National Centre for Cell Science (NCCS), Savitribai Phule Pune University Campus, Pune, India.
Bionivid Technology Pvt Ltd, Bangalore, India.
PLoS Biol. 2018 Oct 8;16(10):e2004204. doi: 10.1371/journal.pbio.2004204. eCollection 2018 Oct.
Long noncoding RNAs constitute a major fraction of the eukaryotic transcriptome, and together with proteins, they intricately fine-tune various growth regulatory signals to control cellular homeostasis. Here, we describe the functional characterisation of a novel pair of long intergenic noncoding RNAs (lincRNAs) comprised of complementary, fully overlapping sense and antisense transcripts Genomic Instability Inducing RNA (Ginir) and antisense RNA of Ginir (Giniras), respectively, from mouse cells. This transcript pair is expressed in a spatiotemporal manner during embryonic development. The individual levels of the sense and antisense transcripts are finely balanced during embryonic growth and in adult tissues. Functional studies of the individual transcripts performed using overexpression and knock-down strategies in mouse cells has led to the discovery that Ginir RNA is a regulator of cellular proliferation and can act as an oncogene having a preeminent role in malignant transformation. Mechanistically, we demonstrate that the oncogenic function of Ginir is mediated by its interaction with centrosomal protein 112 (Cep112). Additionally, we establish here a specific interaction between Cep112 with breast cancer type 1 susceptibility protein (Brca1), another centrosome-associated protein. Next, we prove that the mutual interaction between Cep112 with Brca1 is significant for mitotic regulation and maintenance of genomic stability. Furthermore, we demonstrate that the Cep112 protein interaction with Brca1 protein is impaired when an elevated level of Ginir RNA is present in the cells, resulting in severe deregulation and abnormality in mitosis, leading to malignant transformation. Inhibiting the Ginir RNA function in transformed cells attenuates transformation and restores genomic stability. Together, these findings unravel, to our knowledge, a hitherto-unknown mechanism of oncogenesis mediated by a long noncoding RNA and establishes a unique role of Cep112-Brca1 interaction being modulated by Ginir RNA in maintaining mitotic fidelity.
长非编码 RNA 构成真核转录组的主要部分,它们与蛋白质一起,精细地微调各种生长调节信号,以控制细胞内稳态。在这里,我们描述了由互补的、完全重叠的正义和反义转录物组成的一对新的长基因间非编码 RNA(lincRNA)的功能特征,即来自小鼠细胞的基因组不稳定性诱导 RNA(Ginir)和 Ginir 的反义 RNA(Giniras)。该转录对在胚胎发育过程中具有时空表达模式。在胚胎生长和成年组织中,正义和反义转录物的水平精细平衡。在小鼠细胞中使用过表达和敲低策略进行的单个转录物的功能研究导致发现 Ginir RNA 是细胞增殖的调节剂,并可作为致癌基因发挥作用,在恶性转化中具有突出作用。从机制上讲,我们证明 Ginir 的致癌功能是通过其与中心体蛋白 112(Cep112)的相互作用介导的。此外,我们在这里建立了 Cep112 与乳腺癌 1 型易感性蛋白(Brca1),另一种中心体相关蛋白之间的特异性相互作用。接下来,我们证明 Cep112 与 Brca1 之间的相互作用对于有丝分裂调节和维持基因组稳定性是重要的。此外,我们证明当细胞中存在高水平的 Ginir RNA 时,Cep112 与 Brca1 蛋白之间的相互作用受损,导致有丝分裂严重失调和异常,导致恶性转化。在转化细胞中抑制 Ginir RNA 功能可减弱转化并恢复基因组稳定性。总之,这些发现揭示了一种以前未知的长非编码 RNA 介导的致癌机制,并确立了由 Ginir RNA 调节的 Cep112-Brca1 相互作用在维持有丝分裂保真度方面的独特作用。