Placenta
Volume 28, Supplement , Pages S41-S47, April 2007

Animal Models of Human Placentation – A Review

  • A.M. Carter

      Affiliations

    • Corresponding Author InformationTel.: +45 6550 3716; fax: +45 6613 3479.

Department of Physiology and Pharmacology, University of Southern Denmark, Winsloewparken 21, Third Floor, DK-5000 Odense, Denmark

Accepted 14 November 2006. published online 28 December 2006.

Article Outline

Abstract 

This review examines the strengths and weaknesses of animal models of human placentation and pays particular attention to the mouse and non-human primates. Analogies can be drawn between mouse and human in placental cell types and genes controlling placental development. There are, however, substantive differences, including a different mode of implantation, a prominent yolk sac placenta, and fewer placental hormones in the mouse. Crucially, trophoblast invasion is very limited in the mouse and transformation of uterine arteries depends on maternal factors. The mouse also has a short gestation and delivers poorly developed young. Guinea pig is a good alternative rodent model and among the few species known to develop pregnancy toxaemia. The sheep is well established as a model in fetal physiology but is of limited value for placental research. The ovine placenta is epitheliochorial, there is no trophoblast invasion of uterine vessels, and the immunology of pregnancy may be quite different. We conclude that continued research on non-human primates is needed to clarify embryonic–endometrial interactions. The interstitial implantation of human is unusual, but the initial interaction between trophoblast and endometrium is similar in macaques and baboons, as is the subsequent lacunar stage. The absence of interstitial trophoblast cells in the monkey is an important difference from human placentation. However, there is a strong resemblance in the way spiral arteries are invaded and transformed in the macaque, baboon and human. Non-human primates are therefore important models for understanding the dysfunction that has been linked to pre-eclampsia and fetal growth restriction. Models that are likely to be established in the wake of comparative genomics include the marmoset, tree shrew, hedgehog tenrec and nine-banded armadillo.

Keywords: Endotheliochorial placenta, Epitheliochorial placenta, Guinea pig, Haemochorial placenta, Mouse, Non-human primate, Phylogeny, Placentation, Rabbit, Sheep, Trophoblast

 

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1. Introduction 

Compared to that of most other mammals, the human placenta is rather odd. Peculiarities in our fetal membrane development include primary interstitial implantation in a simplex uterus, the absence of yolk sac placentation, and the occurrence of an allantoic stalk rather than an allantoic sac. Non-human primates share several of these features, but in most of them implantation is superficial and trophoblast invasion of the endometrium more restricted than in humans. There is no ideal model for human placentation, but this review will examine the strengths and weaknesses of those available to us.

Established laboratory animals such as mice, rats and rabbits have the advantage of short generation times and large litters. Following a brief pregnancy they give birth to rather immature offspring (altricial young). An exception is the guinea pig, which has a longer gestation, a smaller litter and well-developed neonates (precocial young). Small mammals require less space and housing costs are lower. In some experimental settings, however, small size is a disadvantage. Most of the larger laboratory animals are domesticated species such as the sheep, which is widely used in fetal physiology. Ethical considerations tend to increase with the size of the animal and legislation is stricter for cats, dogs and hoofed animals. Ethical concerns are even greater for non-human primates. In addition they are costly to house, have long gestations and usually a single offspring. The obvious advantage that outweighs these shortcomings is that monkeys and apes are our close relatives.

Indeed, in choosing appropriate models for human pregnancy, one criterion might be how close they are to humans from a phylogenetic standpoint. We are now in a better position to understand the relation between primates and other orders because of improved understanding about how mammals evolved [1]. These insights have come to us through the relatively new science of molecular phylogenetics. In the near future, comparative genomics will supplement this information and provide new tools for understanding placentation in man and other mammals. We will here pay closest attention to the mouse and non-human primates with a briefer coverage of the guinea pig, rabbit and sheep. In a final section it will be asked if other species are likely to be introduced as laboratory animals, perhaps in the wake of comparative genomics, and whether they might provide fresh insights into human pregnancy.

This paper is dedicated to the memory of Maurice Panigel. He fully recognized the value of animal models, particularly non-human primates. Thus he studied the maternal placental circulation of monkeys by angiography and later by magnetic resonance imaging. These studies were a natural complement to his work with human placenta using the perfused placental lobule [2]. He assuredly would have had strong views on the question implicit in this review: do we have the right models for research on human pregnancy and placentation?

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2. Mouse 

Advantages of the mouse include its small size and short generation time. A major benefit compared to other rodents lies in the availability of embryonic stem cells, which facilitates gene targeting and the development of transgenic lines.

