Search

An overview is given of variations in placentation with particular focus on yolk sac, paraplacenta, and other structures important to histotrophic nutrition. The placenta proper varies in general shape, internal structure, and the number of tissues in the interhemal barrier. Yolk sac membranes persist to term in insectivores, colugos, rodents, and lagomorphs. In the latter two orders, they are of known importance for maternal-fetal transfer of antibodies, vitamins, lipids, and proteins. The detached yolk sac of bats is also active throughout gestation. A vascular paraplacenta, or smooth chorioallantois, has known functions in ruminants and carnivores and is found in several other orders of mammal where its function has yet to be explored. In human gestation, the chorion (avascular chorioallantois) is important for hormone synthesis. The true chorion of squirrels and hedgehogs is avascular but may nevertheless allow transfer from mother to fetus through the exocelom. Hemophagous areas with columnar trophoblast are paraplacental structures in carnivores and elephants but occur also within the placenta as in hyenas and moles. In shrews, it is the yolk sac that ingests and processes red cells. Areolas and chorionic vesicles are other structures important for absorption of uterine secretions and ingestion of cellular debris. In conclusion, we find that paraplacental structures, while showing less variation than the placenta proper, contribute not just to the integrity of overall placentation, but in various ways to maternal-fetal interrelationships., (Copyright © 2016 Elsevier Inc. All rights reserved.)

Background: Transmission electron microscopy (TEM) was first applied to study placental ultrastructure in the 1950's. We review those early studies and mention the scientists that employed or encouraged the use of TEM., Findings: Among the pioneers Edward W. Dempsey was a key figure who attracted many other scientists to Washington University in St. Louis. Work on human placental ultrastructure was initiated at Cambridge and Kyoto whilst domestic animals were initially studied by Björkman in Stockholm and electron micrographs of bat placenta were published by Wimsatt of Cornell University., Conclusions: Prior to the introduction of better fixation techniques, TEM images were of modest technical quality. Nevertheless they gave important insights into placental ultrastructure, particularly the nature of the maternal-fetal interface., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Introduction: The Laotian rock rat is a relict species in a sister group relationship to hystricognath rodents (Hystricognathi). We asked whether there were similarities in placentation that might reflect this relationship or differences that might cast light on the evolution of Hystricognathi., Methods: We examined the reproductive tract of nonpregnant (n = 5), early (n = 3) and mid to late gestation (n = 2) females. Selected characters were mapped to a phylogenetic tree to examine their evolution in rodents., Results: The chorionic placenta was discoid and labyrinthine with a spongy zone but without internal lobes. The interhemal region was hemodichorial with syncytiotrophoblast lining maternal blood spaces and an inner layer of vacuolated cytotrophoblast. There was no subplacenta. The yolk sac was well developed with a villous portion that faced the placental disk but no fibrovascular ring. There was a single fetus that very likely would be precocial at birth., Discussion: A lobulated labyrinth and the presence of a subplacenta and a fibrovascular ring emerged as synapomorphies for Hystricognathi. Laonastes, Ctenodactylus and stem Hystricognathi all had precocial young, whereas altriciality was the plesiomorphic condition for rodents. A hemomonochorial interhemal region was plesiomorphic for rodents and Hystricognathi, and the hemodichorial condition found in Laonastes, and possibly in Ctenodactylus, was unlike that of any rodent studied to date., Conclusion: Similar to Hystricognathi, Laonastes bears precocial young, but this species lacks placental adaptations such as the subplacenta, suggesting they were evolved subsequent to a change in reproductive strategy in the common ancestor of Laonastes and Hystricognathi., (Copyright © 2013 Elsevier Ltd. All rights reserved.)

