Abstract
Hormones from the fetally derived placenta signal to the mother throughout pregnancy to ensure optimal fetal growth and prepare the mother for her new role in nurturing her offspring. Through evolution, placental hormones have under gone remarkable diversification and species-specific expansions thought to be due to constant rebalancing of resource allocation between mother and offspring. Genomic imprinting, an epigenetic process in which parental germlines silence genes in the offspring, is thought to be the physical embodiment of a second conflicting interest, between the male and female mammal. Several genes silenced by paternal imprints normally function to limit the placental endocrine lineages of the mouse placenta. We hypothesized that paternal imprinting has adapted to overcome the rapid evolution of placental hormone gene families by directly regulating the lineages that express these hormones rather than individual hormones. This predicts the existence of genes maternally silenced in the offspring counteracting the influence of the paternal imprint. Here we report on the consequences of loss of function of Paternally expressed gene 3 (Peg3), on placental endocrine lineages. Mutant male placenta displayed a marked loss of the spongiotrophoblast, a key endocrine lineage of the placenta, and the glycogen cell lineage alongside reduced stores of placental glycogen and changes in expression of the normal repertoire of placental hormones. Peg3 is known to transcriptionally repress placental hormone genes. Peg3 consequently both positively and negatively regulates placental hormones through two independent and opposing mechanisms. Female placenta showed moderate response to loss of Peg3 with minor alterations to the junctional zone lineages and few changes in gene expression. These data highlight the important fact that female placenta compensate for the loss of Peg3 better than male placenta. This work lends further support to our novel hypothesis that the parental genomes are competing over the endocrine function of the mouse placenta and further suggests that a conflict between males and females begins in utero.
Highlights
Eutherian mammals provide nutrients to their young in utero via the fetally derived placenta enabling prolonged gestation and the birth of relatively mature offspring central to their reproductive success (John and Hemberger, 2012)
We bred Paternally expressed gene 3 (Peg3)−/+ Mus musculus 129 mouse strain males derived from the original line (Li et al, 1999; Curley et al, 2004) with wild type (WT) 129 females to generate Peg3+/− and matched Peg3+/+ (WT) fetuses and placenta at E14.5
There were no differences in fetal weights at E14.5 between WT and Peg3 knock out (KO) fetuses, and no difference by fetal sex (Figure 1A)
Summary
Eutherian mammals provide nutrients to their young in utero via the fetally derived placenta enabling prolonged gestation and the birth of relatively mature offspring central to their reproductive success (John and Hemberger, 2012). Across mammalian species there are a wide variety of placental shapes, sizes, and structures (Carter and Enders, 2004; Capellini et al, 2011) as well as an extensive diversification of several placental hormone gene families (Rawn and Cross, 2008). These rapid changes are thought to reflect the antagonistic yet interdependent relationship between mother and offspring with higher growth rates favoring the offspring and counter-adaptation by the mother to preserve her future reproductive potential (Haig, 1996). Evidence for maternal silencing of genes to counteract the action of the paternal genome providing more compelling support for this hypothesis is lacking
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