Department of RNA Biology and Neuroscience, Graduate School of Medicine, Osaka University, Suita, Japan.
Integrated Frontier Research for Medical Science Division, Institute for Open and Transdisciplinary Research Initiatives (OTRI), Osaka University, Suita, Japan.
PLoS Genet. 2021 May 13;17(5):e1009516. doi: 10.1371/journal.pgen.1009516. eCollection 2021 May.
Adenosine deaminase acting on RNA 1 (ADAR1), an enzyme responsible for adenosine-to-inosine RNA editing, is composed of two isoforms: nuclear p110 and cytoplasmic p150. Deletion of Adar1 or Adar1 p150 genes in mice results in embryonic lethality with overexpression of interferon-stimulating genes (ISGs), caused by the aberrant recognition of unedited endogenous transcripts by melanoma differentiation-associated protein 5 (MDA5). However, among numerous RNA editing sites, how many RNA sites require editing, especially by ADAR1 p150, to avoid MDA5 activation and whether ADAR1 p110 contributes to this function remains elusive. In particular, ADAR1 p110 is abundant in the mouse brain where a subtle amount of ADAR1 p150 is expressed, whereas ADAR1 mutations cause Aicardi-Goutières syndrome, in which the brain is one of the most affected organs accompanied by the elevated expression of ISGs. Therefore, understanding RNA editing-mediated prevention of MDA5 activation in the brain is especially important. Here, we established Adar1 p110-specific knockout mice, in which the upregulated expression of ISGs was not observed. This result suggests that ADAR1 p150-mediated RNA editing is enough to suppress MDA5 activation. Therefore, we further created Adar1 p110/Adar2 double knockout mice to identify ADAR1 p150-mediated editing sites. This analysis demonstrated that although the elevated expression of ISGs was not observed, only less than 2% of editing sites were preserved in the brains of Adar1 p110/Adar2 double knockout mice. Of note, we found that some sites were highly edited, which was comparable to those found in wild-type mice, indicating the presence of ADAR1 p150-specific sites. These data suggest that RNA editing at a very limited sites, which is mediated by a subtle amount of ADAR1 p150, is sufficient to prevents MDA5 activation, at least in the mouse brain.
RNA 1 腺苷酸脱氨酶(ADAR1)是一种负责腺苷酸到肌苷酸 RNA 编辑的酶,由两个同工型组成:核 p110 和细胞质 p150。在小鼠中敲除 Adar1 或 Adar1 p150 基因会导致胚胎致死,同时过度表达干扰素刺激基因(ISGs),这是由于黑色素瘤分化相关蛋白 5(MDA5)异常识别未编辑的内源性转录本所致。然而,在众多 RNA 编辑位点中,有多少 RNA 位点需要编辑,特别是由 ADAR1 p150 进行编辑,以避免 MDA5 激活,以及 ADAR1 p110 是否有助于此功能,目前仍不清楚。特别是 ADAR1 p110 在小鼠大脑中含量丰富,而 ADAR1 p150 的表达量却很低,而 ADAR1 突变会导致 Aicardi-Goutières 综合征,其中大脑是受影响最严重的器官之一,同时伴有 ISGs 的表达升高。因此,了解大脑中 ADAR1 介导的 RNA 编辑对 MDA5 激活的预防作用尤为重要。在这里,我们建立了 ADAR1 p110 特异性敲除小鼠,其中未观察到 ISGs 的上调表达。这一结果表明,ADAR1 p150 介导的 RNA 编辑足以抑制 MDA5 的激活。因此,我们进一步创建了 Adar1 p110/Adar2 双敲除小鼠,以鉴定 ADAR1 p150 介导的编辑位点。这项分析表明,尽管未观察到 ISGs 的上调表达,但在 Adar1 p110/Adar2 双敲除小鼠的大脑中,只有不到 2%的编辑位点被保留下来。值得注意的是,我们发现一些位点的编辑程度很高,与野生型小鼠中的编辑程度相当,这表明存在 ADAR1 p150 特异性位点。这些数据表明,在大脑中,至少在小鼠大脑中,由少量 ADAR1 p150 介导的非常有限的位点的 RNA 编辑足以预防 MDA5 的激活。