The distribution of cytokeratin-positive interstitial trophoblast cells in the endometrium of the macaque during placental development was examined. Such cells are moderately abundant only from the 15th through the 22th day of pregnancy, although there is considerable individual variation. During this period of gestation, interstitial trophoblast cells are distributed in the perivascular stroma immediately surrounding spiral arteries, including coils of arteries already invaded by endovascular trophoblast. The interstitial trophoblast cells are not seen to directly intrude into the smooth muscle of the spiral arteries. Very few interstitial trophoblast cells are present from days 12 through 14 of gestation when the arteries are first invaded by endovascular trophoblast. Even fewer interstitial trophoblast cells are seen after day 30 of gestation. The brief time in gestation when interstitial trophoblast cells are abundant coincides with a time when spiral arteries are undergoing rapid modification into patent uteroplacental arteries. It is suggested that during this period, the interstitial trophoblast cells may facilitate changes in shape of the spiral arteries by alterations of the perivascular connective tissue, perhaps through interactions with other cellular constituents rather than by directly modifying the arteries per se., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

Endotheliochorial placentas occur in orders from all four major clades of eutherian mammal. Species with this type of placenta include one of the smallest (pygmy shrew) and largest (African elephant) land mammals. The endotheliochorial placenta as a definitive form has an interhemal area consisting of maternal endothelium, interstitial lamina, trophoblast, individual or conjoint basal laminas, and fetal endothelium. We commonly think of such placentas as having hypertrophied maternal endothelium with abundant rough endoplasmic reticulum (rER), and as having hemophagous regions. Considering them as a whole, the trophoblast may be syncytial or cellular, fenestrated or nonfenestrated, and there may or may not be hemophagous regions. Variations also appear in the extent of hypertrophy of the maternal endothelium and in the abundance of rER in these cells. This combination of traits and a few other features produces many morphological variants. In addition to endotheliochorial as a definitive condition, a transitory endotheliochorial condition may appear in the course of forming a hemochorial placenta. In some emballonurid bats the early endotheliochorial placenta has two layers of trophoblast, but the definitive placenta lacks an outer syncytial trophoblast layer. In mollosid bats a well developed endotheliochorial placenta is present for a short time even after a definitive hemochorial placenta has developed in a different region. It is concluded that the endotheliochorial placenta is more widespread and diversified than originally thought, with the variant with cellular trophoblast in particular appearing in several species studied recently., (Copyright © 2012. Published by Elsevier Ltd.)

The way in which maternal blood is associated with trophoblast prior to the formation of the different types of hemochorial placenta may be conveniently grouped into four main patterns: a transitory endotheliochorial condition; maternal blood released into a mass of trophoblast; maternal blood confined to lacunae; and fetal villi entering preexisting maternal blood sinuses. Although it might be considered logical that developing placentas would pass through an endotheliochorial stage to become hemochorial, this developmental pattern is seen only as a transient stage in several species of bats and sciuromorph rodents. More commonly a mass of trophoblast at the junction with the endometrium serves as a meshwork through which maternal blood passes, with subsequent organization of a labyrinth when the fetal vascular component is organized. The initial trophoblast meshwork may be cellular or syncytial, often leading to a similar relationship in the spongy zone and labyrinth. Old World monkeys, apes and humans have a lacunar stage prior to establishing a villous hemochorial condition. New World monkeys lack a true lacunar stage, retaining portions of maternal vessels for some time and initially forming a trabecular arrangement similar to though differently arrived at than that in the tarsier. In armadillos, preexisting maternal venous sinuses are converted into an intervillous blood space by intruding fetal villi. Variations from the major patterns of development also occur. The way in which the definitive placental form is achieved developmentally should be considered when using placental structure to extrapolate evolution of placentation., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

Bats are a highly successful, widely distributed group, with considerable variation in placental structure. The Egyptian slit-faced bat Nycteris thebaica is a member of one of the few families with previously undescribed placentation. It was found that, although the interhemal type of the Nycteris placenta is endotheliochorial with a single layer of cytotrophoblast, the arborizing pattern of the maternal vessels and especially the extraordinary major placental artery differs from the placenta of the emballonurid bats to which this family is considered to be most closely related. The major placental artery providing maternal blood to the vessels of the placental disk has a highly glycosylated matrix surrounded by two-layered folds of trophoblast, forming an apparently rigid structure of unique morphology. The yolk sac is collapsed, with hypertrophied endodermal and mesothelial cells similar to many other bat species. The paraplacenta is extensive with abundant fetal vessels underlying cytotrophoblast and syncytial trophoblast layers, fronting on an endometrium that largely lacks uterine epithelial cells but has large decidual cells and is poorly vascularized. The placenta of Nycteris lacks a hemophagous region, unlike the emballonurid bats Taphozous and Saccopteryx. Although the latter two species have similar placentas, the placental structure of Nycteris does little to relate it to the other family within the Emballonuroidea. Shared and divergent reproductive characters are discussed in relationship to bat phylogenetic relationships.

