Morphogenesis of neurons and glia within an epithelium

Abstract

To sense the outside world, some neurons protrude across epithelia, the cellular barriers that line every surface of our bodies. To study the morphogenesis of such neurons, we examined the C. elegans amphid, in which dendrites protrude through a glial channel at the nose. During development, amphid dendrites extend by attaching to the nose via DYF-7, a type of protein typically found in epithelial apical ECM. Here, we show that amphid neurons and glia exhibit epithelial properties, including tight junctions and apical-basal polarity, and develop in a manner resembling other epithelia. We find that DYF-7 is a fibril-forming apical ECM component that promotes formation of the tube-shaped glial channel, reminiscent of roles for apical ECM in other narrow epithelial tubes. We also identify a requirement for FRM-2, a homolog of EPBL15/moe/Yurt that promotes epithelial integrity in other systems. Finally, we show that other environmentally exposed neurons share a requirement for DYF-7. Together, our results suggest that these neurons and glia can be viewed as part of an epithelium continuous with the skin, and are shaped by mechanisms shared with other epithelia.

AC. elegansZona Pellucida domain protein functions via its ZPc domain

“…To test whether the LET-653 ZPc domain polymerizes or aggregates, we expressed tagged LET-653 fragments in Drosophila S2R+ cells. Although, as previously observed, another C. elegans ZP protein, DYF-7, formed large fibrils on the surface of S2R+ cells (Low et al, 2019), LET-653 fragments formed no such structures and instead appeared diffuse ( Figure S3).…”

“…pAC5.1:: SfGFP:: SfGFP::LET-653(ZP) amplified from pRFR21 (Gill et al, 2016), PCR sewn with unc-54 3'UTR from pCW14 (Low et al, 2019), and inserted into pAC5.1 as XbaI-ApaI fragment. pJC99 pAC5.1::LET-653(ZP):: SfGFP LET-653(ZP)::SfGFP amplified from pJC21, PCR sewn with unc-54 3'UTR from pCW14 (Low et al, 2019), and inserted into pAC5.1 as XbaI-ApaI fragment. pJC100 pAC5.1::…”

“…LET-653(ZP, AYAA)::SfGF P LET-653(ZP, AYAA)::SfGFP amplified from pJC53, PCR sewn with unc-54 3'UTR from pCW14 (Low et al, 2019), and inserted into pAC5.1 as XbaI-ApaI fragment. pJC103 let-653pro::…”

“…ZP proteins are important structural components of cuticle and other aECMs in invertebrates, including Caenorhabditis elegans and Drosophila Plaza et al, 2010). C. elegans has an unusually large set of ZP proteins (Cohen et al, 2019), many of which affect shaping of specific epithelia (Forman-Rubinsky, Cohen, & Sundaram, 2017;Gill et al, 2016;Kelley et al, 2015;Low et al, 2019;Muriel et al, 2003;Sapio, Hilliard, Cermola, Favre, & Bazzicalupo, 2005;Sebastiano, Lassandro, & Bazzicalupo, 1991;Vuong-Brender, Suman, & Labouesse, 2017;Yu, Nguyen, Hall, & Chow, 2000). Furthermore, C. elegans is genetically tractable and is transparent, allowing live imaging of the aECM (Corsi, Wightman, & Chalfie, 2015).…”

A direct glia-to-neuron natural transdifferentiation ensures nimble sensory-motor coordination of male mating behaviour

“…Each sensillum is composed of the dendrites of one or more sensory neurons enveloped by a channel, usually composed of a single sheath glial cell and a single socket glial cell. These sensilla can be viewed as part of an epithelium, continuous with the skin, and are shaped by mechanisms shared with other epithelia 21 . Socket glial cells are highly polarised and adhere to the hypodermis at the distal end of their process where they form a small, ringlike hollow pore in the cuticle through which the sensory dendrites can access the outside world.…”