Wnt-Ror-Dvl signalling and the dystrophin complex organize planar-polarized membrane compartments inC. elegansmuscles

Abstract

The plasma membrane of excitable cells is highly structured and molecular scaffolds recruit proteins to specific membrane compartments. Here, we show that potassium channels and proteins belonging to the dystrophin-associated protein complex define multiple types of planar-polarized membrane compartments at the surface of C. elegans muscle cells. Surprisingly, conserved planar cell polarity proteins are not required for this process. However, we implicate a Wnt signaling module involving the Wnt ligand EGL-20, the Wnt receptor CAM-1, and the intracellular effector DSH-1/disheveled in the formation of this cell polarity pattern. Moreover, using time-resolved and tissue-specific protein degradation, we demonstrate that muscle cell polarity is a dynamic state, requiring continued presence of DSH-1 throughout post-embryonic life. Our results reveal the intricate, highly reproducible, and entirely unsuspected complexity of the worm's sarcolemma. This novel case of planar cell polarity in a tractable genetic model organism may provide valuable insight into the molecular and cellular mechanisms that regulate cellular organization, allowing specific functions to be compartmentalized within distinct plasma membrane domains.

Evolution and developmental functions of the dystrophin-associated protein complex: beyond the idea of a muscle-specific cell adhesion complex

“…During fly neck formation, it is not known whether DAPC function relies on its effect on BM and/or on integrins or whether it reflects a more direct function in actin organization (Villedieu et al, 2023). Beside these studies showing an impact on cytoskeleton organization, a recent preprint reveals a striking planar polarized pattern requiring DAPC in C. elegans muscle cells, suggesting that subcellular polarized targeting might be a general feature for this complex (Peysson et al, 2023). Overall, a first set of morphogenetic events controlled by dystroglycan are linked to its involvement in BM assembly, whereas a second set orients the cell cytoskeleton reorganization, although both can coexist with some interdependence in the same tissue.…”