Stimulation of the proliferation of human normal esophageal epithelial cells by fumonisin B1 and its mechanism

Wang,Shao‑Kang; Wang,Ting‑Ting; Huang,Gui‑Ling; Shi,Ruo‑Fu; Yang,Li‑Gang; Sun,Gui‑Ju

doi:10.3892/etm.2013.1364

Stimulation of the proliferation of human normal esophageal epithelial cells by fumonisin B1 and its mechanism

Authors:
- Shao‑Kang Wang
- Ting‑Ting Wang
- Gui‑Ling Huang
- Ruo‑Fu Shi
- Li‑Gang Yang
- Gui‑Ju Sun
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Affiliations: Key Laboratory of Environmental Medicine and Engineering, Ministry of Education, School of Public Health, Southeast University, Nanjing, Jiangsu 210009, P.R. China
Published online on: October 25, 2013 https://doi.org/10.3892/etm.2013.1364
Pages: 55-60

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Abstract

Previous epidemiological studies have demonstrated a correlation between fumonisin B1 (FB1) and human esophageal cancer in China, Iran and South Africa. The purpose of this study was to investigate the effects of FB1 on the proliferation, cell‑cycle and apoptosis of normal human esophageal epithelial cells (HEECs) and to explore the molecular mechanisms of these effects. The proliferation of HEECs treated with FB1 was assessed using a colorimetric assay, while analyses of the cell cycle and apoptosis were performed using flow cytometry and the measurement of the protein expressions of genes associated with the cell cycle was conducted using western blotting. The results showed that FB1 stimulated the proliferation of HEECs, decreased the percentage of cells in the G0/G1 phase and reduced apoptosis. The western blotting results showed that FB1 significantly increased the protein expression of cyclin D1 and significantly decreased the protein expression of cyclin E, p21 and p27. The results indicated that FB1 stimulated the proliferation of HEECs by affecting the cell cycle and apoptosis. This mechanism was associated with changes in cyclin D1, cyclin E, p21 and p27 expression.

