The most abundant maternal lncRNA Sirena1 acts post-transcriptionally and impacts mitochondrial distribution

0525646 - ÚMG 2021 RIV GB eng J - Journal Article
Ganesh, Sravya - Horvat, Filip - Drutovič, Dávid - Efenberková, Michaela - Pinkas, Dominik - Jindrová, Anna - Pasulka, Josef - Iyyappan, Rajan - Malík, Radek - Šušor, Andrej - Vlahovicek, K. - Šolc, Petr - Svoboda, Petr
The most abundant maternal lncRNA Sirena1 acts post-transcriptionally and impacts mitochondrial distribution.
Nucleic Acids Research. Roč. 48, č. 6 (2020), s. 3211-3227. ISSN 0305-1048. E-ISSN 1362-4962
R&D Projects: GA MŠMT LO1419; GA MŠMT(CZ) LO1609; GA MŠMT(CZ) LM2011032; GA MŠMT(CZ) LM2015040; GA MŠMT(CZ) ED1.1.00/02.0109; GA MŠMT(CZ) LM2015062; GA ČR(CZ) GA18-19395S
Grant - others:GA MŠk(CZ) LM2015042
Institutional support: RVO:68378050 ; RVO:67985904
Keywords : gene-expression * messenger-rna * mouse oocytes * maturation * single * cell * normalization * transcription * evolution * sirnas
OECD category: Reproductive biology (medical aspects to be 3); Cell biology (UZFG-Y)
Impact factor: 16.971, year: 2020
Method of publishing: Open access
https://academic.oup.com/nar/article/48/6/3211/5709715

Tens of thousands of rapidly evolving long non-coding RNA (lncRNA) genes have been identified, but functions were assigned to relatively few of them. The lncRNA contribution to the mouse oocyte physiology remains unknown. We report the evolutionary history and functional analysis of Sirena1, the most expressed lncRNA and the 10th most abundant poly(A) transcript in mouse oocytes. Sirena1 appeared in the common ancestor of mouse and rat and became engaged in two different post-transcriptional regulations. First, antisense oriented Bob pseudogene insertion into Sirena1 exon 1 is a source of small RNAs targeting Sob mRNA via RNA interference. Second, Sirena1 evolved functional cytoplasmic polyadenylation elements, an unexpected feature borrowed from translation control of specific maternal mRNAs. Sirena1 knock-out does not affect fertility, but causes minor dysregulation of the maternal transcriptome. This includes increased levels of Elob and mitochondrial mRNAs. Mitochondria in Sirena1(-/-) oocytes disperse from the perinuclear compartment, but do not change in number or ultrastructure. Taken together, Sirenal contributes to RNA interference and mitochondrial aggregation in mouse oocytes. Sirena1 exemplifies how lncRNAs stochastically engage or even repurpose molecular mechanisms during evolution. Simultaneously, Sirenai1 expression levels and unique functional features contrast with the lack of functional importance assessed under laboratory conditions.
Permanent Link: http://hdl.handle.net/11104/0309757