a   Ocker, Matthias ^a   Montalbano, Roberta ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Cell death; Endoplasmic Reticulum; Histone deacetylase inhibitors

Indexed keywords

ACYLTRANSFERASE; BELINOSTAT; BUTYRIC ACID; CASPASE 12; CASPASE 4; CYCLIN DEPENDENT KINASE INHIBITOR 1; DACINOSTAT; DEPSIPEPTIDE; ENTINOSTAT; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HISTONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; NONHISTONE PROTEIN; PANOBINOSTAT; REACTIVE OXYGEN METABOLITE; ROMIDEPSIN; TACEDINALINE; TRICHOSTATIN A; VALPROIC ACID; VORINOSTAT;

CELL DEATH; CHROMATIN; CUTANEOUS T CELL LYMPHOMA; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HEMATOLOGIC MALIGNANCY; HUMAN; NEOPLASM; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; UNFOLDED PROTEIN RESPONSE;

ANIMALS; CELL DEATH; ENDOPLASMIC RETICULUM STRESS; HISTONE DEACETYLASE INHIBITORS; HUMANS; NEOPLASMS;

EID: 84873450866     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112802501962     Document Type: Review

References (75)

1. Ciavarella, S.; Milano, A.; Dammacco, F.; Silvestris, F. Targeted therapies in cancer. BioDrugs, 2010, 24(2), 77-88.
2. Jana, S.; Paliwal, J. Apoptosis: potential therapeutic targets for new drug discovery. Curr. Med. Chem., 2007, 14(22), 2369-2379.
3. Schneider-Stock, R.; Ocker, M. Epigenetic therapy in cancer: molecular background and clinical development of histone deacetylase and DNA methyltransferase inhibitors. IDrugs, 2007, 10(8), 557-561.
4. Tan, J.; Cang, S.; Ma, Y.; Petrillo, R. L.; Liu, D. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J. Hematol. Oncol., 2010, 3, 5.
5. Gallinari, P.; Di Marco, S.; Jones, P.; Pallaoro, M.; Steinkuhler, C. HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics. Cell Res., 2007, 17(3), 195-211.
6. Kekatpure, V. D.; Dannenberg, A. J.; Subbaramaiah, K. HDAC6 modulates Hsp90 chaperone activity and regulates activation of aryl hydrocarbon receptor signaling. J. Biol. Chem., 2009, 284(12), 7436-7445.
7. Mahalingam, D.; Swords, R.; Carew, J. S.; Nawrocki, S. T.; Bhalla, K.; Giles, F. J. Targeting HSP90 for cancer therapy. Br. J. Cancer, 2009, 100(10), 1523-1529.
8. Yang, Y.; Rao, R.; Shen, J.; Tang, Y.; Fiskus, W.; Nechtman, J.; Atadja, P.; Bhalla, K. Role of acetylation and extracellular location of heat shock protein 90alpha in tumor cell invasion. Cancer Res., 2008, 68(12), 4833-4842.
9. Fiskus, W.; Ren, Y.; Mohapatra, A.; Bali, P.; Mandawat, A.; Rao, R.; Herger, B.; Yang, Y.; Atadja, P.; Wu, J.; Bhalla, K. Hydroxamic acid analogue histone deacetylase inhibitors attenuate estrogen receptor-alpha levels and transcriptional activity: a result of hyperacetylation and inhibition of chaperone function of heat shock protein 90. Clin. Cancer Res., 2007, 13(16), 4882-4890.
10. Roy, S.; Tenniswood, M. Site-specific acetylation of p53 directs selective transcription complex assembly. J. Biol. Chem., 2007, 282(7), 4765-4771.
11. Zhao, Y.; Lu, S.; Wu, L.; Chai, G.; Wang, H.; Chen, Y.; Sun, J.; Yu, Y.; Zhou, W.; Zheng, Q.; Wu, M.; Otterson, G. A.; Zhu, W. G. Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol. Cell Biol., 2006, 26(7), 2782-2790.
12. Ocker, M. Deacetylase inhibitors-focus on non-histone targets and effects. World J. Biol. Chem., 2010, 1(5).
13. Wlodkowic, D.; Skommer, J.; McGuinness, D.; Hillier, C.; Darzynkiewicz, Z. ER-Golgi network--a future target for anticancer therapy. Leuk Res., 2009, 33(11), 1440-1447.
