Plasma membrane transformation: a common response of uterine epithelial cells during the peri-implantation period

The plasma membrane of uterine epithelial cells and its changes during early pregnancy are reviewed. The review first examines morphological alterations in rats and mice and laboratory rodents and finds that similar changes in membrane organization accompany the peri-implantation period: long, thin, regular microvilli are gradually converted into irregular, flattened projections. It is also found however, that in many other species related plasma membrane alterations are seen during early pregnancy. Molecular alterations in the membrane are also examined and although the evidence is so far limited, striking similarities are noted across species. The review also examines some new morphological studies on the alterations in the plasma membrane of uterine epithelial cells during early pregnancy and concludes that a process of plasma membrane transformation may be a common response across species.     

The plasma membrane transformation facilitates pregnancy in both reptiles and mammals

Mechanisms of placentation are very diverse in mammals and range from types in which the uterine epithelium is breached by the implanting blastocyst to those where the epithelium remains intact. Despite these differences in mechanisms, the initial response of the plasma membrane of uterine epithelial cells is remarkably similar across mammalian species which has led to the term 'plasma membrane transformation' to encapsulate the concept of a common beginning to implantation. Membrane phenomena similar to those of mammals have now been observed in some viviparous lizards at the ultrastructural level during early pregnancy, and we propose extending the concept of 'plasma membrane transformation' to lizards with live birth.     

Desmoglein‐2 during pregnancy and its role in the evolution of viviparity in a marsupial (Sminthopsis crassicaudata; Dasyuridae)

Attachment of the blastocyst and formation of the placenta during pregnancy is dependent on structural and cellular changes occurring in the uterine epithelium and in particular to the plasma membrane of these uterine cells. Desmosome expression decreases during pregnancy in eutherians and some squamates, presumably allowing for remodeling of the uterine epithelium and invasion of the trophoblast during implantation. Marsupials are a distinct mammalian amniote lineage of viviparity, with a short implantation or attachment period and varying levels of invasive placentation. To test the generality of changes to the uterine epithelium during pregnancy across mammals, we characterized the distribution of desmosomes in the uterine epithelial cells of a marsupial, Sminthopsis crassicaudata, using electron microscopy and immunohistochemistry. The absolute number of desmosomes along the lateral plasma membrane decreases during pregnancy and desmosomes are redistributed towards the apical region of the lateral plasma membrane as pregnancy proceeds, similar to what occurs during pregnancy in eutherian mammals. Despite the lower level of maternal investment in pregnancy and the noninvasive structure of fetal membranes in marsupials there are similarities in number and redistribution of desmosomes along the plasma membrane and changes to the morphology of the uterine epithelial cells suggesting that similar plasma membrane changes occur across all lineages of amniote vertebrates. J. Morphol. 276:261–272, 2015. © 2014 Wiley Periodicals, Inc.     

Uterine epithelial cell changes during pregnancy in a marsupial (Sminthopsis crassicaudata; Dasyuridae)

Formation of a placenta requires intimate contact between the embryonic and maternal uterine epithelia in early pregnancy. Contact is accompanied by a characteristic suite of changes to the plasma membranes of uterine epithelial cells, termed the plasma membrane transformation. The plasma membrane transformation occurs in eutherian mammals and in viviparous (live‐bearing) squamate reptiles, and may be fundamental to the evolution of viviparity in amniotes. Marsupials provide an excellent opportunity to test the generality of this phenomenon. Here, we present the first detailed study of the plasma membrane transformation in a marsupial. We combine electron microscopy and immunohistochemistry to describe morphological and molecular features of uterine epithelial cells during pregnancy in the fat‐tailed dunnart (Sminthopsis crassicaudata; Dasyuridae). Cell morphology changes dramatically in S. crassicaudata during pregnancy. Apical microvilli are replaced by irregular blunt projections, then by spiky projections postimplantation. Cell surfaces flatten and ciliated cells are lost. Junctional complexes between adjacent cells increase in depth, then decrease just before implantation, which is consistent with junctional protein localization in this region of the cell membrane. The uterine cellular changes in S. crassicaudata are consistent with a plasma membrane transformation, and support the idea that this phenomenon is fundamental to the evolution of viviparity in amniote vertebrates. J. Morphol. 275:1081–1092, 2014. © 2014 Wiley Periodicals, Inc.     

