Original Article
Copyright ©2014 Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Sep 21, 2014; 20(35): 12542-12550
Published online Sep 21, 2014. doi: 10.3748/wjg.v20.i35.12542
Role of ERK-MAPK signaling pathway in pentagastrin-regulated growth of large intestinal carcinoma
Jia-Ding Mao, Pei Wu, Jian-Xiong Huang, Jian Wu, Guang Yang
Jia-Ding Mao, Pei Wu, Jian-Xiong Huang, Jian Wu, Guang Yang, Department of General Surgery, the First Affiliated Yijishan Hospital of Wannan Medical College, Wuhu 241001, Anhui Province, China
Author contributions: Mao JD, Wu P and Huang JX designed research and performed research; Huang JX contributed new reagents/analytic tools; Mao JD analyzed data and wrote the paper; Wu J and Yang G contributed equally to this work.
Supported by Natural Science Foundation of Anhui Province, No. 1408085MH148; Natural Science Fund of Education Bureau of Anhui Province, No. kj2010b242; Natural Science Fund of Wannan Medical College, No. wk2012zf02; and The key science and technology project of Wuhu City, No. health-2-4
Correspondence to: Pei Wu, Professor, Department of General Surgery, the First Affiliated Yijishan Hospital of Wannan Medical College, 10 Weiliu Road, Wuhu 241001, Anhui Province, China. maojiading0205@sina.com
Telephone: +86-553-5739107 Fax: +86-553-5738100
Received: October 10, 2013
Revised: March 28, 2014
Accepted: May 28, 2014
Published online: September 21, 2014
Processing time: 343 Days and 20.5 Hours
Abstract

AIM: To explore the role and mechanisms of extracellular signal-regulated protein kinase-mitogen-activated protein kinase (ERK-MAPK) signaling in pentagastrin-regulated growth of large intestinal carcinoma.

METHODS: HT-29 cells were incubated in different media and divided into the control group, pentagastrin group, proglumide group, and pentagastrin + proglumide group. No reagent was added to the control group, and other groups were incubated with reagent at different concentrations. Changes in proliferation of HT-29 cells were detected by MTT assay, and the optimal concentrations of pentagastrin and proglumide were determined. The changes in proliferation index (PI) and apoptosis rate (AR) of HT-29 cells were detected by Annexin V-fluorescein isothiocyanate flow cytometry. mRNA expression of pentagastrin receptor/cholecystokinin-B receptor (CCK-BR), ERK1/2 and K-ras were detected by reverse transcriptase polymerase chain reaction. The protein and phosphorylation level of ERK1/2 and K-ras were detected by western blotting. All data were analyzed by analysis of variance and SNK-q test.

RESULTS: The proliferation of HT-29 cells was stimulated by pentagastrin at a concentration of 6.25-100 mg/L, and the optimal concentration of pentagastrin was 25.0 mg/L (F = 31.36, P < 0.05). Proglumide had no obvious effect on the proliferation of HT-29 cells, while it significantly inhibited the proliferation of HT-29 cells stimulated by pentagastrin when the concentration of proglumide was 8.0-128.0 mg/L, and the optimal concentration was 32.0 mg/L (F = 24.31, P < 0.05). The PI of the pentagastrin (25.0 mg/L) group was 37.5% ± 5.2%, which was significantly higher than 27.7% ± 5.0% of the control group and 27.3% ± 5.8% of the pentagastrin (25.0 mg/L) + proglumide (32.0 mg/L) group (Q = 4.56-4.75, P < 0.05). The AR of the pentagastrin (25.0 mg/L) group was 1.9% ± 0.4%, which was significantly lower than 2.5% ± 0.4% of the control group and 2.4% ± 0.3% of the pentagastrin (25.0 mg/L) + proglumide (32.0 mg/L) group (Q = 4.23-4.06, P < 0.05). mRNA expression of CCK-BR was detected in HT-29 cells. The phosphorylation levels of ERK1/2 protein and phosphorylated K-ras protein of the pentagastrin group were 0.43% ± 0.04% and 0.45% ± 0.06%, which were significantly higher than 0.32% ± 0.02% and 0.31% ± 0.05% of the control group (Q = 7.78-4.95, P < 0.05), and 0.36% ± 0.01% and 0.35% ± 0.04% of the pentagastrin + proglumide group (Q = 5.72-4.08, P < 0.05). There were no significant differences in the mRNA and protein expression of ERK1/2 and K-ras among the control, pentagastrin, proglumide and pentagastrin + proglumide groups (F = 0.52, 0.72, 0.78, 0.28; P > 0.05).

CONCLUSION: Gastrin stimulates proliferation of HT-29 cells and inhibits apoptosis by upregulating phosphorylation of ERK and K-ras through the Ras-Raf-MEK1/2-ERK1/2 pathway, and this is restrained by proglumide.

Keywords: Gastrin; Mitogen-activated protein kinase; Extracellular signal-regulated protein kinase 1/2; K-ras; Large intestinal carcinoma

Core tip: We have demonstrated that large intestinal carcinoma is related to abnormal expression of gastrin. Gastrin promoted growth of large intestinal cancer cell via gastrin receptor, but the detailed molecular mechanism is not fully known. We elucidated the molecular mechanisms of gastrin-induced growth of large intestinal cancer in relation to the extracellular signal-regulated protein kinase-mitogen-activated protein kinase (ERK-MAPK) signaling pathway. We attempted to establish a new gastrin-ERK-MAPK pathway in gastrin-dependent large intestinal cancer; provide a new way to interfere with the signaling pathway of gastrin-induced growth of large intestinal cancer; and to offer a new target for gene therapy of large intestinal carcinoma.