Wojcicka Anna, Piekielko-Witkowska Agnieszka, Kedzierska Hanna, Rybicka Beata, Poplawski Piotr, Boguslawska Joanna, Master Adam, Nauman Alicja
Department of Biochemistry and Molecular Biology, Centre of Postgraduate Medical Education, Warsaw, Poland; Genomic Medicine, Department of General, Transplant and Liver Surgery, Medical University of Warsaw, Warsaw, Poland.
Department of Biochemistry and Molecular Biology, Centre of Postgraduate Medical Education, Warsaw, Poland.
PLoS One. 2014 May 21;9(5):e97624. doi: 10.1371/journal.pone.0097624. eCollection 2014.
Thyroid hormone receptor beta (THRB) gene is commonly deregulated in cancers and, as strengthened by animal models, postulated to play a tumor-suppressive role. Our previous studies revealed downregulation of THRB in clear cell renal cell carcinoma (ccRCC), but the culpable mechanisms have not been fully elucidated. Since epigenetic regulation is a common mechanism influencing the expression of tumor suppressors, we hypothesized that downregulation of THRB in renal cancer results from epigenetic aberrances, including CpG methylation and microRNA-dependent silencing. Our study revealed that ccRCC tumors exhibited a 56% decrease in THRB and a 37% increase in DNA methyltransferase 1 (DNMT1) expression when compared with paired non-neoplastic control samples. However, THRB CpG methylation analysis performed using BSP, SNaPshot and MSP-PCR consistently revealed no changes in methylation patterns between matched tumor and control samples. In silico analysis resulted in identification of four microRNAs (miR-155, miR-425, miR-592, and miR-599) as potentially targeting THRB transcript. Luciferase assay showed direct binding of miR-155 and miR-425 to 3'UTR of THRB, and subsequent in vivo analyses revealed that transfection of UOK171 cell line with synthetic miR-155 or miR-425 resulted in decreased expression of endogenous TRHB by 22% and 64%, respectively. Finally, real-time PCR analysis showed significant upregulation of miR-155 (354%) and miR-425 (162%) in ccRCC when compared with matched controls. Moreover, microRNA levels were negatively correlated with the amount of THRB transcript in tissue samples. We conclude that CpG methylation is not the major mechanism contributing to decreased THRB expression in ccRCC. In contrast, THRB is targeted by microRNAs miR-155 and miR-425, whose increased expression may be responsible for downregulation of THRB in ccRCC tumors.
甲状腺激素受体β(THRB)基因在癌症中通常表达失调,并且动物模型研究表明该基因具有肿瘤抑制作用。我们之前的研究发现,在透明细胞肾细胞癌(ccRCC)中THRB表达下调,但其潜在机制尚未完全阐明。由于表观遗传调控是影响肿瘤抑制因子表达的常见机制,我们推测肾癌中THRB表达下调是由表观遗传异常引起的,包括CpG甲基化和微小RNA依赖性沉默。我们的研究发现,与配对的非肿瘤对照样本相比,ccRCC肿瘤中THRB表达降低了56%,而DNA甲基转移酶1(DNMT1)表达增加了37%。然而,使用亚硫酸氢盐测序法(BSP)、单碱基延伸分型法(SNaPshot)和甲基化特异性PCR(MSP-PCR)对THRB CpG甲基化进行分析,结果显示匹配的肿瘤样本和对照样本之间甲基化模式没有变化。通过计算机分析,我们鉴定出四种微小RNA(miR-155、miR-425、miR-592和miR-599)可能靶向THRB转录本。荧光素酶报告基因检测显示miR-155和miR-425可直接与THRB的3'非翻译区(3'UTR)结合,随后的体内分析表明,用合成的miR-155或miR-425转染UOK171细胞系后,内源性TRHB的表达分别降低了22%和64%。最后,实时定量PCR分析显示,与匹配的对照相比,ccRCC中miR-155(354%)和miR-425(162%)显著上调。此外,组织样本中微小RNA水平与THRB转录本数量呈负相关。我们得出结论,CpG甲基化不是导致ccRCC中THRB表达降低的主要机制。相反,THRB是微小RNA miR-155和miR-425的靶标,它们表达增加可能是ccRCC肿瘤中THRB表达下调的原因。