Closure of the uterine lumen and the plasma membrane transformation do not require blastocyst implantation

Ultrastructural changes in the plasma membrane of uterine epithelial cells in the pseudopregnant rat were examined to determine if these changes resemble those found during normal pregnancy and also to examine if the well-known membrane alterations of early pregnancy are intrinsic to uterine epithelial cells. Changes in the surface contours of uterine epithelial cells from the afternoon of day 6 to the morning of day 9 of pseudopregnancy were similar to those present after attachment in normal pregnancy although somewhat delayed. The presence of short, irregular microvilli was seen from as early as day 7 of pseudopregnancy, with regular microvilli returning to the epithelial surface by days 8-9 of pseudopregnancy but to a slightly lesser extent as compared to normal pregnancy. Furthermore, observations made on the afternoon of day 6 to the morning of day 7 of pseudopregnancy showed that the uterine lumen was closed down and that complete membrane flattening between opposing uterine epithelial cells was seen all along the uterus in the absence of a blastocyst. These observations establish that the "plasma membrane transformation" does not depend on blastocyst implantation.     

Caveolins redistribute in uterine epithelial cells during early pregnancy in the rat: An epithelial polarisation strategy?

At the time of implantation, uterine luminal epithelial cells undergo a dramatic change in all plasma membrane domains. Changes in the basolateral plasma membrane at the time of implantation include progression from smooth to highly tortuous, as well as a loss of integrin-based focal adhesions. Another aspect of the basolateral plasma membrane that has not been studied in uterine epithelial cells are caveolae, which are omega-shaped invaginations of the plasma membrane known to be involved in endocytosis and contribute to membrane curvature. The current study investigated caveolin, a major protein of caveolae, to explore the possible roles that they play in the remodelling of the basolateral plasma membrane of uterine epithelial cells during early pregnancy in the rat. Morphological caveolae were found at the time of implantation and were significantly increased compared to day 1 of pregnancy. Caveolins 1 and 2 were found to shift to the basolateral plasma membrane of uterine epithelial cells at the time of implantation as well as when treated with progesterone alone, and in combination with oestrogen. A statistically significant increase in the amount of caveolin-1 and a decrease in caveolin-2 protein in uterine epithelial cells was observed at the time of implantation. Caveolin-1 also co-immunoprecipitated with integrin β1 on day 1 of pregnancy, which is a protein that has been reported to be found in integrin-based focal adhesions at the basolateral membrane on day 1 of pregnancy. The localisation and expression of caveolin-1 at the time of implantation is consistent with the presence and increase of morphological caveolae seen at this time. The localisation and expression of caveolins 1 and 2 in luminal uterine epithelium at the time of implantation suggest a role in trafficking proteins and the maintenance of a polarised epithelium.     

Urogenital vasculature and local steroid concentrations in the uterine branch of the ovarian vein of the female tammar wallaby (Macropus eugenii)

The urogenital vasculature of the tammar comprises 4 major paired arteries and veins: the ovarian, the cranial urogenital, the caudal urogenital and the internal pudendal artery and vein. The ovarian artery and vein and their uterine branches which supply the ovary, oviduct and uterus, ramify extensively. Each anterior urogenital artery and vein supplies the caudal regions of the ipsilateral uterus, lateral and median vagina and cranial parts of the urogenital sinus. The caudal urogenital arteries and veins supply the urogenital sinus and caudal regions of the bladder. The internal pudendal artery and vein vascularize the cloacal region, with some anastomoses with branches of the external pudendal vessels. Anastomoses connect the uterine branch of the ovarian artery with the uterine branch of the cranial urogenital and cranial branches of the caudal urogenital arteries, and connect the caudal urogenital and the internal pudendal arteries. Anastomotic connections between the left and right arterial supply also occur across the midline of the cervical regions of the uteri and the anterior lateral vaginae. Similar connections are seen in the venous system. The uterine branch of the ovarian artery ramifies extensively very close to the ovary, giving a plexiform arrangement with the ovarian veins, and also with the uterine venous system on the lateral side of each uterus. This plexiform structure provides an anatomical arrangement which could allow a local transfer of ovarian hormones from ovarian vein into the uterine arterial supply, and thence to the ipsilateral uterus. Progesterone concentrations in plasma from the mesometrial side of the uterine branch of the ovarian vein are markedly higher than in tail vein plasma, especially during the 'Day 5 peak' early in pregnancy, and also at full term. There is also a marked decrease in progesterone concentration from all sites immediately before birth as previously reported for peripheral plasma. These results support the suggestion of a countercurrent transfer mechanism, at least for progesterone, and possibly other hormones, between the ovarian vein and uterine artery. Such a local transfer could explain the different morphological responses of the endometria of the two adjacent uteri during pregnancy in macropodid marsupial species.     

