Impact of histone deacetylase 1 and metastasis‑associated gene 1 expression in esophageal carcinogenesis

Miyashita,Tomoharu; Tajima,Hidehiro; Munemoto,Masayoshi; Shah,Furhawn  A.; Harmon,John  W.; Watanabe,Toshifumi; Shoji,Masatoshi; Okamoto,Koichi; Nakanuma,Shinichi; Sakai,Seisho; Kinoshita,Jun; Makino,Isamu; Nakamura,Keishi; Hayashi,Hironori; Oyama,Katsunobu; Inokuchi,Masafumi; Nakagawara,Hisatoshi; Takamura,Hiroyuki; Ninomiya,Itasu; Kitagawa,Hirohisa; Fushida,Sachio; Mukaisho,Kenichi; Fujimura,Takashi; Ohta,Tetsuo

doi:10.3892/ol.2014.2176

Impact of histone deacetylase 1 and metastasis‑associated gene 1 expression in esophageal carcinogenesis

Authors:
- Tomoharu Miyashita
- Hidehiro Tajima
- Masayoshi Munemoto
- Furhawn A. Shah
- John W. Harmon
- Toshifumi Watanabe
- Masatoshi Shoji
- Koichi Okamoto
- Shinichi Nakanuma
- Seisho Sakai
- Jun Kinoshita
- Isamu Makino
- Keishi Nakamura
- Hironori Hayashi
- Katsunobu Oyama
- Masafumi Inokuchi
- Hisatoshi Nakagawara
- Hiroyuki Takamura
- Itasu Ninomiya
- Hirohisa Kitagawa
- Sachio Fushida
- Kenichi Mukaisho
- Takashi Fujimura
- Tetsuo Ohta
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Affiliations: Department of Gastroenterological Surgery, Kanazawa University Hospital, Kanazawa, Ishikawa 920‑8641, Japan, Department of Surgery, Johns Hopkins Bayview Medical Center, Johns Hopkins University School of Medicine, Baltimore, MD 21224, USA, Department of Pathology, Shiga University of Medical Science, Otsu, Shiga 520‑2192, Japan
Published online on: May 26, 2014 https://doi.org/10.3892/ol.2014.2176
Pages: 758-764

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Abstract

Animal models are important for the development of novel therapies for esophageal cancer. Histone deacetylase 1 (HDAC1)/metastasis‑associated gene (MTA1) complexes inhibit p53 acetylation and thus, inhibit p53‑induced apoptosis. The aim of the present study was to evaluate HDAC1 and MTA1 expression in esophageal carcinogenesis in rats. The rats underwent a total gastrectomy followed by esophagojejunostomy to induce chronic duodenal content reflux esophagitis. The rats were sacrificed sequentially at 20, 30, 40 and 50 weeks post‑surgery and the esophagi were examined. Immunohistochemical analysis was conducted to assess the expression and localization of HDAC1 and MTA1. At 20 weeks post‑surgery, squamous proliferative hyperplasia and Barrett's metaplasia (BM) were observed. While, adenocarcinoma‑associated BM and squamous cell carcinoma were observed at 30‑50 weeks post‑surgery. The nuclear expression of HDAC1 and MTA1 was observed in all of the stages of squamous carcinogenesis and adenocarcinogenesis, although not in the normal esophageal epithelium. The expression of HDAC1 and MTA1 may be involved in duodenoesophageal reflux‑induced neoplastic transformation of the esophageal mucosa into cancer cells with squamous and adeno differentiation.

