A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites

Abstract

Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in Drosophila and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in Drosophila. Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons.

Tissue-Specific Transcriptomes Reveal Gene Expression Trajectories in Two Maturing Skin Epithelial Layers in Zebrafish Embryos

“…Axons first innervate the region between basal and periderm cells, but then become enveloped exclusively by basal cells in glial-like ensheathment channels. Formation of these channels requires specific lipid microdomains, association with actin, and the formation of autotypic junctions (Jiang et al 2019), but the signals that initiate ensheathment are unknown. The basal cell-specific genes we identified suggest candidate receptors for ensheathment signals, actin regulatory proteins that could promote membrane invagination, and specific components of autotypic junctions.…”

“…Befitting their function as the embryo’s main barrier to the external environment, periderm cells are connected to one another by tight junctions (Morita et al 2002; O’Brien et al 2012; Yoshida et al 2012; Richardson et al 2014), whereas basal cells lack tight junctions, but have hemidesmosomes that attach them to the basement membrane (Le Guellec et al 2004; Li et al 2011a; O’Brien et al 2012; Muroyama and Lechler 2012). Zebrafish basal cells have a unique interaction with the touch-sensing axon endings that innervate the zebrafish skin: initially, sensory axons innervate the region between the two cell layers, but, by 54 hr post-fertilization (hpf), the apical membranes of basal cells have begun wrapping around axons to ensheath them in structures reminiscent of sheaths formed by non-myelinating Schwann cells (O’Brien et al 2012; Jiang et al 2019). Since zebrafish are externally fertilized, and transgenic reporters for basal cells and periderm cells are available, zebrafish embryos are an ideal model for studying these early events in epithelial development.…”

DeTerm: Software for automatic detection of neuronal dendritic branch terminals via an artificial neural network

“…Previous studies showed that dendritic morphology of class IV neurons is regulated by both genetic and environmental factors (Dong, Shen, & Bülow, ; Jan & Jan, ; Valnegri, Puram, & Bonni, ; Watanabe, Furumizo, Usui, Hattori, & Uemura, ; Yang & Chien, ). Genetic analyses have revealed contributions of transcription factors, vesicular transport, cytoskeletal elements and ligand‐receptor complexes to dendritic pattern formation of class IV neurons (e.g., Hattori et al, ; Hoyer et al, ; Jiang et al, ; Yadav et al, ). On the other hand, dendritic arborization of class IV neurons is also influenced by nutritional conditions; arbors become more complex when larvae are fed on a low‐yeast diet, which contains lower amounts of amino acids and other ingredients, compared to a high‐yeast diet (Watanabe et al, ).…”

Cortical myosin minifilaments orchestrate the arrangement of microridge protrusions on epithelial cell surfaces

“…Previously characterized plasmids in this paper include krt5:Myl12.1-EGFP (van Loon et al, 2020) and UAS:mRuby-PH-PLC (Jiang et al, 2019). krt5-Myh9a-mCherry was constructed using the Gateway-based Tol2-kit (Kwan et al, 2007).…”