Abstract
BackgroundThe formation of the vertebrate kidney is tightly regulated and relies on multiple evolutionarily conserved inductive events. These are present in the complex metanephric kidney of higher vertebrates, but also in the more primitive pronephric kidney functional in the larval stages of amphibians and fish. Wnts have long been viewed as central in this process. Canonical β-Catenin-dependent Wnt signaling establishes kidney progenitors and non-canonical β-Catenin-independent Wnt signaling participate in the morphogenetic processes that form the highly sophisticated nephron structure. While some individual Wnt signaling components have been studied extensively in the kidney, the overall pathway has not yet been analyzed in depth.Methodology/Principal FindingsHere we report a detailed expression analysis of all Wnt ligands, receptors and several downstream Wnt effectors during pronephros development in Xenopus laevis using in situ hybridization. Out of 19 Wnt ligands, only three, Wnt4, Wnt9a and Wnt11, are specifically expressed in the pronephros. Others such as Wnt8a are present, but in a broader domain comprising adjacent tissues in addition to the kidney. The same paradigm is observed for the Wnt receptors and its downstream signaling components. Fzd1, Fzd4, Fzd6, Fzd7, Fzd8 as well as Celsr1 and Prickle1 show distinct expression domains in the pronephric kidney, whereas the non-traditional Wnt receptors, Ror2 and Ryk, as well as the majority of the effector molecules are rather ubiquitous. In addition to this spatial regulation, the timing of expression is also tightly regulated. In particular, non-canonical Wnt signaling seems to be restricted to later stages of pronephros development.Conclusion/SignificanceTogether these data suggest a complex cross talk between canonical and non-canonical Wnt signaling is required to establish a functional pronephric kidney.
Highlights
In vertebrates the kidney is an essential organ required to excrete nitrogenous waste and maintain salt and water balance
Expression of Wnt Ligands While Wnt signaling components have been previously analyzed in Xenopus, their expression was not studied in respect to pronephros formation
We examined multiple stages in between these time points, but the subsequent figures depict two stages: stage 25, when the pronephros has been specified, but mesenchymal-epithelial transition required for tubulogenesis has not yet commenced; stage 35, when the epithelial tubules have formed and the pronephros is patterned along the proximo-distal axis
Summary
In vertebrates the kidney is an essential organ required to excrete nitrogenous waste and maintain salt and water balance. While the mesonephros is the adult kidney of fish and amphibians, the metanephros is found in higher vertebrates such as mammals and avians [1,2,3]; the pronephros, the most primitive kidney form is present in all vertebrates during embryonic development It is often not functional and degenerates later on, but is of particular importance for larval stages of aquatic animals and is necessary to regulate their osmotic balance with the surrounding medium [2]. The formation of the vertebrate kidney is tightly regulated and relies on multiple evolutionarily conserved inductive events These are present in the complex metanephric kidney of higher vertebrates, and in the more primitive pronephric kidney functional in the larval stages of amphibians and fish. While some individual Wnt signaling components have been studied extensively in the kidney, the overall pathway has not yet been analyzed in depth
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