Comparative Placentation and Animal Models: Patterns of Trophoblast Invasion – A Workshop Report

Abstract

Keywords: Epitheliochorial placentation; Endotheliochorial placentation; Haemochorial placentation; Placenta;TrophoblastINTRODUCTIONThe degree of trophoblast invasion is very variable betweenspecies [1]. However, the factors influencing it, and benefitsderiving from it, are little understood. In the epitheliochorialplacentation of pig, camel, and horse, trophoblast microvilliinterdigitate with those of the maternal uterine epithelium,and there is no trophoblast invasion as such. One modificationof this is synepitheliochorial placentation where some special-ised trophoblast cells detach and migrate through to the mater-nal epithelium and fuse with it, as is seen in ovine and bovineplacentae. Another is the trophoblast girdle cell invasion intothe endometrium to form the cups in the early horse placenta.In endotheliochorial placentation there is some invasion intothe maternal stroma, stopping short at maternal blood vessels,while the most invasive form is haemochorial, found in human,rodent, bat and other species, where the maternal endotheliumis stripped away so that the trophoblast is in direct contactwith maternal blood. There is at present some controversyabout which form is the most primitive and what evolutionarypressures influenced the development of the different placentaltypes [2,3].In order to understand these systems and their relevance tohuman pregnancy, it is important to examine the modes of pla-centation of various other species. The contributors to thisworkshop covered many different facets of this subject aswell as a wide range of animals, from the elephant to themouse.CONTRASTING PATTERNS OF TROPHOBLASTINVASION IN THE RAT AND MOUSER. Pijnenborg discussed work done with L. Vercruysse, andshowed how, as in the human, both rat and mouse have twopathways of trophoblast invasion, a vascular and an interstitialpathway. Vascular invasion in the mouse is limited to the de-cidua, and follows a perivascular route, showing gradual re-placement of the endothelium from the outside. Vascularsmooth muscle is absent in decidua, and much thinned inthe noninvaded mesometrial triangle. The remodelling istherefore independent of trophoblast. Areas of intense vascularremodelling are associated with high numbers of uterine natu-ral killer (uNK) cells which, when underdeveloped, allow peri-vascular trophoblast invasion into the distal decidua [4],suggesting a possible reciprocal relationship between tropho-blast invasion and uNK cell distribution. In contrast, vascularinvasion in the rat extends into the mesometrial triangle, isendovascular, and is followed by endothelial replacementfrom the inside, while the thinned vascular smooth muscle layershows severe fragmentation [5]. In the mesometrial triangle ofdeciduomata (without trophoblast) vascular smooth muscleshows similar thinning as in mice. Further muscle breakdownin placental sites of the rat is clearly associated with tropho-blast. In the rat, uNK distribution is more associated withthe spiral arteries than in the mouse, but might have a similarfunction in initial vascular remodelling. Rat spiral arterychanges include fibrinoid deposition between trophoblast andvessel wall and, as in the human, re-endothelialization aftermural incorporation of invaded trophoblast. Interstitial inva-sion follows vascular invasion and arises from trophospongialglycogen cells in both species. However, deep interstitial inva-sion beyond the decidua occurs only in the rat, extending intothe mesometrial triangle from day 16 and filling most of itfrom day 18 onwards [6].