Regulation of Nuclear Transcription by Mitochondrial RNA

Author:

Sriram KiranORCID,Qi Zhijie,Yuan Dongqiang,Malhi Naseeb K.ORCID,Liu Xuejing,Calandrelli RiccardoORCID,Luo Yingjun,Jin Shengyan,Shi Ji,Salas Martha,Dang Runrui,Armstrong Brian,Priceman Saul J.,Wang Ping,Liao Jiayu,Natarajan Rama,Zhong ShengORCID,Chen Zhen B.ORCID

Abstract

AbstractChromatin-associated RNAs (caRNAs) form a relatively poorly recognized layer of the epigenome. The caRNAs reported to date are transcribed from the nuclear genome. Here, leveraging a recently developed assay for detection of caRNAs and their genomic association, we report that mitochondrial RNAs (mtRNAs) are attached to the nuclear genome and constitute a subset of caRNA, which we termed mt-caRNA. In four human cell types analyzed, mt-caRNAs preferentially attach to promoter regions. In human endothelial cells (ECs), the level of mt-caRNA-promoter attachment changes in response to environmental stress that mimics diabetes. Suppression of a non-coding mt-caRNA in ECs attenuates stress-induced nascent RNA transcription from the nuclear genome, including that of critical genes regulating cell adhesion, and abolishes stress-induced monocyte adhesion, a hallmark of dysfunctional ECs. Finally, we report increased nuclear localization of multiple mtRNAs in the ECs of human diabetic donors, suggesting many mtRNA translocate to the nucleus in a cell stress and disease-dependent manner. These data nominate mt-caRNAs as messenger molecules responsible for mitochondrial-nuclear communication and connect the immediate product of mitochondrial transcription with the transcriptional regulation of the nuclear genome.

Publisher

Cold Spring Harbor Laboratory

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