Combination of the novel histone deacetylase inhibitor YCW1 and radiation induces autophagic cell death through the downregulation of BNIP3 in triple-negative breast cancer cells in vitro and in an orthotopic mouse model

Molecular Cancer

Volumn 15, Issue 1, 2016, Pages

  Chiu, Hui Wen ^a,b   Yeh, Ya Ling ^c   Wang, Yi Ching ^d   Huang, Wei Jan ^e   Ho, Sheng Yow ^f,g   Lin, Pinpin ^h   Wang, Ying Jan ^c,i,j  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^f CHI MEI MEDICAL CENTER   (Taiwan)

^g CHANG JUNG CHRISTIAN UNIVERSITY   (Taiwan)

^h NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

ⁱ ASIA UNIVERSITY   (Taiwan)

^j CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

more..

Author keywords

Autophagy; Histone deacetylase inhibitor; Radiation; Triple negative breast cancer

Indexed keywords

ANTINEOPLASTIC AGENT; OCTANEDIOIC ACID [3 [2 (5 METHOXY 1H INDOL 1 YL)ETHOXY]PHENYL]AMIDE N HYDROXYAMIDE; PROTEIN BNIP3; UNCLASSIFIED DRUG; 1,3 DIOXOLANE DERIVATIVE; BNIP3 PROTEIN, HUMAN; HISTONE DEACETYLASE INHIBITOR; MEMBRANE PROTEIN; ONCOPROTEIN; TRIAZOLE DERIVATIVE; YCZ-18;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER CELL LINE; CANCER RADIOTHERAPY; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; ENDOPLASMIC RETICULUM STRESS; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IONIZING RADIATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TRIPLE NEGATIVE BREAST CANCER; TUMOR VOLUME; ANIMAL; CELL PROLIFERATION; CELL SURVIVAL; CHEMORADIOTHERAPY; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; PROCEDURES; RADIATION RESPONSE; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

ANIMALS; AUTOPHAGY; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CHEMORADIOTHERAPY; DIOXOLES; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASE INHIBITORS; HUMANS; MEMBRANE PROTEINS; MICE; PROTO-ONCOGENE PROTEINS; TRIAZOLES; TRIPLE NEGATIVE BREAST NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84976884578     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-016-0531-5     Document Type: Article

References (51)

1. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011;121:2750-67.
2. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007;13:4429-34.
3. Viani GA, Manta GB, Fonseca EC, De Fendi LI, Afonso SL, Stefano EJ. Whole brain radiotherapy with radiosensitizer for brain metastases. J Exp Clin Cancer Res. 2009;28:1.
4. Chiu HW, Ho SY, Guo HR, Wang YJ. Combination treatment with arsenic trioxide and irradiation enhances autophagic effects in U118-MG cells through increased mitotic arrest and regulation of PI3K/Akt and ERK1/2 signaling pathways. Autophagy. 2009;5:472-83.
5. Chiu HW, Lin JH, Chen YA, Ho SY, Wang YJ. Combination treatment with arsenic trioxide and irradiation enhances cell-killing effects in human fibrosarcoma cells in vitro and in vivo through induction of both autophagy and apoptosis. Autophagy. 2010;6:353-65.
6. Chiu HW, Yeh YL, Wang YC, Huang WJ, Chen YA, Chiou YS, et al. Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, enhances radiosensitivity and suppresses lung metastasis in breast cancer in vitro and in vivo. PLoS One. 2013;8:e76340.
7. Dent P, Yacoub A, Fisher PB, Hagan MP, Grant S. MAPK pathways in radiation responses. Oncogene. 2003;22:5885-96.
8. Schuurbiers OC, Kaanders JH, van der Heijden HF, Dekhuijzen RP, Oyen WJ, Bussink J. The PI3-K/AKT-pathway and radiation resistance mechanisms in non-small cell lung cancer. J Thorac Oncol. 2009;4:761-7.
9. Li Y, Tennekoon GI, Birnbaum M, Marchionni MA, Rutkowski JL. Neuregulin signaling through a PI3K/Akt/Bad pathway in Schwann cell survival. Mol Cell Neurosci. 2001;17:761-7.
10. Wang TT, Phang JM. Effects of estrogen on apoptotic pathways in human breast cancer cell line MCF-7. Cancer Res. 1995;55:2487-9.
11. Hanna RA, Quinsay MN, Orogo AM, Giang K, Rikka S, Gustafsson AB. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem. 2012;287:19094-104.
12. Zhang S, Zhang Z, Sandhu G, Ma X, Yang X, Geiger JD, et al. Evidence of oxidative stress-induced BNIP3 expression in amyloid beta neurotoxicity. Brain Res. 2007;1138:221-30.
13. Burton TR, Gibson SB. The role of Bcl-2 family member BNIP3 in cell death and disease: NIPping at the heels of cell death. Cell Death Differ. 2009;16:515-23.
14. Burton TR, Henson ES, Baijal P, Eisenstat DD, Gibson SB. The pro-cell death Bcl-2 family member, BNIP3, is localized to the nucleus of human glial cells: Implications for glioblastoma multiforme tumor cell survival under hypoxia. Int J Cancer. 2006;118:1660-9.
15. Sowter HM, Ferguson M, Pym C, Watson P, Fox SB, Han C, et al. Expression of the cell death genes BNip3 and NIX in ductal carcinoma in situ of the breast; correlation of BNip3 levels with necrosis and grade. J Pathol. 2003;201:573-80.
16. Marks PA, Xu WS. Histone deacetylase inhibitors: Potential in cancer therapy. J Cell Biochem. 2009;107:600-8.
17. Marks PA. The clinical development of histone deacetylase inhibitors as targeted anticancer drugs. Expert Opin Investig Drugs. 2010;19:1049-66.
18. Pandolfi PP. Histone deacetylases and transcriptional therapy with their inhibitors. Cancer Chemother Pharmacol. 2001;48 Suppl 1:S17-9.
19. Wang J, Kim TH, Ahn MY, Lee J, Jung JH, Choi WS, et al. Sirtinol, a class III HDAC inhibitor, induces apoptotic and autophagic cell death in MCF-7 human breast cancer cells. Int J Oncol. 2012;41:1101-9.
20. Dokmanovic M, Clarke C, Marks PA. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res. 2007;5:981-9.
21. Huang WJ, Chen CC, Chao SW, Yu CC, Yang CY, Guh JH, et al. Synthesis and evaluation of aliphatic-chain hydroxamates capped with osthole derivatives as histone deacetylase inhibitors. Eur J Med Chem. 2011;46:4042-9.
22. Huang WJ, Tang YA, Chen MY, Wang YJ, Hu FH, Wang TW, et al. A histone deacetylase inhibitor YCW1 with antitumor and antimetastasis properties enhances cisplatin activity against non-small cell lung cancer in preclinical studies. Cancer Lett. 2014;346:84-93.
23. Duvic M, Talpur R, Ni X, Zhang C, Hazarika P, Kelly C, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood. 2007;109:31-9.
24. He L, Kim SO, Kwon O, Jeong SJ, Kim MS, Lee HG, et al. ATM blocks tunicamycin-induced endoplasmic reticulum stress. FEBS Lett. 2009;583:903-8.
