Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic Implantation

Background: In western swine breeds, up to 30% of embryonic losses occur during early pregnancy, and the majority of embryonic losses happens during implantation. In this period, maternal recognition of pregnancy begins to occur and blastocysts undergo dramatic morphologic changes. As with other spe...

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Main Authors: Linjun Hong, Ruize Liu, Xiwu Qiao, Xingwang Wang, Shouqi Wang, Jiaqi Li, Zhenfang Wu, Hao Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-07-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.00661/full
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record_format Article
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language English
format Article
sources DOAJ
author Linjun Hong
Linjun Hong
Ruize Liu
Xiwu Qiao
Xiwu Qiao
Xingwang Wang
Xingwang Wang
Shouqi Wang
Shouqi Wang
Jiaqi Li
Jiaqi Li
Zhenfang Wu
Zhenfang Wu
Hao Zhang
Hao Zhang
spellingShingle Linjun Hong
Linjun Hong
Ruize Liu
Xiwu Qiao
Xiwu Qiao
Xingwang Wang
Xingwang Wang
Shouqi Wang
Shouqi Wang
Jiaqi Li
Jiaqi Li
Zhenfang Wu
Zhenfang Wu
Hao Zhang
Hao Zhang
Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic Implantation
Frontiers in Genetics
porcine
endometrium
microRNAs
differential expression
implantation
author_facet Linjun Hong
Linjun Hong
Ruize Liu
Xiwu Qiao
Xiwu Qiao
Xingwang Wang
Xingwang Wang
Shouqi Wang
Shouqi Wang
Jiaqi Li
Jiaqi Li
Zhenfang Wu
Zhenfang Wu
Hao Zhang
Hao Zhang
author_sort Linjun Hong
title Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic Implantation
title_short Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic Implantation
title_full Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic Implantation
title_fullStr Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic Implantation
title_full_unstemmed Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic Implantation
title_sort differential microrna expression in porcine endometrium involved in remodeling and angiogenesis that contributes to embryonic implantation
publisher Frontiers Media S.A.
series Frontiers in Genetics
issn 1664-8021
publishDate 2019-07-01
description Background: In western swine breeds, up to 30% of embryonic losses occur during early pregnancy, and the majority of embryonic losses happens during implantation. In this period, maternal recognition of pregnancy begins to occur and blastocysts undergo dramatic morphologic changes. As with other species, changes in the uterine environment plays an important role in the process of embryo implantation in pigs. Erhualian (ER) pigs, one of the Chinese Taihu swine breeds, are known to have the highest litter size in the world. Experiments demonstrated that the greater embryonic survival on gestation day (GD) 12 in Chinese Taihu pigs is one important factor that contributes to enhanced litter size. This is largely controlled by maternal genes. In this study, endometrial samples were collected from pregnant Landrace×Large Yorkshire (LL) sows (parity 3) and ER sows (parity 3) on GD12 and the expression profiles of microRNAs (miRNAs) in the endometrium were compared between ER and LL using miRNA-seq technology.Results: A total of 288 miRNAs were identified in the pig endometrium, including 202 previously known and 86 novel miRNAs. The Kyoto Encyclopedia of Genes and Genomes pathway analysis revealed that highly abundant miRNAs might affect endometrial remodeling. Comparison between LL and ER sows revealed that 96 known miRNAs were differentially expressed between the two groups (including 78 up-regulated and 18 down-regulated miRNAs in ER compared to LL). Bioinformatics analysis showed that the target genes of some differentially expressed miRNAs were involved in pathways related to angiogenesis, proliferation, apoptosis, and tissue remodeling, which play critical roles in implantation by regulating endometrial structural changes and secretions of hormones, growth factors, and nutrients. Furthermore, the results demonstrated that insulin-like growth factor-1 protein expression was directly inhibited by miR-206. The lower expression of miR-206 in ER compared to LL might facilitate the angiogenesis of the endometrium during embryo implantation.Conclusions: The identified miRNAs that are differentially expressed in the endometrium of ER and LL pigs will contribute to the understanding of the role of miRNAs in embryonic implantation and the molecular mechanisms of the highest embryonic survival in Chinese ER pigs.
topic porcine
endometrium
microRNAs
differential expression
implantation
url https://www.frontiersin.org/article/10.3389/fgene.2019.00661/full
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spelling doaj-687a5adb391843de9b619b676e9da4fb2020-11-24T21:54:38ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-07-011010.3389/fgene.2019.00661454907Differential microRNA Expression in Porcine Endometrium Involved in Remodeling and Angiogenesis That Contributes to Embryonic ImplantationLinjun Hong0Linjun Hong1Ruize Liu2Xiwu Qiao3Xiwu Qiao4Xingwang Wang5Xingwang Wang6Shouqi Wang7Shouqi Wang8Jiaqi Li9Jiaqi Li10Zhenfang Wu11Zhenfang Wu12Hao Zhang13Hao Zhang14National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, ChinaStanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, United StatesNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, Guangzhou, ChinaBackground: In western swine breeds, up to 30% of embryonic losses occur during early pregnancy, and the majority of embryonic losses happens during implantation. In this period, maternal recognition of pregnancy begins to occur and blastocysts undergo dramatic morphologic changes. As with other species, changes in the uterine environment plays an important role in the process of embryo implantation in pigs. Erhualian (ER) pigs, one of the Chinese Taihu swine breeds, are known to have the highest litter size in the world. Experiments demonstrated that the greater embryonic survival on gestation day (GD) 12 in Chinese Taihu pigs is one important factor that contributes to enhanced litter size. This is largely controlled by maternal genes. In this study, endometrial samples were collected from pregnant Landrace×Large Yorkshire (LL) sows (parity 3) and ER sows (parity 3) on GD12 and the expression profiles of microRNAs (miRNAs) in the endometrium were compared between ER and LL using miRNA-seq technology.Results: A total of 288 miRNAs were identified in the pig endometrium, including 202 previously known and 86 novel miRNAs. The Kyoto Encyclopedia of Genes and Genomes pathway analysis revealed that highly abundant miRNAs might affect endometrial remodeling. Comparison between LL and ER sows revealed that 96 known miRNAs were differentially expressed between the two groups (including 78 up-regulated and 18 down-regulated miRNAs in ER compared to LL). Bioinformatics analysis showed that the target genes of some differentially expressed miRNAs were involved in pathways related to angiogenesis, proliferation, apoptosis, and tissue remodeling, which play critical roles in implantation by regulating endometrial structural changes and secretions of hormones, growth factors, and nutrients. Furthermore, the results demonstrated that insulin-like growth factor-1 protein expression was directly inhibited by miR-206. The lower expression of miR-206 in ER compared to LL might facilitate the angiogenesis of the endometrium during embryo implantation.Conclusions: The identified miRNAs that are differentially expressed in the endometrium of ER and LL pigs will contribute to the understanding of the role of miRNAs in embryonic implantation and the molecular mechanisms of the highest embryonic survival in Chinese ER pigs.https://www.frontiersin.org/article/10.3389/fgene.2019.00661/fullporcineendometriummicroRNAsdifferential expressionimplantation