Li Zhengrong, Li Daojiang, Zhang Guoyang, Xiong Jianbo, Jie Zhigang, Cheng Heping, Cao Yi, Jiang Mengmeng, Lin Liangqing, Le Zhibiao, Tan Shengxing, Zou Wenyu, Gong Binbin, Lin Shengrong, Yang Ke
Department of Gastrointestinal Surgery, First Affiliated Hospital, Nanchang University Nanchang, Jiangxi province, 330000, China.
Nanchang University Medical College Nanchang, Jiangxi province, 330000, China.
Am J Cancer Res. 2014 Nov 19;4(6):648-62. eCollection 2014.
MicroRNAs (miRNAs) are small non-coding RNAs that function as endogenous silencers of target genes, previous studies have shown that miR-335 play an important role in suppressing metastasis and migration in human cancer including gastric cancer (GC). However, the mechanisms which result in aberrant expression of miR-335 in GC are still unknown. Recent studies have shown that the silencing of some miRNAs is associated with DNA hypermethylation. In this study, we find the promoter of miR-335 we embedded in CpG island by accessing to bioinformatics data and the low expression of miR-335 in 5 gastric cell lines can be restored by 5-aza-2'-deoxycytidine (5-Aza-dC) treatment. So we postulated that the miR-335 genes undergo epigenetic inactivation in GC. Subsequently, in GC cells and tissues, we performed quantitative real-time PCR (RTQ-PCR) to assess the expression of miR-335, and methylation-specific PCR (MSP) and bisulfite sequence-PCR (BSP) to evaluate the DNA methylation status in the CpG islands upstream of MiR-335. The result showed that the expression of miR-335 was significantly reduce in gastric cancer cell lines and tumor tissues compared to matched normal gastric tissues, and cell lines, and which is inverse correlation with DNA hypermethylation of miR-335 both in GC cells lines and tissues, but not in normal tissues. In addition, we found that the lower miR-335 expression induced by abnormal methylation may be mainly involved in gastric cell invasion and metastasis in GC tissues. No statistical significance was found about miR-335 expression and methylation level between healthy individuals with and without H. pylori (HP) infection. Finally, we carry out miRNA transfection, RTQ-PCR and western blot assay to find the RAS p21 protein activator (GTPase activating protein) 1 (RASA1) may be the possible target genes which lead to the gastric cell invasion and metastasis, furthermore, the re-expression of endogenous miR-335 by 5-Aza-dC treatment can exert effects similar to exogenous miRNAs transfection. Taken together, our results suggest that miR-335 may be silenced by promoter hypermethylation and play important roles in gastric cell invasion and metastasis through its target genes, such as RASA1. Its methylation level might be a predictive epigenetic marker of GC and remodeling on the expression by demethylation can provided a potential therapeutic strategy.
微小RNA(miRNA)是一类小的非编码RNA,作为靶基因的内源性沉默子发挥作用。先前的研究表明,miR-335在抑制包括胃癌(GC)在内的人类癌症的转移和迁移中起重要作用。然而,导致GC中miR-335异常表达的机制仍不清楚。最近的研究表明,一些miRNA的沉默与DNA高甲基化有关。在本研究中,我们通过获取生物信息学数据发现miR-335的启动子位于CpG岛中,并且5-氮杂-2'-脱氧胞苷(5-Aza-dC)处理可以恢复5种胃癌细胞系中miR-335的低表达。因此,我们推测miR-335基因在GC中经历表观遗传失活。随后,在GC细胞和组织中,我们进行了定量实时PCR(RTQ-PCR)以评估miR-335的表达,并进行了甲基化特异性PCR(MSP)和亚硫酸氢盐序列PCR(BSP)以评估miR-335上游CpG岛中的DNA甲基化状态。结果表明,与匹配的正常胃组织和细胞系相比,miR-335在胃癌细胞系和肿瘤组织中的表达显著降低,并且在GC细胞系和组织中,其与miR-335的DNA高甲基化呈负相关,但在正常组织中并非如此。此外,我们发现异常甲基化诱导的较低miR-335表达可能主要参与GC组织中的胃细胞侵袭和转移。在有和没有幽门螺杆菌(HP)感染的健康个体之间,未发现miR-335表达和甲基化水平有统计学意义。最后,我们进行了miRNA转染、RTQ-PCR和蛋白质免疫印迹分析,发现RAS p21蛋白激活剂(GTP酶激活蛋白)1(RASA1)可能是导致胃细胞侵袭和转移的潜在靶基因,此外,5-Aza-dC处理使内源性miR-335重新表达可产生与外源性miRNA转染类似的效果。综上所述,我们的结果表明,miR-335可能通过启动子高甲基化而沉默,并通过其靶基因(如RASA1)在胃细胞侵袭和转移中发挥重要作用。其甲基化水平可能是GC的一种预测性表观遗传标志物,通过去甲基化重塑其表达可为GC提供潜在的治疗策略。