The placentation of the Hottentot golden mole (Amblysomus hottentotus) has been examined using light and electron microscopy and lectin histochemistry of nine specimens at both mid and late gestation. The placentae were lobulated towards the allantoic surface and the lobules contained roughly parallel arrays of labyrinthine structures converging on a central spongy zone. At mid gestation, the arrays were composed of an inner cellular and outer syncytial trophoblast layer, the inner layer enclosing scant connective tissue and fetal capillaries. Maternal blood spaces coursed through the outer trophoblast and were lined by trophoblastic microvilli; the blood spaces were narrow in mid gestation but enlarged near term, while the inner trophoblast layer became thinner and seemed to be syncytial. These features were confirmed by transmission electron microscopy. The microvillous surfaces and dispersed cytoplasmic particles were heavily glycosylated, as shown by lectin histochemistry, and exhibited changes with maturation, particularly a loss in N-acetyl glucosamine oligomers bound by Phytolacca americana lectin on the microvilli lining the maternal blood spaces and outer trophoblast particles. A substantial yolk sac was present both in mid and late gestation stages. It was clearly unattached to the uterus in the later stages. These morphological features are discussed in relation to the phylogenetic position of Amblysomus with respect to other members of Afrosoricida and Afrotheria.

Many early embryonic stages are nearly indistinguishable in different Eutheria. However, implantation stages and placental morphological types vary tremendously. A number of factors favor this conflicting diversity. 1. Whereas embryo development takes place in the isolation of the amniotic cavity, the extraembryonic membranes of the conceptus develop in close association with the uterus of a genetically different organism. 2. Early conditions for the developing conceptus are anaerobic whereas later in development efficient aerobic conditions are essential for continued growth of the fetus. 3. Developing extraembryonic membranes have the potential to form two partially sequential placentas. The yolk sac can participate in forming a choriovitelline placenta, including an interhemal region, and can be adapted to various non-respiratory functions as gestation proceeds. Development of the chorioallantoic placenta begins later than the choriovitelline placenta but can overlap with this before supplanting it. The original development of the extraembryonic membranes occurs when the conceptus is sufficiently small that neither its nutritional requirements nor its respiratory needs are the burden to the maternal organism that they are later in gestation. Despite these developmental factors promoting different methods of forming the definitive placenta, the placental type is consistent within most families indicating that the divergence in placental structure accompanied evolution of differences between groups.

The reproductive tract was examined in four non-pregnant and two gravid specimens of Myzopoda. The ovaries had little interstitial tissue. The uterus was bicornuate and the lenticular placental disk was situated mesometrially in one horn. The interhaemal barrier of the placental labyrinth was of the endotheliomonochorial type. There was a single layer of trophoblast cells. The cells of the maternal endothelium were large and basophilic, contained abundant rough endoplasmic reticulum, and rested on an irregular basement membrane. Blunt projections of endometrium extended into the placental disk and clusters of large cells occurred between the endometrial stroma and labyrinth. At the margins of the disk folds of trophoblast occurred and at the cranial end they formed an haemophagous region. The folds lateral to the disk included some peculiar tubular-appearing structures. There was a persistent yolk sac containing large endodermal cells around a largely collapsed lumen. Several features of placentation, such as the interhaemal barrier and the haemophagous region, are consistent with an association of Myzopodidae with Emballonuridae. No support was found for alternative hypotheses that include Myzopodidae in the noctilionoid or vespertilionoid lineages.

