Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in Chickens

Although lncRNAs have been identified as playing critical roles in the development of germ cells, their potential involvement in the development of PGCs in chickens remains poorly understood. Differentially expressed lncRNAs (DELs) from previous RNA-seq of embryonic stem cells (ESCs), PGCs, and sper...

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Main Authors: Jingyi Jiang, Chen Chen, Shaoze Cheng, Xia Yuan, Jing Jin, Chen Zhang, Xiaolin Sun, Jiuzhou Song, Qisheng Zuo, Yani Zhang, Guohong Chen, Bichun Li
Format: Article
Language:English
Published: MDPI AG 2021-01-01
Series:Animals
Subjects:
Online Access:https://www.mdpi.com/2076-2615/11/2/292
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author Jingyi Jiang
Chen Chen
Shaoze Cheng
Xia Yuan
Jing Jin
Chen Zhang
Xiaolin Sun
Jiuzhou Song
Qisheng Zuo
Yani Zhang
Guohong Chen
Bichun Li
author_facet Jingyi Jiang
Chen Chen
Shaoze Cheng
Xia Yuan
Jing Jin
Chen Zhang
Xiaolin Sun
Jiuzhou Song
Qisheng Zuo
Yani Zhang
Guohong Chen
Bichun Li
author_sort Jingyi Jiang
collection DOAJ
description Although lncRNAs have been identified as playing critical roles in the development of germ cells, their potential involvement in the development of PGCs in chickens remains poorly understood. Differentially expressed lncRNAs (DELs) from previous RNA-seq of embryonic stem cells (ESCs), PGCs, and spermatogonial stem cells (SSCs) were analyzed by K-means clustering, from which a key candidate, lncRNA (lncRNA PGC regulator, <i>LncPGCR</i>) was obtained. We confirmed that <i>LncPGCR</i> plays a positive role in the development of PGCs by increasing the expression of the PGC marker gene (<i>Cvh</i> and <i>C-kit</i>), while downregulating the pluripotency-associated gene (<i>Nanog</i>) in vitro and in vivo. The activation and expression of <i>LncPGCR</i> are regulated by histone acetylation, and transcription factor TCF7L2. Mechanistically, a rescue assay was performed to further confirm that <i>LncPGCR</i> contributed to the development of PGCs by regulating the gga-miR-6577-5p/<i>Btrc</i> signaling pathway. Adsorption of gga-miR-6577-5p activated the WNT signaling cascade by relieving the gga-miR-6577-5p-dependent inhibition of <i>Btrc</i> expression. Taken together, our study discovered the growth-expedited role of <i>LncPGCR</i> in PGCs development, showing the potential <i>LncPGCR</i>/miR-6577-5p/<i>Btrc</i> pathway. The results and findings provide a novel insight into the development of PGCs.
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spelling doaj.art-4ba4178573324c91a10a539f775162702023-12-03T14:30:31ZengMDPI AGAnimals2076-26152021-01-0111229210.3390/ani11020292Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in ChickensJingyi Jiang0Chen Chen1Shaoze Cheng2Xia Yuan3Jing Jin4Chen Zhang5Xiaolin Sun6Jiuzhou Song7Qisheng Zuo8Yani Zhang9Guohong Chen10Bichun Li11Key Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaAnimal & Avian Sciences, University of Maryland, College Park, MD 20741, USAKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaKey Laboratory of Animal Breeding Reproduction and Molecular Design for Jiangsu Province, College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, Jiangsu, ChinaAlthough lncRNAs have been identified as playing critical roles in the development of germ cells, their potential involvement in the development of PGCs in chickens remains poorly understood. Differentially expressed lncRNAs (DELs) from previous RNA-seq of embryonic stem cells (ESCs), PGCs, and spermatogonial stem cells (SSCs) were analyzed by K-means clustering, from which a key candidate, lncRNA (lncRNA PGC regulator, <i>LncPGCR</i>) was obtained. We confirmed that <i>LncPGCR</i> plays a positive role in the development of PGCs by increasing the expression of the PGC marker gene (<i>Cvh</i> and <i>C-kit</i>), while downregulating the pluripotency-associated gene (<i>Nanog</i>) in vitro and in vivo. The activation and expression of <i>LncPGCR</i> are regulated by histone acetylation, and transcription factor TCF7L2. Mechanistically, a rescue assay was performed to further confirm that <i>LncPGCR</i> contributed to the development of PGCs by regulating the gga-miR-6577-5p/<i>Btrc</i> signaling pathway. Adsorption of gga-miR-6577-5p activated the WNT signaling cascade by relieving the gga-miR-6577-5p-dependent inhibition of <i>Btrc</i> expression. Taken together, our study discovered the growth-expedited role of <i>LncPGCR</i> in PGCs development, showing the potential <i>LncPGCR</i>/miR-6577-5p/<i>Btrc</i> pathway. The results and findings provide a novel insight into the development of PGCs.https://www.mdpi.com/2076-2615/11/2/292chicken (<i>Gallus gallus</i>)LncRNAprimordial germ cellTCF7L2<i>Btrc</i>ceRNA
spellingShingle Jingyi Jiang
Chen Chen
Shaoze Cheng
Xia Yuan
Jing Jin
Chen Zhang
Xiaolin Sun
Jiuzhou Song
Qisheng Zuo
Yani Zhang
Guohong Chen
Bichun Li
Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in Chickens
Animals
chicken (<i>Gallus gallus</i>)
LncRNA
primordial germ cell
TCF7L2
<i>Btrc</i>
ceRNA
title Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in Chickens
title_full Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in Chickens
title_fullStr Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in Chickens
title_full_unstemmed Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in Chickens
title_short Long Noncoding RNA <i>LncPGCR</i> Mediated by TCF7L2 Regulates Primordial Germ Cell Formation in Chickens
title_sort long noncoding rna i lncpgcr i mediated by tcf7l2 regulates primordial germ cell formation in chickens
topic chicken (<i>Gallus gallus</i>)
LncRNA
primordial germ cell
TCF7L2
<i>Btrc</i>
ceRNA
url https://www.mdpi.com/2076-2615/11/2/292
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