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Genome Biol Evol. 2016 Aug 25;8(8):2459-73. doi: 10.1093/gbe/evw168.

The Transcriptomic Evolution of Mammalian Pregnancy: Gene Expression Innovations in Endometrial Stromal Fibroblasts.

Author information

1
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut Yale Systems Biology Institute, Yale University, West Haven, Connecticut.
2
Yale Systems Biology Institute, Yale University, West Haven, Connecticut.
3
Department of Animal Science, Center for Reproductive Biology and Health, Pennsylvania State University, Stage College, Pennsylvania.
4
Department of Genetics, Yale School of Medicine, Yale University, New Haven, Connecticut.
5
Department of Human Genetics, University of Chicago, Chicago, Illinois.
6
Department of Pediatrics, Cincinnati Children's Hospital and Medical Center, Cincinnati, Ohio.
7
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut Yale Systems Biology Institute, Yale University, West Haven, Connecticut Department of Obstetrics, Gynecology and Reproductive Sciences, Yale Medical School, New Haven, Connecticut Department of Obstetrics and Gynecology, Wayne State University, Detroit, Michigan gunter.wagner@yale.edu.

Abstract

The endometrial stromal fibroblast (ESF) is a cell type present in the uterine lining of therian mammals. In the stem lineage of eutherian mammals, ESF acquired the ability to differentiate into decidual cells in order to allow embryo implantation. We call the latter cell type "neo-ESF" in contrast to "paleo-ESF" which is homologous to eutherian ESF but is not able to decidualize. In this study, we compare the transcriptomes of ESF from six therian species: Opossum (Monodelphis domestica; paleo-ESF), mink, rat, rabbit, human (all neo-ESF), and cow (secondarily nondecidualizing neo-ESF). We find evidence for strong stabilizing selection on transcriptome composition suggesting that the expression of approximately 5,600 genes is maintained by natural selection. The evolution of neo-ESF from paleo-ESF involved the following gene expression changes: Loss of expression of genes related to inflammation and immune response, lower expression of genes opposing tissue invasion, increased markers for proliferation as well as the recruitment of FOXM1, a key gene transiently expressed during decidualization. Signaling pathways also evolve rapidly and continue to evolve within eutherian lineages. In the bovine lineage, where invasiveness and decidualization were secondarily lost, we see a re-expression of genes found in opossum, most prominently WISP2, and a loss of gene expression related to angiogenesis. The data from this and previous studies support a scenario, where the proinflammatory paleo-ESF was reprogrammed to express anti-inflammatory genes in response to the inflammatory stimulus coming from the implanting conceptus and thus paving the way for extended, trans-cyclic gestation.

KEYWORDS:

Eutheria; Marsupialia; cell type evolution; endometrial stromal cells; transcriptome evolution

PMID:
27401177
PMCID:
PMC5010902
DOI:
10.1093/gbe/evw168
[Indexed for MEDLINE]
Free PMC Article
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