Uterine focal adhesion dynamics during pregnancy in a marsupial (<i>Sminthopsis crassicaudata</i>; Dasyuridae)

Laird, Melanie K.; Turancova, Michaela; McAllan, Bronwyn M.; Murphy, Christopher R.; Thompson, Michael B.

doi:10.1002/ar.23535

Cited by 10 publications

(10 citation statements)

References 46 publications

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“…7A). The changes to the luminal epithelial cells and the density of cell-adhesion molecules in the opossum attachment reaction are similar to the implantation reaction in human and rodent pregnancy (50,51). Several of the changes that support implantation in eutherians also occur at term in M. domestica (Fig.…”

Section: Discussionmentioning

confidence: 61%

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Griffith

Chavan

Protopapas

et al. 2017

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

200

162

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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: Discussionmentioning

confidence: 61%

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Griffith

Chavan

Protopapas

et al. 2017

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

200

162

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“…Downregulation and redistribution of desmosomes may facilitate maternal trophoblast adhesion during implantation in some species (Dudley et al, ). Redistribution of desmoglein‐2 to the apical portion of the lateral plasma membrane at implantation coincides with the detachment of uterine epithelium from the underlying basal lamina (Enders and Schlafke, ; Kaneko et al, ; Laird et al, ) and may provide structural support to adjacent cells before they are sloughed in sheets. Studies of the presence of desmoglein‐2 in knockout mice show that it also has a crucial function in embryonal stem cell development and early embryonic survival at implantation (Eshkind et al, ).…”

Section: Discussionmentioning

confidence: 99%

Uterine Epithelial Cells Undergo a Plasma Membrane Transformation During Early Pregnancy in the Domestic Cat (Felis catus)

Dudley

Murphy

Thompson

et al. 2018

The Anatomical Record

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Mammals exhibit similar changes in uterine epithelial morphology during early pregnancy despite having a diverse range of placental types. The uterine epithelium undergoes rapid morphological and molecular change ("plasma membrane transformation") during the early stages of pregnancy to allow attachment of the blastocyst. The domestic cat, Felis catus is in the order Carnivora; all species within the Carnivora studied so far develop an endotheliochorial placenta during pregnancy. The endotheliochorial placental type is a common form of placental invasion in mammals. The molecular changes that allow remodeling of the uterine epithelium in preparation for implantation are unknown in most mammals but would provide us with an understanding of what molecules underpin successful implantation and pregnancy among Carnivora. We used immunofluorescence microscopy to localize the key adherens junction proteins desmoglein-2 and E-cadherin in the lateral plasma membrane of the uterine epithelium of F. catus during pregnancy. We show that redistribution of desmoglein-2 and E-cadherin likely facilitates reduction of cell-to-cell adhesion allowing for implantation of the blastocyst and formation of the placenta. The ultrastructural and molecular changes to the uterine epithelium during early pregnancy in F. catus are similar to that in species with other levels of placental invasiveness, suggesting that key molecules such as desmoglein-2 and E-cadherin are crucial to successful pregnancy across all mammals.Despite significant diversity in the structure and function of the eutherian mammalian placenta, this structure arose from a single common ancestor over 130 million years ago (Nilsson et al., 2010).

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“…Similar localization of Talin occurs in preparation for invasive implantation in S. crassicaudata, during which Talin is recruited to reinforce the uterine epithelium against the invading embryo (Laird et al, 2015;Laird, Turancova, et al, 2017). Such molecular reinforcement of the uterine epithelium may be a maternal strategy to regulate embryonic invasion in S. crassicaudata (Laird et al, 2015;Laird, Turancova, et al, 2017), and likely evolved to mitigate conflict between mother and embryo (Fowden & Moore, 2012).…”

Section: Western Blottingmentioning

confidence: 93%

“…Since embryonic implantation in the common ancestor of living marsupials was probably invasive, non‐invasive placentation in marsupials is most likely secondarily derived (Freyer et al, ). Further, the persistence of maternal defences against the marsupial embryo in pregnancy suggest that less‐invasive and non‐invasive modes of embryonic attachment may have evolved by accumulating maternal defences against the invading embryo (Carter & Mess, ; Crespi & Semeniuk, ; Laird et al, ; Laird, Turancova, et al, ; Vogel, ). We tested this hypothesis by conducting the first study of focal adhesion dynamics during pregnancy in marsupial species with non‐invasive embryonic attachment—the tammar wallaby, Macropus eugenii, and the brush tail possum, Trichosurus vulpecula .…”

Section: Introductionmentioning

confidence: 99%

Uterine molecular changes for non‐invasive embryonic attachment in the marsupials Macropus eugenii (Macropodidae) and Trichosurus vulpecula (Phalangeridae)

Laird

Dargan

Paterson

et al. 2017

Molecular Reproduction Devel

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Pregnancy in mammals requires remodeling of the uterus to become receptive to the implanting embryo. Remarkably similar morphological changes to the uterine epithelium occur in both eutherian and marsupial mammals, irrespective of placental type. Nevertheless, molecular differences in uterine remodeling indicate that the marsupial uterus employs maternal defences, including molecular reinforcement of the uterine epithelium, to regulate embryonic invasion. Non-invasive (epitheliochorial) embryonic attachment in marsupials likely evolved secondarily from invasive attachment, so uterine defences in these species may prevent embryonic invasion. We tested this hypothesis by identifying localization patterns of Talin, a key basal anchoring molecule, in the uterine epithelium during pregnancy in the tammar wallaby (Macropus eugenii; Macropodidae) and the brush tail possum (Trichosurus vulpecula; Phalangeridae). Embryonic attachment is non-invasive in both species, yet Talin undergoes a clear distributional change during pregnancy in M. eugenii, including recruitment to the base of the uterine epithelium just before attachment, that closely resembles that of invasive implantation in the marsupial species Sminthopsis crassicaudata. Basal localization occurs throughout pregnancy in T. vulpecula, although, as for M. eugenii, this pattern is most specific prior to attachment. Such molecular reinforcement of the uterine epithelium for non-invasive embryonic attachment in marsupials supports the hypothesis that less-invasive and non-invasive embryonic attachment in marsupials may have evolved via accrual of maternal defences. Recruitment of basal molecules, including Talin, to the uterine epithelium may have played a key role in this transition.

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Uterine focal adhesion dynamics during pregnancy in a marsupial (Sminthopsis crassicaudata; Dasyuridae)

Cited by 10 publications

References 46 publications

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Embryo implantation evolved from an ancestral inflammatory attachment reaction

Uterine Epithelial Cells Undergo a Plasma Membrane Transformation During Early Pregnancy in the Domestic Cat (Felis catus)

Uterine molecular changes for non‐invasive embryonic attachment in the marsupials Macropus eugenii (Macropodidae) and Trichosurus vulpecula (Phalangeridae)

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