Data accumulated over several years of investigating implantation in macaque monkeys have been used to estimate the rate of expansion of the initial implantation site, the increase in volume of the site, and the rate of arterial invasion by cytotrophoblast columns. In addition the expansion of the secondary implantation site has also been estimated. The primary implantation site expands from an average diameter of 0.268 mm on day 10 to 4.93 mm on day 16-17. It expands in thickness from 0.064 mm on day 10 to 0.96 mm on day 16-17, and in volume from 0.0036 mm(3) on day 10 to 18.34 mm(3) on day 16-17. During this period of rapid expansion in extent and volume of the implantation site, trophoblast invades the endometrium, forms a lacunar stage, and initiates villus formation; consequently these very considerable changes in structure occur when the implantation is still very small yet growing rapidly. The secondary site expands from 0.23 mm in diameter on day 12 to 2.8mm on day 17. The rate of penetration of cytotrophoblast into endometrial arteries diminishes from 0.602 mm per day on day 12 to 0.171 mm per day on day 16, using the straight-line method of estimation. This diminution in rate is consistent with the hypothesis that cytotrophoblast cells generated at the anchoring villi migrate over cytotrophoblast cells that have attached to the endothelium of the endometrial arteries in advancing the intraluminal columns of trophoblast. It is hoped that the summaries provided will be useful to investigators using macaque monkeys to analyze aspects of implantation in primates.

Placentation in tenrecs of the subfamily Oryzorictinae, family Tenrecidae, has not been described previously. The structure of the placenta of this group and especially of the genus Microgale was investigated to determine its similarity or dissimilarity to previously described placentas of the tenrec subfamilies Potamogalinae and Tenrecinae. Fifteen specimens of the genus Microgale ranging from an early yolk sac stage to near term were available for study. Placentation in Microgale was found to be different from other tenrecids in that there is an early simple lateral rather than central haemophagous region. In addition, a more villous portion of the placental disk forms before the formation of a more compact labyrinth. Although the definitive placenta is cellular haemomonochorial, it lacks the spongy zone found in the Tenrecinae. Neither does it resemble the endotheliochorial condition found in the Potamogalinae. Of the two genera of the subfamily Oryzorictinae represented by single specimens, the placenta of Limnogale resembled that of the Microgale but Oryzorictes had several differences including a lobulated placental disk. It is concluded that there is more variation in placentation both within the subfamily Oryzorictinae and within the family Tenrecidae than would ordinarily be expected.

The present study determined whether estrogen plays a role in regulating invasion and remodeling of the uterine spiral arteries by extravillous trophoblasts during early baboon pregnancy. The level of trophoblast invasion of spiral arteries was assessed on day 60 of gestation (term is 184 days) in baboons untreated or treated on days 25-59 with estradiol or aromatizable androstenedione. The administration of estradiol or androstenedione increased (P<0.01) maternal serum estradiol levels approximately 3-fold above normal. The mean+/-SE percentage of spiral arteries/arterioles invaded by extravillous cytotrophoblasts in estradiol-treated baboons for vessels with diameters of 26-50 microm (0.0+/-0.0), 51-100 microm (1.2+/-0.7) and >100 microm (13.2+/-5.5) was 100%, 90%, and 75% lower (P<0.001), respectively, than in untreated baboons (2.4+/-1.2%; 11.0+/-5.5%, and 54.5+/-8.5%, respectively). Similar results were obtained with androstenedione treatment. However, the distribution of uterine spiral arteries grouped by diameter or number of arteries per basal plate area, i.e. microvessel density, were similar in untreated and estrogen-treated baboons. We suggest, therefore, that the low levels of estrogen exhibited during early primate pregnancy are required to permit normal progression of trophoblast vascular invasion and that the surge in estrogen which occurs during the second-third of normal pregnancy has a physiological role in suppressing further arterial trophoblast invasion. Consequently, we propose that the estrogen-dependent restraint of spiral artery invasion/remodeling ensures optimal blood flow dynamics across the uteroplacental vascular bed to promote normal fetal growth and development.

