Elsevier

Biomedicine & Pharmacotherapy

Volume 83, October 2016, Pages 1239-1246
Biomedicine & Pharmacotherapy

Lobaplatin induces BGC-823 human gastric carcinoma cell apoptosis via ROS- mitochondrial apoptotic pathway and impairs cell migration and invasion

https://doi.org/10.1016/j.biopha.2016.08.053Get rights and content

Abstract

Human gastric cancer is the fifth common cancer with considerable metastasis potential, and its high incidence and mortality rate threaten public health. In this study, we examined the anticancer effects of lobaplatin on the human gastric carcinoma cell line BGC-823 in vitro, and explored its relative mechanisms. The results of MTT assay showed dose- and time-dependent cytotoxicity in BGC-823 cells with lobaplatin. Flow cytometry (FCM) assay indicated that lobaplatin affected BGC-823 cells’ survival by inducing apoptosis. Western blot analysis also demonstrated that the occurrence of its apoptosis was associated with activation of Cleaved caspase-3 and Bax, downregulation of Bcl-2. Moreover, lobaplatin could also increase the reactive oxygen species (ROS) slightly and decrease the mitochondrial membrane potentialYm) obviously, elucidating that lobaplatin may induce apoptosis via mitochondria-dependent apoptotic pathway. Furthermore, lobaplatin markedly blocked BGC-823 cells migration and invasion, and the reduction of matrix metalloproteinase (MMP) MMP-2 and MMP-9 expression were also observed in vitro. Our findings demonstrated the chemotherapeutic potential of lobaplatin for treatment of human gastric carcinoma cell line BGC-823 by inhibiting proliferation, inducing apoptosis and attenuating cell migration and invasion.

Introduction

Human gastric carcinoma, or stomach carcinoma, is the fifth most common type of cancer overall, with an estimated 952,000 new cases worldwide in 2012. There were estimated 723,000 deaths from gastric carcinoma in 2012, accounting for 8.8% of all sexes cancer deaths and ranking third [1]. It is estimated that 420,489 men and women were diagnosed with gastric cancer in China in 2011, accounting for 12.47% of all new cancer cases [2]. High-incidence areas include East Asia, Eastern Europe, Central and South America, Japan and Korea, which is considered to mostly be associated with variations in diet [3], [4]. In spite of the declined worldwide mortality rates of gastric carcinoma in the last decade, the survival rate remains low [5].

Among other third-generation platinum antineoplastic agents, lobaplation received only regional approval. Lobaplatin was approved in China for the therapy of metastatic breast cancer, chronic myelogenous leukemia and small cell lung cancer. Its dose-limited toxicity is thrombocytopenia [6], [7]. Except these diseases, some clinical trials and published researches exhibited that lobaplation also had antitumor activities in many other tumor types, such as human esophageal cancer, ovarian cancer, colorectal carcinoma, hepatocellular carcinoma, cholangio carcinoma, and cervical cancer, melanoma, etc [8], [9], [10], [11], [12], [13].

However, there is limited evidence for the effects of lobaplation on the underlying mechanisms in human gastric cancer [14]. The aim of present study was to clarify the mode of action of lobaplation in the context of its anti-tumor activity, which could provide more evidences for the clinical application of lobaplatin in human gastric cancer treatment.

Section snippets

Reagents and chemicals

Lobaplatin was purchased from Hainan Chang’an International Pharmaceutical Co., Ltd. (China). 3-(4, 5-Dimethylthiazol-2-yl)-2, 5-diphenyltetrazoliumbromide (MTT), dimethyl sulfoxide (DMSO), propidium iodide (PI), Rhodamine-123 (Rh123) and 2′,7′-dichlorodihydrofluorescein diacetate (DCFH-DA) were purchased from Sigma (St Louis, MO). The following primary antibodies were used in this research: Bcl-2, Bax, Cleaved caspase-3, MMP9 and MMP2 were purchased from Cell Signaling Technology Company