14. Phillips, D. M. The presence of acetyl groups of histones. Biochem. J., 1963, 87, 258-263.
15. Glozak, M. A.; Seto, E. Histone deacetylases and cancer. Oncogene, 2007, 26(37), 5420-5432.
16. Rathkopf, D.; Wong, B. Y.; Ross, R. W.; Anand, A.; Tanaka, E.; Woo, M. M.; Hu, J.; Dzik-Jurasz, A.; Yang, W.; Scher, H. I. A phase I study of oral panobinostat alone and in combination with docetaxel in patients with castration-resistant prostate cancer. Cancer Chemother. Pharmacol., 2010, 66(1), 181-189.
17. Duvic, M.; Talpur, R.; Ni, X.; Zhang, C.; Hazarika, P.; Kelly, C.; Chiao, J. H.; Reilly, J. F.; Ricker, J. L.; Richon, V. M.; Frankel, S. R. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood, 2007, 109(1), 31-39.
18. Shao, W.; Growney, J. D.; Feng, Y.; O'Connor, G.; Pu, M.; Zhu, W.; Yao, Y. M.; Kwon, P.; Fawell, S.; Atadja, P. Activity of deacetylase inhibitor panobinostat (LBH589) in cutaneous T-cell lymphoma models: Defining molecular mechanisms of resistance. Int. J. Cancer, 2010, 127(9),2199-2208.
19. Ocker, M.; Schneider-Stock, R. Histone deacetylase inhibitors: signalling towards p21cip1/waf1. Int. J. Biochem. Cell Biol., 2007, 39(7-8), 1367-1374.
20. Ellis, L.; Atadja, P. W.; Johnstone, R. W. Epigenetics in cancer: targeting chromatin modifications. Mol. Cancer Ther., 2009, 8(6), 1409-1420.
21. Carlisi, D.; Vassallo, B.; Lauricella, M.; Emanuele, S.; D'Anneo, A.; Di Leonardo, E.; Di Fazio, P.; Vento, R.; Tesoriere, G. Histone deacetylase inhibitors induce in human hepatoma HepG2 cells acetylation of p53 and histones in correlation with apoptotic effects. Int. J. Oncol., 2008, 32(1), 177-184.
22. Nishioka, C.; Ikezoe, T.; Yang, J.; Komatsu, N.; Bandobashi, K.; Taniguchi, A.; Kuwayama, Y.; Togitani, K.; Koeffler, H. P.; Taguchi, H. Histone deacetylase inhibitors induce growth arrest and apoptosis of HTLV-1-infected T-cells via blockade of signaling by nuclear factor kappaB. Leuk Res., 2008, 32(2), 287-296.
23. Tan, J.; Zhuang, L.; Jiang, X.; Yang, K. K.; Karuturi, K. M.; Yu, Q. Apoptosis signal-regulating kinase 1 is a direct target of E2F1 and contributes to histone deacetylase inhibitor-induced apoptosis through positive feedback regulation of E2F1 apoptotic activity. J. Biol. Chem., 2006, 281(15), 10508-10515.
24. Zopf, S.; Neureiter, D.; Bouralexis, S.; Abt, T.; Glaser, K. B.; Okamoto, K.; Ganslmayer, M.; Hahn, E. G.; Herold, C.; Ocker, M. Differential response of p53 and p21 on HDAC inhibitor-mediated apoptosis in HCT116 colon cancer cells in vitro and in vivo. Int. J. Oncol., 2007, 31(6), 1391-1402.
25. Prystowsky, M. B.; Adomako, A.; Smith, R. V.; Kawachi, N.; McKimpson, W.; Atadja, P.; Chen, Q.; Schlecht, N. F.; Parish, J. L.; Childs, G.; Belbin, T. J. The histone deacetylase inhibitor LBH589 inhibits expression of mitotic genes causing G2/M arrest and cell death in head and neck squamous cell carcinoma cell lines. J. Pathol., 2009, 218(4), 467-477.
26. Lane, A. A.; Chabner, B. A. Histone deacetylase inhibitors in cancer therapy. J. Clin. Oncol., 2009, 27(32), 5459-5468.