Rodents and lagomorphs (collectively Glires) are the sister group to primates and are included in the same superorder (Euarchontoglires). This association is strongly supported by molecular phylogenetics [3], but it must be recalled that it has never been suggested by morphological evidence [4].

Indeed, even though the mouse is close to primates in an evolutionary context, this edge has been dulled by an unusually high rate of mutation [5]. This is a feature shared by other murid rodents, which include the rat and hamster. The differences are sufficient for the mouse to be inappropriate as a model in some areas of research. As an example, the genes controlling the cell cycle are often more unlike human than in any other mammal [6]. In addition, it is apparent from comparative genomics that there has been considerable fragmentation of the genome. As a result, chromosome painting, which gives meaningful results in most orders, does not work well in rats and mice [7].

2.1. Placentation 

The structural homologies and dissimilarities between mouse and human placenta are fairly well understood [8]. Many of the genes determining placental development are known and often analogous to those expressed in human placenta [9].

One potential disadvantage of the mouse for functional studies is its small size. However, this is being addressed by the development of sophisticated techniques for imaging [10], [11] and placental perfusion [12]. There are, however, many differences between murine and human placentation that affect the utility of the mouse as a model (Table 1).

Table 1. Comparison of pregnancy and placentation in mouse and human
MouseHuman
ImplantationSecondarily interstitialPrimarily interstitial
Yolk sacInverted yolk sac placenta functions to termYolk sac floats free in exocoelom during first trimester
Trophoblast invasion of uterine arteriesShallow; limited to proximal deciduaExtensive; reaching myometrial vessels
Transformation of uterine arteriesDependent on maternal factors (uterine natural killer cells)Dependent on trophoblast
Placental exchange areaLabyrinthineVillous
Interhaemal barrierThree trophoblast layers; outer one cellular, inner two syncytialSingle layer of syncytial trophoblast (Langhans layer not part of barrier)
TrophospongiumExtensiveAbsent
Placental hormonesPlacental lactogensChorionic gonadotropin, chorionic somato-mammotrophin, placental growth hormone; major source of progesterone
GestationThree weeksNine months

In contrast to human, trophoblast invasion in the mouse is shallow [13], [14]. This applies particularly to the arteries as even the blood vessels of the decidua are lined by endothelium rather than trophoblast [10], [13]. Indeed, in the mouse, uterine natural killer cells are more important than trophoblast in arterial remodelling [15], [16]. The mouse model is therefore less than optimal for studies of trophoblast invasion and vascular remodelling. These are processes that are key to our understanding of fetal growth restriction and pre-eclampsia in human pregnancy.

Possible immunological differences between the two species are the topic of a recent review [16]. It is not clear whether uterine natural killer cells play the same role or use the same molecular mechanisms in mouse and man. Much reasoning about the maternal immune response is based on the concept of the fetus as an allograft. Therefore it is important to bear in mind that pregnancies involving cloned mice are essentially syngeneic [16].

Mouse and human placental endocrine functions are very different [17]. Ovarian progesterone production is required throughout pregnancy in the mouse. At first the corpus luteum is maintained by pituitary prolactin, later placental lactogen from the trophoblastic giant cells takes over this function. In human pregnancy, maintenance of the corpus luteum depends on hCG produced by the trophoblast. However, from about eight weeks of gestation, progesterone production by the syncytiotrophoblast is sufficient to maintain pregnancy even after ovariectomy. Chorionic gonadotropin appeared fairly late in the evolution of primates and is found neither in tarsiers nor in the lorises and lemurs [18], [19]. The presence of an equine chorionic gonadotropin (PMSG) in horses is thought to reflect convergent evolution [18]. Human placental endocrine function is also characterized by secretion of human chorionic somato-mammotrophic hormone and human placental growth hormone.

Such functional differences between mouse and human placenta may reflect the great difference in gestation length and the birth of altricial young in the mouse. It is important to bear in mind that pregnancy lasts for just three weeks in mice and the chorioallantoic placenta functions for only half of that time. Many of the developmental processes that occur in humans during intrauterine life are postnatal events in rats and mice. Humans and other primates have relatively long gestation periods and typically give birth to single, well-developed offspring with open eyes and ears. The young are in most respects precocial, although they remain reliant on parental care during postnatal brain development, and for this reason are sometimes referred to as secondarily altricial [20].

