The evolution of the placenta

Roberts, R. Michael; Green, Jonathan A.; Schulz, Laura C.

doi:10.1530/rep-16-0325

Cited by 174 publications

(143 citation statements)

References 77 publications

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“…In hemochorial placentation, the maternal blood comes in direct contact with the fetal chorion, facilitating efficient transfer of nutrients and oxygen to the growing fetus (4,53). Although the placenta is a transient organ, recent studies demonstrate that is highly adaptive across placental mammals (54,55). The adaptive ability of the placenta is evident from its function that ensures development of the fetus in stressful conditions such as hypoxia and undernutrition (56).…”

Section: Discussionmentioning

confidence: 99%

Evidence for functional interactions between the placenta and brain in pregnant mice

2018

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The placenta plays a pivotal role in the development of the fetal brain and also influences maternal brain function, but our understanding of communication between the placenta and brain remains limited. Using a gene expression and network analysis approach, we provide evidence that the placenta transcriptome is tightly interconnected with the maternal brain and fetal brain in d 15 pregnant C57BL/6J mice. Activation of serotonergic synapse signaling and inhibition of neurotrophin signaling were identified as potential mediators of crosstalk between the placenta and maternal brain and fetal brain, respectively. Genes encoding specific receptors and ligands were predicted to affect functional interactions between the placenta and brain. Paralogous genes, such as sex comb on midleg homolog 1/scm‐like with 4 mbt domains 2 and polycomb group ring finger (Pcgf) 2/Pcgf5, displayed antagonistic regulation between the placenta and brain. Additionally, conditional ablation of forkhead box a2 (Foxa2) in the glands of the uterus altered the transcriptome of the d 15 placenta, which provides novel evidence of crosstalk between the uterine glands and placenta. Furthermore, expression of cathepsin 6 and monocyte to macrophage differentiation associated 2 was significantly different in the fetal brain of Foxa2 conditional knockout mice compared with control mice. These findings provide a better understanding of the intricacies of uterus‐placenta‐brain interactions during pregnancy and provide a foundation and model system for their exploration.—Behura, S. K., Kelleher, A. M., Spencer, T. E. Evidence for functional interactions between the placenta and brain in pregnant mice. FASEB J. 33, 4261–4272 (2019). http://www.fasebj.org

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Section: Discussionmentioning

confidence: 99%

Evidence for functional interactions between the placenta and brain in pregnant mice

2018

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“…Most Introduction 39 The placenta is a unique, transient organ shared by two organisms. Placental morphology is 40 surprisingly diverse across vertebrates and is subject to rapid evolutionary change and 41 convergent evolution (Blackburn 1993;Reznick et al 2002;Roberts et al 2016; Armstrong et al 42 2017). In most eutherian mammals, including mice and humans, successful blastocyst 43 implantation relies on endometrial invasion by the embryonic trophoblast cells that give rise to 44 the mature placenta (Cross et al 1994).…”

mentioning

confidence: 99%

Placental effects on maternal brain revealed by disrupted placental gene expression in mouse hybrids

Arévalo

Campbell

2019

Preprint

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The mammalian placenta is both the physical interface between mother and fetus, and the source of endocrine signals that target the maternal hypothalamus, priming females for parturition, lactation and motherhood. Despite the importance of this connection, the effects of altered placental signaling on the maternal brain are understudied. Here, we show that placental dysfunction alters gene expression in the maternal brain, with the potential to affect maternal behavior. Using a cross between the house mouse and the Algerian mouse in which hybrid placental development is abnormal, we sequenced late gestation placental and maternal medial preoptic area transcriptomes and quantified differential expression and placenta-maternal brain co-expression between normal and hybrid pregnancies. The expression of Fmn1, Drd3, Caln1 and Ctsr was significantly altered in the brains of females exposed to hybrid placentas. Most strikingly, expression patterns of placenta-specific gene families and Drd3 in the brains of house mouse females carrying hybrid litters matched those of female Algerian mice, the paternal species in the cross. Our results indicate that the paternally-derived placental genome can influence the expression of maternal-fetal communication genes, including placental hormones, suggesting an effect of the offspring’s father on the mother’s brain.

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“…The evolution of maternal recognition of pregnancy signals has not been defined in many species, but what is known is that these signals usually are derived from the trophoblast cell, are highly variable, and they appear to be evolving rapidly (Roberts et al 2016). For example, higher primates and Suinae, both of which lack IFNT, utilize CG and estrogens respectively, as their pregnancy recognition factors.…”

Section: Interferons At the Placental-maternal Interfacementioning

confidence: 99%

“…There are many examples of gene family expansions, but the process appears to be particularly common for families whose members are expressed in the placenta (Rawn & Cross 2008, Roberts et al 2016. Examples include (1) growth hormone-related and prolactin-related proteins found in primates, rodents and ruminants, (2) the CG beta gene family in primates, (3) pregnancy-specific proteins found in primates and rodents, (4) pregnancy-associated glycoproteins found in ruminants and swine and (5) IFNT in ruminants.…”

Section: The Multiplicity Of Ifnt Genes and Allelesmentioning

confidence: 99%

The evolution of interferon-tau

Ealy¹,

Wooldridge²

2017

Reproduction

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Thirty years ago, a novel type I interferon (IFN) was identified by molecular cloning of cDNA libraries constructed from RNA extracted from ovine and bovine pre-implantation embryos. This protein was eventually designated as IFN-tau (IFNT) to highlight its trophoblast-dependent expression. IFNT function is not immune related. Instead, it interacts with the maternal system to initiate the establishment and maintenance of pregnancy. This activity is indispensable for the continuation of pregnancy. Our review will describe how IFNT evolved from other type I IFNs to function in this new capacity. IFNT genes have only been identified in pecoran ruminants within the Artiodactyla order (e.g. cattle, sheep, goats, deer, antelope, giraffe). The ancestral IFNT gene emerged approximately 36 million years ago most likely from rearrangement and/or insertion events that combined an ancestral IFN-omega (IFNW) gene with a trophoblast-specifying promoter/enhancer. Since then, IFNT genes have duplicated, likely through conversion events, and mutations have allowed them to adapt to their new function in concert with the emergence of different species. Multiple IFNT polymorphisms have been identified in cattle, sheep and goats. These genes and gene alleles encode proteins that do not display identical antiviral, antiproliferative and antiluteolytic activities. The need for multiple IFNT genes, numerous alleles and distinct activities remains debatable, but the consensus is that this complexity in IFNT expression and biological activity must be needed to provide the best opportunity for pregnancy to be recognized by the maternal system so that gestation may continue. Reproduction (2017) 154 F1-F10

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The evolution of the placenta

Cited by 174 publications

References 77 publications

Evidence for functional interactions between the placenta and brain in pregnant mice

Evidence for functional interactions between the placenta and brain in pregnant mice

Placental effects on maternal brain revealed by disrupted placental gene expression in mouse hybrids

The evolution of interferon-tau

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