27. Rao, R.; Nalluri, S.; Kolhe, R.; Yang, Y.; Fiskus, W.; Chen, J.; Ha, K.; Buckley, K. M.; Balusu, R.; Coothankandaswamy, V.; Joshi, A.; Atadja, P.; Bhalla, K. N. Treatment with panobinostat induces glucose-regulated protein 78 acetylation and endoplasmic reticulum stress in breast cancer cells. Mol. Cancer Ther., 2010, 9(4), 942-952.
28. Boelens, J.; Lust, S.; Offner, F.; Bracke, M. E.; Vanhoecke, B. W. Review. The endoplasmic reticulum: a target for new anticancer drugs. In Vivo, 2007, 21(2), 215-226.
29. Kim, R.; Emi, M.; Tanabe, K.; Murakami, S. Role of the unfolded protein response in cell death. Apoptosis, 2006, 11(1), 5-13.
30. Santos, C. X.; Tanaka, L. Y.; Wosniak, J.; Laurindo, F. R. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal, 2009, 11(10), 2409-2427.
31. Malhotra, J. D.; Kaufman, R. J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal, 2007, 9(12), 2277-2293.
32. Wouters, B. G.; Koritzinsky, M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat. Rev. Cancer, 2008, 8(11), 851-864.
33. Koumenis, C.; Wouters, B. G. "Translating" tumor hypoxia: unfolded protein response (UPR)-dependent and UPR-independent pathways. Mol. Cancer Res., 2006, 4(7), 423-436.
34. Kapoor, A.; Sanyal, A. J. Endoplasmic reticulum stress and the unfolded protein response. Clin. Liver Dis., 2009, 13(4), 581-590.
35. Dudek, J.; Benedix, J.; Cappel, S.; Greiner, M.; Jalal, C.; Muller, L.; Zimmermann, R. Functions and pathologies of BiP and its interaction partners. Cell Mol. Life Sci., 2009, 66(9), 1556-1569.
36. Quinones, Q. J.; de Ridder, G. G.; Pizzo, S. V. GRP78: a chaperone with diverse roles beyond the endoplasmic reticulum. Histol. Histopathol., 2008, 23(11), 1409-1416.
37. Gething, M. J. Role and regulation of the ER chaperone BiP. Semin. Cell Dev. Biol., 1999, 10(5), 465-472.
38. Plongthongkum, N.; Kullawong, N.; Panyim, S.; Tirasophon, W. Ire1 regulated XBP1 mRNA splicing is essential for the unfolded protein response (UPR) in Drosophila melanogaster. Biochem. Biophys. Res. Commun., 2007, 354(3), 789-794.
39. Oyadomari, S.; Mori, M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ., 2004, 11(4), 381-389.
40. Aarti, I.; Rajesh, K.; Ramaiah, K. V. Phosphorylation of eIF2 alpha in Sf9 cells: a stress, survival and suicidal signal. Apoptosis, 2010, 15(6), 679-692.
41. Chen, Y. J.; Tan, B. C.; Cheng, Y. Y.; Chen, J. S.; Lee, S. C. Differential regulation of CHOP translation by phosphorylated eIF4E under stress conditions. Nucleic Acids Res., 2010, 38(3), 764-777.
42. Heath-Engel, H. M.; Chang, N. C.; Shore, G. C. The endoplasmic reticulum in apoptosis and autophagy: role of the BCL-2 protein family. Oncogene, 2008, 27(50), 6419-6433.
43. Gupta, S.; Cuffe, L.; Szegezdi, E.; Logue, S. E.; Neary, C.; Healy, S.; Samali, A. Mechanisms of ER Stress-Mediated Mitochondrial Membrane Permeabilization. Int. J. Cell Biol., 2010, 2010, 170215.
44. Wang, X.; Olberding, K. E.; White, C.; Li, C. Bcl-2 proteins regulate ER membrane permeability to luminal proteins during ER stress-induced apoptosis. Cell Death Differ., 2010, 18(1),38-47.
45. Rasheva, V. I.; Domingos, P. M. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis, 2009, 14(8), 996-1007.
46. Kim, I.; Xu, W.; Reed, J. C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov., 2008, 7(12), 1013-1030.
47. Mori, K. Signalling pathways in the unfolded protein response: development from yeast to mammals. J. Biochem., 2009, 146(6), 743-750.