There are further differences between mouse and human placenta that need to be borne in mind, such as the greater role of yolk sac placentation, the labyrinthine rather than villous structure of the exchange area and the presence of three layers of trophoblast in the interhaemal membrane. If the focus of research is on overall exchange between fetal blood and maternal blood, disparities like the yolk sac uptake of immunoglobulins and the trilaminar interhaemal membrane may make little difference. But if one is interested in what trophoblast is capable of accomplishing, then one finds that most of the hormonal activity in the mouse placenta is achieved by the trophoblast layer that is adjacent to maternal blood, whereas the transport and barrier functions are achieved by the other two trophoblast layers, which are linked by gap junctions.

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3. Guinea pig 

The guinea pig is one of the hystricognath rodents and does not suffer from the accelerated mutation rates seen in rats and mice. Therefore it was recommended by Waddell et al. [6] as a promising alternative to murid rodents. The guinea pig genome is close to completion although it lacks annotation. Guinea pigs deliver precocial young after a long gestation. Thus many events that occur during human fetal developmental also occur during fetal life in guinea pigs. This is in contrast to rodents that have a short gestation and altricial young, where many of these processes occur during postnatal development.

On the downside, guinea pigs occupy more space than mice and have a longer generation time. Experiments not requiring fetal manipulation can be done in the unstressed animal, but guinea pigs are not as versatile as sheep in this respect.

3.1. Placentation 

The guinea pig is a well-established model for the study of placental transfer [21], [22] and fetal growth restriction [23], [24]. As in human the placenta is haemomonochorial [25], but the advantage of this is sometimes overstressed. Hystricognath rodents have a subplacenta [26], a structure that has no functional equivalent in the human placenta. Like murid rodents, they retain a yolk sac placenta until term. However, there is an extensive trophoblast invasion that extends well into the walls of the uterine arteries [27], [28]. It is reported that pregnancy toxaemia occurs in guinea pigs and can be experimentally induced [29], [30], but no major study has confirmed this as a useful model of pre-eclampsia.

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4. Rabbit 

The rabbit is well established as a laboratory animal and has been used for studies of placental circulation and placental transfer [31], [32]. It is less used today in part because of stricter guidelines for housing of this rather large animal. However, the rabbit is among species selected for genome sequencing and is no more distant from primates than the mouse or guinea pig. Gestation lasts about three weeks and the young are precocial.

4.1. Placentation 

As in rodents, an inverted yolk sac placenta functions throughout pregnancy. The chorioallantoic placenta is haemodichorial [25]. The extensive decidual zone beneath the labyrinth is an unusual feature [33]. The maternal vessels are lined by multinucleated cells but it is not clear that these are trophoblastic in origin [34].

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5. Sheep 

Sheep have a long development in utero and deliver precocial young. At term the fetal lamb weighs about the same as a human fetus and this has contributed to the popularity of the model in obstetrical research. Sheep are easy to handle and pregnant animals tolerate invasive procedures. Therefore sophisticated techniques have been developed for functional studies in utero after full recovery from anaesthesia and surgery [35]. As a result our knowledge of fetal physiology is greater for sheep than any other species.

The main disadvantages of this model are that sheep are phylogenetically distant from primates and have a very different placentation. Sheep are placed in a different superorder from rodents and primates (Laurasiatheria). They are also quite expensive to house and large-scale experiments requiring several experimental groups are feasible only in Australia and New Zealand [36], [37].

5.1. Placentation 

The interhaemal barrier of the placenta is of the epitheliochorial type. This is widely regarded as a derived form of placentation rather than a primitive state [38]. Sheep share this feature with other artiodactyls, but in addition have developed cotyledons. It recently was suggested that the development of a cotyledonary placenta might be related to diminished availability of glucose, associated with the development of fore stomach fermentation in ruminants [39]. The sheep is likely a poor model for substrate transfer across the human placenta, although it seems ideal for studies of gaseous exchange [40]. Because the uterine epithelium remains intact, the immunology of pregnancy may be very different in sheep, with the fetus and placenta being less like an allograft and more like commensal bacteria [16].

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6. Non-human primates (Old World monkeys) 

The order Primates includes lemurs and lorises, tarsiers, New and Old World monkeys and the great apes. There is evidence of interstitial implantation in all of the great apes and the villous part of the placenta looks identical to the human one. Unfortunately, we know very little about early stages of development and about trophoblast invasion of the decidua and spiral arteries. The species commonly kept at primate centres and used in studies of placentation belong to the Old World monkeys (Cercopithecidae) and include macaques and baboons. Like the human placenta, theirs are villous and haemochorial. New World monkey placentas tend to be more trabecular than villous. Tarsiers have haemochorial placentas that develop differently from those of higher primates and are less invasive. The lemurs of Madagascar and lorises of East Africa and Asia have epitheliochorial placentas [41].

