Physiology of Placental Transfer in Mammals

Faber, J. Job; Thornburg, Kent L.; Binder, Nancy D.

doi:10.1093/icb/32.2.343

Cited by 45 publications

(20 citation statements)

References 19 publications

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“…The efficiency of exchange can be predicted by interdigitation and the placental shape. In labyrinthine placentae, counter-current flow with cross-current components is the most common arrangement Miglino et al 2004), with counter-current flow considered the most effective for maternofetal exchange (Faber et al 1992); whereas the predominant cross-current flow in villous placentae are buttressed by the ratio of maternofetal blood flow (Schroder and Power 1997; also see Moll 1972;Benirschke and Kaufmann 2000, pp. 35-38).…”

Section: Diffusion and Exchangementioning

confidence: 99%

Life-History Correlates of Placental Structure in Eutherian Evolution

Lewitus

Soligo

2011

Evol Biol

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The eutherian placenta shows remarkable evolutionary plasticity. To date, however, success in identifying selection pressures behind the observed diversity of placental structures has been limited. Evolutionary convergence among definitive placental morphologies and between placental morphologies and life-history variables can be used to suggest functions of derived aspects of placentation. In this paper, we use, for the first time, a comprehensive phylogenetic comparative approach to map phenotypic character states of both placental morphologies and life-history characteristics of species onto hypotheses of phylogenetic relationships in Eutheria. We employ phylogenetic methods for ancestral reconstruction, mutational mapping, and association analysis to resolve associations between five aspects of placental structure and to identify dominant combinations, or syndromes, of placental morphology. We map twenty life-history characters onto the eutherian phylogeny to examine how they correlate, over evolutionary time, with the multivariate diversification of placental structures. We identify two distinct eutherian constellations, based on associations between life-history and placental structure, which broadly reflect a dichotomy between slow and fast life-history strategies. In addition, we suggest that the observed association between placental invasiveness and group size is indicative of the effect of social behavior on the utility of genomicimprinting in eutherian evolution.

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Section: Diffusion and Exchangementioning

confidence: 99%

Life-History Correlates of Placental Structure in Eutherian Evolution

Lewitus

Soligo

2011

Evol Biol

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“…While it is surely true that characters involved in fetal membranes provide valuable clues to mammalian evolutionary relationships, in view of the direct implications of placentation for reproductive success it seems highly unlikely that differences between mammalian groups lack any functional significance. Faber et al (1992) aptly noted that there is no other mammalian organ whose structure and functions show such diversity among species as those of the placenta (see also Vogel 2005). The only direct functional conclusion that has commonly been drawn is that the three basic types of placenta recognized by Grosser (1909) differ in ''efficiency''.…”

Section: Placenta Type and Efficiencymentioning

confidence: 99%

“…Unfortunately, studies on placental transfer in mammals have been limited to just a few species, so there is no adequate basis for broad comparisons. However, Faber et al (1992) provided an illuminating review of basic principles of placental transfer. They drew an important distinction between diffusion-limited and flow-limited types of placentation and emphasized the significance of counter-current systems for efficient maternal/fetal exchange.…”

Section: Placenta Type and Efficiencymentioning

confidence: 99%

Evolution of Placentation in Primates: Implications of Mammalian Phylogeny

Martín

2008

Evol Biol

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Primates are quite unique among placental mammals in that the two extreme types of placentation are present within a single order. Strepsirrhines (lemurs and lorisiforms) have non-invasive epitheliochorial placentation, whereas haplorhines (tarsiers and higher primates) have highly invasive haemochorial placentation. Resemblance in placenta type in fact provided the first evidence that tarsiers are linked to higher primates and distinct from lemurs and lorisiforms. Tree-shrews differ from both primate subgroups in having moderately invasive endotheliochorial placentation, while colugos have invasive haemochorial placentation like haplorhines. All three kinds of placentation have been identified as primitive for placentals by different authors, but until recently the prevailing interpretation has been that non-invasive epitheliochorial placentation is primitive and ''less efficient''. Opposing this interpretation, Martin (Primate origins and evolution: a phylogenetic reconstruction, 1990) proposed that moderately invasive endotheliochorial placentation is primitive. Epitheliochorial placentation is unlikely to be primitive because it is predominantly associated with large body size, relatively long gestation periods and precocial offspring. Furthermore, some strepsirrhines and other placental mammals with epitheliochorial placentation retain indications of former invasiveness of the placenta. The recent availability of comprehensive molecular phylogenies for placental mammals has provided an independent framework to determine the most parsimonious interpretation of the evolution of placenta types and other reproductive features. It has consistently emerged that epitheliochorial placentation is best explained as a derived condition, although opinions differ as to whether the ancestral condition for placental mammals (and hence for primates) was endotheliochorial or haemochorial. It is argued that on balance the most likely ancestral condition is endotheliochorial. Comparative evidence across placentals clearly indicates that epitheliochorial placentation is not less efficient than more invasive forms of placentation, at least with respect to growth in overall fetal body mass. The ratio of neonate mass to gestation period (a simple indicator of average daily maternal investment in fetal growth) shows no difference according to placenta type. Differential evolution of placentation is hence presumably linked to immunological factors, parent/offspring conflict and/or genomic imprinting.