In considering the diversity of Eutherian mammalian placental structure, it is helpful to keep in mind that both phylogenetically and ontogenetically a functional yolk sac placenta precedes development of the chorioallantoic placenta. Usually the chorioallantoic placenta progressively displaces the area of contact of the yolk sac placenta with the endometrium. It is also closely applied to the endometrium, increasing respiratory efficiency but tending to decrease histotrophic nutrition. Catarrhine primates have minimal histotrophic uptake, using haemotrophic mechanisms throughout most of gestation. Rodents, by using partial or complete inversion of the yolk sac, have extensive regions available to histotroph in later pregnancy. Most mammals, however, have developed specialized regions of the chorioallantoic placenta for ingestion of uterine secretions, cell debris and erythrocytes. These regions vary from simple saccular areolae to more complex areolae such as the chorionic vesicles of prosimian primates to specialized haemophagous areas. All such structures are consistently lined by columnar cellular trophoblast. Examples of these structures, many of which can ingest both glandular secretions and erythrocytes (i.e. they are heterophagous), can be found in species whose definitive placenta is epitheliochorial. They are common but not universal in species whose definitive placenta is endotheliochorial and are even found in a few species with definitive haemochorial placentas. Restriction of phagocytosis to regions of columnar cells provides polarized cells appropriately oriented for ingestion, breakdown and transport, and limits the type of ingestion of both beneficial and potentially toxic materials to expendable individual cells.

The otter shrews of mainland Africa are the closest relatives of the Madagascar tenrecs. We sought for similarities in placentation between the two groups and, in a wider context, with other mammals of the Afrotheria clade. Specimens of the Nimba otter shrew (Micropotamogale lamottei) were obtained from the Ivory Coast and examples of the giant otter shrew (Potamogale velox) from the Hill Collection. The Nimba otter shrew has a central haemophagous organ similar to that in tenrecs. The labyrinth of the Nimba otter shrew, however, is endotheliochorial with syncytial trophoblast enclosing the maternal vessels. On the other hand tenrecs have cellular haemomonochorial placentae and an associated spongy zone, which is not present in the Nimba otter shrew. The placenta of the giant otter shrew is also endotheliochorial. The central region of its placenta is particularly interesting, since the juxtafetal portion is clearly a haemophagous region whereas the labyrinth feeding this region is endotheliochorial. Thus there is considerable variation in placental morphology within Tenrecidae. Importantly, however, both otter shrews have a large allantoic sac divided into four intercommunicating lobes by two pairs of septal folds. A similar arrangement has been described for representatives of each of the remaining five orders within Afrotheria. This is significant because previous anatomical studies have failed to establish a single synapomorphy in support of Afrotheria.

Our purpose was to determine how the central haemophagous region and cellular haemomonochorial labyrinth of the tenrec placenta are formed. The haemophagous region is preceded by a region of invasion of the endometrium by trophoblast comprising a cytotrophoblast layer covered by syncytial trophoblast and contiguous with numerous masses of multinucleate trophoblast. The trophoblast intrudes into the endometrium, eliminating the stroma, although small vessels and clumps of glandular epithelium persist. This extensive central region is connected to the forming disk by a ring of chorioallantois covered by a single layer of columnar trophoblast. Later the multinucleate masses and syncytial trophoblast degenerate. The unilaminar cytotrophoblast remains, is elaborated into folds, and phagocytoses glandular secretion, cell debris and erythrocytes. As the central area is transforming, fetal capillaries move into the cytotrophoblast pads surrounding the central zone. Prior to this, the cytotrophoblast has formed a multilayered structure and interrupted maternal vessels to create an anastomotic network of blood spaces lined by cytotrophoblast. The invasion of fetal capillaries transforms this preplacental pad into a cellular haemomonochorial labyrinth with the uninvaded portion forming an underlying spongy zone. Thus interaction of the trophoblast with the endometrium is substantially different in the central zone compared to the area of the preplacental pad., ((c) Elsevier Ltd. All rights reserved.)

