Glycosylation and immunocytochemistry of binucleate cells in pronghorn (Antilocapra americana, Antilocapridae) show features of both Giraffidae and Bovidae
Graphical abstract
Introduction
The pronghorn (Antilocapra americana, Antilocapridae) is an artiodactyl mammal indigenous to North America and is often referred to locally as an antelope. However, phylogenetically Antilocapridae occurs in a superfamily, Giraffoidea, with giraffes and okapi (Giraffidae). In the Pleistocene period, there were 12 taxa of the family Antilocapridae but now the pronghorn is the only extant species. It bears characteristic forked horns [1] that are covered in skin as in giraffes, but in the pronghorn this becomes a keratinous sheath which is shed and regrown on an annual basis [2].
An important feature of the ruminant placenta is the fetal chorionic binucleate cell (BNC) which migrates across the microvillous membrane to fuse with maternal cells, forming fetomaternal trinucleate cells or syncytial masses [3]. These binucleate cells contain heavily glycosylated granules which have been shown to contain placental lactogens which, on migration, pass over to the maternal circulation [4]. Recently, we showed that the placental binucleate cell (BNC) of the giraffe and okapi has a different pattern of glycosylation from other ruminant BNCs that we have studied [5]: greater malayan chevrotain (Tragulidae); fallow deer, red deer, Chinese water deer (Cervidae), domestic goat, springbok, impala, domestic cow and sheep (Bovidae) with little or no expression of terminal αN-acetylgalactosamine bound by Dolichos biflorus and Vicia villosa agglutinins which instead bind to placental blood vessels [6]. We also demonstrated different patterns of protein expression in the BNC [7].
It appeared that Giraffidae BNC developed different pathways in their glycan biosynthesis and protein expression following their split from the Bovidae, with further differences evolving as okapi and giraffe diverged from each other. Because the pronghorn-giraffe clade (or Antilocapridae-Giraffidae clade) diverged from Bovidae [8], it is possible that pronghorn BNC might be different from bovine BNC. We therefore examined placentae from six specimens in order to characterise the glycosylation and protein expression of the binucleate cells and to compare them with those from the giraffe, okapi and bovine.
Section snippets
Animals
All procedures for collection of animals and tissues were approved by the Fort Keogh Institutional Animal Care and Use Committee (IACUC No. 032415-1). The six pronghorn placental samples (Table 1) were collected and fixed within 20 min after death as part of a wider investigation of pronghorn biology carried out in eastern Montana. Whole placentomes, consisting of fetal cotyledons in close association via microvillous interdigitation with maternal caruncles that form button-like outgrowths on
General structure of the placentome
As in all ruminant placentomes, development starts from a flat apposition of trophoblast and uterine epithelium. Mutual growth of the fetal and maternal layers produces placentomes consisting of chorionic villi interdigitating with maternal villi. The fetal digitiform primary villi branch off short, leaf-like secondary villi at right angles to the primary ones while the endometrial villi contain secondary villi to house the secondary fetal villi (Fig. 1A and B). The maternal villi are covered
Discussion
The position of the pronghorn in relation to the Cervidae, Bovidae and Giraffidae has been disputed for some time. The pronghorn is Bovid- and Giraffoid-like in that they both have permanent bony horns and not annually grown and shed antlers like all Cervids. In addition Bovids and Giraffids have over fifty placentomes per placenta, whereas Cervids rarely have more than five or six; in pronghorn the number ranges from 46 to 180, with an average of 92 [15]. However, most anatomical characters
Conflict of interest
We wish to confirm that there are no conflict of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Acknowledgement
The authors would like to express their appreciation of the contribution of Professor William Joseph Silvia (1956–2015) who unfortunately passed away before finalisation of the paper. He was born in Providence, Rhode Island and obtained his undergraduate degree in Animal Science at Cornell University followed by an MSc in Reproductive Physiology (West Virginia University) and PhD in Reproductive Endocrinology (Colorado State University). Dr Silvia was a passionate and untiring scholar of
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