Fully grown mammalian oocytes store a large amount of RNA synthesized during the transcriptionally active growth stage. A large part of the stored RNA belongs to the long non-coding class which contain either transcriptional noise or important contributors to cellular physiology. Despite the expanding number of studies related to lncRNAs, their influence on oocyte physiology remains enigmatic. We found an oocyte specific antisense, long non-coding RNA, "Rose" (lncRNA in Oocyte Specifically Expressed) expressed in two variants containing two and three non-coding exons, respectively. Rose is localized in the nucleus of transcriptionally active oocyte and in embryo with polysomal occupancy in the cytoplasm. Experimental overexpression of Rose in fully grown oocyte did not show any differences in meiotic maturation. However, knocking down Rose resulted in abnormalities in oocyte cytokinesis and impaired preimplantation embryo development. In conclusion, we have identified an oocyte-specific maternal lncRNA that is essential for successful mammalian oocyte and embryo development.

Laboratory of Biochemistry and Molecular Biology of Germ Cells Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Rumburska 89 277 21 Libechov Czech Republic

Laboratory of Developmental Biology Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Rumburska 89 277 21 Libechov Czech Republic

School of Animal Sciences AgCenter Louisiana State University Baton Rouge LA 70820 United States

Zobrazit více v PubMed

Breschi A., Gingeras T.R., Guigó R. Comparative transcriptomics in human and mouse. Nat. Rev. Genet. 2017;18:425–440. doi: 10.1038/nrg.2017.19. PubMed DOI PMC

Mattick J.S., Makunin I.V. Non-coding RNA. Hum. Mol. Genet. 2006;15:R17–R29. doi: 10.1093/hmg/ddl046. PubMed DOI

Zhang X., Wang W., Zhu W., Dong J., Cheng Y., Yin Z., Shen F. Mechanisms and functions of long non-coding RNAs at multiple regulatory levels. Int. J. Mol. Sci. 2019;20:5573. doi: 10.3390/ijms20225573. PubMed DOI PMC

He R.Z., Luo D.X., Mo Y.Y. Emerging roles of lncRNAs in the post-transcriptional regulation in cancer. Genes Dis. 2019;6:6–15. doi: 10.1016/j.gendis.2019.01.003. PubMed DOI PMC

Charon C., Moreno A.B., Bardou F., Crespi M. Non-protein-coding RNAs and their interacting RNA-binding proteins in the plant cell nucleus. Mol. Plant. 2010;3:729–739. doi: 10.1093/mp/ssq037. PubMed DOI

Ulitsky I., Bartel D.P. XLincRNAs: genomics, evolution, and mechanisms. Cell. 2013;154:26–46. doi: 10.1016/j.cell.2013.06.020. PubMed DOI PMC

Chen L.L. Linking long noncoding RNA localization and function. Trends Biochem. Sci. 2016;41:761–772. doi: 10.1016/j.tibs.2016.07.003. PubMed DOI

Joshi M., Rajender S. Long non-coding RNAs (lncRNAs) in spermatogenesis and male infertility. Reprod. Biol. Endocrinol. 2020;18:1–18. doi: 10.1186/s12958-020-00660-6. PubMed DOI PMC

Lee T.L., Xiao A., Rennert O.M. Identification of novel long noncoding RNA transcripts in male germ cells. Methods Mol. Biol. 2012;825:105–114. doi: 10.1007/978-1-61779-436-0_9. PubMed DOI PMC

Ganesh S., Horvat F., Drutovic D., Efenberkova M., Pinkas D., Jindrova A., Pasulka J., Iyyappan R., Malik R., Susor A., Vlahovicek K., Solc P., Svoboda P. The most abundant maternal lncRNA Sirena1 acts post-transcriptionally and impacts mitochondrial distribution. Nucleic Acids Res. 2020;48:3211–3227. doi: 10.1093/nar/gkz1239. PubMed DOI PMC

Tetkova A., Jansova D., Susor A. Spatio-temporal expression of ANK2 promotes cytokinesis in oocytes. Sci. Rep. 2019;9:1–13. doi: 10.1038/s41598-019-49483-5. PubMed DOI PMC

Masek T., del Llano E., Gahurova L., Kubelka M., Susor A., Roucova K., Lin C.-J., Bruce A.W., Pospisek M. Identifying the translatome of mouse NEBD-stage oocytes via SSP-profiling; A novel polysome fractionation method. Int. J. Mol. Sci. 2020;21:1254. doi: 10.3390/ijms21041254. PubMed DOI PMC