Primates are our closest relatives and likely to resemble us in their biology. The baboon, in particular, has proven its worth as a model for endometriosis [42] and the evaluation of assisted reproductive technologies [43]. Primates are a major focus in comparative genomics [44].

Primate colonies are expensive to maintain, however, and the ethical concerns are much greater. One fear is for vulnerable or endangered species, especially the great apes [45]. For baboons and green monkeys, which are agricultural pests, this is less of a problem. The other ethical concern arises from the very closeness of their relationship to us. Based on the similarity of their genomes and an implied divergence as recent as 6–7mya, it has even been suggested that the bonobo and chimpanzee belong in the genus Homo [46].

6.1. Placentation 

For Old World monkeys, similarities to human placenta include the villous structure, the nature of the interhaemal barrier, and the pattern of circulation in the intervillous space [47], [48], [49]. There is remodelling of the spiral arteries following trophoblast invasion [50], [51].

The initial stages of implantation are remarkably similar in Old World monkeys and man, with syncytiotrophoblast working its way through the uterine epithelium to establish a foothold in the endometrium [52]. However, in Old World monkeys a large part of the blastocyst remains in the uterine cavity, whereas in humans the blastocyst is pulled just beneath the surface. Probably too much is made of the difference between superficial and interstitial implantation. The interaction between trophoblast and endometrium is similar [50], and the baboon and macaque have a trophoblast plate and lacunar stage, as does the human [52]. They therefore offer much better models for implantation than, for example, the guinea pig, where implantation is interstitial but very different, or murid rodents, where interstitial implantation is a secondary process [53].

Indeed, although superficially implanted, the trophoblast of the monkey is initially more aggressive, appearing in spiral arteries beneath the placenta earlier than has been seen in the human [54]. However, an important difference arises as cytotrophoblasts spread out from the anchoring villi to form a trophoblastic shell. In the macaque and the baboon the shell is continuous, slightly thicker and above all sharply delineated from the underlying endometrium [54], [55]. In human placenta the shell is much less uniform and the extravillous trophoblast can be seen streaming off into the endometrium. The paucity of interstitial trophoblast cells in the monkey is an important difference from human placentation. In human placenta extravillous trophoblast invades the decidua and plays a role in vascular remodelling that complements that of the endovascular trophoblast [14].

Fortunately the difference does not extend to the extravillous trophoblast that invades the arteries. There is a strong resemblance in the way spiral arteries are invaded and transformed in the macaque, baboon and human [51]. Non-human primates are therefore important models for understanding the dysfunction that has been linked to pre-eclampsia and fetal growth restriction.

Although pre-eclampsia is sometimes seen as a uniquely human disease [20], there are reports in Old World monkeys [56] and great apes [57] of symptoms that resemble pre-eclampsia. This further underlines their utility as models of human pregnancy and disease. Recently it was shown that baboons develop the classical signs of pre-eclampsia as a result of uteroplacental ischaemia provoked by uterine artery ligation in pregnancy [58]. Most significantly, these animals show the same renal pathology as seen in the human disease. They also have elevated levels of soluble Flt.

There seems to be a difference in how soon maternal placental circulation is established in monkeys and humans. The current consensus is that little circulation occurs within the intervillous space during the first trimester of human pregnancy [59]. In contrast, using ultrasonography with an echo-enhancement agent, onset of an effective circulation within the intervillous space of the cynomolgus placenta could be demonstrated towards the end of the third week postconception [60].

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7. Alternative models 

Studies of comparative placentation satisfy our innate curiosity and help us to understand how the placentas has evolved [61]. In addition, by studying differences in placentation we may gain new insights into human pregnancy. Comparative studies are gaining fresh impetus in the wake of molecular phylogenetics and genomics. Sequencing of the human and mouse genomes has been followed by those of other species. Table 2 lists annotated genomes currently in the public domain as well as some of the species scheduled for sequencing [62], [63], [64]. Although large amounts of nucleotide sequence are available for the latter, they are not yet assembled or annotated. In tandem with the comparative genome project, new species are likely to be introduced as laboratory animals. Some of these might prove useful as models for human pregnancy. The hope is that comparative genomics will offer insights into disease processes; not least diseases like pre-eclampsia that are common in humans but rare in other mammals. To realize this aim, we need to know more about the associated phenotypes and continue to probe comparative morphology, physiology and immunology.