Lobaplatin inhibited BGC-823 cells proliferation and influenced the cell morphology

The chemical structure of lobaplatin was shown in Fig. 1. Prior to investigating the pharmacological potential of lobaplatin for affecting human gastric cancer cell viability, we first assayed the cytotoxicity of lobaplatin by treating BGC-823 cells with different concentrations (0, 1, 2, 4, 8, 16 and 32 μg/mL) for 24, 48 and 72 h using an MTT assay. As shown in Fig. 2A, lobaplatin inhibited the growth of BGC-823 cells in concentration- and time-dependent manner. What’s more, decreased

Discussion and conclusion

It had been well known that gastric cancer leaded the fifth-most cancer. Its incidence rate in Asia is higher than North America, whereas mortality rate are consistently high in all parts of the world [28]. Risk factors for stomach cancers include H. pylori and Epstein-Barr virus infection, low socioeconomic status, smoking, intake of salty and smoked food, low consumption of fruits and vegetables, et al. [29], [30], [31], [32], [33], [34]. Effective prevention strategies have been implemented,

Disclosure of interest

The authors declare no competing interests.

Acknowledgements

We gratefully acknowledge Boguang Sun for helping in cell culturing. This study was funded by the grants from the National Natural Science Foundation of China (81500054), China Postdoctoral Science Foundation (2015M570788, 2016T90859) and Undergraduate Innovation Project of Sichuan University (201510610647).

References (48)

  • K.D. Crew et al.

    Epidemiology of gastric cancer

    World J. Gastroenterol.

    (2006)
  • C.L. Patru et al.

    Current issues in gastric cancer epidemiology

    Rev. Med. Chir. Soc. Med. Nat. Iasi.

    (2013)
  • S. Dilruba et al.

    Platinum-based drugs: past, present and future

    Cancer Chemother. Pharmacol.

    (2016)
  • N.J. Wheate et al.

    The status of platinum anticancer drugs in the clinic and in clinical trials

    Dalton Trans.

    (2010)
  • M.J. McKeage

    Lobaplatin: a new antitumour platinum drug

    Expert. Opin. Invest. Drugs

    (2001)
  • Q. Wu et al.

    Lobaplatin arrests cell cycle progression in human hepatocellular carcinoma cells

    J. Hematol. Oncol.

    (2010)
  • C. Yin et al.

    Lobaplatin inhibits growth of gastric cancer cells by inducing apoptosis

    World J. Gastroenterol.

    (2014)
  • T. Ye et al.

    The Anthelmintic drug niclosamide induces apoptosis, impairs metastasis and reduces immunosuppressive cells in breast cancer model

    PLoS One

    (2014)
  • C. Gaul et al.

    The migrastatin family: discovery of potent cell migration inhibitors by chemical synthesis

    J. Am. Chem. Soc.

    (2004)
  • J. Tsai et al.

    Licochalcone A induces autophagy through PI3K/Akt/mTOR inactivation and autophagy suppression enhances Licochalcone A-induced apoptosis of human cervical cancer cells

    Oncotarget

    (2015)
  • X. Peng et al.

    SKLB-163, a new benzothiazole-2-thiol derivative, exhibits potent anticancer activity by affecting RhoGDI/JNK-1 signaling pathway

    Cell Death Dis.

    (2014)
  • F. Yang et al.

    Nifuroxazide induces apoptosis and impairs pulmonary metastasis in breast cancer model

    Cell Death Dis.

    (2015)
  • Y. Zhu et al.

    A novel small-molecule YLT205 induces apoptosis in human colorectal cells via mitochondrial apoptosis pathway in vitro and inhibits tumor growth in vivo

    Cell. Physiol. Biochem.

    (2014)
  • Q. Zhang et al.

    The novel protective role of P27 in MLN4924-treated gastric cancer cells

    Cell Death Dis.

    (2015)
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