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Placenta-specific lncRNA 1600012P17Rik is expressed in spongiotrophoblast and glycogen trophoblast cells of mouse placenta

Abstract

A few long noncoding RNAs (long ncRNAs, lncRNAs) exhibit trophoblast cell type-specific expression patterns and functional roles in mouse placenta. However, the cell- and stage-specific expression patterns and functions of most placenta-derived lncRNAs remain unclear. In this study, we explored mouse placenta-associated lncRNAs using a combined bioinformatic and experimental approach. We used the FANTOM5 database to survey lncRNA expression in mouse placenta and found that 1600012P17Rik (MGI: 1919275, designated P17Rik), a long intergenic ncRNA, was the most highly expressed lncRNA at gestational day 17. Polymerase chain reaction analysis confirmed that P17Rik was exclusively expressed in placenta and not in any of the adult organs examined in this study. In situ hybridization analysis revealed that it was highly expressed in spongiotrophoblast cells and to a lesser extent in glycogen trophoblast cells, including migratory glycogen trophoblast cells invading the decidua. Moreover, we found that it is a polyadenylated lncRNA localized mainly to the cytoplasm of these trophoblast cells. As these trophoblast cells also expressed the neighboring protein-coding gene, pappalysin 2 (Pappa2), we investigated the effects of P17Rik on Pappa2 expression using Pappa2-expressing MC3T3-E1 cells and found that P17Rik transfection increased the messenger RNA (mRNA) and protein levels of Pappa2. These results indicate that mouse placenta-specific lncRNA P17Rik modulates the expression of the neighboring protein-coding gene Pappa2 in spongiotrophoblast and glycogen trophoblast cells of mouse placenta during late gestation.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

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Acknowledgements

The authors are indebted to Mr. Takuji Kosuge and Ms. Masumi Shimizu (Nippon Medical School) for their excellent technical assistance and Dr. Aya Misawa (Nippon Medical School) for her advice on ViewRNA.

Funding

This work was supported by the Grants-in-Aid for Scientific Research (nos. 17K11256 and 20K09611 to To.T.) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT)/Japan Society for the Promotion of Science, Japan, and by the Nippon Medical School Grant-in-Aid for Medical Research (2018) to To.T.

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Contributions

To.T. conceived and designed the experiments; J.W. performed bioinformatic analysis; J.W., S.N., Ta.T., Y.N., R.M., and To.T. performed experimental analysis: J.W., S.N., Ta.T., and To.T. analyzed the data; J.W. and To.T. drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Toshihiro Takizawa.

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The authors report no conflicts of interest.

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Wang, J., Noguchi, S., Takizawa, T. et al. Placenta-specific lncRNA 1600012P17Rik is expressed in spongiotrophoblast and glycogen trophoblast cells of mouse placenta. Histochem Cell Biol 158, 65–78 (2022). https://doi.org/10.1007/s00418-022-02109-w

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  • DOI: https://doi.org/10.1007/s00418-022-02109-w

Keywords

  • 1600012P17Rik
  • In situ hybridization
  • Long noncoding RNA
  • Mouse placenta
  • Pappa2