Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, College of Life Sciences, South China Agricultural University, Guangzhou, 510642, China.
Key Laboratory of Zoonosis of Ministry of Agriculture and Rural Affairs, South China Agricultural University, Guangzhou, 510642, P.R. China.
RNA Biol. 2020 Apr;17(4):584-595. doi: 10.1080/15476286.2020.1719750. Epub 2020 Feb 6.
Deoxynivalenol (DON) is one of the most abundant mycotoxins and has adverse effects on several biological processes, posing risks of protein synthesis-disrupting effects and ribotoxic response. Therefore, chronic exposure to DON would fundamentally reshape the global expression pattern. Whether DON causes toxic effects on mRNA splicing, a fundamental biological process, remains unclear. In this study, we found that administration of the relative low dosage of DON dramatically changed the alternative splicing of pre-mRNA in HepG2 cells. The overall number of transcripts with aberrant selection of 3' splice sites was significantly increased in DON-exposed HepG2 cells. This effect was further confirmed in two other human cell lines, HEK293 and Caco-2, suggesting that this DON-induced alteration in splicing patterns was universal in human cells. Among these DON-induced changes in alternative splicing, the expression levels of two related splicing factors, SF1 and U2AF1, which are essential for 3' splice site recognitions, were strongly suppressed. Overexpression of either of the two splicing factors strongly alleviated the DON-induced aberrant selection of 3' splice sites. Moreover, SF1 was required for human cell proliferation in DON exposure, and the restoration of SF1 expression partially reinstated the proliferation potential for DON-treated cells. In conclusion, our study suggests that DON, even at a low dosage, has great potential to change gene expression globally by affecting not only protein synthesis but also mRNA processing in human cells.
脱氧雪腐镰刀菌烯醇(DON)是最丰富的霉菌毒素之一,对多种生物过程具有不良影响,具有破坏蛋白质合成和核糖体毒性反应的风险。因此,慢性暴露于 DON 将从根本上重塑全球表达模式。DON 是否对 mRNA 剪接这一基本的生物学过程产生毒性作用尚不清楚。在本研究中,我们发现相对低剂量 DON 的给药会显著改变 HepG2 细胞中前体 mRNA 的可变剪接。在 DON 暴露的 HepG2 细胞中,3'剪接位点选择异常的转录本总数显著增加。这一效应在另外两种人类细胞系 HEK293 和 Caco-2 中进一步得到证实,表明这种 DON 诱导的剪接模式改变在人类细胞中是普遍存在的。在这些 DON 诱导的可变剪接变化中,两个相关剪接因子 SF1 和 U2AF1 的表达水平被强烈抑制,这两个剪接因子对于 3'剪接位点的识别至关重要。这两种剪接因子中的任何一种的过表达都能强烈缓解 DON 诱导的 3'剪接位点异常选择。此外,SF1 是 DON 暴露下人细胞增殖所必需的,SF1 表达的恢复部分恢复了 DON 处理细胞的增殖潜力。总之,我们的研究表明,DON 即使在低剂量下,也有可能通过影响人类细胞中的蛋白质合成和 mRNA 处理来全局改变基因表达。