Developmental Basis of Pronephric Defects in Xenopus Body Plan Phenotypes

Abstract

We have used monoclonal antibodies that recognize the pronephric tubules or pronephric duct to explore the induction of the embryonic kidney in developing Xenopus embryos. Morphogenesis of the pronephros was examined in UV-ventralized and lithium-dorsalized embryos. We find that the pronephric tubules are present in all but the strongest UV-induced phenotypes, but absent from relatively moderate lithium phenotypes. Interestingly the pronephric duct, which develops from the ventroposterior portion of the pronephric anlage, is missing from more of the mild UV phenotypes than are pronephric tubules. The loss of the capacity to form pronephroi in UV-ventralized embryos is caused by the loss of tissues capable of inducing the pronephric mesoderm, as marginal zone explants from ventralized embryos are still competent to respond to pronephric-inductive signals. Explant recombination experiments indicate that the tissue responsible for both the loss of pronephroi in UV-ventralized embryos and the induction of pronephroi during normal development is the anterior somites. The absence of pronephroi in relatively mild lithium phenotypes has a developmental basis different from that of the UV phenotype, as explants from lithium-treated embryos are effective inducers of pronephroi in recombinants with competent mesoderm, even though they themselves do not form pronephroi in isolation. Together these data indicate that dorsal tissues, especially the anterior somites, are responsible for the establishment of the intermediate mesoderm and the induction of the embryonic kidneys and that even mild dorsalization destroys the capacity to form cells competent to receive this signal.

Cell fate specification along the anterior–posterior axis of the intermediate mesoderm

“…The second theme suggests that IM that lies anterior to the sixth somite axial level does not express kidney genes, as a consequence of a change in the competence of these cells to respond to kidney-inductive signals as proposed above in two alternative mechanisms. This result is a reminiscent of previous observations in lithium-dorsalized Xenopus embryos, showing the loss of capacity to form cell competence to respond to kidney-inductive signals emanating from dorsal tissues (Seufert et al, 1999). These conclusions may provide a cellular mechanism to explain the formation of the sharp anterior border of kidney genes at the sixth somite axial level.…”

“…Consistent with previous observation made by James and Schultheiss (2003), Pax-2 and Lim-1 were detected in the cultured tissue (data not shown), suggesting that the posterior IM8 is already specified. Previous studies have found that paraxial tissue plays a role in patterning the IM (Seufert et al, 1999;Mauch et al, 2000;James and Schultheiss, 2003). Therefore, to confirm the absence of any paraxial tissue in these cultures, Pax-7 was served as a paraxial marker, be- 8 is already determined to its kidney fate and is autonomous.…”

“…Previous studies have suggested that kidney-inductive signals emanate from the paraxial mesoderm (Seufert et al, 1999;Mauch et al, 2000), although none of these studies have shown kidney induction anterior to the normal kidney morphogenetic field. Moreover, the study by Mauch et al (2000) provides evidence that signaling from the paraxial mesoderm is both required and sufficient for the induction of the pronephros and that the neural tube and notochord are not a source of such inductive signals consistent with another study in Xenopus (Seufert et al, 1999). In our barrier experiments, we also show that kidney-inductive signals in anterior regions emanate from tissues that are located medial to the IM.…”

“…The region of anterior IM6 (in which the graft was transplanted in that experiment, transplantation 2) is still in a migratory state before the formation of the first somites. Previous studies have demonstrated a role for the adjacent paraxial mesoderm in positive regulation of kidney genes in posterior IM (Seufert et al, 1999;Mauch et al, 2000;James and Schultheiss, 2003).…”

“…James and Schultheiss (2003), in turn, suggested that the ectoderm is essential for cell survival but not for kidney gene induction and that the lateral plate mesoderm in different experimental conditions can induce kidney properties in the paraxial mesoderm. Finally, although trunk paraxial mesoderm has been shown to have a critical role in kidney induction, the molecular mechanisms that control this induction remain unknown (Seufert et al, 1999;Mauch et al, 2000;James and Schultheiss, 2003).…”