Desmosomes in uterine epithelial cells decrease at the time of implantation: an ultrastructural and morphometric study

Displacement of uterine epithelial cells is an important aspect of implantation in the rat and other species, allowing invasion of the blastocyst into the endometrial stroma. Desmosomes, which are part of the lateral junctional complex, function in cell-to-cell adhesion, and are therefore likely to be involved in displacement of uterine epithelial cells at the time of implantation. This study used transmission electron microscopy to study rat uterine epithelial cells during the peri-implantation period to investigate the change in the number of structural desmosomes along the lateral plasma membrane of uterine epithelial cells. We found a significant decrease in the number of desmosomes along the entire lateral plasma membrane as pregnancy progressed. Furthermore, there were also significant decreases in the number of desmosomes on the apical portion of the lateral plasma membrane between all days of pregnancy examined. In addition, on day 6 of pregnancy, the time of attachment, desmosomes were larger and seen as "giant desmosomes." For the first time, this study has shown that there is a significant reduction in cell height and actual number of ultrastructurally observable desmosomes at the time of implantation in the rat. It is proposed that this reduction in desmosome number leads to a decrease in lateral adhesion between uterine epithelial cells at the time of implantation, and hence is involved in the loss of uterine epithelial cells to facilitate blastocyst invasion.     

Molecular mechanisms of membrane interaction at implantation

Successful pregnancy is dependent upon the implantation of a competent embryo into a receptive endometrium. Despite major advancement in our understanding of reproductive medicine over the last few decades, implantation failure still occurs in both normal pregnancies and those created artificially by assisted reproductive technology (ART). Consequently, there is significant interest in elucidating the etiology of implantation failure. The complex multistep process of implantation begins when the developing embryo first makes contact with the plasma membrane of epithelial cells within the uterine environment. However, although this biological interaction marks the beginning of a fundamental developmental process, our knowledge of the intricate physiological and molecular processes involved remains sparse. In this synopsis, we aim to provide an overview of our current understanding of the morphological changes which occur to the plasma membrane of the uterine endothelium, and the molecular mechanisms that control communication between the early embryo and the endometrium during implantation. A multitude of molecular factors have been implicated in this complex process, including endometrial integrins, extracellular matrix molecules, adhesion molecules, growth factors, and ion channels. We also explore the development of in vitro models for embryo implantation to help researchers investigate mechanisms which may underlie implantation failure. Understanding the precise molecular pathways associated with implantation failure could help us to generate new prognostic/diagnostic biomarkers, and may identify novel therapeutic targets. Birth Defects Research (Part C) 108:19–32, 2016. © 2016 Wiley Periodicals, Inc.     

Mechanics of spreading cells probed by atomic force microscopy

Cellular adhesion and motility are fundamental processes in biological systems such as morphogenesis and tissue homeostasis. During these processes, cells heavily rely on the ability to deform and supply plasma membrane from pre-existing membrane reservoirs, allowing the cell to cope with substantial morphological changes. While morphological changes during single cell adhesion and spreading are well characterized, the accompanying alterations in cellular mechanics are scarcely addressed. Using the atomic force microscope, we measured changes in cortical and plasma membrane mechanics during the transition from early adhesion to a fully spread cell. During the initial adhesion step, we found that tremendous changes occur in cortical and membrane tension as well as in membrane area. Monitoring the spreading progress by means of force measurements over 2.5 h reveals that cortical and membrane tension become constant at the expense of excess membrane area. This was confirmed by fluorescence microscopy, which shows a rougher plasma membrane of cells in suspension compared with spread ones, allowing the cell to draw excess membrane from reservoirs such as invaginations or protrusions while attaching to the substrate and forming a first contact zone. Concretely, we found that cell spreading is initiated by a transient drop in tension, which is compensated by a decrease in excess area. Finally, all mechanical parameters become almost constant although morphological changes continue. Our study shows how a single cell responds to alterations in membrane tension by adjusting its overall membrane area. Interference with cytoskeletal integrity, membrane tension and excess surface area by administration of corresponding small molecular inhibitors leads to perturbations of the spreading process.     

