Abstract
BackgroundAfter a short gestation, marsupials give birth to immature neonates with lungs that are not fully developed and in early life the neonate partially relies on gas exchange through the skin. Therefore, significant lung development occurs after birth in marsupials in contrast to eutherian mammals such as humans and mice where lung development occurs predominantly in the embryo. To explore the mechanisms of marsupial lung development in comparison to eutherians, morphological and gene expression analysis were conducted in the gray short-tailed opossum (Monodelphis domestica).ResultsPostnatal lung development of Monodelphis involves three key stages of development: (i) transition from late canalicular to early saccular stages, (ii) saccular and (iii) alveolar stages, similar to developmental stages overlapping the embryonic and perinatal period in eutherians. Differentially expressed genes were identified and correlated with developmental stages. Functional categories included growth factors, extracellular matrix protein (ECMs), transcriptional factors and signalling pathways related to branching morphogenesis, alveologenesis and vascularisation. Comparison with published data on mice highlighted the conserved importance of extracellular matrix remodelling and signalling pathways such as Wnt, Notch, IGF, TGFβ, retinoic acid and angiopoietin. The comparison also revealed changes in the mammalian gene expression program associated with the initiation of alveologenesis and birth, pointing to subtle differences between the non-functional embryonic lung of the eutherian mouse and the partially functional developing lung of the marsupial Monodelphis neonates. The data also highlighted a subset of contractile proteins specifically expressed in Monodelphis during and after alveologenesis.ConclusionThe results provide insights into marsupial lung development and support the potential of the marsupial model of postnatal development towards better understanding of the evolution of the mammalian bronchioalveolar lung.
Highlights
After a short gestation, marsupials give birth to immature neonates with lungs that are not fully developed and in early life the neonate partially relies on gas exchange through the skin
Postnatal lung development in Monodelphis Histology of lung samples collected from Monodelphis at post-natal days 1, 8, 14, 29, 35, 61 and adult stages (Fig. 1 and Additional file 1: Figure S1 for high resolution images) revealed that the lungs collected 1 day after birth consisted only of a few large air sacs surrounded by a thick layer of epithelial cells (Fig. 1a) typical of the late canalicular stage of development
The sacs were lined with a single layer of cells and were connected with a single respiratory duct, indicating the lungs were transiting from the canalicular to the saccular stage
Summary
Marsupials give birth to immature neonates with lungs that are not fully developed and in early life the neonate partially relies on gas exchange through the skin. Studies of the respiratory mechanism of Julia Creek dunnart and tammar wallaby have demonstrated that neonates perform respiration through the skin during early postnatal development in order to fulfil the requirement for oxygen This limited development changes gradually as lungs mature to perform efficient respiration [12, 16]. Marsupial neonates are similar in development to a late eutherian foetus corresponding to the 40–100 day old human foetal stage, foetal rat at E13-E14 or mice E12-E13 [17, 18], and the immature lung is required to develop further during early lactation to become fully functional This provides improved opportunities to investigate the progressive changes in the gene expression of the postnatal lung and identify mechanisms and factors involved in lung maturation
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