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Article Dans Une Revue Matrix Biology Année : 2022

Regulation of the collagen IV network by the basement membrane protein perlecan is crucial for squamous epithelial cell morphogenesis and organ architecture

Résumé

All epithelia are surrounded by a specialized extracellular matrix, the basement membrane (BM). During development, this BM contributes to the morphogenesis of epithelial organs through different functions, the most recently added one being the shaping of the tissue. Seminal studies highlight the importance of the mechanical properties of the BM in this process. These rely on two of its core components, Collagen type IV and Perlecan, the first one supplying the BM with rigidity to constrain the tissue, the second one antagonizing this effect. Nevertheless, the number of organs that has been inspected is still scarce, and given that epithelial tissues exhibit a wide array of shapes, their forms are bound to be regulated by distinct mechanisms. This is underscored by mounting evidence that BM composition and assembly/biogenesis is tissue-specific. Moreover, previous reports have essentially focused on the mechanical role of the BM in morphogenesis at the tissue scale, but not the cell scale. Here, we took advantage of the robust conservation of core BM proteins and the limited genetic redundancy of the Drosophila model system to address how this matrix shapes a complex organ comprising a squamous, a cuboidal and a columnar epithelium. We show that Perlecan depletion affects the morphogenesis of the three epithelia, but particularly that of the squamous one, whose planar surface becomes extremely narrow. This defect is due to no other cellular function of Perlecan than its control of the squamous shape of the cells. Furthermore, we find that the lack of Perlecan modifies the structure of the Collagen type IV lattice in the BM of the squamous epithelium, and that the global reduction of Collagen type IV in the Perlecan mutant context substantially restores the morphogenesis of this epithelium. In addition, a stronger decrease in Collagen type IV exclusively in the BM of the squamous epithelium significantly rescues the organization of the two other epithelia. Our data thus sustain a model in which Perlecan counters the rigidity conveyed by Collagen type IV to the BM of the squamous epithelium through the regulation of the assembly of its scaffold, allowing the spreading of the squamous cells, spreading which is compulsory for the architecture of the whole organ.
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hal-03897825 , version 1 (14-12-2022)

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Raphaël Bonche, Prune Smolen, Aline Chessel, Séverine Boisivon, Sabrina Pisano, et al.. Regulation of the collagen IV network by the basement membrane protein perlecan is crucial for squamous epithelial cell morphogenesis and organ architecture. Matrix Biology, 2022, 114, pp.35-66. ⟨10.1016/j.matbio.2022.10.004⟩. ⟨hal-03897825⟩
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