Porcine endometrial expression of kininogen,factor XII,and plasma kallikrein in cyclic and pregnant gilts

Establishment of pregnancy in the pig is accompanied by a localized uterine acute inflammatory response and increase in uterine blood flow. Following rapid trophoblast elongation on Day 12 of pregnancy there is an increase in tissue kallikrein activity and release of bradykinin into the uterine lumen, suggesting the kallikrein-kininogen-kinin system is active in the porcine uterus. The present study investigated endometrial expression and presence of the various factors of the kallikrein-kininogen-kinin system. Endometrial L- and H-kininogen gene expression as well as presence of kininogens in the uterine flushings was evaluated throughout the estrous cycle and early pregnancy in the pig. The possible involvement of plasma kallikrein and Factor XII, activators of the kallikrein-kininogen-kinin system, were evaluated through analysis of gene expression in endometrial and conceptus tissues. Gene expression for plasma kallikrein, Factor XII, and H-kininogen were detected in endometrium but not early conceptus tissues. Factor XII and H-kininogen gene expression were similar across the days of the estrous cycle and early pregnancy. Endometrial plasma kallikrein gene expression was low but increased on Day 15 of the estrous cycle, whereas expression was similar across the days of early pregnancy. In comparison to cyclic gilts, endometrial L-kininogen gene expression increased fourfold on Days 15 and 18 of pregnancy. Both L- and H-kininogen were detected in the uterine flushings of cyclic and pregnant gilts. Presence of L- and H-kininogen in the porcine uterus and endometrial gene expression of plasma kallikrein and Factor XII provide evidence that the kallikrein-kininogen-kinin system is biologically active during establishment of pregnancy in the pig.     

Viviparous lizard, Eulamprus tympanum, shows changes in the uterine surface epithelium during early pregnancy that are similar to the plasma membrane transformation of mammals

The "plasma membrane transformation" describes a series of ultrastructural, biochemical, and morphological changes that occur in the uterus of many mammals at the time of blastocyst attachment. These changes, regardless of placental type or length of gestation, include alterations to microvillar length and density and the presence or absence of pinopods or uterodomes. Scanning electron microscopy (SEM) was used to 1) document the topographical ultrastructure of the uterus of Eulamprus tympanum, an eastern Australian viviparous skink with a simple chorioallantoic placenta, for the first time; and 2) determine whether changes identified as "plasma membrane transformation" in mammals occur in E. tympanum. Tissues collected over three seasons from nonreproductive subadult females, preovulatory, postovulatory, and early to mid-gestational females were examined. At low magnification the uterine epithelium of subadults displays a distinctive pattern of tissue folding that includes rectangular areas of tissue delineated by deep lateral and transverse folds. At higher magnification, the uterine epithelium surface is composed of two dominant cell types, i.e., those covered by microvilli and ciliated cells. The folding pattern observed in subadults is less evident in vitellogenic females and the cell surfaces appear highly secretory, with bulging cell apices. Tissue from postovulatory lizards has no distinctive folding pattern and cell surfaces are frequently smooth and lack microvilli. Uterine egg chambers lack ciliated cells at the embryonic pole, but display abundant secretory droplets. Thus, the uterus of E. tympanum undergoes a plasma membrane transformation. The scope of this transformation is not fully understood but may be related to the complexity of placental structure and the development of the embryo/fetus at parturition.     

Oviductal structure in a viviparous New Zealand gecko,Hoplodactylus maculatus

Oviductal structure is described in New Zealand's common gecko, Hoplodactylus maculatus, over four reproductive stages (early/mid-vitellogenesis, late vitellogenesis, early pregnancy, late pregnancy), using light, scanning electron, and transmission electron microscopy. Five regions of the oviduct are recognized: infundibulum, uterine tube, isthmus, uterus, and vagina. Up to three cell types make up the luminal epithelium of the oviduct: ciliated, nonciliated, and bleb cells. The function of bleb cells (seen in the infundibulum only) is unknown, but observation of these cells using transmission electron microscopy suggests that they are involved in secretory activity. Mucosal glands in the uterine tube possess large numbers of secretory granules of varying electron densities. Additionally, these glands appear to function as sperm storage tubules. Numerous sperm are seen in the glands during late vitellogenesis and early pregnancy. Very few uterine mucosal (shell) glands are seen during vitellogenesis, which is consistent with the observation that only a fine shell membrane covers the egg during early pregnancy. By late pregnancy, extraembryonic membranes lie adjacent to the uterus allowing the formation of the omphalo- and chorioallantoic placentas. Maximum cell height in the luminal epithelium is seen during vitellogenesis. The maximum percentage of ciliated cells making up the epithelial layer is seen during pregnancy. The low number of uterine mucosal glands seen in H. maculatus is a feature typical of other viviparous reptiles described, despite independent evolutions of viviparity. Although oviductal structure has been described in the literature for various reptiles, several ultrastructural features seen in this study highlight the lack of detailed understanding of this tissue. J. Morphol. 234:51-68, 1997. © 1997 Wiley-Liss, Inc.     

