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Abstract
The mammary gland represents a unique tissue to study organogenesis as it predominantly develops in the post-natal animal and undergoes dramatic morphogenetic changes during puberty and the reproductive cycle. The physiological function of the mammary gland is to produce milk to sustain the newborn. Here we view the lactating gland through three-dimensional confocal imaging of intact tissue. We observed that the majority of secretory alveolar cells are binucleated. These cells first arise in very late pregnancy due to failure of cytokinesis and are larger than mononucleated cells. Augmented expression of Aurora kinase-A and Polo-like kinase-1 at the lactogenic switch likely mediates the formation of binucleated cells. Our findings demonstrate an important physiological role for polyploid mammary epithelial cells in lactation, and based on their presence in five different species, suggest that binucleated cells evolved to maximize milk production and promote the survival of offspring across all mammalian species.
Highlights
The mammary gland represents a unique tissue to study organogenesis as it predominantly develops in the post-natal animal and undergoes dramatic morphogenetic changes during puberty and the reproductive cycle
Labelling assays have indicated that cell proliferation rapidly declines after mid-pregnancy as the gland commits to differentiation, and that a synchronized round of DNA synthesis occurs in early lactation[3,4,5]
We show that Aurora kinase-A (AURKA) and Polo-like kinase-1 (PLK-1) likely control the generation of binucleated cells at the switch to lactation, in response to signals that include prolactin and epidermal growth factor (EGF)
Summary
The mammary gland represents a unique tissue to study organogenesis as it predominantly develops in the post-natal animal and undergoes dramatic morphogenetic changes during puberty and the reproductive cycle. Our findings demonstrate an important physiological role for polyploid mammary epithelial cells in lactation, and based on their presence in five different species, suggest that binucleated cells evolved to maximize milk production and promote the survival of offspring across all mammalian species. Understanding the tissue remodelling processes that underlie the formation of the specialized milk-producing alveoli requires a comprehensive view of the cellular structure of the mammary gland. We have applied three-dimensional (3D) imaging technology to provide a unique view of the mouse mammary gland and uncovered the presence of a large population of binucleated alveolar cells in lactation. These cells first appear in late pregnancy owing to failed cytokinesis rather than cell fusion. Our findings that binucleated cells are required for lactation represent one of the few physiological functions ascribed to polyploid mammalian cells far
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