Lung Development of Monotremes: Evidence for the Mammalian Morphotype

Ferner, Kirsten; Zeller, Ulrich; Renfree, Marilyn B.

doi:10.1002/ar.20825

Cited by 20 publications

(22 citation statements)

References 31 publications

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“…The structure of the mammalian lung is highly conserved among mammals [78]. The morphogenetic processes of alveolarization and septal maturation across species are similar, but the timing of lung maturation and the degree of lung maturity at birth varies considerably among species, reflecting their gestational lengths [79], [80]. Since a rich capillary network and close apposition of endothelial cells and alveolar epithelial cells must be present for efficient gas exchange, the structural maturation of the lung at birth varies from the late canalicular to early terminal sac stage [81].…”

Section: Discussionmentioning

confidence: 99%

Transcriptional Programs Controlling Perinatal Lung Maturation

Wang

Besnard

et al. 2012

PLoS ONE

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The timing of lung maturation is controlled precisely by complex genetic and cellular programs. Lung immaturity following preterm birth frequently results in Respiratory Distress Syndrome (RDS) and Broncho-Pulmonary Dysplasia (BPD), which are leading causes of mortality and morbidity in preterm infants. Mechanisms synchronizing gestational length and lung maturation remain to be elucidated. In this study, we designed a genome-wide mRNA expression time-course study from E15.5 to Postnatal Day 0 (PN0) using lung RNAs from C57BL/6J (B6) and A/J mice that differ in gestational length by ∼30 hr (B6

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Section: Discussionmentioning

confidence: 99%

Transcriptional Programs Controlling Perinatal Lung Maturation

Wang

Besnard

et al. 2012

PLoS ONE

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“…; Ferner et al. ). Among the major marsupial groups, a range of neonate developmental states exists (G1–G3), and each type shows a characteristic state of lung development (Mess & Ferner, ).…”

Section: Resultsmentioning

confidence: 97%

“…The ontogeny of internal organ development has been examined in several mammalian species for a long time (Hill & Hill, 1955;M€ uller, 1972;Griffiths, 1978;Krause et al 1979a,b;Walker & Gemmell, 1983;Langston et al 1984;Gemmell & Selwood, 1994;Buaboocha & Gemmell, 1997;Makanya et al 2007;Szdzuy et al 2008;Ferner et al 2010;Simpson et al 2011;Modepalli et al 2015). However, comparative studies on the structural developmental state of mammalian neonates, in particular in view of mammalian evolution, are rare (M€ uller, 1972;Szdzuy et al 2008;Ferner et al 2009).…”

Section: Introductionmentioning

confidence: 99%

Comparative anatomy of neonates of the three major mammalian groups (monotremes, marsupials, placentals) and implications for the ancestral mammalian neonate morphotype

2017

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The existing different modes of reproduction in monotremes, marsupials and placentals are the main source for our current understanding of the origin and evolution of the mammalian reproduction. The reproductive strategies and, in particular, the maturity states of the neonates differ remarkably between the three groups. Monotremes, for example, are the only extant mammals that lay eggs and incubate them for the last third of their embryonic development. In contrast, marsupials and placentals are viviparous and rely on intra-uterine development of the neonates via choriovitelline (mainly marsupials) and chorioallantoic (mainly placentals) placentae. The maturity of a newborn is closely linked to the parental care strategy once the neonate is born. The varying developmental degrees of neonates are the main focus of this study. Monotremes and marsupials produce highly altricial and nearly embryonic offspring. Placental mammals always give birth to more developed newborns with the widest range from altricial to precocial. The ability of a newborn to survive and grow in the environment it was born in depends highly on the degree of maturation of vital organs at the time of birth. Here, the anatomy of four neonates of the three major extant mammalian groups is compared. The basis for this study is histological and ultrastructural serial sections of a hatchling of Ornithorhynchus anatinus (Monotremata), and neonates of Monodelphis domestica (Marsupialia), Mesocricetus auratus (altricial Placentalia) and Macroscelides proboscideus (precocial Placentalia). Special attention was given to the developmental stages of the organs skin, lung, liver and kidney, which are considered crucial for the maintenance of vital functions. The state of the organs of newborn monotremes and marsupials are found to be able to support a minimum of vital functions outside the uterus. They are sufficient to survive, but without capacities for additional energetic challenges. The organs of the altricial placental neonate are further developed, able to support the maintenance of vital functions and short-term metabolic increase. The precocial placental newborn shows the most advanced state of organ development, to allow the maintenance of vital functions, stable thermoregulation and high energetic performance. The ancestral condition of a mammalian neonate is interpreted to be similar to the state of organ development found in the newborns of marsupials and monotremes. In comparison, the newborns of altricial and precocial placentals are derived from the ancestral state to a more mature developmental degree associated with advanced organ systems.