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1	Theumer MG, Clop EM, Rubinstein HR and Perillo MA: The lipid-mediated hypothesis of fumonisin B1 toxicodynamics tested in model membranes. Colloids Surf B Biointerfaces. 64:22–33. 2008. View Article : Google Scholar : PubMed/NCBI
2	Stockmann-Juvala H and Savolainen K: A review of the toxic effects and mechanisms of action of fumonisin B1. Hum Exp Toxicol. 27:799–809. 2008. View Article : Google Scholar : PubMed/NCBI
3	Cano-Sancho G, Ramos AJ, Marin S and Sanchis V: Occurrence of fumonisins in Catalonia (Spain) and an exposure assessment of specific population groups. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 29:799–808. 2012. View Article : Google Scholar : PubMed/NCBI
4	van der Westhuizen L, Shephard GS, Rheeder JP and Burger HM: Individual fumonisin exposure and sphingoid base levels in rural populations consuming maize in South Africa. Food Chem Toxicol. 48:1698–1703. 2010.PubMed/NCBI
5	Alizadeh AM, Rohandel G, Roudbarmohammadi S, et al: Fumonisin B1 contamination of cereals and risk of esophageal cancer in a high risk area in northeastern Iran. Asian Pac J Cancer Prev. 13:2625–2628. 2012. View Article : Google Scholar : PubMed/NCBI
6	Sun G, Wang S, Hu X, et al: Fumonisin B1 contamination of home-grown corn in high-risk areas for esophageal and liver cancer in China. Food Addit Contam. 24:181–185. 2007. View Article : Google Scholar : PubMed/NCBI
7	Schwerdt G, Königs M, Holzinger H, Humpf HU and Gekle M: Effects of the mycotoxin fumonisin B(1) on cell death in human kidney cells and human lung fibroblasts in primary culture. J Appl Toxicol. 29:174–182. 2009. View Article : Google Scholar : PubMed/NCBI
8	Galvano F, Russo A, Cardile V, Galvano G, Vanella A and Renis M: DNA damage in human fibroblasts exposed to fumonisin B(1). Food Chem Toxicol. 40:25–31. 2002. View Article : Google Scholar : PubMed/NCBI
9	Seefelder W, Humpf HU, Schwerdt G, Freudinger R and Gekle M: Induction of apoptosis in cultured human proximal tubule cells by fumonisins and fumonisin metabolites. Toxicol Appl Pharmacol. 192:146–153. 2003. View Article : Google Scholar : PubMed/NCBI
10	Kouadio JH, Mobio TA, Baudrimont I, Moukha S, Dano SD and Creppy EE: Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology. 213:56–65. 2005. View Article : Google Scholar : PubMed/NCBI
11	Bondy GS, Barker MG, Lombaert GA, et al: A comparison of clinical, histopathological and cell-cycle markers in rats receiving the fungal toxins fumonisin B1 or fumonisin B2 by intraperitoneal injection. Food Chem Toxicol. 38:873–886. 2000. View Article : Google Scholar : PubMed/NCBI
12	Wang SK, Liu S, Yang LG, et al: Effect of fumonisin B1 on the cell cycle of normal human liver cells. Mol Med Rep. 7:1970–1976. 2013.PubMed/NCBI
13	Czerednik A, Busscher M, Bielen BA, Wolters-Arts M, de Maagd RA and Angenent GC: Regulation of tomato fruit pericarp development by an interplay between CDKB and CDKA1 cell cycle genes. J Exp Bot. 63:2605–2617. 2012. View Article : Google Scholar : PubMed/NCBI
14	Yamamoto S, Kohsaka S and Nakajima K: Role of cell cycle-associated proteins in microglial proliferation in the axotomized rat facial nucleus. Glia. 60:570–581. 2012. View Article : Google Scholar : PubMed/NCBI
15	Moreira PR, Guimarães MM, Guimarães AL, et al: Methylation of P16, P21, P27, RB1 and P53 genes in odontogenic keratocysts. J Oral Pathol Med. 38:99–103. 2009. View Article : Google Scholar : PubMed/NCBI
16	de Andrade BA, León JE, Carlos R, Delgado-Azañero W, Mosqueda-Taylor A and de Almeida OP: Immunohistochemical expression of p16, p21, p27 and cyclin D1 in oral nevi and melanoma. Head Neck Pathol. 6:297–304. 2012.PubMed/NCBI
17	Myburg RB, Dutton MF and Chuturgoon AA: Cytotoxicity of fumonisin B1, diethylnitrosamine, and catechol on the SNO esophageal cancer cell line. Environ Health Perspect. 110:813–815. 2002. View Article : Google Scholar : PubMed/NCBI
18	Wang H, Wei H, Ma J and Luo X: The fumonisin B1 content in corn from North China, a high-risk area of esophageal cancer. J Environ Pathol Toxicol Oncol. 19:139–141. 2000.PubMed/NCBI
