The Epidermis Is a Source of Directional Information for the Migrating Pronephric Duct inAmbystoma mexicanumEmbryos

Abstract

In the urodele Ambystoma mexicanum, the pronephric duct (PND) is formed from a coherent group of cells that migrate from the pronephros to the cloaca along a pathway immediately ventral to the developing somites. The guidance cues used by the migrating PND primordium to find the cloaca are a local property of the migration substratum, are temporally regulated, and are both polarized and oriented. Since the pronephric duct migrates between two tissues--the underlying lateral mesoderm and the overlying epidermis--we performed a study to identify the tissue(s) in which PND guidance cues originate. Through direct manipulation of the epidermis overlying the duct pathway, we show that the migrating PND reads epidermally derived cues (1) along the anterior-posterior axis that direct migration from anterior to posterior and (2) along the dorsal-ventral axis that constrain migration to the duct pathway. Heterochronic grafting experiments reveal that the ability to direct PND migration is a stable property of flank epidermis throughout the period of PND migration. Epidermal cues are, therefore, not responsible for the observed temporal restrictions on PND migration. Thus, the region of the embryo within which the advancing PND tip can migrate actually represents an area where two distinct but required sets of PND migration cues overlap. The epidermis overlying the duct pathway provides directional information; temporal restriction of duct migration is hypothesized to be a property of the flank mesoderm.

Axolotl pronephric duct migration requires an epidermally derived,laminin 1-containing extracellular matrix and the integrin receptorα6β1

“…We show here that the direction of PND migration can be similarly altered by reorientation of epidermally derived ECM collected on polycarbonate carriers. Furthermore, rotated 'E' carriers are as efficient at reorienting PND migration as rotated epidermal grafts [compare results presented here with those in Drawbridge et al (Drawbridge et al, 1995)]. From these observations, we conclude that the directional information previously shown to be a property of the epidermis overlying the migrating PND resides in the epidermal ECM.…”

“…2C). In these experiments, some embryos also exhibited 'DV flaring'; that is, the PND tip spread both dorsally and ventrally, as previously described (Drawbridge et al, 1995). Unconditioned carriers restrained PND migration when placed over migrating host PNDs.…”

“…Epidermal ECM provides directional information to the migrating PND In studies of the effects of epidermal grafts upon axolotl PND migration, Drawbridge et al (Drawbridge et al, 1995) first reported on the role of the overlying epidermis in providing directional cues to the migrating PND. These results showed that the direction of PND migration could be altered by reorienting the overlying epidermis, indicating that the overlying epidermis is a source of directional PND guidance information.…”

“…By transplantation and rotation of epidermal grafts, Drawbridge et al (Drawbridge et al, 1995) have shown that overlying epidermis provides directional cues to the migrating PND. The PND 'reads' this information along the anterior-posterior (AP) axis to direct migration from anterior to posterior (A→P) and along the dorsal-ventral (DV) axis to constrain migration to the PND pathway.…”

Patterning the embryonic kidney: BMP signaling mediates the differentiation of the pronephric tubules and duct in Xenopus laevis

“…This observation further supports a role for BMP signaling in pronephric morphogenesis. Furthermore, BMPs have been shown to be necessary for proper duct migration in amphibians including Xenopus laevis and Ambystoma mexicanum (Drawbridge et al, 1995). These observations sug-gest a model in which BMP signaling also plays a later role during the patterning and differentiation of the cells within the embryonic pronephros.…”