Abstract
BackgroundThe formation and/or maturation of adult organs in vertebrates often takes place during postembryonic development, a period around birth in mammals when thyroid hormone (T3) levels are high. The T3-dependent anuran metamorphosis serves as a model to study postembryonic development. Studies on the remodeling of the intestine during Xenopus (X.) laevis metamorphosis have shown that the development of the adult intestine involves de novo formation of adult stem cells in a process controlled by T3. On the other hand, X. tropicalis, highly related to X. laevis, offers a number of advantages for studying developmental mechanisms, especially at genome-wide level, over X. laevis, largely due to its shorter life cycle and sequenced genome. To establish X. tropicalis intestinal metamorphosis as a model for adult organogenesis, we analyzed the morphological and cytological changes in X. tropicalis intestine during metamorphosis.Methodology/Principal FindingsWe observed that in X. tropicalis, the premetamorphic intestine was made of mainly a monolayer of larval epithelial cells surrounded by little connective tissue except in the single epithelial fold, the typhlosole. During metamorphosis, the larval epithelium degenerates and adult epithelium develops to form a multi-folded structure with elaborate connective tissue and muscles. Interestingly, typhlosole, which is likely critical for adult epithelial development, is present along the entire length of the small intestine in premetamorphic tadpoles, in contrast to X. laevis, where it is present only in the anterior 1/3. T3-treatment induces intestinal remodeling, including the shortening of the intestine and the typhlosole, just like in X. laevis. Conclusions/SignificanceOur observations indicate that the intestine undergoes similar metamorphic changes in X. laevis and X. tropicalis, making it possible to use the large amount of information available on X. laevis intestinal metamorphosis and the genome sequence information and genetic advantages of X. tropicalis to dissect the pathways governing adult intestinal development.
Highlights
The development of many vertebrate organs takes place in two steps, the formation of an immature but functional organ during embryogenesis followed by the maturation into the adult form
The Metamorphosis of the Small Intestine in X. tropicalis Involves Degeneration of the Larval Epithelium Followed by the Formation of the New Adult Epithelium
To examine the changes in the intestine during metamorphosis, cross-sections of the anterior small intestine from X. tropicalis tadpoles at different stages of metamorphosis were stained with Methyl Green Pyronin Y (MGPY), which distinguishes the proliferating adult epithelial cells from the dying larval epithelial cells based on their RNA content
Summary
The development of many vertebrate organs takes place in two steps, the formation of an immature but functional organ during embryogenesis followed by the maturation into the adult form. In mouse, the intestinal epithelium lacks crypts at birth and the villus-crypt axis is formed in the first few weeks after birth as the plasma T3 concentration rises to a peak [2,9,10] In amphibians such as Xenopus (X.) laevis, the transition from the tadpole/larval intestine to the adult form occurs during metamorphosis [2,3,8,11], a process that shares many similarities with postembryonic development in mammals, including the requirement for high levels of T3 [1,12]. We have discovered a distinct difference, that is, the presence of the typhlosole throughout premetamorphic small intestine in X. tropicalis while only in the anterior 1/3 of the small intestine in X. laevis, suggesting possibly distinct regulation of the stem cell development along the anterior-posterior axis of the intestine
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