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“…With consideration of the chemical structure of glucuronides, paracellular transport mechanisms, transfer through syncytial pores, or the assistance of transport carrier proteins would be required for passage through lipid membranes (Faber et al, 1992). Although the mechanisms by which glucuronide metabolites cross the placenta are unclear, it is known that transporters are abundant in the placenta, and several may have an affinity for glucuronides (St-Pierre et al, 2000;Pascolo et al, 2003;van de Wetering et al, 2007).…”

Section: Disposition Of M3g In Pregnancymentioning

confidence: 99%

“…The sheep has an epitheliochorial placenta with four distinct membranes intervening between the fetal and maternal circulations, whereas the maternal spiral arteries of the primate hemomonochorial placenta end directly in lacunae where maternal blood bathes the fetal syncytiotrophoblast that is almost fused with the walls of the fetal villous capillaries to form two closely opposed layers. Although each placental type evolved to minimize the diffusional distance, the permeability for hydrophilic substances in the sheep is markedly reduced for a substance with a molecular radius greater than 0.45 nm (Faber et al, 1992;Enders and Carter, 2004). The guinea pig placenta is also hemomonochorial in nature, and permeability similar to that of the primate placenta might be expected.…”

Section: Disposition Of M3g In Pregnancymentioning

confidence: 99%

Placental Transfer and Fetal Elimination of Morphine-3-β-glucuronide in the Pregnant Baboon

Garland¹,

Abildskov²,

Kiu³

et al. 2008

Drug Metab Dispos

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ABSTRACT:The glucuronide metabolites of several widely used drugs are detected in fetal plasma after maternal drug administration. However, the disposition of these metabolites is poorly understood and clinical concerns have been raised about accumulation of active metabolites in the fetus. For this reason, morphine-3-␤-glucuronide (M3G), an active metabolite of morphine, was studied to provide quantitative data on disposition. Maternal, fetal, and bidirectional placental clearances of M3G were measured in three pregnant baboons. During maternal infusion of M3G to steadystate, the glucuronide metabolite readily appeared in fetal plasma achieving a mean ؎ S.D. fetal-to-maternal concentration ratio of 0.79 ؎ 0.04. In paired maternal and fetal infusions, steady-state clearances were 53 ؎ 3 (maternal), 1.5 ؎ 0.5 (maternal-to-fetal), 2.6 ؎ 0.1 (fetal-to-maternal), and ؊0.70 ؎ 0.6 ml ⅐ min ؊1 (fetal). Glucuronidation is a major drug elimination pathway. The glucuronide metabolites of several drugs have been detected in fetal plasma after maternal drug administration, raising the question of their origin. It has been shown that the sheep and primate fetus can contribute to the presence of glucuronide metabolites through metabolism (Wang et al., 1986(Wang et al., , 1990Olsen et al., 1988;Garland et al., 2005Garland et al., , 2006. In sheep, glucuronide metabolites have extremely low placental permeability suggesting little contribution from the mother (Wang et al., 1985;Olsen et al., 1988). However, the contribution from placental transfer has not been determined in primates. The information that is available suggests that the primate placenta is more permeable than that of the sheep. The similarity of fetal and maternal metabolite concentrations under steady-state conditions after maternal drug or metabolite administration in human and nonhuman primates supports a considerable transplacental contribution from the mother to the fetal metabolite pool (Gerdin et al., 1990a,b;Garland et al., 1998b Garland et al., ,c, 2001).The limited consideration given to metabolite disposition in pregnancy may be accounted for by the fact that the metabolites of many drugs are inactive and the commonly held concept that fetal metabolism has little impact on overall drug disposition. However, the glucuronide metabolites of morphine, morphine-3-␤-glucuronide (M3G) and morphine-6-␤-glucuronide (M6G) have demonstrated distinct activities that may contribute to the effects of the parent drug (Labella et al., 1979;Pasternak et al., 1987;Skarke et al., 2005). Furthermore, recent studies in the pregnant baboon demonstrate that fetal metabolism not only significantly decreases fetal drug concentrations, but also can result in concentrations of metabolites that exceed those in the mother (Garland et al., 2001). The extensive parallels between human and nonhuman primates suggest that studies of fetal metabolism and exposure to metabolites in baboons are relevant to the human fetus (Garland et al., 1996b(Garland et al., , 1998aCaspersen et al., 20...

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Physiology of Placental Transfer in Mammals

Cited by 45 publications

References 19 publications

Life-History Correlates of Placental Structure in Eutherian Evolution

Life-History Correlates of Placental Structure in Eutherian Evolution

Evolution of Placentation in Primates: Implications of Mammalian Phylogeny

Placental Transfer and Fetal Elimination of Morphine-3-β-glucuronide in the Pregnant Baboon

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