19	Severino L, Russo R, Luongo D, De Luna R, Ciarcia R and Rossi M: Immune effects of four Fusarium-toxins (FB1, ZEA, NIV, DON) on the proliferation of Jurkat cells and porcine lymphocytes: in vitro study. Vet Res Commun. 32(Suppl 1): S311–S313. 2008. View Article : Google Scholar : PubMed/NCBI
20	Taranu I, Marina DE, Burlacu R, Pinton P, Damian V and Oswald IP: Comparative aspects of in vitro proliferation of human and porcine lymphocytes exposed to mycotoxins. Arch Anim Nutr. 64:383–393. 2010. View Article : Google Scholar : PubMed/NCBI
21	Gelderblom WC, Galendo D, Abel S, Swanevelder S, Marasas WF and Wild CP: Cancer initiation by fumonisin B(1) in rat liver - role of cell proliferation. Cancer Lett. 169:127–137. 2001. View Article : Google Scholar : PubMed/NCBI
22	McKean C, Tang L, Tang M, et al: Comparative acute and combinative toxicity of aflatoxin B1 and fumonisin B1 in animals and human cells. Food Chem Toxicol. 44:868–876. 2006. View Article : Google Scholar : PubMed/NCBI
23	Marin DE, Gouze ME, Taranu I and Oswald IP: Fumonisin B1 alters cell cycle progression and interleukin-2 synthesis in swine peripheral blood mononuclear cells. Mol Nutr Food Res. 51:1406–1412. 2007. View Article : Google Scholar : PubMed/NCBI
24	Fornelli F, Minervini F and Mulè G: Cytotoxicity induced by nivalenol, deoxynivalenol, and fumonisin B1 in the SF-9 insect cell line. In Vitro Cell Dev Biol Anim. 40:166–171. 2004. View Article : Google Scholar : PubMed/NCBI
25	Seegers JC, Joubert AM, Panzer A, et al: Fumonisin B1 influenced the effects of arachidonic acid, prostaglandins E2 and A2 on cell cycle progression, apoptosis induction, tyrosine- and CDC2-kinase activity in oesophageal cancer cells. Prostaglandins Leukot Essent Fatty Acids. 62:75–84. 2000. View Article : Google Scholar
26	Mobio TA, Anane R, Baudrimont I, et al: Epigenetic properties of fumonisin B(1): cell cycle arrest and DNA base modification in C6 glioma cells. Toxicol Appl Pharmacol. 164:91–96. 2000. View Article : Google Scholar : PubMed/NCBI
27	Ramljak D, Calvert RJ, Wiesenfeld PW, et al: A potential mechanism for fumonisin B(1)-mediated hepatocarcinogenesis: cyclin D1 stabilization associated with activation of Akt and inhibition of GSK-3beta activity. Carcinogenesis. 21:1537–1546. 2000. View Article : Google Scholar : PubMed/NCBI
28	Canavese M, Santo L and Raje N: Cyclin dependent kinases in cancer: Potential for therapeutic intervention. Cancer Biol Ther. 13:451–457. 2012. View Article : Google Scholar : PubMed/NCBI
29	Douville JM, Cheung DY, Herbert KL, Moffatt T and Wigle JT: Mechanisms of MEOX1 and MEOX2 regulation of the cyclin dependent kinase inhibitors p21 and p16 in vascular endothelial cells. PLoS One. 6:e290992011. View Article : Google Scholar : PubMed/NCBI
30	Canepa ET, Scassa ME, Ceruti JM, et al: INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life. 59:419–426. 2007. View Article : Google Scholar : PubMed/NCBI
31	Ito Y, Yoshida H, Matsuzuka F, et al: Expression of the components of the Cip/Kip family in malignant lymphoma of the thyroid. Pathobiology. 71:164–170. 2004. View Article : Google Scholar : PubMed/NCBI
32	Sugimoto M, Martin N, Wilks DP, et al: Activation of cyclin D1-kinase in murine fibroblasts lacking both p21(Cip1) and p27(Kip1). Oncogene. 21:8067–8074. 2002. View Article : Google Scholar : PubMed/NCBI
33	Verlinden L, Verstuyf A, Convents R, Marcelis S, Van Camp M and Bouillon R: Action of 1,25(OH)₂D3 on the cell cycle genes, cyclin D1, p21 and p27 in MCF-7 cells. Mol Cell Endocrinol. 142:57–65. 1998.
34	Hirai T, Kuwahara M, Yoshida K, Osaki A and Toge T: The prognostic significance of p53, p21 (Waf1/Cip1), and cyclin D1 protein expression in esophageal cancer patients. Anticancer Res. 19:4587–4591. 1999.PubMed/NCBI
35	Faria MH, Patrocinio RM, Moraes Filho MO and Rabenhorst SH: Immunoexpression of tumor suppressor genes p53, p21 WAF1/CIP1 and p27 KIP1 in human astrocystic tumors. Arq Neuropsiquiatr. 65:1114–1122. 2007. View Article : Google Scholar : PubMed/NCBI
36	Huang XP, Rong TH, Lin P, et al: Cyclin D1 overexpression in esophageal cancer from southern China and its clinical significance. Cancer Lett. 231:94–101. 2006. View Article : Google Scholar : PubMed/NCBI
37	Anayama T, Furihata M, Takeuchi T, et al: Insufficient effect of p27(KIP1) to inhibit cyclin D1 in human esophageal cancer in vitro. Int J Oncol. 18:151–155. 2001.PubMed/NCBI