48. Kersse, K.; Vanden Berghe, T.; Lamkanfi, M.; Vandenabeele, P. A phylogenetic and functional overview of inflammatory caspases and caspase-1-related CARD-only proteins. Biochem. Soc. Trans, 2007, 35(Pt 6), 1508-1511.
49. Momoi, T. Caspases involved in ER stress-mediated cell death. J. Chem. Neuroanat, 2004, 28(1-2), 101-105.
50. Szegezdi, E.; Fitzgerald, U.; Samali, A. Caspase-12 and ER-stressmediated apoptosis: the story so far. Ann. N Y. Acad. Sci., 2003, 1010, 186-194.
51. Rodriguez-Gonzalez, A.; Lin, T.; Ikeda, A. K.; Simms-Waldrip, T.; Fu, C.; Sakamoto, K. M. Role of the aggresome pathway in cancer: targeting histone deacetylase 6-dependent protein degradation. Cancer Res., 2008, 68(8), 2557-2560.
52. Nawrocki, S. T.; Carew, J. S.; Pino, M. S.; Highshaw, R. A.; Andtbacka, R. H.; Dunner, K., Jr.; Pal, A.; Bornmann, W. G.; Chiao, P. J.; Huang, P.; Xiong, H.; Abbruzzese, J. L.; McConkey, D. J. Aggresome disruption: a novel strategy to enhance bortezomib-induced apoptosis in pancreatic cancer cells. Cancer Res., 2006, 66(7), 3773-3781.
53. Sorokin, A. V.; Kim, E. R.; Ovchinnikov, L. P. Proteasome system of protein degradation and processing. Biochemistry (Mosc), 2009, 74(13), 1411-1442.
54. Pratt, W. B.; Morishima, Y.; Peng, H. M.; Osawa, Y. Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Exp. Biol. Med., (Maywood), 2010, 235(3), 278-289.
55. Garrido, C.; Brunet, M.; Didelot, C.; Zermati, Y.; Schmitt, E.; Kroemer, G. Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle, 2006, 5(22), 2592-2601.
56. Gahr, S.; Peter, G.; Wissniowski, T. T.; Hahn, E. G.; Herold, C.; Ocker, M. The histone-deacetylase inhibitor MS-275 and the CDKinhibitor CYC-202 promote anti-tumor effects in hepatoma cell lines. Oncol. Rep., 2008, 20(5), 1249-1256.
57. Gahr, S.; Ocker, M.; Ganslmayer, M.; Zopf, S.; Okamoto, K.; Hartl, A.; Leitner, S.; Hahn, E. G.; Herold, C. The combination of the histone-deacetylase inhibitor trichostatin A and gemcitabine induces inhibition of proliferation and increased apoptosis in pancreatic carcinoma cells. Int. J. Oncol., 2007, 31(3), 567-576.
58. Conti, C.; Leo, E.; Eichler, G. S.; Sordet, O.; Martin, M. M.; Fan, A.; Aladjem, M. I.; Pommier, Y. Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res., 2010, 70(11), 4470-4480.
59. Habold, C.; Poehlmann, A.; Bajbouj, K.; Hartig, R.; Korkmaz, K. S.; Roessner, A.; Schneider-Stock, R. Trichostatin A causes p53 to switch oxidative-damaged colorectal cancer cells from cell cycle arrest into apoptosis. J. Cell Mol. Med., 2008, 12(2), 607-621.
60. Schuchmann, M.; Schulze-Bergkamen, H.; Fleischer, B.; Schattenberg, J. M.; Siebler, J.; Weinmann, A.; Teufel, A.; Worns, M.; Fischer, T.; Strand, S.; Lohse, A. W.; Galle, P. R. 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., 2006, 15(1), 227-230.
61. Fulda, S. Modulation of TRAIL-induced apoptosis by HDAC inhibitors. Curr. Cancer Drug Targets, 2008, 8(2), 132-140.
62. Carlisi, D.; Lauricella, M.; D'Anneo, A.; Emanuele, S.; Angileri, L.; Di Fazio, P.; Santulli, A.; Vento, R.; Tesoriere, G. The histone deacetylase inhibitor suberoylanilide hydroxamic acid sensitises human hepatocellular carcinoma cells to TRAIL-induced apoptosis by TRAIL-DISC activation. Eur. J. Cancer, 2009, 45(13), 2425-2438.
