Suberoyl bis-hydroxamic acid activates Notch1 signaling and induces apoptosis in anaplastic thyroid carcinoma through p53

Li,Jiansen; Zheng,Xiangqian; Gao,Ming; Zhao,Jingzhu; Li,Yigong; Meng,Xiangrui; Qian,Biyun; Li,Jiafeng

doi:10.3892/or.2016.5281

Suberoyl bis-hydroxamic acid activates Notch1 signaling and induces apoptosis in anaplastic thyroid carcinoma through p53

Authors:
- Jiansen Li
- Xiangqian Zheng
- Ming Gao
- Jingzhu Zhao
- Yigong Li
- Xiangrui Meng
- Biyun Qian
- Jiafeng Li
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Affiliations: Department of Anesthesiology, Tianjin Medical University Cancer Institute and Hospital, Key Laboratory of Cancer Prevention and Therapy, Tianjin National Clinical Research Center for Cancer, Tianjin 300060, P.R. China, Department of Thyroid and Neck Tumor, Tianjin Medical University Cancer Institute and Hospital, Key Laboratory of Cancer Prevention and Therapy, Tianjin National Clinical Research Center for Cancer, Tianjin 300060, P.R. China, Department of Lymphoma, Tianjin Medical University Cancer Institute and Hospital, Key Laboratory of Cancer Prevention and Therapy, Tianjin National Clinical Research Center for Cancer, Tianjin 300060, P.R. China, Department of Epidemiology, School of Public Health, Shanghai Jiao Tong University, Shanghai 200030, P.R. China
Published online on: November 29, 2016 https://doi.org/10.3892/or.2016.5281
Pages: 458-464

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Abstract

Anaplastic thyroid cancer (ATC), usually derived from well-differentiated thyroid cancers is one of the most lethal human endocrine malignancies. In the present study, we report that in human ATC tumor tissue samples exist undetectable Notch1 and the active Notch1 intracellular domain could not be detected in ATC-CAL-62 cells. Interesting, suberoyl bis-hydroxamic acid (SBHA) administration could induce Notch1 intracellular domain levels in a dose-dependent manner, coupled with the increase of p53 and p21. Furthermore, ectopic expression of Notch1 or deletion of p53 with small-interfering RNA was able to abolish the effects of SBHA to elevation of Notch1 and p53 in ATC cells. As a result, SBHA treatment efficiently induced ATC cell apoptosis. These results indicate that SBHA may play antitumor functions via regulating Notch1/p53 signals, and highlight that SBHA could have clinical potential to benefit the therapy of ATC patients.

