Non-canonical apical constriction shapes emergent matrices inC. elegans

Abstract

Specialized epithelia produce apical matrices with distinctive topographies by enigmatic mechanisms. Here, we describe a holistic mechanism that integrates cortical actomyosin dynamics with apical matrix remodeling to pattern C. elegans cuticles. Therein, axial AFBs appear near the surface of lateral epidermal syncytia during an interval of transverse apical constriction (AC). AC gives rise to three temporary semi-circular cellular protrusions beneath a provisional matrix (sheath). In turn, sheath components pattern durable ridges along the midline of adult cuticles (alae). We propose that forces generated by AC are relayed via the sheath to sculpt the the acellular adult cuticle manifest several hours later. Furthermore, we provide evidence that circumferential actin filament bundles (CFBs) near the surface of the adjacent syncytia (hyp7) are largely dispensable for the propagation of annular cuticle structures from one larval stage to the next. Rather, the temporary CFBs extend from actin bundles overlying body wall muscles, which are situated between Ce. hemidesmosomes. Similar mechanisms may contribute to the morphogenesis of integumentary organs in higher metazoans.

A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen inCaenorhabditis elegans

“…Here we show that a spatially and temporally dynamic aECM assembles and disassembles within the vulva lumen during morphogenesis. This aECM shares components with the glycocalyx-like sheath or pre-cuticle matrix that coats other apical surfaces in C. elegans prior to each round of cuticle secretion (Forman-Rubinsky, Cohen, & Sundaram, 2017;Gill et al, 2016;Katz, Maybrun, Maul-Newby, & Frand, 2018;Kelley et al, 2015;Labouesse, 2012;Lazetic & Fay, 2017;Mancuso et al, 2012;Priess & Hirsh, 1986;Vuong-Brender, Suman, & Labouesse, 2017). It contains both fibrillar and gel-like or granular components, and also extracellular vesicles, as observed at the ultrastructural level.…”

“…Transgenes used included: csIs64 (Gill et al, 2016), csIs66[let-653pro::SfGFP::LET-653(ZP);let-653pro::PH::mCherry;lin-48pro::mRFP] X (Cohen, Flatt, Schroeder, & Sundaram, 2019), csEx766[lin-48pro::LET-653 (Honigberg & Kenyon, 2000), mfIs4 (Félix, 2007] (Hong et al, 2001). Transgene aaaIs12 [fbn-1pro::FBN-1::mCherry; ttx-3pro::GFP] was derived from array aaaEx78 (Katz et al, 2018) and expresses full-length FBN-1 tagged internally with mCherry inserted just prior to the ZP domain. aaaEx78 rescued fbn-1(tm290) molt defects and other larval lethality from 85% (n=236) in non-transgenic siblings to 10% (n=1676) in transgenic animals.…”

A multi-layered and dynamic apical extracellular matrix shapes the vulva lumen in Caenorhabditis elegans

“…Transgene aaaIs12 [fbn-1pro::FBN-1::mCherry; ttx-3pro::GFP] was derived from array aaaEx78 (Katz et al, 2018) and expresses full-length FBN-1 tagged internally with mCherry inserted just prior to the ZP domain. aaaEx78 rescued fbn-1(tm290) molt defects and other lethality from 85% (n=236) in non-transgenic siblings to 10% (n=1676) in transgenic animals.…”

“…Here, we show that a spatially and temporally dynamic aECM assembles and disassembles within the vulva lumen during morphogenesis. This transient aECM shares components with the glycocalyx-like sheath or pre-cuticle matrix that coats other apical surfaces in C. elegans prior to each round of cuticle secretion ( Forman-Rubinsky et al, 2017 ; Gill et al, 2016 ; Katz et al, 2018 ; Kelley et al, 2015 ; Labouesse, 2012 ; Lažetić and Fay, 2017 ; Mancuso et al, 2012 ; Priess and Hirsh, 1986 ; Vuong-Brender et al, 2017 ). It contains both fibrillar and granular components, and also extracellular vesicles, as observed at the ultrastructural level.…”

Epithelial Shaping by Diverse Apical Extracellular Matrices Requires the Nidogen Domain Protein DEX-1 in Caenorhabditis elegans

“…The epidermal precuticle ensheaths the developing embryo beginning between the bean and 1.5-fold stages (Priess and Hirsh 1986), and later serves as a template for building the cuticle (Costa et al 1997;Forman-Rubinsky et al 2017;Katz et al 2018). A morphologically similar aECM lines developing tubes, such as the excretory duct and pore, that connect to the epidermis (Mancuso et al 2012), but possible molecular distinctions among these precuticle matrices have not been described.…”