The diversity of placental structures in Eutherian mammals is such that drawing generalizations from the definitive forms is problematic. There are always areas of reduced interhaemal distance whether the placenta is epitheliochorial, synepitheliochorial, endotheliochorial or haemochorial. However, the thinning may be achieved by different means. The presence of a haemophagous area as an iron transport facilitator is generally associated with endotheliochorial placentae but is also found in sheep and goats (synepitheliochorial) and in tenrecs and hyaenas (haemochorial). Although similar chorioallantoic placentae are found within families, structure begins to diverge at the ordinal level and there is little correlation at the supraordinal level of phylogeny. Differences in formation and function of the yolk sac provide additional variation. There would appear to be considerable adaptive pressure for development or retention of the haemochorial type of chorioallantoic placenta. This type of placenta has several possible drawbacks including more ready passage of fetal cells to the maternal organism and, should the haemochorial condition be achieved early, oxidative stress. At any rate no animal larger than the human and gorilla has this type of placenta. The endotheliochorial condition is found in animals as large as the bears, manatee and elephants. In addition to the ungulates, the epitheliochorial condition is present in the largest animals with the longest gestation periods, the whales. Considering the length of time since the early stages of mammalian evolution, it is probable that few unmodified structural features are present in any currently surviving mammal. Nevertheless, more complete studies of divergent types of mammalian placenta should help our understanding of mammalian interrelationships as well as placental function.

Until recently, tenrecs were classified with insectivores in the order Lipotyphla, but nucleotide sequence data suggest they have closer affinities with a group of African mammals called Afrotheria. The placenta of Echinops has not been described and no studies involving electron microscopy of the placenta of any species of tenrec have been published. We used light and transmission electron microscopy to examine fixed placentae of embryos ranging from 25-66 mm in length. The placental disk is situated in the antimesometrial portion of the bicornuate uterus. The greater part of the disk consists of a labyrinth underlain by a spongy zone. The interhaemal barrier is unusual in that the trophoblastic component is a single layer of cytotrophoblast. These trophoblast cells have thick areas especially near the nuclei and extensive thin flanges but only occasionally have membrane-closed pore regions. The luminal surface has isolated patches of microvilli, and pinocytotic vesicles are numerous both apically and basally. In the centre of the placental disk is an elaborately folded haemophagous region. The primary folds have allantoic endoderm at one surface and columnar cytotrophoblast at the other. These trophoblast cells have numerous lipid droplets and vesicles, and often contain large yellow pigment crystalloids. The labyrinthine zone ends abruptly at the margins of the placental disk. However, the endoderm and connective tissue of the allantois and a layer of cytotrophoblast extend beyond the placental disk as a paraplacental region. Some of these distinctive features of Echinops placenta are shared with individual afrotherians, but no significant characteristic of definitive placentation is shared by all the Afrotheria.

An individual embryo from day 15 of gestation in the rhesus monkey showed partial separation of the cranial end of the embryonic shield into two separate cell masses with separate amnions but with a common yolk sac. Although what the fate of this conceptus might have been is not known, it demonstrates that the physical features of implantation in this primate are permissive of relatively late division of the epiblast, which suggests that monozygotic twinning may occur as late as the embryonic shield stage just prior to primitive streak formation., (Copyright 2002 Elsevier Science Ltd.)

In the course of a study on reproduction in the nine-banded armadillo, conceptuses between the beginning of implantation and primitive streak formation were examined to determine the manner of trophoblast differentiation during invasion of the endometrium and the sequence involved in formation of four identical quadruplets. The armadillo blastocyst implants in the fundic recess of the uterus. A single amnion and cup-shaped epiblastic plate are formed, and an exocelom develops between the amnion and trophoblast of the implantation site. Loss of the abembryonic trophoblast exposes both visceral and parietal endoderm to the uterine lumen, inverting the yolk sac. Continued expansion of the exocelom facilitates the intrusion of the forming conceptus into the uterine lumen and is accompanied by enlargement of the epiblastic plate. Separate areas of condensations of epiblast cells are the first indication of formation of the four identical quadruplets. The single layer of microvillous trophoblast with basal infoldings (designated absorptive trophoblast) is most likely to contribute extensively to movement of fluid into the exocelom. The resulting expansion of the exocelom not only enlarges the implantation site but also displaces the collapsing common amnion, limiting the amnion to the areas of the forming embryos., (Copyright 2002 Harcourt Publishers Ltd.)