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1	Hongo M, Nagasaki Y and Shoji T: Epidemiology of esophageal cancer: Orient to occident. Effects of chronology, geography and ethnicity. J Gastroenterol Hepatol. 24:729–735. 2009.
2	Wheeler JB and Reed CE: Epidemiology of esophageal cancer. Surg Clin North Am. 92:1077–1087. 2012.
3	Bollschweiler E, Wolfgarten E, Gutschow C and Hölscher AH: Demographic variations in the rising incidence of esophageal adenocarcinoma in white males. Cancer. 92:549–555. 2001.
4	Reid BJ, Li X, Galipeau PC and Vaughan TL: Barrett’s oesophagus and oesophageal adenocarcinoma: time for a new synthesis. Nat Rev Cancer. 10:87–101. 2010.
5	Engel LS, Chow WH, Vaughan TL, et al: Population attributable risks of esophageal and gastric cancers. J Natl Cancer Inst. 95:1404–1413. 2003.
6	Lagergren J, Bergström R, Lindgren A and Nyrén O: Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 340:825–831. 1999.
7	Jankowski JA, Harrison RF, Perry I, Balkwill F and Tselepis C: Barrett’s metaplasia. Lancet. 356:2079–2085. 2000.
8	Miwa K, Segawa M, Takano Y, et al: Induction of oesophageal and forestomach carcinomas in rats by reflux of duodenal contents. Br J Cancer. 70:185–189. 1994.
9	Miwa K, Sahara H, Segawa M, et al: Reflux of duodenal or gastro-duodenal contents induces esophageal carcinoma in rats. Int J Cancer. 67:269–274. 1996.
10	Miyashita T, Ohta T, Fujimura T, et al: Duodenal juice stimulates oesophageal stem cells to induce Barrett’s oesophagus and oesophageal adenocarcinoma in rats. Oncol Rep. 15:1469–1475. 2006.
11	Miyashita T, Miwa K, Fujimura T, et al: The severity of duodeno-esophageal reflux influences the development of different histological types of esophageal cancer in a rat model. Int J Cancer. 132:1496–1504. 2013.
12	Bonde P, Sui G, Dhara S, et al: Cytogenetic characterization and gene expression profiling in the rat reflux-induced esophageal tumor model. J Thorac Cardiovasc Surg. 133:763–769. 2007.
13	Nawa A, Nishimori K, Lin P, et al: Tumor metastasis-associated human MTA1 gene: its deduced protein sequence, localization, and association with breast cancer cell proliferation using antisense phosphorothioate oligonucleotides. J Cell Biochem. 79:202–212. 2000.
14	Toh Y, Ohga T, Endo K, et al: Expression of the metastasis-associated MTA1 protein and its relationship to deacetylation of the histone H4 in esophageal squamous cell carcinomas. Int J Cancer. 110:362–367. 2004.
15	Toh Y, Pencil SD and Nicolson GL: Analysis of the complete sequence of the novel metastasis-associated candidate gene, mta1, differentially expressed in mammary adenocarcinoma and breast cancer cell lines. Gene. 159:97–104. 1995.
16	Iguchi H, Imura G, Toh Y and Ogata Y: Expression of MTA1, a metastasis-associated gene with histone deacetylase activity in pancreatic cancer. Int J Oncol. 16:1211–1214. 2000.
17	Higashijima J, Kurita N, Miyatani T, et al: Expression of histone deacetylase 1 and metastasis-associated protein 1 as prognostic factors in colon cancer. Oncol Rep. 26:343–348. 2011.
18	Nicolson GL, Nawa A, Toh Y, Taniguchi S, Nishimori K and Moustafa A: Tumor metastasis-associated human MTA1 gene and its MTA1 protein product: role in epithelial cancer cell invasion, proliferation and nuclear regulation. Clin Exp Metastasis. 20:19–24. 2003.
19	Moon WS, Chang K and Tarnawski AS: Overexpression of metastatic tumor antigen 1 in hepatocellular carcinoma: Relationship to vascular invasion and estrogen receptor-alpha. Hum Pathol. 35:424–429. 2004.
20	Kai L, Samuel SK and Levenson AS: Resveratrol enhances p53 acetylation and apoptosis in prostate cancer by inhibiting MTA1/NuRD complex. Int J Cancer. 126:1538–1548. 2010.
