The evolution of genomic imprinting: Epigenetic control of mammary gland development and postnatal resource control

Abstract

Genomic imprinting is an epigenetically regulated process leading to gene expression according to its parental origin. Imprinting is essential for prenatal growth and development, regulating nutritional resources to offspring, and contributing to a favored theory about the evolution of imprinting being due to a conflict between maternal and paternal genomes for the control of prenatal resources—the so‐called kinship hypothesis. Genomic imprinting has been mainly studied during embryonic and placental development; however, maternal nutrient provisioning is not restricted to the prenatal period. In this context, the mammary gland acts at the maternal‐offspring interface providing milk to the newborn. Maternal care including lactation supports the offspring, delivering nutrients and bioactive molecules protecting against infections and contributing to healthy organ development and immune maturation. The normal developmental cycle of the mammary gland—pregnancy, lactation, involution—is vital for this process, raising the question of whether genomic imprinting might also play a role in postnatal nutrient transfer by controlling mammary gland development. Characterizing the function and epigenetic regulation of imprinted genes in the mammary gland cycle may therefore provide novel insights into the evolution of imprinting since the offspring's paternal genome is absent from the mammary gland, in addition to increasing our knowledge of postnatal nutrition and its relation to life‐long health. This article is categorized under: Developmental Biology > Developmental Processes in Health and Disease

Livestock species as emerging models for genomic imprinting

“…While Grb10 suppresses growth in offspring, it increases milk production in mother ( Cowley et al, 2014 ). Hanin and Ferguson-Smith (2020) support the idea suggested by Stringer et al (2014) according to which mammary gland represents the functional equivalent of the placenta in the postnatal stage of eutherian mammals, contributing then to the development and growth of offspring. Indeed, mammary gland, by providing milk to the newborn, contributes further to maternal effects on offspring phenotypes, in addition to those that occur during fetal life.…”

“…Milk provides the neonate with essential nutritional components and non-nutritional bio-active components, such as growth factors including IGF2 that has been shown to be an important biological regulator of milk production in dairy cattle ( Berkowicz et al, 2011 ). Many studies, mainly in mice, showed that the maternal-offspring interface through lactation is a critical period, suggesting that genetic variation and maternal diets may affect milk composition, leading to lasting effects with alteration of lifelong health ( Hanin and Ferguson-Smith, 2020 ; Rodríguez-González et al, 2020 ; Lean et al, 2022 ).…”

Genomic Imprinting in the New Omics Era: A Model for Systems-Level Approaches

“…These include a better understanding of the early evolutionary history and diversification of GI. A closer look at GI in certain taxa and tissues through integrative omics approaches could for example help clarify the constraints applied to imprinted clusters, the mechanisms that enabled the acquisition of DMRs and the role of transposable elements in the evolution of mammalian development ( Bogutz et al, 2019 ; Hanin and Ferguson-Smith, 2020 ; Hanna and Kelsey, 2021 ; Senft and Macfarlan, 2021 ). Comprehensive genome scans for imprinted genes in species with little or no previous evidence for GI bring important information, since it promotes the understanding of both GI evolution and related phenomena such as methylation reprogramming and allele-specific expression, which regulate key biological processes in vertebrates ( Frésard et al, 2014 ; Zhuo et al, 2017 ; Skvortsova et al, 2019 ).…”

Thirteenth Annual ENBDC Workshop: Methods in Mammary Gland Biology and Breast Cancer

“…Those pups become obese and grow faster than control pups, due to upregulated milk protein synthesis in mice that lack the imprinting regulation. Finally, Hanin hypothesised, that the mammary gland, the source of postnatal nutrition, is similar to the placenta, the prenatal nutrition source, where both have a high rate of parentally imprinted genes [ 20 ].…”