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

Focus Article

Geula Hanin, Anne C. Ferguson‐Smith

Published Online: Dec 26 2019

DOI: 10.1002/wsbm.1476

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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

Schematic representation of genomic imprinting. Paternal chromosome is blue, maternal is pink. The unmethylated regulatory regions are represented as white circles, and methylation as dark gray circles. The Dlk1‐Dio3 imprinted domain is shown as an example, it is comprised of Meg3 and multiple small‐noncoding RNA that are expressed from the maternally inherited chromosome, and three protein‐coding genes, Dlk1, Rtl1, and Dio3 that are expressed from the paternal chromosome. Arrows indicate the direction of transcription

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(a) A schematic representation of the various cell types comprising the adult mammary gland. (b) Table showing the currently available data on imprinted gene expression in mammary gland cells, allelic expression in the mammary gland if available and the relevant reference. Background color represents the corresponding cell type in (a). White background represents information which does not refer to a single cell type

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Illustration of the developmental cycle of the adult mammary gland, initiated from the adult virgin state (top), where tertiary structures of mammary ducts populate the mammary fat pad, represented as a gray circle. During pregnancy, upon the exposure to circulating hormones like Progesterone and Prolactin, the mammary gland differentiates to form milk‐producing alveoli (right) which will become functional after parturition. During lactation, the mammary gland becomes fully populated by alveoli to produce milk, this is mostly regulated by prolactin (bottom). Upon cessation of lactation, Involution begins (left) and a two‐stage process is initiated, removing milk‐producing alveoli and remodeling of the tissue back to a simple ductal architecture

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Diagram illustrating the common features of the placenta and mammary gland. These organs function pre‐ and postnatally respectively to provide the ultimate support to the offspring

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