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SmithRNAs: Could Mitochondria "Bend" Nuclear Regulation?

ABSTRACT: Typically, animal mitochondria have very compact genomes, with few short intergenic regions, and no introns. Hence, it may seem that there is little space for unknown functions in mitochondrial DNA (mtDNA). However, mtDNA can also operate through RNA interference, as small non coding RNAs (sncRNAs) produced by mtDNA have already been proposed for humans. We sequenced sncRNA libraries from isolated mitochondria of Ruditapes philippinarum (Mollusca Bivalvia) gonads, a species with doubly uniparental inheritance of mitochondria, and identified several putative sncRNAs of mitochondrial origin. Some sncRNAs are transcribed by intergenic regions that form stable stem-hairpin structures, which makes them good miRNA-like candidates. We decided to name them small mitochondrial highly-transcribed RNAs (smithRNAs). Many concurrent data support that we have recovered sncRNAs of mitochondrial origin that might be involved in gonad formation and able to affect nuclear gene expression. This possibility has been never suggested before. If mtDNA can affect nuclear gene expression through RNA interference, this opens a plethora of new possibilities for it to interact with the nucleus, and makes metazoan mtDNA a much more complex genome than previously thought.

SUBMITTER: Pozzi A

PROVIDER: S-EPMC5850712 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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SmithRNAs: Could Mitochondria "Bend" Nuclear Regulation?

Pozzi Andrea A Plazzi Federico F Milani Liliana L Ghiselli Fabrizio F Passamonti Marco M

Molecular biology and evolution 20170801 8

Typically, animal mitochondria have very compact genomes, with few short intergenic regions, and no introns. Hence, it may seem that there is little space for unknown functions in mitochondrial DNA (mtDNA). However, mtDNA can also operate through RNA interference, as small non coding RNAs (sncRNAs) produced by mtDNA have already been proposed for humans. We sequenced sncRNA libraries from isolated mitochondria of Ruditapes philippinarum (Mollusca Bivalvia) gonads, a species with doubly uniparent ...[more]

PMID: 28444389

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Project description:MicroRNAs (miRNAs) are small non-coding RNAs that associate with Argonaute proteins to regulate gene expression at the post-transcriptional level in the cytoplasm. However, recent studies have reported that some miRNAs localize to and function in other cellular compartments. Mitochondria harbour their own genetic system that may be a potential site for miRNA mediated post-transcriptional regulation. We aimed at investigating whether nuclear-encoded miRNAs can localize to and function in human mitochondria. To enable identification of mitochondrial-enriched miRNAs, we profiled the mitochondrial and cytosolic RNA fractions from the same HeLa cells by miRNA microarray analysis. Mitochondria were purified using a combination of cell fractionation and immunoisolation, and assessed for the lack of protein and RNA contaminants. We found 57 miRNAs differentially expressed in HeLa mitochondria and cytosol. Of these 57, a signature of 13 nuclear-encoded miRNAs was reproducibly enriched in mitochondrial RNA and validated by RT-PCR for hsa-miR-494, hsa-miR-1275 and hsa-miR-1974. The significance of their mitochondrial localization was investigated by characterizing their genomic context, cross-species conservation and instrinsic features such as their size and thermodynamic parameters. Interestingly, the specificities of mitochondrial versus cytosolic miRNAs were underlined by significantly different structural and thermodynamic parameters. Computational targeting analysis of most mitochondrial miRNAs revealed not only nuclear but also mitochondrial-encoded targets. The functional relevance of miRNAs in mitochondria was supported by the finding of Argonaute 2 localization to mitochondria revealed by immunoblotting and confocal microscopy, and further validated by the co-immunoprecipitation of the mitochondrial transcript COX3. This study provides the first comprehensive view of the localization of RNA interference components to the mitochondria. Our data outline the molecular bases for a novel layer of crosstalk between nucleus and mitochondria through a specific subset of human miRNAs that we termed 'mitomiRs'.

Dataset Information

SmithRNAs: Could Mitochondria "Bend" Nuclear Regulation?

Publications

SmithRNAs: Could Mitochondria "Bend" Nuclear Regulation?

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