63. Kauh, J.; Fan, S.; Xia, M.; Yue, P.; Yang, L.; Khuri, F. R.; Sun, S. Y. c-FLIP degradation mediates sensitization of pancreatic cancer cells to TRAIL-induced apoptosis by the histone deacetylase inhibitor LBH589. PLoS One, 2010, 5(4), e10376.
64. Pathil, A.; Armeanu, S.; Venturelli, S.; Mascagni, P.; Weiss, T. S.; Gregor, M.; Lauer, U. M.; Bitzer, M. HDAC inhibitor treatment of hepatoma cells induces both TRAIL-independent apoptosis and restoration of sensitivity to TRAIL. Hepatology, 2006, 43(3), 425-434.
65. Shankar, S.; Davis, R.; Singh, K. P.; Kurzrock, R.; Ross, D. D.; Srivastava, R. K. Suberoylanilide hydroxamic acid (Zolinza/vorinostat) sensitizes TRAIL-resistant breast cancer cells orthotopically implanted in BALB/c nude mice. Mol. Cancer Ther., 2009, 8(6), 1596-1605.
66. Sung, E. S.; Kim, A.; Park, J. S.; Chung, J.; Kwon, M. H.; Kim, Y. S. Histone deacetylase inhibitors synergistically potentiate death receptor 4-mediated apoptotic cell death of human T-cell acute lymphoblastic leukemia cells. Apoptosis, 2010, 15(10),1256-1269.
67. Vigushin, D. M.; Coombes, R. C. Targeted histone deacetylase inhibition for cancer therapy. Curr. Cancer Drug Targets, 2004, 4(2), 205-218.
68. Ellis, L.; Bots, M.; Lindemann, R. K.; Bolden, J. E.; Newbold, A.; Cluse, L. A.; Scott, C. L.; Strasser, A.; Atadja, P.; Lowe, S. W.; Johnstone, R. W. The histone deacetylase inhibitors LAQ824 and LBH589 do not require death receptor signaling or a functional apoptosome to mediate tumor cell death or therapeutic efficacy. Blood, 2009, 114(2), 380-393.
69. Suzuki, M.; Endo, M.; Shinohara, F.; Echigo, S.; Rikiishi, H. Enhancement of cisplatin cytotoxicity by SAHA involves endoplasmic reticulum stress-mediated apoptosis in oral squamous cell carcinoma cells. Cancer Chemother. Pharmacol., 2009, 64(6), 1115-1122.
70. 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, E. G.; Ocker, M. The pan-deacetylase inhibitor panobinostat inhibits growth of hepatocellular carcinoma models by alternative pathways of apoptosis. Cell Oncol., 2010, 32(4), 285-300.
71. Di Sano, F.; Fazi, B.; Tufi, R.; Nardacci, R.; Piacentini, M. Reticulon-1C acts as a molecular switch between endoplasmic reticulum stress and genotoxic cell death pathway in human neuroblastoma cells. J. Neurochem., 2007, 102(2), 345-353.
72. Kahali, S.; Sarcar, B.; Fang, B.; Williams, E. S.; Koomen, J. M.; Tofilon, P. J.; Chinnaiyan, P. Activation of the unfolded protein response contributes toward the antitumor activity of vorinostat. Neoplasia, 2010, 12(1), 80-86.
73. Virrey, J. J.; Dong, D.; Stiles, C.; Patterson, J. B.; Pen, L.; Ni, M.; Schonthal, A. H.; Chen, T. C.; Hofman, F. M.; Lee, A. S. Stress chaperone GRP78/BiP confers chemoresistance to tumorassociated endothelial cells. Mol. Cancer Res., 2008, 6(8), 1268-1275.
74. Baumeister, P.; Dong, D.; Fu, Y.; Lee, A. S. Transcriptional induction of GRP78/BiP by histone deacetylase inhibitors and resistance to histone deacetylase inhibitor-induced apoptosis. Mol. Cancer Ther., 2009, 8(5),1086-1094
75. Scott, D. W.; Longpre, J. M.; Loo, G. Upregulation of GADD153 by butyrate: involvement of MAPK. DNA Cell Biol., 2008, 27(11), 607-614.