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1	Davies L and Welch HG: Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA. 295:2164–2167. 2006. View Article : Google Scholar : PubMed/NCBI
2	Nilubol N and Kebebew E: Should small papillary thyroid cancer be observed? A population-based study. Cancer. 121:1017–1024. 2014. View Article : Google Scholar : PubMed/NCBI
3	Smallridge RC, Ain KB, Asa SL, Bible KC, Brierley JD, Burman KD, Kebebew E, Lee NY, Nikiforov YE and Rosenthal MS: American Thyroid Association Anaplastic Thyroid Cancer Guidelines Taskforce: American Thyroid Association guidelines for management of patients with anaplastic thyroid cancer. Thyroid. 22:1104–1139. 2012. View Article : Google Scholar : PubMed/NCBI
4	Kebebew E, Greenspan FS, Clark OH, Woeber KA and McMillan A: Anaplastic thyroid carcinoma. Treatment outcome and prognostic factors. Cancer. 103:1330–1335. 2005.
5	McIver B, Hay ID, Giuffrida DF, Dvorak CE, Grant CS, Thompson GB, van Heerden JA and Goellner JR: Anaplastic thyroid carcinoma: a 50-year experience at a single institution. Surgery. 130:1028–1034. 2001. View Article : Google Scholar : PubMed/NCBI
6	Sugitani I, Miyauchi A, Sugino K, Okamoto T, Yoshida A and Suzuki S: Prognostic factors and treatment outcomes for anaplastic thyroid carcinoma: ATC Research Consortium of Japan cohort study of 677 patients. World J Surg. 36:1247–1254. 2012. View Article : Google Scholar : PubMed/NCBI
7	Neff RL, Farrar WB, Kloos RT and Burman KD: Anaplastic thyroid cancer. Endocrinol Metab Clin North Am. 37:525–538. 2008. View Article : Google Scholar : PubMed/NCBI
8	Chen J, Tward JD, Shrieve DC and Hitchcock YJ: Surgery andradiotherapy improves survival in patients with anaplastic thyroid carcinoma: Analysis of the surveillance, epidemiology, and end results 1983–2002. Am J Clin Oncol. 31:460–464. 2008. View Article : Google Scholar : PubMed/NCBI
9	ONeill JP and Shaha AR: Anaplastic thyroid cancer. Oral Oncol. 49:702–706. 2013. View Article : Google Scholar : PubMed/NCBI
10	Ranganathan P, Weaver KL and Capobianco AJ: Notch signalling in solid tumours: A little bit of everything but not all the time. Nat Rev Cancer. 11:338–351. 2011. View Article : Google Scholar : PubMed/NCBI
11	Takebe N, Harris PJ, Warren RQ and Ivy SP: Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol l8. 97–106. 2011. View Article : Google Scholar
12	Kopan R and Ilagan MX: The canonical Notch signaling pathway: unfolding the activation mechanism. Cell. 137:216–233. 2009. View Article : Google Scholar : PubMed/NCBI
13	Roy M, Pear WS and Aster JC: The multifaceted role of Notch in cancer. Curr Opin Genet Dev. 17:52–59. 2007. View Article : Google Scholar : PubMed/NCBI
14	Kunnimalaiyaan M and Chen H: Tumor suppressor role of Notch-1 signaling in neuroendocrine tumors. Oncologist. 12:535–542. 2007. View Article : Google Scholar : PubMed/NCBI
15	Xiao X, Ning L and Chen H: Notch1 mediates growth suppression of papillary and follicular thyroid cancer cells by histone deacetylase inhibitors. Mol Cancer Ther. 8:350–356. 2009. View Article : Google Scholar : PubMed/NCBI
16	Ferretti E, Tosi E, Po A, Scipioni A, Morisi R, Espinola MS, Russo D, Durante C, Schlumberger M, Screpanti I, et al: Notch signaling is involved in expression of thyrocyte differentiation markers and is down-regulated in thyroid tumors. J Clin Endocrinol Metab. 93:4080–4087. 2008. View Article : Google Scholar : PubMed/NCBI
17	Oswald F, Kostezka U, Astrahantseff K, Bourteele S, Dillinger K, Zechner U, Ludwig L, Wilda M, Hameister H, Knöchel W, et al: SHARP is a novel component of the Notch/RBP-Jkappa signalling pathway. EMBO J. 21:5417–5426. 2002. View Article : Google Scholar : PubMed/NCBI
18	Federico M and Bagella L: Histone deacetylase inhibitors in the treatment of hematological malignancies and solid tumors. J Biomed Biotechnol. 2011:4756412011. View Article : Google Scholar : PubMed/NCBI
19	Meng J, Zhang HH, Zhou CX, Li C, Zhang F and Mei QB: The histone deacetylase inhibitor trichostatin A induces cell cycle arrest and apoptosis in colorectal cancer cells via p53-dependent and -independent pathways. Oncol Rep. 28:384–388. 2012.PubMed/NCBI
20	Phan T, Yu XM, Kunnimalaiyaan M and Chen H: Antiproliferative effect of chrysin on anaplastic thyroid cancer. J Surg Res. 170:84–88. 2011. View Article : Google Scholar : PubMed/NCBI
21	Sippel RS, Carpenter JE, Kunnimalaiyaan M, Lagerholm S and Chen H: Raf-1 activation suppresses neuroendocrine marker and hormone levels in human gastrointestinal carcinoid cells. Am J Physiol Gastrointest Liver Physiol. 285:G245–G254. 2003. View Article : Google Scholar : PubMed/NCBI
22	Kunnimalaiyaan M, Vaccaro AM, Ndiaye MA and Chen H: Overexpression of the NOTCH1 intracellular domain inhibits cell proliferation and alters the neuroendocrine phenotype of medullary thyroid cancer cells. J Biol Chem. 281:39819–39830. 2006. View Article : Google Scholar : PubMed/NCBI
