Opossum Mammary Maturation as It Relates to Immune Cell Infiltration and Nutritional Gene Transcription

Abstract

Synopsis The mammary gland has evolved to accommodate the developmental needs of offspring in species-specific ways. This is particularly true for marsupials. Marsupial milk content changes dramatically throughout lactation in ways appearing timed with neonatal ontogeny and behavior. Here we investigate morphological restructuring within the mammaries throughout lactation in the gray short-tailed opossum, Monodelphis domestica. Substantial remodeling of the mammaries occurs throughout the first half of active lactation. It is not until the latter half of lactation that opossum mammaries appear histologically similar to active eutherian mammaries. Noteworthy was the presence of eosinophils in early developing mammary tissue, which correlated with elevated abundance of transcripts encoding the chemokine IL-16. The presence and abundance of whey protein transcripts within the opossum mammaries were also quantified. Whey acidic protein (WAP) transcript abundance peaked in the latter half of lactation and remained elevated through weaning. Minimal transcripts for the marsupial-specific Early and Late Lactation Proteins (ELP/LLP) were detected during active lactation. Elevated abundance of LLP transcripts was only detected prior to parturition. Overall, the results support the role of eosinophils in mammary restructuring appearing early in mammalian evolution, and describe key similarities and differences in nutritional protein transcript abundance among marsupial species.

Marsupial and monotreme milk—a review of its nutrient and immune properties

“…Also noteworthy is the appearance of eosinophils early in the postnatal period when the mammary tissue is undergoing significant remodeling in the opossum. The presence of eosinophils correlates with local expression of the cytokine interleukin-16, a known chemotactic factor for eosinophils (Fehrenkamp & Miller, 2019a). It has been speculated that in eutherians eosinophils play a role in mammary remodeling, whether the same is true in marsupials is unknown, but this appears to be an ancient conserved feature in mammals.…”

Morphological and immunohistochemical characterization and molecular classification of spontaneous mammary gland tumors in macropods

“…6,7 At week 5 of lactation and beyond, the mammary glands of macropods appear developmentally similar to lactating mammary glands of domestic mammals, notably there is replacement of the abundant connective tissue by ducts and secretory alveoli. 6…”

“…There is absence of distinct lobules composed of alveoli with prominent open lumina, attenuated epithelium with foamy cytoplasm, and complex ductal structures. 6,7,17…”

“…13 Lobular architecture begins to emerge during pregnancy; however, mammary glands remain predominantly composed of connective tissue with few alveoli. 6,7 These alveoli are round, have small lumina, and secretion may be found near the end of pregnancy. 7 Normal lactation will ensue if a sucking stimulus is applied to the gland at the correct stage of the cycle.…”

“…6,7 At week 5 of lactation and beyond, the mammary glands of macropods appear developmentally similar to lactating mammary glands of domestic mammals, notably there is replacement of the abundant connective tissue by ducts and secretory alveoli. 6 Histologically, the nonlactating mammary gland of macropods appears relatively amorphous and distinct lobules are difficult to recognize as the normal architecture is obscured by abundant amounts of collagenous stroma. 13 Tubules and acini are small, with indistinct lumina, lined by a single layer of cuboidal epithelial cells, 6,17 and are widely separated by moderately cellular connective tissue that contains blood vessels and striated muscle (Fig.…”