Glycosylation at the Fetomaternal Interface in Hemomonochorial Placentae from Five Widely Separated Species of Mammal: Is There Evidence for Convergent Evolution?

Abstract

Hemomonochorial placentation occurs in diverse species. We have examined placental glycosylation in five widely separated mammals with this type of placentation – lesser hedgehog tenrec (Echinops telfairi), spotted hyena (Crocuta crocuta), nine-banded armadillo (Dasypus novemcinctus), human (Homo sapiens) and guinea pig (Cavia porcellus) – in order to assess whether evolutionary convergence to the hemomonochorial state is accompanied by a similar convergence of glycan expression. Placentae from 2 E. telfairi, 3 C. crocuta, 1 D. novemcinctus, 4 womenand 1 C. porcellus were fixed and processed into epoxy resin. Binding of twenty-three lectins was assessed using a semiquantitative ranking system. The trophoblast apical/microvillous membrane of all five species showed marked similarities in glycosylation. In the N-linked series, there were abundant bi/tri-antennary complex chains, while the non-bisected variants were much scarcer. All species had plentiful N-acetyl lactosamine sequences; at chain termini, binding to Galβ1,4GlcNAc and Galβ1,3GalNAc sequences was greatly enhanced after neuraminidase treatment. In all species, terminal NeuNAcα2,3 residues were detected. The tenrec had unusually abundant terminal N-acetyl galactosamine. The basal plasma membrane/basal lamina showed glycosylation patterns distinct from the microvillous membrane in each case, indicating chemical diversity of the two opposite faces of trophoblast. Similar classes of glycan at the hemochorial interface suggest conservation of function. The observed lectin binding patterns suggest broad similarities of glycosylation that may have arisen by convergent evolution.

Adhesion Molecules in Human Trophoblast – A Review. I. Villous Trophoblast

“…Siglec-6 immunolocalises to the syncytial MVM in human term placenta [50]. Though lectin histochemistry has suggested that human term placenta has rather low levels of terminal α2,6-linked sialic acid, showing more α2,3-linkages [51], trophoblast (including the extravillous population) does contain glycoproteins with siglec-6 recognition capacity. Siglec-6 also binds leptin [50]; thus, the siglec-6 binding site in villous trophoblast may be occupied by cis-ligands.…”

Glycosylation at the fetomaternal interface: does the glycocode play a critical role in implantation?

“…The presence of Siglec-6 at the syncytial surface suggests the possibility that cis-interactions with sialylated ligands in the trophoblast may contribute to plasma membrane organisation [46]. There appears to be convergent evolution of glycosylation at this tissue-blood interface [47]. Five widely separated species of mammal with hemochorial placentation (lesser hedgehog tenrec Echinops telfairi, spotted hyena Crocuta crocuta, nine-banded armadillo Dasypus novemcinctus, human Homo sapiens and guinea pig Cavia porcellus) have marked similarities in glycosylation of the trophoblast apical/microvillous membrane.…”

Placentation in the Hottentot Golden Mole, Amblysomus hottentotus (Afrosoricida: Chrysochloridae)

“…The inner trophoblast layer exhibited an increase in non-bisected bi/tri-antennary complex N-glycan (PSA) as well as N-acetyl galactosamine (SBA) and glucosamine oligomers (WGA) with maturity, but other changes were of a minor degree. Sialic acid in a2,3-linkage, bound by MAA, was not found in the trophoblast at any stage, which is unusual for haemochorial placentae [23], while fucosyl residues in a1,2-linkage were also weak or absent, as shown by the lack of binding of LTA and UEA-1. The difference in glycosylation between the two microvillous surfaces may reflect altered functional requirements.…”

“…Non-osmicated plastic embedded specimens were sectioned at 0.75 mm and stained with a panel of 24 biotinylated lectins, followed by an avidin-peroxidase revealing system as previously described [22,23]. Sections were assessed using a semiquantitative ranking system where staining intensity was allocated a grade from 0 (negative) to 4 (intense staining).…”

“…One is adjacent to maternal blood and may therefore require higher levels of sialylation with increased negative charge to block adherence and/ or immunorecognition by maternal lymphocytes, while the interface between the inner and outer trophoblast may involve mechanisms of interepithelial adhesion (selectins, galectins) and as such exhibit different properties. An unusual attribute shared between Amblysomus and the tenrec Echinops is the presence of WFA-and VVA-binding N-acetyl galactosamine residues in the trophoblast, which is not seen in haemochorial placentae of non-tenrecoid mammals (human, armadillo, hyena, guinea pig) [23]. There are, however, important differences between tenrec and golden mole glycosylation in that strong staining with DBA in the cytotrophoblast of the labyrinth in Echinops is absent in Amblysomus and SBA, WGA, PAA and BSA-1B 4 staining, which is prominent in the Amblysomus labyrinth, is virtually absent in that of Echinops.…”