Heninger A.-K., Buchholz F. Production of endoribonuclease-prepared short interfering RNAs (esiRNAs) for specific and effective gene silencing in mammalian cells. Cold Spring Harb. Protoc. 2007 doi: 10.1101/pdb.prot4824. PubMed DOI

Mann M., Wright P.R., Backofen R. IntaRNA 2.0: enhanced and customizable prediction of RNA-RNA interactions. Nucleic Acids Res. 2017;45:435–439. doi: 10.1093/nar/gkx279. PubMed DOI PMC

Wang L., Park H.J., Dasari S., Wang S., Kocher J.P., Li W. CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res. 2013 doi: 10.1093/nar/gkt006. PubMed DOI PMC

Lecuyer E., Yoshida H., Parthasarathy N., Alm C., Babak T., Tomancak P., Krause H. Global analysis of mRNA localization reveals a prominent role in the organization of cellular architecture and function. Dev. Biol. 2008;131:174–187. doi: 10.1016/j.ydbio.2008.05.012. PubMed DOI

Aleshkina D., Iyyappan R., Lin C.J., Masek T., Pospisek M., Susor A. ncRNA BC1 influences translation in the oocyte. RNA Biol. 2021 doi: 10.1080/15476286.2021.1880181. PubMed DOI PMC

Pintacuda G., Young A.N., Cerase A. Function by structure: spotlights on xist long non-coding RNA. Front. Mol. Biosci. 2017;4:90. doi: 10.3389/fmolb.2017.00090. PubMed DOI PMC

Honda S., Miki Y., Miyamoto Y., Kawahara Y., Tsukamoto S., Imai H., Minami N. Oocyte-specific gene Oog1 suppresses the expression of spermatogenesis-specific genes in oocytes. J. Reprod. Dev. 2018;64:297–301. doi: 10.1262/jrd.2018-024. PubMed DOI PMC

Jansova D., Tetkova A., Koncicka M., Kubelka M., Susor A. Localization of RNA and translation in the mammalian oocyte and embryo. PloS One. 2018;13 doi: 10.1371/journal.pone.0192544. PubMed DOI PMC

Philpott C.C., Ringuette M.J., Dean J. Oocyte-specific expression and developmental regulation of ZP3, the sperm receptor of the mouse zona pellucida. Dev. Biol. 1987;121:568–575. doi: 10.1016/0012-1606(87)90192-8. PubMed DOI

Liang L.F., Soyal S.M., Dean J. FIGα, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development. 1997;124:4939–4947. PubMed

McGrath S.A., Esquela A.F., Lee S.J. Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 1995;9:131–136. doi: 10.1210/mend.9.1.7760846. PubMed DOI

Washietl S., Kellis M., Garber M. Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res. 2014;24:616–628. doi: 10.1101/gr.165035.113. PubMed DOI PMC

Gudenas B.L., Wang L. Prediction of LncRNA subcellular localization with deep learning from sequence features. Sci. Rep. 2018 doi: 10.1038/s41598-018-34708-w. PubMed DOI PMC

Tantale K., Mueller F., Kozulic-Pirher A., Lesne A., Victor J.M., Robert M.C., Capozi S., Chouaib R., Bäcker V., Mateos-Langerak J., Darzacq X., Zimmer C., Basyuk E., Bertrand E. A single-molecule view of transcription reveals convoys of RNA polymerases and multi-scale bursting. Nat. Commun. 2016 doi: 10.1038/ncomms12248. PubMed DOI PMC

Miao H., Wang L., Zhan H., Dai J., Chang Y., Wu F., Liu T., Liu Z., Gao C., Li L., Song X. A long noncoding RNA distributed in both nucleus and cytoplasm operates in the PYCARD-regulated apoptosis by coordinating the epigenetic and translational regulation. PLoS Genet. 2019 doi: 10.1371/journal.pgen.1008144. PubMed DOI PMC

Fatica A., Bozzoni I. Long non-coding RNAs: New players in cell differentiation and development. Nat. Rev. Genet. 2014;15:7–21. doi: 10.1038/nrg3606. PubMed DOI

Verheyden Y., Goedert L., Leucci E. Control of nucleolar stress and translational reprogramming by lncRNAs. Cell Stress. 2019;3:19–26. doi: 10.15698/cst2019.01.172. PubMed DOI PMC

Carlevaro-Fita J., Rahim A., Guigó R., Vardy L.A., Johnson R. Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells. RNA. 2016;22:867–882. doi: 10.1261/rna.053561.115. PubMed DOI PMC

Nakagawa S., Naganuma T., Shioi G., Hirose T. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J. Cell Biol. 2011;193:31–39. doi: 10.1083/jcb.201011110. PubMed DOI PMC