Plasticity of lung development in the amphibian, Xenopus laevis

Abstract

SummaryContrary to previous studies, we found that Xenopus laevis tadpoles raised in normoxic water without access to air can routinely complete metamorphosis with lungs that are either severely stunted and uninflated or absent altogether. This is the first demonstration that lung development in a tetrapod can be inhibited by environmental factors and that a tetrapod that relies significantly on lung respiration under unstressed conditions can be raised to forego this function without adverse effects. This study compared lung development in untreated, air-deprived (AD) and air-restored (AR) tadpoles and frogs using whole mounts, histology, BrdU labeling of cell division and antibody staining of smooth muscle actin. We also examined the relationship of swimming and breathing behaviors to lung recovery in AR animals. Inhibition and recovery of lung development occurred at the stage of lung inflation. Lung recovery in AR tadpoles occurred at a predictable and rapid rate and correlated with changes in swimming and breathing behavior. It thus presents a new experimental model for investigating the role of mechanical forces in lung development. Lung recovery in AR frogs was unpredictable and did not correlate with behavioral changes. Its low frequency of occurrence could be attributed to developmental, physical and behavioral changes, the effects of which increase with size and age. Plasticity of lung inflation at tadpole stages and loss of plasticity at postmetamorphic stages offer new insights into the role of developmental plasticity in amphibian lung loss and life history evolution.

<em>Daphnia magna</em> and<em> Xenopus laevis</em> as in vivo models to probe toxicity and uptake of quantum dots functionalized with gH625

“…The early lung use is important in determining the probability of a successful metamorphosis. 66,67 Before metamorphosis, Xenopus lung development at the cellular and molecular levels is comparable to embryonic stages of mouse respiratory system development between embryonic days 8.5 and 10.5. Therefore, it could be considered as a model to define the programs controlling early respiratory system development.…”

Xenopus as a Model for GI/Pancreas Disease

“…In addition to its well known role as a model for early patterning events and posterior foregut development, Xenopus has emerged as a good model system for studying development of the respiratory system [59, 60]. Unique among aquatic model systems, Xenopus embryos rapidly develop lungs in the first few days of embryogenesis, which at the molecular and histological level are similar to early mouse lungs [60••].…”

Caging, but not air deprivation, slows tadpole growth and development in the amphibian Xenopus laevis

“…Though the pathways by which most factors exert their influence remain unstudied, some appear to act through chemical cues and visual and tactile stimuli (Griffiths et al, ; Rot‐Nikcevic et al, ; Gouchie et al, ; Schoeppner and Relyea, ) and many act through complex networks of interactions (Relyea, ; Indermaur et al, ; Brown et al, ; Searle et al, ). Adding to the list, Rose and James () found that raising Xenopus tadpoles in cages that prevent them from breathing air delays the completion of metamorphosis.…”

“…Nonetheless, there are at least two justifications for understanding how the elimination of air breathing might affect tadpole growth and developmental rates. First, air‐deprived (AD) Xenopus tadpoles have been proposed as an experimental model for investigating the changes in gene expression, cell differentiation, and lung morphogenesis that are triggered by the initial entry of air into the lung (Rose and James, ). This event, which shall be referred to here as lung inflation, is inherently difficult to study because it coincides with hatching or birth in amniotes and occurs at variably timed larval stages in amphibians (Wassersug and Seibert, ; Burggren and Just, ; Ultsch et al, ).…”

“…This event, which shall be referred to here as lung inflation, is inherently difficult to study because it coincides with hatching or birth in amniotes and occurs at variably timed larval stages in amphibians (Wassersug and Seibert, ; Burggren and Just, ; Ultsch et al, ). By giving AD Xenopus tadpoles access to air, one can induce lung inflation within a 48 hr period and in a lung rudiment whose development has proceeded in the absence of inflation (Rose and James, ). This allows one to isolate developmental changes that are a direct result of lung inflation.…”