Dynein and EFF-1 control dendrite morphology by regulating the localization pattern of SAX-7 in epidermal cells

Abstract

Our previous work showed that the cell adhesion molecule SAX-7 forms an elaborate pattern in epidermal cells, which instructs PVD dendrite branching. However, the molecular mechanism forming the SAX-7 pattern in the epidermis is not fully understood. Here, we report that the dynein light intermediate chain DLI-1 and the fusogen EFF-1 are required in epidermal cells to pattern SAX-7. While previous reports suggest that these two molecules act cell-autonomously in the PVD, our results show that the disorganized PVD dendritic arbors in these mutants are due to the abnormal SAX-7 localization patterns in epidermal cells. Three lines of evidence support this notion. First, the epidermal SAX-7 pattern was severely affected in and mutants. Second, the abnormal SAX-7 pattern was predictive of the ectopic PVD dendrites. Third, expression of DLI-1 or EFF-1 in the epidermis rescued both the SAX-7 pattern and the disorganized PVD dendrite phenotypes, whereas expression of these molecules in the PVD did not. We also show that DLI-1 functions cell-autonomously in the PVD to promote distal branch formation. These results demonstrate the unexpected roles of DLI-1 and EFF-1 in the epidermis in the control of PVD dendrite morphogenesis.

Morphogenesis of neurons and glia within an epithelium

“…For example, our sense of touch is mediated by mechanosensory neurons that branch along the basal ('inner') side of the skin epithelium. The skin plays a major role in shaping these sensory neurons, and these epithelia-neuron interactions have been extensively studied in vertebrates (Wang et al, 2013;Zimmerman et al, 2014), Drosophila (Parrish et al, 2009;Han et al, 2012;Kim et al, 2012;Jiang et al, 2014;Tenenbaum et al, 2017) and C. elegans (Dong et al, 2013;Liang et al, 2015;Díaz-Balzac et al, 2016;Liu et al, 2016;Zou et al, 2016;Zhu et al, 2017;Celestrin et al, 2018). Similarly, our senses of hearing and taste are mediated by afferent neurons that are positioned at the basal surfaces of epithelia and receive information from specialized non-neuronal sensory cells (hair cells, taste cells) within these epithelia (Roper, 2013;Frank and Goodrich, 2018).…”

Morphogenesis of neurons and glia within an epithelium

“…For example, our sense of touch is mediated by mechanosensory neurons that branch along the basal ("inner") side of the skin epithelium. The skin plays a major role in shaping these sensory neurons, and these epithelia-neuron interactions have been extensively studied in vertebrates (Wang et al, 2013;Zimmerman et al, 2014), Drosophila (Parrish et al, 2009;Han et al, 2012;Kim et al, 2012;Jiang et al, 2014;Tenenbaum et al, 2017), and C. elegans (Dong et al, 2013;Liang et al, 2015;Díaz-Balzac et al, 2016;Liu et al, 2016;Zou et al, 2016;Zhu et al, 2017;Celestrin et al, 2018). Similarly, our senses of hearing and taste are mediated by afferent neurons that are positioned at the basal surfaces of epithelia and receive information from specialized non-neuronal sensory cells (hair cells, taste cells) within these epithelia (Roper, 2013;Frank and Goodrich, 2018).…”

Lessons from Worm Dendritic Patterning

“…In contrast to this model, a recent study supports a cell non-autonomous, indirect function for EFF-1 in PVD morphogenesis (Zhu et al 2017). In a conditional hypomorphic eff-1 mutant, a PVD-specific expression of EFF-1 does not rescue its dendritic phenotypes, whereas epithelial expression of EFF-1 does (Zhu et al 2017). Intriguingly, the study shows that SAX-7 localization is disturbed in eff-1 animals, and its patch-like distribution coincides with hypodermal cells which failed to fuse.…”

“…A recent paper discovered that mig-14/Wntless has a conserved role in (Figure 3a and c). In contrast to this model, a recent study supports a cell non-autonomous, indirect function for EFF-1 in PVD morphogenesis (Zhu et al 2017). In a conditional hypomorphic eff-1 mutant, a PVD-specific expression of EFF-1 does not rescue its dendritic phenotypes, whereas epithelial expression of EFF-1 does (Zhu et al 2017).…”