ICAM-2 and lipid rafts disappear from the basal plasma membrane of uterine epithelial cells during early pregnancy in rats

Adhesion molecules are redistributed in rat uterine epithelial cells (UECs) during early pregnancy for endometrial receptivity and implantation. Intercellular adhesion molecule-2 (ICAM-2) is located as an oligomer on the basal plasma membrane of non-receptive UECs on day 1 of pregnancy and colocalizes with the lipid raft marker flotillin-2. At the time of implantation in rats and in ovariectomized rats primed with progesterone, ICAM-2 disappears from the basal plasma membrane and lipid rafts redistribute to the apical membrane. The loss of ICAM-2 might render UECs less adherent to the underlying basal lamina and more prone to apoptosis. Flotillin-2 in the apical plasma membrane at the time of implantation might provide an anchoring point for several adhesion molecules that are known to localize to this region at this time. We suggest that flotillin-2 is involved with adhesion between UECs and the implanting blastocyst, whereas ICAM-2 is associated with the ability for UECs to be removed at the time of implantation.     

Changes in renal morphology and renin secretion in the golden-mantled ground squirrel (Spermophilus lateralis) during activity and hibernation

Summary Chronological changes in renal glomerular morphology and plasma renin activity were investigated during active and hibernating periods in the golden-mantled ground squirrel Spermophilus lateralis. The objective of this study was to determine whether the glomerular endothelium, visceral epithelium (podocytes), basement membrane, mesangial cells, proximal convoluted tubule cells and plasma renin activity exhibit measurable sequential differences between as well as within active and hibernating states at various time points. Limitations in the size of the experimental population prevented an evaluation of changes in these parameters during other important periods such as periodic arousal between hibernation bouts. In this study, glomerular endothelial pore number and epithelial filtration slit number significantly decreased by early hibernation when compared to those during summer activity, and then they increased back toward summer levels by late hibernation. In contrast, podocytic pedicel width along the glomerular basement membrane increased from summer activity to early hibernation, before significantly decreasing again by late hibernation. Mesangial cell and proximal convoluted tubule cell activity appeared increased during hibernation as compared to summer activity, whereas the width of the glomerular basement membrane showed no significant alterations throughout. Plasma renin activity significantly increased during early hibernation and mid-hibernation when compared to summer levels but had decreased by late hibernation toward summer values. The glomerular and plasma renin activity changes observed in this study clearly illustrate the drastic structural and functional adjustments which hibernating species make during torpor and also correlate well with the reported decrease in renal perfusion pressure and urine formation during hibernation. The observed morphological changes during hibernation do not appear to be temperature-dependent, because significant alterations in most of the parameters studied occurred during this period despite the fact that cold-room temperatures were kept constant throughout. The chronological approach to this study and its morphometric evaluation represent a pilot attempt at accurately documenting these changes during two critical states in the hibernator's cycle and may eventually lead to the characterization of these changes during the entire circannual cycle.     

Changes to the uterine epithelium during the reproductive cycle of two viviparous lizard species (Niveoscincus spp.)

We investigated morphological differences in uterine epithelia of the reproductive cycle between two closely related viviparous skinks, Niveoscincus metallicus (lecithotrophic) and Niveoscincus ocellatus (placentotrophic), which have similar placental complexity but different degrees of placentotrophy. Scanning (SEM) and transmission electron microscopy (TEM) revealed that the uterine surface of non‐reproductive females of both species is mainly covered by ciliated cells. As vitellogenesis begins, the uterine epithelium consists of ciliated and non‐ciliated cells under a thin glycocalyx. Microvilli are greatly reduced at mid‐pregnancy, and the uterus differentiates into two structurally distinct regions: the chorioallantoic and the omphaloplacenta. At late stages of pregnancy, the uterine epithelium of chorioallantoic placenta in both species is further ridged, forming a knobbly uterine surface. The ultrastructural evidence between N. metallicus and N. ocellatus cannot strictly account for the distinct differences in their placentotrophy; as yet unexplored molecular nutrient transport mechanisms that are not reflected in uterine ultrastructure must play significant roles in nutrient transportation. Characteristics consistent with a plasma membrane transformation were confirmed in both species.     