The development of the baboon anchoring villus has been studied from day 14 to day 48 of gestation, using light and electron microscopy. At day 14, cords of trophoblast could be seen streaming into the endometrium, invading maternal vessels and forming blood-filled lacunae; by 20 days gestation some of these had differentiated into distinctive anchoring villi, with an outer covering of syncytiotrophoblast and inner cytotrophoblast cells which differed from those of floating villi in that a subpopulation detached from the syncytium to form an interconnecting network of cells within the centre of the villus. Subsequent migration of cytotrophoblast into the endometrium formed the cytotrophoblastic shell while fibrillin-like extracellular matrix biosynthesis within the body of the villus provided a firm mechanical support. At the trophoblast-decidual interface, a zone of necrosis and phagocytosis initially developed, which became less extensive with time, so that by 40 days a stable interface was evident with only residual pockets of necrosis. During this period, there was differentiation of decidual cells which by 28 days developed characteristic pedunculated cell processes, and later became surrounded by a basal lamina. The factors that control detachment of cytotrophoblast from the syncytium and the biosynthesis of the specialized, fibrillar extracellular matrix, features that are not apparent in other placental villi, require further investigation, possibly by carefully controlled in vitro experimentation., (Copyright 2001 Harcourt Publishers Ltd.)

Anchoring villi of first trimester placentae of the macaque, baboon and human were examined by light and electron microscopy. The anchoring villi of the baboon and macaque are similar in having more elongated cell columns than those of the human and in having more extracellular matrix between cytotrophoblast cells. These species also have a thicker and more uniform trophoblastic shell. The generative region of cytotrophoblast cells adjacent to the villous mesenchyme is similar in all three species, with the aspect of the core abutting this area being lined by a thickened basal lamina. Similarly, migratory cytotrophoblast cells form extracellular matrix in all three species, but matrix-rich regions of the anchoring villi and shell are more extensive in the non-human primates. The extracellular matrix and especially the material resembling fibrillin may serve to strengthen the villi, particularly the elongated villi of the non-human primate, and also may prevent maternal cells migrating into the trophoblastic shell. The baboon and macaque cytotrophoblast cells that form this matrix tend to be linked by gap and desmosomal junctions and are in contiguous arrays, whereas those in the human that are blocked from reaching normal decidua form abundant extracellular matrix but have no gap junctions. Whether the lack of extensive invasion of the endometrium by baboon and macaque cytotrophoblast cells is related to the increased amount of extracellular matrix, their greater distance from the mesenchymal core, or their intercellular linkages is not known. The investigation of isolated villi from the macaque or baboon, as has been extensively carried out in the human, might help to determine whether the cytotrophoblast cells are intrinsically different or are responding to different environmental cues., (Copyright 2001 Harcourt Publishers Ltd.)

The free allantois and allantochorion of conceptuses from 17 mares between 20 and 90 days of gestation were examined to determine the manner in which the associated mesodermal derivatives differentiated. It was found that a robust basement membrane developed under the allantoic endoderm, and that this basement membrane was partially isolated from the vascular layer of the allantois by a mesothelial layer and an exocelom-like space. The exocelom-like space persisted until approximately the stage of villous formation, and remnants of the space persisted over larger allantoic vessels even later. It is suggested that originally the presence of the mesothelial layer facilitates type I collagen formation in the thick basement membrane under the basal lamina of the allantoic endoderm. The basement membrane maintains the integrity of the allantois while the underlying space allows some slippage between the allantois and its vascular layer which is more closely associated with the endometrial and exocelomic surfaces, respectively., (Copyright 2000 Harcourt Publishers Ltd.)

