Non‐invasive placentation in the marsupials Macropus eugenii (Macropodidae) and Trichosurus vulpecula (Phalangeridae) involves redistribution of uterine Desmoglein‐2

Abstract

In mammalian pregnancy, the uterus is remodeled to become receptive to embryonic implantation. Since non-invasive placentation in marsupials is likely derived from invasive placentation, and is underpinned by intra-uterine conflict between mother and embryo, species with non-invasive placentation may employ a variety of molecular mechanisms to maintain an intact uterine epithelium and to prevent embryonic invasion. Identifying such modifications to the uterine epithelium of marsupial species with non-invasive placentation is key to understanding how conflict is mediated during pregnancy in different mammalian groups. Desmoglein-2, involved in maintaining lateral cell-cell adhesion of the uterine epithelium, is redistributed before implantation to facilitate embryo invasion in mammals with invasive placentation. We identified localization patterns of this cell adhesion molecule throughout pregnancy in two marsupial species with non-invasive placentation, the tammar wallaby (Macropus eugenii; Macropodidae), and the brushtail possum (Trichosurus vulpecula; Phalangeridae). Interestingly, Desmoglein-2 redistribution also occurs in both M. eugenii and T. vulpecula, suggesting that cell adhesion, and thus integrity of the uterine epithelium, is reduced during implantation regardless of placental type, and may be an important component of uterine remodeling. Desmoglein-2 also localizes to the mesenchymal stromal cells of M. eugenii and to epithelial cell nuclei in T. vulpecula, suggesting its involvement in cellular processes that are independent of adhesion and may compensate for reduced lateral adhesion in the uterine epithelium. We conclude that non-invasive placentation in marsupials involves diverse and complementary strategies to maintain an intact epithelial barrier.

The role of mammalian foetal membranes in early embryogenesis: Lessons from marsupials

“…Tammar wallaby common brushtail possum (Trichosurus vulpecula), is a derived state (Laird et al, 2018;Laird, Hansen, McAllan, Murphy, & Thompson, 2020;Mess & Ferner, 2010).…”

“…The trophoblast is moderately invasive in many marsupials including the four‐eyed opossum ( Philander opossum ; Enders & Enders, 1969) and fat‐tailed dunnart ( Sminthopsis crassicaudata ; Roberts & Breed, 1994a). Recent studies favour the view that the common ancestor of marsupials had an invasive trophoblast, whereas a completely non‐invasive trophoblast, as in the tammar wallaby and common brushtail possum ( Trichosurus vulpecula ), is a derived state (Laird et al, 2018; Laird, Hansen, McAllan, Murphy, & Thompson, 2020; Mess & Ferner, 2010).…”

“…Several studies have probed the uterine responses to pregnancy. A redistribution of desmosomes and associated claudins has been noted in the plasma membrane of epithelial cells in the fat‐tailed dunnart (Buddle et al, 2019; Dudley, Murphy, Thompson, & McAllan, 2015) as well as tammar wallaby and brushtail possum (Laird et al, 2018). This response was comparable to that preceding attachment in viviparous squamates and eutherians (Dudley et al, 2015).…”

Dynamic changes to claudins in the uterine epithelial cells of the marsupial Sminthopsis crassicaudata (Dasyuridae) during pregnancy

“…The least invasive type of placentation seen in vertebrates is epitheliochorial placentation, which involves embryonic attachment to an intact uterine epithelium (Carter & Enders, ). Irrespective of placental invasiveness, the plasma membrane transformation has been demonstrated during early pregnancy in species from all viviparous amniote lineages: reptiles, marsupial mammals, and eutherian mammals (Hughes, ; Roberts & Breed, ; Dudley, Murphy, Thompson, & McAllan, ; Dudley, Murphy, Thompson, & McAllan, ; Dudley, Murphy, Thompson, Carter, & McAllan, ; Laird et al, ; Laird, Thompson, Murphy, & McAllan, ; Murphy, ). Hence, the plasma membrane transformation appears to be a necessary process for uterine receptivity across viviparous amniotes with varying modes of placentation (Murphy, ).…”

“…Modifications to the junctional complexes that laterally connect uterine epithelial cells together are key processes involved in the plasma membrane transformation that are conserved in marsupials and eutherians (Dudley et al, 2015(Dudley et al, , 2017(Dudley et al, , 2018cIllingworth et al, 2000;Laird et al, 2018). Lateral junctional complexes include tight junctions, the adherens junction, and desmosomes (Farquhar & Palade, 1963).…”