Apical plasma membrane-bound enzymes of rabbit uterine epithelium. Pattern changes during the periimplantation phase

In order to monitor changes in the apical cell membrane of rabbit uterine epithelium which are postulated to be a precondition for trophoblast attachment, the marker enzymes: alkaline phosphatase, aminopeptidase M, gamma-glutamyl transferase and dipeptidyl peptidase IV were investigated during the periimplantation phase. Endometrium of early pregnancy (implantation chamber, interblastocyst endometrium; 5-8 days post coitum, d p.c.) was compared with specimens obtained at hCG-induced pseudopregnancy (p. hCG) to distinguish between membrane changes regulated by maternal plasma steroid hormones and such which might be induced locally by blastocyst-derived signals. All enzymes tested showed their main activity at 5 d p.c./p. hCG. The weakest reaction in this series of stages was generally found at 8 d p.c. (interblastocyst segments) or at 8 d p. hCG. In contrast to the rest of the epithelium, the implantation chamber retained high activity of dipeptidyl peptidase IV, and the activity of alkaline phosphatase even raised here again at 7 and 8 d p.c. indicating a direct local influence of the blastocyst on the luminal epithelium. The results suggest that 1) considerable changes occur in the composition of the apical plasma membrane of the uterine epithelium when the endometrium enters the "receptive state", 2) the overall trend is towards a loss of apical-type characteristics of this membrane domain and 3) the changes are modulated both systemically (by plasma steroid hormone levels) and locally by signals from the implanting blastocyst.     

Changing distribution of cadherins during gestation in the uterine epithelium of lizards

The uterine epithelium provides the interface between an embryo and its mother during pregnancy. Calcium-dependent cadherins are adherens junction proteins that undergo major shifts in the uterine epithelium to facilitate the communication between maternal cells and the embryonic milieu during implantation in mammals. They are, therefore, important in trophoblast invasion and the maintenance of pregnancy. We investigated spatiotemporal changes of cadherins throughout pregnancy in the uterine epithelium of two viviparous skinks and one oviparous population, which all exhibit a noninvasive (epitheliochorial) placenta. Cadherins were identified for the first time in squamate reptiles. In all species, cadherins are reduced in the uterine epithelium as gestation progresses, which would lessen the attachment between uterine epithelial cells and allow them to stretch to accommodate embryonic growth. Interestingly, cadherins were reduced sooner after ovulation in the oviparous species than in the viviparous species. In viviparous species, the different expression of cadherins between barren and pregnant uteri from the same mother indicates that expression of cadherins may not be driven solely by maternal hormones, but also by the presence of an embryo. The redistribution of cadherins in squamates is comparable to that of mammals, reflecting establishment of feto-maternal communication during the peri-implantation period. As there is no breaching of maternal tissue in lizards, the change in adherens junctional properties are thus not exclusive to mammals with invasive placentae, which suggests that similar molecular mechanisms regulate changes to uterine epithelia during pregnancy across placental types.     

Fundamentals of viviparity: comparison of seasonal changes in the uterine epithelium of oviparous and viviparous Lerista bougainvillii (Squamata: Scincidae)

Distinct differences in epithelial response between oviparous and viviparous species of skinks led us to investigate morphological differences in the uterus of a species that exhibits bi-modal reproduction and that may indicate specialities for the different requirements of viviparity and oviparity. The uteri of females from oviparous and viviparous populations of the Australian scincid lizard, Lerista bougainvillii, are described in detail to determine whether the occurrence of uterodomes and the plasma membrane transformation, found in other viviparous species but not oviparous species, are indeed features characteristic of viviparity. Oviductal tissue was dissected at three different stages of reproduction from lizards from both populations: 1) vitellogenic, 2) gravid or pregnant, and 3) non-reproductive or quiescent. Tissue was observed using both scanning and transmission electron microscopy. Lerista bougainvillii has a simple placental morphology with simple squamous epithelium. In contrast to mammals and other viviparous skinks, L. bougainvillii does not undergo a plasma membrane transformation, but early signs of placentation in viviparous individuals are indicated by changes in the uterine surface that occur largely after embryonic stage 30. There are no obvious cellular differences between the uteri of oviparous and viviparous L. bougainvillii at the non-reproductive and vitellogenic phase of the reproductive cycle but throughout gestation/gravidity, the cellular differences that could be related to the changing functional requirements with the retention of the viviparous embryo, became apparent. A plasma membrane transformation with ensuing uterodome formation does not occur, which suggests that these more sophisticated changes are a feature of advanced placental development in reptiles.