Using lectin histochemistry on plastic-embedded material, the glycosylation patterns of equine girdle and cup cells, and associated endometrial glands, have been investigated from 37 to 67 days gestation. Results were compared with the glycosylation of the 50-day allantochorionic trophoblast of the established equine placenta that will later form the microcotyledons. The differentiated cup cells, which secrete equine chorionic gonadotropin (eCG), showed a pattern of glycosylation that was distinct both from the progenitor girdle cells and the allantochorionic trophoblast, with granules that bound lectins indicating high levels of alpha2,6 and alpha2,3-linked sialic acid, N-acetyllactosamine and bi/tri antennary non-bisected and bisected complex N-glycan. This is consistent with the known carbohydrate content of eCG. In contrast, the allantochorionic trophoblast at 50 days lacked detectable amounts of sialic acid and showed high levels of tri/tetra-antennary non-bisected complex N-glycan and N-acetyl galactosamine which was absent in the cup cells. During the process of girdle cell migration into maternal tissues, the uterine glands became greatly enlarged and dilated basally, with increased amounts of glycosylated secretory products revealed by lectins, which often seeped out into the extracellular space via ruptures in the apical regions of the gland wall.

The hypothesis that fibrin type fibrinoid deposition on villi is unique to the term human placenta was tested. Bright-field microscopy was used to examine sections of first and second trimester human placental villi and tissues from three animal species that have villous haemochorial placentae similar to the human: the armadillo, the baboon and the rhesus. Sections stained with haematoxylin and eosin showed fibrin type fibrinoid deposits were hypocellular, eosinophilic masses attached to the surface of villi examined from both the human and the animal species. The deposits were located at discontinuities in the syncytiotrophoblast layer, and the fibrinoid provided a matrix for trophoblast re-epithelization of the villous surface. It is concluded that fibrin-type fibrinoid is not unique to the term human placenta. The presence of the syncytiotrophoblast discontinuities associated with the fibrinoid deposition must be considered in models of maternal-fetal exchange in the villous haemochorial placenta.

Pregnancy-specific beta 1-glycoprotein (SP1) is found in maternal serum very early in gestation in both human and non-human primates. As judged by light microscopic immunocytochemistry, the major source of SP1 is the syncytial trophoblast, but little is known of the subcellular localization of SP1 indicative of the cellular pathway involved in secretion of the hormone. To study subcellular distribution of SP1, we used electron microscopic immunocytochemistry carried out on macaque placental villi from early (3-4 weeks) gestation. Both light and electron microscopic results confirmed localization confined to syncytial trophoblast in the villi. Within syncytial trophoblast labeling was predominantly over small granules in the apical cytoplasm. The Golgi complex also showed labeling, and light labeling was associated with the endoplasmic reticulum. For comparison, we also localized cathepsin B, a lysosomal protease. By way of contrast this enzyme was localized primarily in large cytoplasmic granules. The results are consistent with a secretory pathway including synthesis in the ER, processing by the Golgi complex, and exocytotic release into maternal blood in the intervillous space.

Morphological responses to implantation and pregnancy in the human and nonhuman primates include decidualization of the endometrial fibroblasts and accumulation of large numbers of large granular lymphocytes, formerly called endometrial granular cells, and may also include an epithelial plaque response and endothelial cell hypertrophy. Although stromal decidualization occurs in all species, it develops slower in macaques than in the human, and slower in the baboon than in the macaques. Cytologically, however, in all of these species there is extensive modification of the decidual cells by midgestation. Hypertrophy of luminal and gland neck epithelial cells is common in most monkeys and is also seen in the baboon, but has not been reported in humans. Large granular lymphocytes undergo changes in morphology during the first week after implantation in the rhesus monkey, the only species in which they have been studied in the immediate postimplantation period. Later in pregnancy many of the large granular lymphocytes are surrounded by decidual cells in this species. All of the responses can be elicited by trauma and appropriate hormonal conditions, but the epithelial plaque response forms first in the rhesus monkey and baboon. It is suggested that more complete fine structural and immunocytochemical studies of the different decidual regions at different gestational ages, combined with studies of the synthetic and antigenic nature of the different cell types, would allow determination of whether or not there are subpopulations of decidual cells in primates as well as suggesting possible functions of the cells in pregnancy.