Sun Liankang, Cao Junyu, Chen Ke, Cheng Liang, Zhou Cancan, Yan Bin, Qian Weikun, Li Jie, Duan Wanxing, Ma Jiguang, Qi Dan, Wu Erxi, Wang Zheng, Liu Qingguang, Ma Qingyong, Xu Qinhong
Department of Hepatobiliary Surgery, First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi 710061, P.R. China.
Department of Anesthesiology, First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi 710061, P.R. China.
Int J Oncol. 2019 Jan;54(1):98-110. doi: 10.3892/ijo.2018.4604. Epub 2018 Oct 24.
Cancer stem cells (CSCs), which are found in various types of human cancer, including pancreatic cancer, possess elevated metastatic potential, lead to tumor recurrence and cause chemoradiotherapy resistance. Alterations in cellular bioenergetics through the regulation of 5' adenosine monophosphate‑activated protein kinase (AMPK) signaling may be a prerequisite to stemness. Betulinic acid (BA) is a well‑known bioactive compound with antiretroviral and anti‑inflammatory potential, which has been reported to exert anticancer effects on various types of cancer, including pancreatic cancer. The present study aimed to investigate whether BA could inhibit pancreatic CSCs via regulation of AMPK signaling. The proliferation of pancreatic cancer cells was examined by MTT and colony formation assays. The migratory and invasive abilities of pancreatic cancer cells were assessed using wound‑scratch and Transwell invasion assays. In addition, the expression levels of candidate genes were measured by reverse transcription‑quantitative polymerase chain reaction and western blotting. The results revealed that BA inhibited the proliferation and tumorsphere formation of pancreatic cancer cells, suppressed epithelial‑mesenchymal transition (EMT), migration and invasion, and reduced the expression of three pluripotency factors [SRY‑box 2 (Sox2), octamer‑binding protein 4 (Oct4) and Nanog]. Furthermore, immunohistochemical analysis confirmed that there was a significant inverse association between the expression levels of phosphorylated (P)‑AMPK and Sox2 in pancreatic cancer, and it was revealed that BA may activate AMPK signaling. Notably, knockdown of AMPK reversed the suppressive effects of BA on EMT and stemness of pancreatic cancer cells. In addition, BA reversed the effects of gemcitabine on stemness and enhanced the sensitivity of pancreatic cancer cells to gemcitabine. Collectively, these results indicated that BA may effectively inhibit pluripotency factor expression (Sox2, Oct4 and Nanog), EMT and the stem‑like phenotype of pancreatic cancer cells via activating AMPK signaling. Therefore, BA may be considered an attractive therapeutic candidate and an effective inhibitor of the stem‑like phenotype in pancreatic cancer cells. Further investigation into the development of BA as an anticancer drug is warranted.
癌症干细胞(CSCs)存在于包括胰腺癌在内的多种人类癌症类型中,具有较高的转移潜能,可导致肿瘤复发并引起放化疗耐药。通过调节5'-腺苷单磷酸激活蛋白激酶(AMPK)信号传导来改变细胞生物能量学可能是干性的一个先决条件。桦木酸(BA)是一种具有抗逆转录病毒和抗炎潜力的著名生物活性化合物,据报道对包括胰腺癌在内的多种癌症具有抗癌作用。本研究旨在探讨BA是否能通过调节AMPK信号传导来抑制胰腺CSCs。通过MTT和集落形成试验检测胰腺癌细胞的增殖情况。使用划痕试验和Transwell侵袭试验评估胰腺癌细胞的迁移和侵袭能力。此外,通过逆转录定量聚合酶链反应和蛋白质印迹法检测候选基因的表达水平。结果显示,BA抑制胰腺癌细胞的增殖和肿瘤球形成,抑制上皮-间质转化(EMT)、迁移和侵袭,并降低三种多能性因子[SRY盒2(Sox2)、八聚体结合蛋白4(Oct4)和Nanog]的表达。此外,免疫组织化学分析证实,胰腺癌中磷酸化(P)-AMPK和Sox2的表达水平之间存在显著的负相关,并且发现BA可能激活AMPK信号传导。值得注意的是,敲低AMPK可逆转BA对胰腺癌细胞EMT和干性的抑制作用。此外,BA逆转了吉西他滨对干性的影响,并增强了胰腺癌细胞对吉西他滨的敏感性。总体而言,这些结果表明,BA可能通过激活AMPK信号传导有效抑制胰腺癌细胞多能性因子表达(Sox2、Oct4和Nanog)、EMT和干细胞样表型。因此,BA可能被认为是一种有吸引力的治疗候选物,是胰腺癌细胞干细胞样表型的有效抑制剂。有必要进一步研究将BA开发为抗癌药物。