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Monodelphis domestica induced pluripotent stem cells reveal metatherian pluripotency architecture

ABSTRACT: Marsupials have been a powerful comparative model to understand mammalian biology. However, because of the unique characteristics of their embryology, marsupial pluripotency architecture remains to be fully understood, and nobody has succeeded in developing embryonic stem cells (ESCs) from any marsupial species. We have developed an integration-free induced pluripotent stem cell (iPSC) reprogramming method and established validated iPSC lines from two fully inbred strains of the gray short-tailed opossum (Monodelphis domestica). A comprehensive characterization of the M. domestica skin fibroblasts and their reprogrammed iPSCs was performed by genome-wide mRNA sequencing. The established monoiPSCs showed a significant (6,181 DE genes) but highly uniform (between clone r2 at 95% CI = 0.973 ± 0.007) resetting of the cellular transcriptome during reprogramming and were highly similar to eutherian ESCs and iPSCs in their overall transcriptomic and functional profiles. However, monoiPSCs showed unique regulatory architecture of the core pluripotency transcription factors and were more like epiblasts. Our results suggest POU5F1 and the splice variant specific expression of POU5F3 synergistically regulate the opossum pluripotency gene network. It is plausible that POU5F1, POU5F3 splice variant XM_016427856.1, and SOX2 form a self-regulatory network. NANOG expression, however, was specific to monoiPSCs and epiblasts, and displayed a distinct expression profile in embryonic cells. Furthermore, POU5F1 was highly expressed in trophectoderm cells, whereas all other pluripotency transcription factors were significantly downregulated, suggesting that the regulatory architecture of core pluripotency genes of marsupials may be distinct from that of eutherians.

ORGANISM(S): Monodelphis domestica

PROVIDER: GSE206122 | GEO | 2022/11/02

REPOSITORIES: GEO

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Project description:Production of milk is a key characteristic of mammals, but the features of lactation vary greatly between monotreme, marsupial and eutherian mammals. Marsupials have a short gestation followed by a long lactation period, and the milk constituents vary greatly across lactation to meet the changing needs of the developing young. Marsupials are born immunologically naïve and rely on their mother’s milk for immunological protection. The koala is an iconic Australian species and many are increasingly threatened by disease. Here we use a mammary transcriptome, two milk proteomes and the koala genome to comprehensively characterise the protein components of the milk of the koala, with a key focus on the immune constituents during early and late lactation. We have characterised the most abundant peptides present in milk, examined key differences between early and late lactation, and determined differences between the koala and other marsupial species. The most abundant proteins were well characterised mammalian and marsupial-specific milk proteins including β-lactoglobulin, lactotransferrin, caseins and early lactation protein. We have generated a list of 851 immune compounds identified in the mammary transcriptome and examined a range of immune proteins that were highly abundant in the milk proteomes. These include immunoglobulins, complement components and immune receptors. A host of antimicrobial peptides were identified including cathelicidins, lysozyme, WAP four-disulfide core domain protein 2, Mucin-1 and Peptidoglycan recognition protein. We discovered that the previously described marsupial milk protein Very Early Lactation Protein is an ortholog of the eutherian gene Glycam1 (PP3) and likely has an antimicrobial role in milk. We also identified highly abundant koala endogenous retrovirus sequences in the mammary and milk transcriptome and proteomes, identifying a potential route for retroviral transmission from mother to young. Identifying and characterising the immune components of milk is key to understanding how marsupial young are protected throughout lactation and the novel immune compounds identified may have applications in clinical research.

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Monodelphis domestica induced pluripotent stem cells reveal metatherian pluripotency architecture

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