The plakin domain of <i>C. elegans</i> VAB-10/plectin acts as a hub in a mechanotransduction pathway to promote morphogenesis

Suman, Shashi Kumar; Daday, Csaba; Ferraro, Teresa; Vuong-Brender, Thanh; Tak, Saurabh; Quintin, Sophie; Robin, François; Gräter, Frauke; Labouesse, Michel

doi:10.1242/dev.183780

Cited by 28 publications

(20 citation statements)

References 59 publications

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“…Body cuticle attaches to cell surfaces via hemi-desmosome-like structures (CeHDs) and fibrous organelles (FOs) that span the epidermis and link to body muscle ( Pasti and Labouesse, 2014 ). Apically, the CeHD component VAB-10a (related to spectraplakin) ( Bosher et al, 2003 ) links to the matrillin-like transmembrane proteins MUP-4 ( Hong et al, 2001 ) and MUA-3 ( Bercher et al, 2001 ) to connect the epidermis and cuticle ( Suman et al, 2019 ). However, it is not known whether similar complexes also link other types of aECMs to epithelial cells, particularly in regions where body muscle is not adjacent.…”

Section: Resultsmentioning

confidence: 99%

“…(related to spectraplakin) (Bosher et al, 2003) links to the matrillin-like transmembrane proteins MUP-4 (Hong et al, 2001) and MUA-3 (Bercher et al, 2001) to connect the epidermis and cuticle (Suman et al, 2019). However, it is not known whether similar complexes also link other types of aECMs to epithelial cells, particularly in regions where body muscle is not adjacent.…”

Section: Mup-4/matrillin Expression Coincides With Appearance Of Matumentioning

confidence: 99%

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

Cohen

Sparacio

Belfi

et al. 2020

eLife

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Biological tubes must develop and maintain their proper diameter in order to transport materials efficiently. These tubes are molded and protected in part by apical extracellular matrices (aECMs) that line their lumens. Despite their importance, aECMs are difficult to image in vivo and therefore poorly understood. The C. elegans vulva has been a paradigm for understanding many aspects of organogenesis. Here we describe the vulva luminal matrix, which contains chondroitin proteoglycans, Zona Pellucida (ZP) domain proteins, and other glycoproteins and lipid transporters related to those in mammals. Confocal and transmission electron microscopy revealed, with unprecedented detail, a complex and dynamic aECM. Different matrix factors assemble on the apical surfaces of each vulva cell type, with clear distinctions seen between Ras-dependent (1˚) and Notch-dependent (2˚) cell types. Genetic perturbations suggest that chondroitin and other aECM factors together generate a structured scaffold that both expands and constricts lumen shape.

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Section: Resultsmentioning

confidence: 99%

Section: Mup-4/matrillin Expression Coincides With Appearance Of Matumentioning

confidence: 99%

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

Cohen

Sparacio

Belfi

et al. 2020

eLife

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“…Elucidation of the crystal structure of the cytoskeletal cross-linker plectin and subsequent simulations to analyze stretching and unfolding events indicate that plectin contains an auto-inhibited SH3 domain surrounded by spectrin repeats, which elastically deform under tension and unmask the SH3 domain. [67,68] SH3 domains mediate protein-protein interactions by binding proline-rich regions, yet plectin contains a non-canonical SH3 domain. [69] Furthermore, several tyrosine-phosphorylation sites have been identified in the third and fourth FnIII domains of the 4 cytoplasmic domain that, as judged from the crystal structure of these domains, are not accessible to kinases, but nevertheless have been shown to be phosphorylated.…”

Section: Hemidesmosomes Oppose Mechanotransduction By Focal Adhesionsmentioning

confidence: 99%

Crosstalk between Cell Adhesion Complexes in Regulation of Mechanotransduction

2020

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Physical forces regulate numerous biological processes during development, physiology, and pathology. Forces between the external environment and intracellular actin cytoskeleton are primarily transmitted through integrin-containing focal adhesions and cadherin-containing adherens junctions. Crosstalk between these complexes is well established and modulates the mechanical landscape of the cell. However, integrins and cadherins constitute large families of adhesion receptors and form multiple complexes by interacting with different ligands, adaptor proteins, and cytoskeletal filaments. Recent findings indicate that integrin-containing hemidesmosomes oppose force transduction and traction force generation by focal adhesions. The cytolinker plectin mediates this crosstalk by coupling intermediate filaments to the actin cytoskeleton. Similarly, cadherins in desmosomes might modulate force generation by adherens junctions. Moreover, mechanotransduction can be influenced by podosomes, clathrin lattices, and tetraspanin-enriched microdomains. This review discusses mechanotransduction by multiple integrin-and cadherin-based cell adhesion complexes, which together with the associated cytoskeleton form an integrated network that allows cells to sense, process, and respond to their physical environment.

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“…In addition, their functional sarcomeres also strengthen the connection between apical and basal CeHDs. The contraction of the muscles induces myotactin and VAB-10A-dependent recruitment and maintenance of the G-protein receptor GIT-1 at the CeHDs [99,102]. Here, GIT-1 promotes the activation of the PIX-1-CED-10-PAK-1 axis, resulting in the phosphorylation of the intermediate filament component IFA-3 and its stable localization between both CeHDs.…”

Section: Epidermal-muscle Axismentioning

confidence: 99%

Game of Tissues: How the Epidermis Thrones C. elegans Shape

Carvalho¹,

Broday²

2020

JDB

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The versatility of epithelial cell structure is universally exploited by organisms in multiple contexts. Epithelial cells can establish diverse polarized axes within their tridimensional structure which enables them to flexibly communicate with their neighbors in a 360° range. Hence, these cells are central to multicellularity, and participate in diverse biological processes such as organismal development, growth or immune response and their misfunction ultimately impacts disease. During the development of an organism, the first task epidermal cells must complete is the formation of a continuous sheet, which initiates its own morphogenic process. In this review, we will focus on the C. elegans embryonic epithelial morphogenesis. We will describe how its formation, maturation, and spatial arrangements set the final shape of the nematode C. elegans. Special importance will be given to the tissue-tissue interactions, regulatory tissue-tissue feedback mechanisms and the players orchestrating the process.

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The plakin domain of C. elegans VAB-10/plectin acts as a hub in a mechanotransduction pathway to promote morphogenesis

Abstract: CRISPR-derived deletions reveal the roles of distinct domains from the hemidesmosome sprectraplakin VAB-10 in mechanotransduction during C. elegans

Cited by 28 publications

References 59 publications

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

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

Crosstalk between Cell Adhesion Complexes in Regulation of Mechanotransduction

Game of Tissues: How the Epidermis Thrones C. elegans Shape

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