25. 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.
26. Reimertz C, Kogel D, Rami A, Chittenden T, Prehn JH. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol. 2003;162:587-97.
27. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy. 2007;3:542-5.
28. Bursch W, Ellinger A, Gerner C, Frohwein U, Schulte-Hermann R. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci. 2000;926:1-12.
29. Shen HM, Codogno P. Autophagic cell death: Loch Ness monster or endangered species? Autophagy. 2011;7:457-65.
30. Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med. 2010;363:1938-48.
31. Tan J, Cang S, Ma Y, Petrillo RL, Liu D. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J Hematol Oncol. 2010;3:5.
32. 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 U S A. 2012;109:6561-5.
33. Rao R, Balusu R, Fiskus W, Mudunuru U, Venkannagari S, Chauhan L, et al. Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther. 2012;11:973-83.
34. Shao Y, Gao Z, Marks PA, Jiang X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci U S A. 2004;101:18030-5.
35. Lee YJ, Won AJ, Lee J, Jung JH, Yoon S, Lee BM, et al. Molecular mechanism of SAHA on regulation of autophagic cell death in tamoxifen-resistant MCF-7 breast cancer cells. Int J Med Sci. 2012;9:881-93.
36. Liu Y, Ye Y. Proteostasis regulation at the endoplasmic reticulum: a new perturbation site for targeted cancer therapy. Cell Res. 2011;21:867-83.
37. Sato A, Asano T, Isono M, Ito K, Asano T. Panobinostat synergizes with bortezomib to induce endoplasmic reticulum stress and ubiquitinated protein accumulation in renal cancer cells. BMC Urol. 2014;14:71.
38. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8:519-29.
39. Chiu HW, Fang WH, Chen YL, Wu MD, Yuan GF, Ho SY, et al. Monascuspiloin enhances the radiation sensitivity of human prostate cancer cells by stimulating endoplasmic reticulum stress and inducing autophagy. PLoS One. 2012;7:e40462.
40. Germano IM, Emdad L, Qadeer ZA, Binello E, Uzzaman M. Embryonic stem cell (ESC)-mediated transgene delivery induces growth suppression, apoptosis and radiosensitization, and overcomes temozolomide resistance in malignant gliomas. Cancer Gene Ther. 2010;17:664-74.
41. Benbrook DM, Long A. Integration of autophagy, proteasomal degradation, unfolded protein response and apoptosis. Exp Oncol. 2012;34:286-97.
42. Hetz CA. ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antioxid Redox Signal. 2007;9:2345-55.
43. Tomek M, Akiyama T, Dass CR. Role of Bcl-2 in tumour cell survival and implications for pharmacotherapy. J Pharm Pharmacol. 2012;64:1695-702.
44. Shi M, Wang HN, Xie ST, Luo Y, Sun CY, Chen XL, et al. Antimicrobial peptaibols, novel suppressors of tumor cells, targeted calcium-mediated apoptosis and autophagy in human hepatocellular carcinoma cells. Mol Cancer. 2010;9:26.
45. Zhang J, Ney PA. Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ. 2009;16:939-46.
46. Burton TR, Eisenstat DD, Gibson SB. BNIP3 (Bcl-2 19 kDa interacting protein) acts as transcriptional repressor of apoptosis-inducing factor expression preventing cell death in human malignant gliomas. J Neurosci. 2009;29:4189-99.
47. Sowter HM, Ratcliffe PJ, Watson P, Greenberg AH, Harris AL. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 2001;61:6669-73.
48. Park CW, Hong SM, Kim ES, Kwon JH, Kim KT, Nam HG, et al. BNIP3 is degraded by ULK1-dependent autophagy via MTORC1 and AMPK. Autophagy. 2013;9:345-60.
49. Chen JY, Tang YA, Huang SM, Juan HF, Wu LW, Sun YC, et al. A novel sialyltransferase inhibitor suppresses FAK/paxillin signaling and cancer angiogenesis and metastasis pathways. Cancer Res. 2011;71:473-83.
50. Chiu HW, Ho YS, Wang YJ. Arsenic trioxide induces autophagy and apoptosis in human glioma cells in vitro and in vivo through downregulation of survivin. J Mol Med (Berl). 2011;89:927-41.
51. Peng PL, Kuo WH, Tseng HC, Chou FP. Synergistic tumor-killing effect of radiation and berberine combined treatment in lung cancer: the contribution of autophagic cell death. Int J Radiat Oncol Biol Phys. 2008;70:529-42.