23	Kao HY, Ordentlich P, Koyano-Nakagawa N, Tang Z, Downes M, Kintner CR, Evans RM and Kadesch T: A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev. 12:2269–2277. 1998. View Article : Google Scholar : PubMed/NCBI
24	Platta CS, Greenblatt DY, Kunnimalaiyaan M and Chen H: Valproic acid induces Notch1 signaling in small cell lung cancer cells. J Surg Res. 148:31–37. 2008. View Article : Google Scholar : PubMed/NCBI
25	Adler JT, Hottinger DG, Kunnimalaiyaan M and Chen H: Histone deacetylase inhibitors upregulate Notch-1 and inhibit growth in pheochromocytoma cells. Surgery. 144:956–961. 2008. View Article : Google Scholar : PubMed/NCBI
26	Ning L, Greenblatt DY, Kunnimalaiyaan M and Chen H: Suberoyl bis-hydroxamic acid activates Notch-1 signaling and induces apoptosis in medullary thyroid carcinoma cells. Oncologist. 13:98–104. 2008. View Article : Google Scholar : PubMed/NCBI
27	Greenblatt DY, Cayo MA, Adler JT, Ning L, Haymart MR, Kunnimalaiyaan M and Chen H: Valproic acid activates Notch1 signaling and induces apoptosis in medullary thyroid cancer cells. Ann Surg. 247:1036–1040. 2008. View Article : Google Scholar : PubMed/NCBI
28	Ebrahimi M and Shamabadi N: Endocrine disrupting chemicals in pesticides and herbicide in Fars Province, Iran. Pak J Biol Sci. 10:3175–3179. 2007. View Article : Google Scholar : PubMed/NCBI
29	Stockhausen MT, Sjölund J, Manetopoulos C and Axelson H: Effects of the histone deacetylase inhibitor valproic acid on Notch signalling in human neuroblastoma cells. Br J Cancer. 92:751–759. 2005. View Article : Google Scholar : PubMed/NCBI
30	Kim SB, Chae GW, Lee J, Park J, Tak H, Chung JH, Park TG, Ahn JK and Joe CO: Activated Notch1 interacts with p53 to inhibit its phosphorylation and transactivation. Cell Death Differ. 14:982–991. 2007.PubMed/NCBI
31	Rooman I, De Medts N, Baeyens L, Lardon J, De Breuck S, Heimberg H and Bouwens L: Expression of the Notch signalingpathway and effect on exocrine cell proliferation in adult rat pancreas. Am J Pathol. 169:1206–1214. 2006. View Article : Google Scholar : PubMed/NCBI
32	Kolev V, Kacer D, Trifonova R, Small D, Duarte M, Soldi R, Graziani I, Sideleva O, Larman B, Maciag T, et al: The intracellular domain of Notch ligand Delta1 induces cell growth arrest. FEBS Lett. 579:5798–5802. 2005. View Article : Google Scholar : PubMed/NCBI
33	Devine T and Dai MS: Targeting the ubiquitin-mediated proteasome degradation of p53 for cancer therapy. Curr Pharm Des. 19:3248–3262. 2013. View Article : Google Scholar : PubMed/NCBI
34	Shan X, Fu YS, Aziz F, Wang XQ, Yan Q and Liu JW: Ginsenoside Rg3 inhibits melanoma cell proliferation through down-regulation of histone deacetylase 3 (HDAC3) and increase of p53 acetylation. PLoS One. 9:e1154012014. View Article : Google Scholar : PubMed/NCBI
35	Qi R, An H, Yu Y, Zhang M, Liu S, Xu H, Guo Z, Cheng T and Cao X: Notch1 signaling inhibits growth of human hepatocellular carcinoma through induction of cell cycle arrest and apoptosis. Cancer Res. 63:8323–8329. 2003.PubMed/NCBI
36	Talora C, Cialfi S, Segatto O, Morrone S, Kim Choi J, Frati L, Dotto G Paolo, Gulino A and Screpanti I: Constitutively active Notch1 induces growth arrest of HPV-positive cervical cancer cells via separate signaling pathways. Exp Cell Res. 305:343–354. 2005. View Article : Google Scholar : PubMed/NCBI
37	Yang X, Klein R, Tian X, Cheng HT, Kopan R and Shen J: Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. Dev Biol. 269:81–94. 2004. View Article : Google Scholar : PubMed/NCBI
38	Oswald F, Täuber B, Dobner T, Bourteele S, Kostezka U, Adler G, Liptay S and Schmid RM: p300 acts as a transcriptional coactivator for mammalian Notch-1. Mol Cell Biol. 21:7761–7774. 2001. View Article : Google Scholar : PubMed/NCBI
39	Roperch JP, Alvaro V, Prieur S, Tuynder M, Nemani M, Lethrosne F, Piouffre L, Gendron MC, Israeli D, Dausset J, et al: Inhibition of presenilin 1 expression is promoted by p53 and p21WAF-1 and results in apoptosis and tumor suppression. Nat Med. 4:835–838. 1998. View Article : Google Scholar : PubMed/NCBI
40	Sasaki Y, Ishida S, Morimoto I, Yamashita T, Kojima T, Kihara C, Tanaka T, Imai K, Nakamura Y and Tokino T: The p53 family member genes are involved in the Notch signal pathway. J Biol Chem. 277:719–724. 2002. View Article : Google Scholar : PubMed/NCBI
41	Nair P, Somasundaram K and Krishna S: Activated Notch1 inhibits p53-induced apoptosis and sustains transformation by human papillomavirus type 16 E6 and E7 oncogenes through a PI3K-PKB/Akt-dependent pathway. J Virol. 77:7106–7112. 2003. View Article : Google Scholar : PubMed/NCBI
42	Mungamuri SK, Yang X, Thor AD and Somasundaram K: Survival signaling by Notch1: mammalian target of rapamycin (mTOR)-dependent inhibition of p53. Cancer Res. 66:4715–4724. 2006. View Article : Google Scholar : PubMed/NCBI