Inherited apicobasal polarity defines the key features of axon-dendrite polarity in a sensory neuron

• Published in: Current biology 2021-09, Vol.31 (17), p.3768-3783.e3
• Main Authors: Lee, Joo, Magescas, Jérémy, Fetter, Richard D., Feldman, Jessica L., Shen, Kang
• Format: Article
• Language: English
• Subjects: apical constriction; apical junction; apicobasal polarity; axon-dendrite polarity; ciliogenesis; microtubule organizing center; microtubule polarity; neuronal polarity; par complex; γ-tubulin ring complex
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.06.039

Neurons are highly polarized cells with morphologically and functionally distinct dendritic and axonal processes. The molecular mechanisms that establish axon-dendrite polarity in vivo are poorly understood. Here, we describe the initial polarization of posterior deirid (PDE), a ciliated mechanosensory neuron, during development in vivo through 4D live imaging with endogenously tagged proteins. PDE inherits and maintains apicobasal polarity from its epithelial precursor. Its apical domain is directly transformed into the ciliated dendritic tip through apical constriction, which is followed by axonal outgrowth from the opposite basal side of the cell. The apical Par complex and junctional proteins persistently localize at the developing dendritic domain throughout this transition. Consistent with their instructive role in axon-dendrite polarization, conditional depletion of the Par complex and junctional proteins results in robust defects in dendrite and axon formation. During apical constriction, a microtubule-organizing center (MTOC) containing the microtubule nucleator γ-tubulin ring complex (γ-TuRC) forms along the apical junction between PDE and its sister cell in a manner dependent on the Par complex and junctional proteins. This junctional MTOC patterns neuronal microtubule polarity and facilitate the dynein-dependent recruitment of the basal body for ciliogenesis. When non-ciliated neurons are genetically manipulated to obtain ciliated neuronal fate, inherited apicobasal polarity is required for generating ciliated dendritic tips. We propose that inherited apicobasal polarity, together with apical cell-cell interactions drive the morphological and cytoskeletal polarity in early neuronal differentiation. •Inherited apicobasal polarity is maintained through axon-dendrite polarization•A dendritic tip directly forms from apical constriction of the apical domain•Apical polarity proteins are required for forming axons and dendrites•Neuronal microtubules are organized by the apical junction with a guidepost cell The process of axon-dendrite polarization has rarely been seen within the developing nervous system. Lee et al. use live microscopy to directly visualize the initial polarization of a C. elegans neuron, revealing that apicobasal polarity is translated into axon-dendrite polarity in part by organizing the neuronal microtubules.