Basic Study
Copyright ©The Author(s) 2018. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Dec 7, 2018; 24(45): 5120-5130
Published online Dec 7, 2018. doi: 10.3748/wjg.v24.i45.5120
Glucocorticoid receptor regulates expression of microRNA-22 and downstream signaling pathway in apoptosis of pancreatic acinar cells
Qiang Fu, Chuan-Jiang Liu, Xu Zhang, Zhen-Sheng Zhai, Yu-Zhu Wang, Ming-Xing Hu, Xian-Ling Xu, Hong-Wei Zhang, Tao Qin
Qiang Fu, Chuan-Jiang Liu, Xu Zhang, Zhen-Sheng Zhai, Yu-Zhu Wang, Ming-Xing Hu, Xian-Ling Xu, Hong-Wei Zhang, Tao Qin, Department of Hepatobiliary and Pancreatic Surgery, People’s Hospital of Zhengzhou University (Henan Provincial People’s Hospital), School of Medicine, Zhengzhou University, Zhengzhou 450003, Henan Province, China
Author contributions: Fu Q and Zhang X performed the majority of experiments; Zhang HW and Qin T designed the research and provided financial support for this work; Liu CJ conducted the experimental analysis; Wang YZ provided vital reagents; Hu MX and Xu XL analyzed sequencing data and developed analysis tools; Fu Q and Qin T wrote the paper.
Supported by National Natural Science Foundation of China, No. 31671440.
Correspondence author to: Tao Qin, MD, PhD, Doctor, Professor, Department of Hepatobiliary and Pancreatic Surgery, People’s Hospital of Zhengzhou University (Henan Provincial People’s Hospital), School of Medicine, Zhengzhou University, No. 7, Weiwu Road, Zhengzhou 450003, Henan Province, China. m18937638396@163.com
Telephone: +86-371-65580368 Fax: +86-371-65580368
Received: September 5, 2018
Peer-review started: September 5, 2018
First decision: October 24, 2018
Revised: November 12, 2018
Accepted: November 13, 2018
Article in press: November 13, 2018
Published online: December 7, 2018
Processing time: 93 Days and 22.6 Hours
Abstract
AIM

To elucidate the underlying mechanism that microRNA-22 (miR-22) promotes the apoptosis of rat pancreatic acinar cells (AR42J) and the elements that regulate the expression of miR-22.

METHODS

One hundred nanomoles per liter of caerulein (Cae) was administrated to induce the apoptosis of AR42J cells and the apoptosis rate was detected by flow cytometry analysis. An amylase assay kit was used to measure the amylase expression level in the supernatant. Quantitative real-time PCR (qRT-PCR) was adopted to measure miR-22 expression. We used online tools to predict the potential transcription promoter of miR-22 and the binding sites, which was further identified by using luciferase reporter analysis, chromatin immunoprecipitation (ChIP) and ChIP-qPCR assays. Then, a mimic of miR-22, Nr3c1 plasmid encoding the glucocorticoid receptor (GR), and si-Nr3c1 were used to transfect AR42J cells, respectively. The mRNA expression of miR-22, Nr3c1, and Erb-b2 receptor tyrosine kinase 3 (ErbB3) was confirmed by qRT-PCR and the apoptosis rate of AR42J cells was detected by flow cytometry analysis. Western blot was used to detect the expression of ErbB3, GR, PI3k, PI3k-p85α, Akt, p-Akt, Bad, Bax, Bcl-xl, Bcl-2, and cleaved caspase3.

RESULTS

After inducing apoptosis of AR42J cells in vitro, the expression of miR-22 was significantly increased by 2.20 ± 0.26 and 4.19 ± 0.54 times, respectively, at 3 h and 6 h in comparison with the control group. As revealed by qRT-PCR assay, the expression of miR-22 was 78.25 ± 6.61 times higher in the miR-22 mimic group relative to the miRNA control group, accompanied with an obviously increased acinar cell apoptosis rate (32.53 ± 1.15 vs 18.07 ± 0.89, P = 0.0006). The upregulation of miR-22 could suppress its target gene, ErbB3, and the phosphorylation of PI3k and Akt. Furthermore, we predicted the potential transcription promoter of miR-22 and the binding sites using online tools. Luciferase reporter analysis and site-directed mutagenesis indicated that the binding site (GACAGCCATGTACA) of the GR, which is encoded by the Nr3c1 gene. Downregulation of the expression of GR could upregulate the expression of miR-22, which further promoted the apoptosis of AR42J cells.

CONCLUSION

GR transcriptionally represses the expression of miR-22, which further promotes the apoptosis of pancreatic acinar cells by downregulating the downstream signaling pathway.

Keywords: MicroRNA-22; Apoptosis; Pancreatic acinar cells; Erb-b2 receptor tyrosine kinase 3; Glucocorticoid receptor

Core tip: The severity of acute pancreatitis (AP) is inversely related to the rate of apoptosis of pancreatic acinar cells. MicroRNA-22 (miR-22) might promote caerulein-induced apoptosis of pancreatic acinar cells (AR42J) via down-regulating the expression of its target gene, Erb-b2 receptor tyrosine kinase 3 (ErbB3) and the PI3k/Akt signaling pathway. Glucocorticoid receptor transcriptionally repressed the expression of miR-22 by binding to the miR-22 promoter transcription start site. The upregulation of miR-22 expression resulting from silencing Nr3c1 contributed to the apoptosis of AR42J cells.