Characterization of the placental transcriptome through mid to late gestation in the mare.
Abstract: The placenta is a dynamic organ which undergoes extensive remodeling throughout pregnancy to support, protect and nourish the developing fetus. Despite the importance of the placenta, very little is known about its gene expression beyond very early pregnancy and post-partum. Therefore, we utilized RNA-sequencing to characterize the transcriptome from the fetal (chorioallantois) and maternal (endometrium) components of the placenta from mares throughout gestation (4, 6, 10, 11 m). Within the endometrium, 47% of genes changed throughout pregnancy, while in the chorioallantois, 29% of genes underwent significant changes in expression. Further bioinformatic analyses of both differentially expressed genes and highly expressed genes help reveal similarities and differences between tissues. Overall, the tissues were more similar than different, with ~ 95% of genes expressed in both tissues, and high similarities between the most highly expressed genes (9/20 conserved), as well as marked similarities between the PANTHER pathways identified. The most highly expressed genes fell under a few broad categories, including endocrine and immune-related transcripts, iron-binding proteins, extracellular matrix proteins, transport proteins and antioxidants. Serine protease inhibitors were particularly abundant, including SERPINA3, 6 and 14, as well as SPINK7 and 9. This paper also demonstrates the ability to effectively separate maternal and fetal components of the placenta, with only a minimal amount of chorioallantoic contamination in the endometrium (~8%). This aspect of equine placentation is a boon for better understanding gestational physiology and allows the horse to be used in areas where a separation of fetal and maternal tissues is essential. Overall, these data represent the first large-scale characterization of placental gene expression in any species and include time points from multiple mid- to late-gestational stages, helping further our understanding of gestational physiology.
Publication Date: 2019-11-14 PubMed ID: 31725741PubMed Central: PMC6855469DOI: 10.1371/journal.pone.0224497Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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The study explores placental gene expression in mares during gestation using RNA-sequencing, leading to a greater understanding of pregnancy mechanisms.
Research Context
- The researchers performed a comprehensive analysis of the placenta’s gene activity in horses during pregnancy. Notably, the gene expression of placental tissue during pregnancy, particularly after early pregnancy and before birth, remained relatively unexplored prior to this research.
- The placenta plays a crucial role in supporting, protecting, and nourishing the developing fetus, and its functionality is primarily determined by its gene expression patterns. As such, understanding these patterns can reveal critical insights about gestational physiology.
Research Methodology
- Using RNA-sequencing, the researchers characterized the transcriptome (the entire set of gene readouts in a cell) from both the fetal component (chorioallantois) and the maternal component (endometrium) of the placenta.
- This method was applied at various time points during pregnancy, including months 4, 6, 10, and 11, which allowed for the observation of gene expression changes throughout gestation.
- The team ensured effective separation between maternal and fetal components of the placenta, which minimized contamination and improved the accuracy of the RNA sequencing data. Around 8% contamination was recorded, demonstrating that the horse can be used for studies where clear separation of fetal and maternal tissues is essential.
Findings
- In the endometrium, 47% of genes changed throughout pregnancy, while in the chorioallantois, 29% of genes experienced significant changes in expression.
- Using bioinformatics analysis, the researchers further examined both differentially expressed genes and those that were highly expressed to uncover similarities and differences between the tissues. Generally, the tissues were more alike than different, with approximately 95% of genes being expressed in both tissues.
- The most highly expressed genes were categorized into several broader groups, encompassing endocrine and immune-related transcripts, iron-binding proteins, transport proteins, extracellular matrix proteins, and antioxidants. Serine protease inhibitors were found in abundance, including SERPINA3, 6 and 14, as well as SPINK7 and 9.
- This research represents the inaugural large-scale characterization of placental gene expression evolution, providing considerable insights into gestational physiology.
Cite This Article
APA
Loux SC, Dini P, El-Sheikh Ali H, Kalbfleisch T, Ball BA.
(2019).
Characterization of the placental transcriptome through mid to late gestation in the mare.
PLoS One, 14(11), e0224497.
https://doi.org/10.1371/journal.pone.0224497 Publication
Researcher Affiliations
- Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, United States of America.
- Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, United States of America.
- Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium.
- Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, United States of America.
- Theriogenology Department, Faculty of Veterinary Medicine, University of Mansoura, Mansoura City, Egypt.
- Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, United States of America.
- Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, United States of America.
MeSH Terms
- Animals
- Female
- Gene Expression Profiling
- Gene Expression Regulation, Developmental / physiology
- Gestational Age
- Horses
- Placenta / metabolism
- Pregnancy
- Pregnancy Proteins / biosynthesis
- Transcriptome / physiology
Conflict of Interest Statement
The authors have declared that no competing interests exist.
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Citations
This article has been cited 3 times.- Ciampa EJ, Flahardy P, Srinivasan H, Jacobs C, Tsai L, Karumanchi SA, Parikh SM. Hypoxia-inducible factor 1 signaling drives placental aging and can provoke preterm labor.. Elife 2023 Aug 23;12.
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- Diel de Amorim M, Dong L, Byron M, Foster RA, Klein C, Saleh M, Saleh T, Card C. Characterization of serum and tissue oxytocinase and tissue oxytocin in the pregnant and non-pregnant mare.. Sci Rep 2023 Mar 21;13(1):4616.
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