Table 2. Comparative genomics
Common nameScientific namePlacentation
(a) Whole genome sequences available
HumanHomo sapiensWell studied
ChimpanzeePan troglodytesPoorly known
MouseMus musculusWell studied [8], [9], [10]
RatRattus norvegicusWell studied [74], [75]
DogCanis familiarisSome information available [76], [77]
CowBos taurusFairly well studied [78], [79], [80]

(b) Primates scheduled for sequencinga
OrangutanPongo pygmaeusPoorly known
Rhesus MacaqueMacaca mulattaWell studied [47], [48], [49], [50], [51], [52]
MarmosetCallithrix jacchusSome information available [65]
Bush babyOtolemur garnettiiSome information available on related species [81]

(c) Other species scheduled for sequencinga
Guinea pigCavia porcellusWell studied [25]
RabbitOryctolagus cuniculusFairly well studied [33], [34]
Tree shrewTupaia belangeriFairly well studied [66], [67]
Lesser hedgehog tenrecEchinops telfairiWell studied [70]
African elephantLoxodonta africanaWell studied [82], [83]
Nine-banded armadilloDasypus novemcinctusWell studied [71]

Mammals for which annotated whole genome sequences are in the public domain [62], [63], [64]; primates scheduled for whole genome sequencing; other species mentioned in the text. For each species, an arbitrary assessment is given of current knowledge about its placentation.

aSome information is already available for rhesus monkey, rabbit, tenrec, elephant and armadillo [64].

7.1. Primates 

Among New World monkeys, the marmoset has been selected for genome sequencing. It has a high fertility rate, often more than one blastocyst and a prolonged early implantation stage [65]. It could be very useful for implantation studies; it might also be of use for the study of trophoblast giant cells and their endometrial invasion.

7.2. Tree shrew 

Tree shrews (order Scandentia) are close to primates – even closer than rodents. They were recommended as laboratory animals by Waddell et al. [6], who claimed that they are easier to handle than primates. The placenta of tree shrews has been well studied [66], [67], but might prove less interesting as a model for human placentation as it is of the endotheliochorial type.

7.3. The lesser hedgehog tenrec 

One exciting outcome of molecular phylogenetics is the recognition of a new superordinal clade called Afrotheria. This group of mammals includes the lesser hedgehog tenrec, which has been selected for genome sequencing [64], [68]. The tenrec can be kept as a laboratory animal [69] and we predict that it will be used in comparative studies that aim to encompass the full range of mammalian diversity. Although the African elephant has also been selected for genome sequencing [64] it is not likely to find a role in experimental studies. The tenrec has a haemochorial placenta with a prominent haemophagous region [70]. It is not, however, an obvious choice as a model for human pregnancy.

7.4. The nine-banded armadillo 

The oldest of the mammalian superorders is Xenarthra, which comprises sloths, anteaters and armadillos. The nine-banded armadillo has been selected for genome sequencing [64]. It has a villous haemomonochorial placenta [71] and is potentially useful for physiological studies [72]. This species is fairly common in the southern United States and has also been bred in captivity [73].

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8. Conclusion 

Gene targeting and transgene expression in mice will continue to enhance our knowledge of the forces shaping the placenta. From a functional viewpoint, however, the mouse leaves much to be desired as a model for human pregnancy and placentation. It has a different mode of implantation, a prominent yolk sac placenta, and fewer placental hormones. Trophoblast invasion is shallow in the mouse and transformation of the uterine arteries depends on maternal factors. This model is therefore less than optimal for studies of trophoblast invasion and vascular remodelling, processes that play a central role in the pathogenesis of fetal growth restriction and pre-eclampsia. There is, therefore, a continued need for research on non-human primates in order to clarify embryonic–endometrial relations. As has been shown, the interaction between trophoblast and spiral arteries in macaque and cynomolgus monkeys is similar to what occurs in human pregnancy. Rapid advances in comparative genomics will soon enable comparison of whole genome sequences of several primate species, thus making it possible to design even better experiments and further enhancing the value of non-human primates as models for human placentation.

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Acknowledgements 

The author is most grateful to Professor Allen C. Enders for valuable suggestions and comments on an earlier version of the manuscript and he also thanks two anonymous reviewers. The Carlsberg Foundation supported this work.

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PII: S0143-4004(06)00272-4

doi:10.1016/j.placenta.2006.11.002

Placenta
Volume 28, Supplement , Pages S41-S47, April 2007

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