Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculature
Abstract The placenta is a unique organ for ensuring normal embryonic growth in the uterine. Here, we found that maternal RNA transcription in Dlk1-Dio3 imprinted domain is essential for placentation. PolyA signals were inserted into Gtl2 to establish a mouse model to prevent the expression of mater...
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Nature Portfolio
2024-03-01
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Series: | Communications Biology |
Online Access: | https://doi.org/10.1038/s42003-024-06038-3 |
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author | Ximeijia Zhang Hongjuan He Haoran Yu Xiangqi Teng Ziwen Wang Chenghao Li Jiahang Li Haopeng Yang Jiwei Shen Tong Wu Fengwei Zhang Yan Zhang Qiong Wu |
author_facet | Ximeijia Zhang Hongjuan He Haoran Yu Xiangqi Teng Ziwen Wang Chenghao Li Jiahang Li Haopeng Yang Jiwei Shen Tong Wu Fengwei Zhang Yan Zhang Qiong Wu |
author_sort | Ximeijia Zhang |
collection | DOAJ |
description | Abstract The placenta is a unique organ for ensuring normal embryonic growth in the uterine. Here, we found that maternal RNA transcription in Dlk1-Dio3 imprinted domain is essential for placentation. PolyA signals were inserted into Gtl2 to establish a mouse model to prevent the expression of maternal RNAs in the domain. The maternal allele knock-in (MKI) and homozygous (HOMO) placentas showed an expanded junctional zone, reduced labyrinth and poor vasculature impacting both fetal and maternal blood spaces. The MKI and HOMO models displayed dysregulated gene expression in the Dlk1-Dio3 domain. In situ hybridization detected Dlk1, Gtl2, Rtl1, miR-127 and Rian dysregulated in the labyrinth vasculature. MKI and HOMO induced Dlk1 to lose imprinting, and DNA methylation changes of IG-DMR and Gtl2-DMR, leading to abnormal gene expression, while the above changes didn’t occur in paternal allele knock-in placentas. These findings demonstrate that maternal RNAs in the Dlk1-Dio3 domain are involved in placental vasculature, regulating gene expression, imprinting status and DNA methylation. |
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language | English |
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spelling | doaj.art-33777bf4dc3b4944a65a73b2a8a338ea2024-03-24T12:29:24ZengNature PortfolioCommunications Biology2399-36422024-03-017111410.1038/s42003-024-06038-3Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculatureXimeijia Zhang0Hongjuan He1Haoran Yu2Xiangqi Teng3Ziwen Wang4Chenghao Li5Jiahang Li6Haopeng Yang7Jiwei Shen8Tong Wu9Fengwei Zhang10Yan Zhang11Qiong Wu12School of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologySchool of Life Science and Technology, State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of TechnologyAbstract The placenta is a unique organ for ensuring normal embryonic growth in the uterine. Here, we found that maternal RNA transcription in Dlk1-Dio3 imprinted domain is essential for placentation. PolyA signals were inserted into Gtl2 to establish a mouse model to prevent the expression of maternal RNAs in the domain. The maternal allele knock-in (MKI) and homozygous (HOMO) placentas showed an expanded junctional zone, reduced labyrinth and poor vasculature impacting both fetal and maternal blood spaces. The MKI and HOMO models displayed dysregulated gene expression in the Dlk1-Dio3 domain. In situ hybridization detected Dlk1, Gtl2, Rtl1, miR-127 and Rian dysregulated in the labyrinth vasculature. MKI and HOMO induced Dlk1 to lose imprinting, and DNA methylation changes of IG-DMR and Gtl2-DMR, leading to abnormal gene expression, while the above changes didn’t occur in paternal allele knock-in placentas. These findings demonstrate that maternal RNAs in the Dlk1-Dio3 domain are involved in placental vasculature, regulating gene expression, imprinting status and DNA methylation.https://doi.org/10.1038/s42003-024-06038-3 |
spellingShingle | Ximeijia Zhang Hongjuan He Haoran Yu Xiangqi Teng Ziwen Wang Chenghao Li Jiahang Li Haopeng Yang Jiwei Shen Tong Wu Fengwei Zhang Yan Zhang Qiong Wu Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculature Communications Biology |
title | Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculature |
title_full | Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculature |
title_fullStr | Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculature |
title_full_unstemmed | Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculature |
title_short | Maternal RNA transcription in Dlk1-Dio3 domain is critical for proper development of the mouse placental vasculature |
title_sort | maternal rna transcription in dlk1 dio3 domain is critical for proper development of the mouse placental vasculature |
url | https://doi.org/10.1038/s42003-024-06038-3 |
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