21	Toh Y, Yamamoto M, Endo K, et al: Histone H4 acetylation and histone deacetylase 1 expression in esophageal squamous cell carcinoma. Oncol Rep. 10:333–338. 2003.
22	Sun WJ, Zhou X, Zheng JH, et al: Histone acetyltransferases and deacetylases: molecular and clinical implications to gastrointestinal carcinogenesis. Acta Biochim Biophys Sin (Shanghai). 44:80–91. 2012.
23	Toh Y and Nicolson G: MTA1 of the MTA (metastasis-associated) gene family and its encoded proteins: molecular and regulatory functions and role in human cancer progression. Atlas Genet Cytogenet Oncol Haematol. 15:303–315. 2011.
24	Moon HE, Cheon H and Lee MS: Metastasis-associated protein 1 inhibits p53-induced apoptosis. Oncol Rep. 18:1311–1314. 2007.
25	Abdel-Latif MM, Duggan S, Reynolds JV and Kelleher D: Inflammation and esophageal carcinogenesis. Curr Opin Pharmacol. 9:396–404. 2009.
26	Ramsey MR, He L, Forster N, Ory B and Ellisen LW: Physical association of HDAC1 and HDAC2 with p63 mediates transcriptional repression and tumor maintenance in squamous cell carcinoma. Cancer Res. 71:4373–4379. 2011.
27	Langer R, Mutze K, Becker K, et al: Expression of class I histone deacetylases (HDAC1 and HDAC2) in oesophageal adenocarcinomas: an immunohistochemical study. J Clin Pathol. 63:994–998. 2010.
28	Toh Y, Kuwano H, Mori M, Nicolson GL and Sugimachi K: Overexpression of metastasis-associated MTA1 mRNA in invasive oesophageal carcinomas. Br J Cancer. 79:1723–1726. 1999.
29	Tong JK, Hassig CA, Schnitzler GR, Kingston RE and Schreiber SL: Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature. 395:917–921. 1998.
30	Xue Y, Wong J, Moreno GT, Young MK, Côté J and Wang W: NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell. 2:851–861. 1998.
31	Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F and Wolffe AP: Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet. 23:62–66. 1999.
32	Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A and Reinberg D: Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev. 13:1924–1935. 1999.
33	Bowen NJ, Fujita N, Kajita M and Wade PA: Mi-2/NuRD: multiple complexes for many purposes. Biochim Biophys Acta. 1677:52–57. 2004.
34	Toh Y, Kuninaka S, Endo K, et al: Molecular analysis of a candidate metastasis-associated gene, MTA1: possible interaction with histone deacetylase 1. J Exp Clin Cancer Res. 19:105–111. 2000.
35	Kumar R, Wang RA and Bagheri-Yarmand R: Emerging roles of MTA family members in human cancers. Semin Oncol. 30(Suppl 16): S30–S37. 2003.
36	Manavathi B, Peng S, Rayala SK, et al: Repression of Six3 by a corepressor regulates rhodopsin expression. Proc Natl Acad Sci USA. 104:13128–13133. 2007.
37	Toh Y and Nicolson GL: The role of the MTA family and their encoded proteins in human cancers: molecular functions and clinical implications. Clin Exp Metastasis. 26:215–227. 2009.
38	Luo J, Su F, Chen D, Shiloh A and Gu W: Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature. 408:377–381. 2000.
39	Li DQ, Ohshiro K, Reddy SD, et al: E3 ubiquitin ligase COP1 regulates the stability and functions of MTA1. Proc Natl Acad Sci USA. 106:17493–17498. 2009.
40	Miyatani T, Kurita N, Mikami C, et al: Malignant potential of Barrett’s esophagus: special reference to HDAC-1 and MTA-1 expression. Hepatogastroenterology. 58:472–476. 2011.
41	Yoo YG, Na TY, Seo HW, et al: Hepatitis B virus X protein induces the expression of MTA1 and HDAC1, which enhances hypoxia signaling in hepatocellular carcinoma cells. Oncogene. 27:3405–3413. 2008.
42	Hofer MD, Kuefer R, Varambally S, et al: The role of metastasis-associated protein 1 in prostate cancer progression. Cancer Res. 64:825–829. 2004.
43	Taddei A, Roche D, Bickmore WA and Almouzni G: The effects of histone deacetylase inhibitors on heterochromatin: implications for anticancer therapy? EMBO Rep. 6:520–524. 2005.