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

Kin, Koryu; Maziarz, Jamie; Chavan, Arun R.; Kamat, Manasi M.; Vasudevan, Sreelakshmi; Birt, Alyssa; Emera, Deena; Lynch, Vincent J.; Ott, Troy L.; Pavličev, Mihaela; Wagner, Günter P.

doi:10.1093/gbe/evw168

Cited by 44 publications

(57 citation statements)

References 59 publications

(94 reference statements)

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“…Opossums, in particular, are the best model for the configuration from which the eutherian mode of pregnancy evolved, because they retain ancestral features of marsupial pregnancy and, likely, therian pregnancy (25). For these reasons, the opossum has been used to understand the evolutionary origins of pregnancy in live-bearing mammals (28,29).…”

Section: Significancementioning

confidence: 99%

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Griffith

Chavan

Protopapas

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The molecular changes that support implantation in eutherian mammals are necessary to establish pregnancy. In marsupials, pregnancy is relatively short, and although a placenta does form, it is present for only a few days before parturition. However, morphological changes in the uterus of marsupials at term mimic those that occur during implantation in humans and mice. We investigated the molecular similarity between term pregnancy in the marsupials and implantation in eutherian mammals using the gray short-tailed opossum (Monodelphis domestica) as a model. Transcriptomic analysis shows that term pregnancy in the opossum is characterized by an inflammatory response consistent with implantation in humans and mice. This immune response is temporally correlated with the loss of the eggshell, and we used immunohistochemistry to report that this reaction occurs at the materno-fetal interface. We demonstrate that key markers of implantation, including Heparin binding EGF-like growth factor and Mucin 1, exhibit expression and localization profiles consistent with the pattern observed during implantation in eutherian mammals. Finally, we show that there are transcriptome-wide similarities between the opossum attachment reaction and implantation in rabbits and humans. Our data suggest that the implantation reaction that occurs in eutherians is derived from an attachment reaction in the ancestral therian mammal which, in the opossum, leads directly to parturition. Finally, we argue that the ability to shift from an inflammatory attachment reaction to a noninflammatory period of pregnancy was a key innovation in eutherian mammals that allowed an extended period of intimate placentation.placenta | marsupial | inflammation | pregnancy | evolution I n eutherian (so-called "placental") mammals, pregnancy begins when the blastocyst attaches to the uterine wall, followed by the establishment of a stable fetal-maternal interface. Implantation involves the apposition, attachment, and, in many species, the invasion of the blastocyst into the uterus (1). In particular, structural and molecular changes occur in the luminal epithelia that allow the embryo to attach and invade the uterus (2). Epithelial changes are followed by remodeling of the endometrial stroma, generally known as "decidualization," i.e., the transformation of endometrial stromal fibroblasts into decidual stromal cells, as well as modifications of the endometrial vascular bed (3). When these changes do not occur or occur incompletely, blastocysts fail to implant, resulting in early pregnancy failure (4, 5). In humans, 75% of unsuccessful pregnancies are the result of failures of implantation, and implantation failure is the limiting factor for in vitro fertilization treatment. Furthermore, decades of research have failed to produce clinically effective treatments that increase uterine receptivity to implantation (6-8). Given the magnitude of this problem, extensive efforts have been made to characterize the endometrium for signatures of receptivity (9, 10).Implantati...

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Section: Significancementioning

confidence: 99%

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Griffith

Chavan

Protopapas

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

190

162

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“…However, marsupial ESF cannot differentiate into a DSC . In eutherians, and in humans specifically, the DSC differentiates from an ESF, which we label “neo‐ESF” because it can differentiate into a DSC . Figure B shows the cell type tree which implies that human ESF and DSC are sister cell types, as reflected in the similarity of their transcriptomes compared to other mesenchymal cell types …”

Section: Stress Responses Have Shaped the Evolution Of The Dscmentioning

confidence: 99%

Stress‐Induced Evolutionary Innovation: A Mechanism for the Origin of Cell Types

Wagner¹,

Erkenbrack²,

Love

2019

BioEssays

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Understanding the evolutionary role of environmentally induced phenotypic variation (i.e., plasticity) is an important issue in developmental evolution. A major physiological response to environmental change is cellular stress, which is counteracted by generic stress reactions detoxifying the cell. A model, stress‐induced evolutionary innovation (SIEI), whereby ancestral stress reactions and their corresponding pathways can be transformed into novel structural components of body plans, such as new cell types, is described. Previous findings suggest that the cell differentiation cascade of a cell type critical to pregnancy in humans, the decidual stromal cell, evolved from a cellular stress reaction. It is hypothesized that the stress reaction in these cells was elicited ancestrally via inflammation caused by embryo attachment. The present study proposes that SIEI is a distinct form of plasticity‐based evolutionary change leading to the origin of novel structures rather than adaptive transformation of pre‐existing characters.

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“…Recently diverged taxa, such as among primates, may obey assumptions in the model of Brownian motion (Khaitovich, et al 2006;Khaitovich, et al 2004;Yang, et al 2017). In other cases, transcriptome divergence has been observed to saturate (Bedford and Hartl 2009;Kin, et al 2016;Metzger, et al 2017) (Brawand data, Sup. Fig.…”

Section: Modeling Correlated Evolution Is Essential For Reconstructinmentioning

confidence: 99%

Pervasive correlated evolution in gene expression shapes cell type transcriptomes

Liang

Musser

Cloutier

et al. 2016

Preprint

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(250 words limit)The evolution and diversification of cell types is a key means by which animal complexity evolves.Recently, hierarchical clustering and phylogenetic methods have been applied to RNA-seq data to infer cell type evolutionary history and homology. A major challenge for interpreting this data is that cell type transcriptomes may not evolve independently due to correlated changes in gene expression. This non-independence can arise for several reasons, such as when different tissues share common regulatory sequences for regulating genes expressed in multiple tissues, i.e. pleiotropic effects of mutations. We develop a model to estimate the level of correlated transcriptome evolution (LCE) and apply it to different datasets. The results reveal pervasive correlated transcriptome evolution among different cell and tissue types. In general, tissues related by morphology or developmental lineage exhibit higher LCE than more distantly related tissues.Analyzing new data collected from bird skin appendages suggests that LCE decreases with the phylogenetic age of tissues compared, with recently evolved tissues exhibiting the highest LCE.Furthermore, we show correlated evolution can alter patterns of hierarchical clustering, causing different tissue types from the same species to cluster together. Using a dataset with sufficient taxon sampling, we performed a gene-wise estimation of LCE, identifying genes that most strongly contribute to the correlated evolution signal. Removing genes with high LCE allows for accurate reconstruction of evolutionary relationships among tissue types. Our study provides a statistical method to measure and account for correlated gene expression evolution when interpreting comparative transcriptome data.All rights reserved. No reuse allowed without permission.

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

Cited by 44 publications

References 59 publications

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Stress‐Induced Evolutionary Innovation: A Mechanism for the Origin of Cell Types

Pervasive correlated evolution in gene expression shapes cell type transcriptomes

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