Abstract
Sustained polarity and adhesion of epithelial cells is essential for the protection of our organs and bodies, and this epithelial integrity emerges during organ development amidst numerous programmed morphogenetic assaults. Using the developing Caenorhabditis elegans intestine as an in vivo model, we investigated how epithelia maintain their integrity through cell division and elongation to build a functional tube. Live imaging revealed that apical PAR complex proteins PAR-6/Par6 and PKC-3/aPkc remained apical during mitosis while apical microtubules and microtubule-organizing center (MTOC) proteins were transiently removed. Intestine-specific depletion of PAR-6, PKC-3, and the aPkc regulator CDC-42/Cdc42 caused persistent gaps in the apical MTOC as well as in other apical and junctional proteins after cell division and in non-dividing cells that elongated. Upon hatching, gaps coincided with luminal constrictions that blocked food, and larvae arrested and died. Thus, the apical PAR complex maintains apical and junctional continuity to construct a functional intestinal tube.
Highlights
Epithelia are dynamic tissues composed of polarized and adherent epithelial cells that line organs, provide mechanical resiliency, act as selective barriers, and separate animal bodies from the outside world
The apical surfaces of all the cells face the lumen where they secrete digestive 149 enzymes and absorb nutrients through microvilli, and junctional complexes maintain cell adhesion and barrier function while allowing the open lumen to run unobstructed between the intestinal rings (Dimov and Maduro, 2019). 153 PAR complex proteins remain apical during mitosis, when the apical microtubule42 organizing center (MTOC) is transiently 154 removed We first examined the localization of different polarized proteins during mitosis to determine the impact of cell division on their localization
In addition to microtubules and the γ-Tubulin Ring Complex (γ-TuRC) components TBG-1/γ-tubulin and GIP-1/GCP3, all other MTOC and microtubule-associated proteins we examined left the apical surface during mitosis (Figure 1E)
Summary
Epithelia are dynamic tissues composed of polarized and adherent epithelial cells that line organs, provide mechanical resiliency, act as selective barriers, and separate animal bodies from the outside world. PAR-3 is required to establish the apical domain of intestinal cells along a shared central midline, that later forms the lumen, and to recruit other PAR complex proteins and microtubules to the apical surface (Achilleos et al, 2010; Feldman and Priess, 2012); PAR-6 and PKC-3 localize interdependently to the apical surface, and PAR-6 is required for junction formation but not polarity (Montoyo-Rosario et al, 2020; Totong et al, 2007); and CDC-42 is not required for polarity or junction formation (Zilberman et al, 2017). The discontinuities in apical and junctional proteins became more numerous as elongation progressed, with PAR-6 continuing to be required in later stages of embryonic intestinal elongation, and larvae arrested upon hatching with functionally obstructed intestines showing gaps in the lumen, apical surfaces, and junctions Together, these results demonstrate the importance of these highly conserved PAR complex proteins during development in remodeling the apical domain and junctions to maintain continuity as intestinal cells divide and expand their apical surfaces
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