Abstract
In amniotes, it is widely accepted that WNTs secreted by the dorsal neural tube form a concentration gradient that regulates early somite patterning and myotome organization. Here we demonstrate in the chicken embryo that WNT protein is not secreted to act at a distance, but rather loaded onto migrating neural crest cells that deliver it to somites. Inhibiting neural crest migration or ablating their population has a profound impact on the WNT response in somites. Furthermore, we show that a central player in the efficient delivery of WNT to somites is the heparan sulfate proteoglycan GPC4, expressed by neural crest. Together, our data describe a novel mode of signaling whereby WNT proteins hitch a ride on migratory neural crest cells to pattern the somites at a distance from its source.
Highlights
Somites are blocks of cells sequentially generated through the epithelialization of the segmental plate (Christ and Ordahl, 1995; Scaal and Christ, 2004)
The dorsomedial lip (DML) plays a crucial role as a myotome-organizing center, as it expresses a secreted factor, WNT11, which acts as a directional cue for the elongation of early myocytes in the anteroposterior axis of the chick embryo
We investigated the mode of signaling of WNTs from the dorsal neural tube to the DML, and uncovered a novel mechanism for long-range WNT signaling, whereby WNT expressed in the dorsal neural tube is loaded onto migrating cells that physically transport the signal to the receiving cells of the DML
Summary
Somites are blocks of cells sequentially generated through the epithelialization of the segmental plate (Christ and Ordahl, 1995; Scaal and Christ, 2004). The DML is the most extensively studied dermomyotome subdomain It plays a crucial role during the initial stage of muscle morphogenesis, during which the primitive muscle (the primary myotome) expands solely from the generation of muscle cells (myocytes) originating from the DML (Denetclaw et al, 2001; Gros et al, 2004; Kahane et al, 1998; Venters and Ordahl, 2002). This production of myocytes at the DML is dependent upon the transient activation of NOTCH signaling in selected epithelial progenitors present in this structure (Rios et al, 2011). WNT11 mediates this effect through the evolutionarily conserved planar cell polarity (PCP) pathway (Gros et al, 2009)
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