The role of glycosaminoglycans in anuran pigment cell migration

Abstract

The migratory pathways of neural crest-derived pigment cells were examined in two anurans, Xenopus laevis and Discoglossus pictus, and correlated with the distribution of glycosaminoglycans (GAG) in the extracellular matrix (ECM) of these pathways. In Xenopus, melanophores in the trunk reach the dermis by initially migrating ventrally, between the neural tube and somites, and then by migrating through the somites to reach the subectodermal space. In Discoglossus, melanophores, iridophores, and xanthophores migrate laterally over the dorsal margin of the somites to reach the dermis. GAG was identified in the light microscope using alcian blue staining and in the electron microscope using ruthenium red staining. The ECM at the dorsal entrance to the lateral pathway in Xenopus and in young Discoglossus (at a stage prior to invasion by pigment cells) is filled with 25-50 nm chondroitin sulphate proteoglycan aggregates. When this ECM in Xenopus is digested in vivo with chondroitinase ABC, melanophores enter the lateral pathway. In older Discoglossus embryos, the migration of pigment cells into the lateral pathway is correlated with increases in the space between the ectoderm and somites and in the number of hyaluronate microfibrils. These observations suggest that chondroitin sulphate proteoglycan in the subectodermal ECM restricts the migration of pigment cells into the lateral pathway by limiting the amount of space for migration and possibly by acting as a less adhesive migratory substratum than the ventral pathway, and that in Discoglossus hyaluronate opens spaces permitting the migration of pigment cells directly over the dorsal margin of the somites.