The expression pattern of thyroid hormone response genes in remodeling tadpole tissues defines distinct growth and resorption gene expression programs

Abstract

Thyroid hormone (TH) induces dramatic skeletal and tissue remodeling of the anuran head and body at metamorphosis. The expression pattern of TH up-regulated genes has been correlated with tissues that either grow or resorb at metamorphosis. Whereas the expression of the thyroid hormone receptors in Xenopus laevis tadpoles is ubiquitous, the locations where many of the TH up-regulated genes are activated fall into distinct classes. Genes in the early response class are expressed predominantly in cartilage and brain regions undergoing cell proliferation and at a higher level in the remodeling and growing body than in the resorbing tail. In contrast, expression of genes in the delayed response class is highest in resorbing tissues and higher in the tail than in the body within the subepidermal fibroblast layer, further indicating that this single cell layer is involved in tissue resorption. The expression boundary of delayed response class genes in the subepidermal fibroblasts in the body correlates with epidermal lamella invasion and subsequent adult skin differentiation. Differences in the expression patterns of stromelysin-3 and the delayed response proteinases in the head delineate separate programs of tissue resorption, one for the loss of epithelial structures, and one for the loss of cartilages. Expression of the type III deiodinase is up-regulated in growing tissues nearing completion of their metamorphic changes, suggesting a role for the deiodinase in modulating the influence of TH on these tissues.