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“…During fetal development the lung undergoes extensive morphological changes and these processes are regulated by both intrinsic and extrinsic factors, including maternal growth factors and hormones (Ferner et al, 2009, Fowden, 1995, Fowden and Forhead, 2009, Sibley et al, 1997). One of the key focuses of this study was to use mass spectrometry to identify candidates as potential signalling factors secreted in milk during tammar lactation.…”

Section: Discussionmentioning

confidence: 99%

“…In all mammals, the extent of development at birth depends on the period of intrauterine development as the factors responsible for fetal development are provided by the maternal placenta and amniotic fluid (Ferner et al, 2009, Fowden, 1995, Fowden and Forhead, 2009, Sibley et al, 1997). Subsequently the eutherian neonate has mature organs for normal function.…”

Section: Introductionmentioning

confidence: 99%

Marsupial tammar wallaby delivers milk bioactives to altricial pouch young to support lung development

Modepalli

Hinds

Sharp

et al. 2016

Mechanisms of Development

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Our research is exploiting the marsupial as a model to understand the signals required for lung development. Marsupials have a unique reproductive strategy, the mother gives birth to altricial neonate with an immature lung and the changes in milk composition during lactation in marsupials appears to provide bioactives that can regulate diverse aspects of lung development, including branching morphogenesis, cell proliferation and cell differentiation. These effects are seen with milk collected between 25 and 100 days postpartum. To better understand the temporal effects of milk composition on postnatal lung development we used a cross-fostering technique to restrict the tammar pouch young to milk composition not extending beyond day 25 for 45 days of its early postnatal life. These particular time points were selected as our previous study showed that milk protein collected prior to ~ day 25 had no developmental effect on mouse embryonic lungs in culture. The comparative analysis of the foster group and control young at day 45 postpartum demonstrated that foster pouch young had significantly reduced lung size. The lungs in fostered young were comprised of large intermediate tissue, had a reduced size of airway lumen and a higher percentage of parenchymal tissue. In addition, expression of marker genes for lung development (BMP4, WNT11, AQP-4, HOPX and SPB) were significantly reduced in lungs from fostered young. Further, to identify the potential bioactive expressed by mammary gland that may have developmental effect on pouch young lungs, we performed proteomics analysis on tammar milk through mass-spectrometry and listed the potential bioactives (PDGF, IGFBP5, IGFBPL1 and EGFL6) secreted in milk that may be involved in regulating pouch young lung development. The data suggest that postnatal lung development in the tammar young is most likely regulated by maternal signalling factors supplied through milk.

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Lung Development of Monotremes: Evidence for the Mammalian Morphotype

Cited by 20 publications

References 31 publications

Transcriptional Programs Controlling Perinatal Lung Maturation

Transcriptional Programs Controlling Perinatal Lung Maturation

Comparative anatomy of neonates of the three major mammalian groups (monotremes, marsupials, placentals) and implications for the ancestral mammalian neonate morphotype

Marsupial tammar wallaby delivers milk bioactives to altricial pouch young to support lung development

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