The Fetal Membranes of the Otter Shrews and a Synapomorphy for Afrotheria

Carter, Anthony Michael; Blankenship, Thomas N.; Enders, A.C.; Vogel, Peter

doi:10.1016/j.placenta.2005.02.019

Cited by 31 publications

(23 citation statements)

References 22 publications

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“…However, we could amplify a large coding fragment, thus strongly suggesting that syncytin-Ten1 is conserved in the entire Tenrecidae lineage. This finding, furthermore, would be consistent with the reported placental structure of Potamogalinae (28), which is closely related to that of Malagasy tenrecs and also displays two distinct regions, a peripheral labyrinthine region and a central hemophagous region. The hemophagous region of Potamogalinae also possesses an ST layer at the tip of fetal villi, where fetal cells are in contact with the maternal tissues (28).…”

Section: Discussionsupporting

confidence: 91%

“…This finding, furthermore, would be consistent with the reported placental structure of Potamogalinae (28), which is closely related to that of Malagasy tenrecs and also displays two distinct regions, a peripheral labyrinthine region and a central hemophagous region. The hemophagous region of Potamogalinae also possesses an ST layer at the tip of fetal villi, where fetal cells are in contact with the maternal tissues (28). Interestingly, the placental structure of a representative species of the closest Tenrecidae outgroup, the A. hottentotus species belonging to the Chrysochloridae, also has been described, and the absence of an hemophagous region has been demonstrated in this species (36).…”

Section: Discussionsupporting

confidence: 91%

“…Again, this peculiar structural organization is consistent with our in situ hybridization results, which show no evidence of syncytin-Ten1 expression in this tissue. Conversely, the labyrinthine region of Potamogalinae is of the endotheliochorial type, with an ST layer surrounding the preserved maternal vessels (28). Thus it would be of interest to analyze the syncytin-Ten1 expression pattern in a Potamogalinae species and to determine if it is expressed in the labyrinthine region, where it could account for ST formation at this fetomaternal interface in addition to the hemophagous region.…”

Section: Discussionmentioning

confidence: 99%

“…As schematized in Fig. 6A, the S. setosus placenta is composed of two concentric regions, the hemophagous central region (CR) and the peripheral labyrinthine placental pad (PP) (24), as also described for the closely related lesser hedgehog tenrec (25,26) and a few other tenrec species (22,28). The peripheral placental pad comprises the labyrinthine zone (LZ), where the maternal blood is in direct contact with a trophoblast cell layer, which separates maternal blood spaces (MBS) from the fetal vessels.…”

Section: Ten-env7mentioning

confidence: 93%

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Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs

Cornelis

Vernochet

Malicorne

et al. 2014

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

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Syncytins are fusogenic envelope (env) genes of retroviral origin that have been captured for a function in placentation. Syncytins have been identified in Euarchontoglires (primates, rodents, Leporidae) and Laurasiatheria (Carnivora, ruminants) placental mammals. Here, we searched for similar genes in species that retained characteristic features of primitive mammals, namely the Malagasy and mainland African Tenrecidae. They belong to the superorder Afrotheria, an early lineage that diverged from Euarchotonglires and Laurasiatheria 100 Mya, during the Cretaceous terrestrial revolution. An in silico search for env genes with full coding capacity within a Tenrecidae genome identified several candidates, with one displaying placenta-specific expression as revealed by RT-PCR analysis of a large panel of Setifer setosus tissues. Cloning of this endogenous retroviral env gene demonstrated fusogenicity in an ex vivo cell-cell fusion assay on a panel of mammalian cells. Refined analysis of placental architecture and ultrastructure combined with in situ hybridization demonstrated specific expression of the gene in multinucleate cellular masses and layers at the materno-fetal interface, consistent with a role in syncytium formation. This gene, which we named "syncytin-Ten1," is conserved among Tenrecidae, with evidence of purifying selection and conservation of fusogenic activity. To our knowledge, it is the first syncytin identified to date within the ancestrally diverged Afrotheria superorder.endogenous retrovirus | envelope protein | syncytiotrophoblast | feto-maternal interface | placenta evolution T he syncytins are genes of retroviral origin that have been co-opted by their host for a function in placentation. They correspond to the envelope (env) gene of ancestral retroviruses that entered the germ line of evolutionarily distant animals and were endogenized (reviewed in refs. 1 and 2). Two such genes, syncytin-1 (3, 4) and syncytin-2 (5, 6), have been identified in simians, and distinct, unrelated ones, syncytin-A and -B (7), have been identified in muroid rodents, syncytin-Ory1 (8) in leporids, syncytin-Car1 (9) in carnivorans, and more recently, syncytinRum1 (10) in ruminants. Their canonical characteristic features leading to their designation as "syncytins" comprise (i) placentaspecific expression, (ii) cell-cell fusion activity, and (iii) conservation during the evolution of mammalian species for extended periods of time (e.g., >10 million years). Syncytin proteins are expected to participate in the formation of the placental syncytiotrophoblast (ST) at the maternal-fetal interface via fusion of the mononucleate cytotrophoblasts (CTs). Some of them also possess an immunosuppressive activity, as classically observed for infectious retroviral envelope glycoproteins, which may be involved in maternal-fetal tolerance (11). Recently, the direct involvement of syncytins in placentation has been demonstrated unambiguously through the generation of knockout mice for syncytin-A and -B (12, 13), whose embryonic placent...

