Original Article
Copyright ©2014 Baishideng Publishing Group Inc. All rights reserved.
World J Clin Oncol. Dec 10, 2014; 5(5): 1068-1077
Published online Dec 10, 2014. doi: 10.5306/wjco.v5.i5.1068
MiR-210 expression reverses radioresistance of stem-like cells of oesophageal squamous cell carcinoma
Xin Chen, Jia Guo, Ru-Xing Xi, Yu-Wei Chang, Fei-Yang Pan, Xiao-Zhi Zhang
Xin Chen, Jia Guo, Ru-Xing Xi, Yu-Wei Chang, Xiao-Zhi Zhang, Radiation Department, First Affiliated Hospital of Medical School of Xi’an Jiaotong University, Xi’an 710061, Shaanxi Provence, China
Fei-Yang Pan, School of Medicine, Queen’s University, Kingston K7L 3N6, Ontario, Canada
Author contributions: Chen X performed the majority of the experiments and analysed the data as well as wrote the manuscript; Xi RX collected the human tissues and the patients’ data; Guo J and Chang YW were both involved in cell culture, transfection, PCR and WB; Pan FY and Zhang XZ designed the experiments and amended the manuscript.
Supported by National Natural Science Foundation of China, No. 30972962
Correspondence to: Xiao-Zhi Zhang, Professor, MD, PhD, Chief Physician and Doctoral Tutor, Radiation Department, First Affiliated Hospital of Medical School of Xi’an Jiaotong University, West Yanta St., Xi’an 710061, Shaanxi Provence, China. zhang9149@sina.com
Telephone: +86-29-85324068 Fax: +86-29-85324068
Received: March 17, 2014
Revised: June 3, 2014
Accepted: August 27, 2014
Published online: December 10, 2014
Processing time: 268 Days and 15.5 Hours
Abstract

AIM: To investigate the expression of miR-210 and the role it plays in the cell cycle to regulate radioresistance in oesophageal squamous cell carcinoma (ESCC).

METHODS: MiR-210 expression was evaluated in 37 pairs of ESCC tissues and matched para-tumorous normal oesophageal tissues from surgical patients who had not received neoadjuvant therapy, and in the cells of two novel radioresistant cell lines, TE-1R and Eca-109R, using quantitative reverse transcription-polymerase chain reaction (qRT-PCR). The transient up-regulation of miR-210 expression in TE-1R and Eca-109R cells was studied using liposomes and was confirmed using qRT-PCR. The rate of cell survival after a series of radio-treatment doses was evaluated using the clone formation assay. Flow cytometry was used to detect the changes to the cell cycle patterns due to radiation treatment. RT-PCR and Western blot were used to detect the expression of ataxia telangiectasia mutated (ATM) and DNA dependent protein kinase (DNA-PKcs) after irradiation, and the cell sphere formation assay was used to evaluate the proliferative ability of the cancer stem-like cells.

RESULTS: The level of miR-210 expression was significantly decreased, by 21.3% to 97.2%, with the average being 39.2% ± 16.1%, in the ESCC tissues of most patients (81.1%, 30 of 37 vs patients with high miR-210 expression, P < 0.05). A low level of expression of miR-210 was correlated with a poorly differentiated pathological type (P < 0.01) but was not correlated with the T-stage or lymph node infiltration (both P > 0.05). Early local recurrences (< 18 mo, n = 19) after radiotherapy were significantly related with low miR-210 expression (n = 13, P < 0.05). The level of miR-210 was decreased by approximately 73% (vs TE-1, 0.27 ± 0.10, P < 0.01) in the established radioresistant TE-IR cell line and by 52% (vs Eca-109, 0.48 ± 0.17, P < 0.05) in the corresponding Eca-109R line. Transient transfection with a miR-210 precursor increased the level of miR-210 expression, leading to a significant increase in cell survival after radiotherapy (P < 0.05). Twenty-four hours after radiation, the proportion of pmiR-210 cells in S phase was increased (vs control cells, 30.4% ± 0.4%, and vs untreated TE-1R cells, 23.3% ± 0.7%, P < 0.05 for both). The levels of DNA-PKcs (0.21 ± 0.07) and ATM (0.12 ± 0.03, P < 0.05) proteins were significantly lower in the PmiR-210 cells than in control cells, but no differences were found in the levels of the corresponding mRNAs in the two cell types (P > 0.05 for all). Exogenous miR-210 expression decreased the diameter of pmiR-210 cell spheres (vs control cells, 0.60 ± 0.14, P < 0.05).

CONCLUSION: MiR-210 expression is negatively correlated with the pathological type and the local survival rate after radiotherapy, and high expression of miR-210 may reverse the radioresistance of ESCC stem-like cells.

Keywords: MiR-210; Oesophageal squamous cell carcinoma; Radiation resistance; Cell cycle arrest; Stem-like cells

Core tip: A low level of miR-210 expression, which is common in oesophageal squamous cell carcinoma (ESCC) tissues, was found to be negatively correlated with the tumour pathological type and the prognosis in ESCC patients after radiotherapy, although the sample size was small. A relatively high level of in vitro miR-210 expression reversed the radioresistance of ESCC stem-like cells by decreasing the extent of ataxia telangiectasia mutated/DNA dependent protein kinase-dependent cell cycle arrest, failure of DNA double-strand break repair and stem cell proliferation.