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Ten-env7mentioning

confidence: 93%

See 2 more Smart Citations

Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs

Cornelis

Vernochet

Malicorne

et al. 2014

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

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“…As in many other endotheliochorial placentas (e.g. the otter shrew; Carter et al, 2006), the maternal endothelium is underlain by a prominent basement membrane. In those bats where the endothelium is lost to achieve the hemochorial condition, the membrane is retained and incorporated into the underlying layer of syncytiotrophoblast.…”

Section: Stem Species Pattern Of Chiropteramentioning

confidence: 77%

Evolution of the placenta and associated reproductive characters in bats

Carter

Mess

2008

J Exp Zool Pt B

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Recent advances in molecular phylogenetics indicate that the order Chiroptera is monophyletic and that one of four lineages of microbats (Rhinolophoidea) shares a common origin with megabats. Against this background we undertook a comprehensive analysis of placental evolution in bats. We defined a range of characters and character states associated with female reproduction, early development, placentation and the neonate. These were then mapped on a preexisting hypothesis of bat relationships that represents the current view from molecular studies. Our purpose was threefold. First, on the assumption of bat monophyly, we wished to establish the stem species pattern of extant chiropterans. Secondly, we asked whether there are derived character conditions in support of a common origin for Rhinolophoidea and the megabats. Thirdly, we looked for evolutionary character transformations that characterize higher-level clades within Chiroptera, i.e. the megabats and the four lineages of microbats. The character condition occurring in the last common ancestor of Chiroptera was unequivocal for 21 of the 25 characters included in the analysis. The data did not offer support for a megabat-rhinolophoid clade or the implication that microbats are paraphyletic. However, analysis of early development, placentation and other reproductive parameters resulted in derived character conditions for the megabats as well as for each of the four major lineages of microbats.

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Conservation of placentation during the tertiary radiation of mammals in South America

Carter

Mess

2013

Journal of Morphology

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The eutherian placenta is considered to possess great plasticity, but it is not clear how this variation reflects adaptation to different ecological niches. Because South America was isolated for most of the Tertiary, it represents a natural laboratory to examine this question. We here describe placentation in three South American groups: Xenarthra have been part of the fauna from at least the mid-Paleocene whereas caviomorph rodents and Neotropical primates are each derived from a single founder that reached South America in the Eocene and Oligocene, respectively. The common ancestor of Xenarthra had a villous, haemochorial placenta, from which the labyrinthine, endotheliochorial placenta of sloths later evolved. Placentation in Caviomorpha follows an extraordinary stable pattern, characterized by a haemomonochorial, labyrinthine and highly lobed structure with specialized growing areas. This pattern was present before arrival of these rodents in South America and enabled a successful radiation especially during the spread of grasslands. Neotropical primates have haemochorial, trabecular placentas with a specialized maternal blood supply; a pattern that contrasts with that of Old World monkeys and may have been present in the founder generation on arrival in South America. In conclusion, there is a dichotomy within Xenarthra but otherwise the ancient South American mammals do not show much variation in principal placental characters. Thus, the successful radiation of these three groups, and their adaptation to diverse ecological niches, did not require substantial alterations in placentation.

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The Fetal Membranes of the Otter Shrews and a Synapomorphy for Afrotheria

Cited by 31 publications

References 22 publications

Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs

Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs

Evolution of the placenta and associated reproductive characters in bats

Conservation of placentation during the tertiary radiation of mammals in South America

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