Preexisting tissue mechanical hypertension at adherens junctions disrupts apoptotic extrusion in epithelia.


Journal

Molecular biology of the cell
ISSN: 1939-4586
Titre abrégé: Mol Biol Cell
Pays: United States
ID NLM: 9201390

Informations de publication

Date de publication:
01 Jan 2024
Historique:
pubmed: 30 10 2023
medline: 30 10 2023
entrez: 30 10 2023
Statut: ppublish

Résumé

Apical extrusion is a tissue-intrinsic process that allows epithelia to eliminate unfit or surplus cells. This is exemplified by the early extrusion of apoptotic cells, which is critical to maintain the epithelial barrier and prevent inflammation. Apoptotic extrusion is an active mechanical process, which involves mechanotransduction between apoptotic cells and their neighbors, as well as local changes in tissue mechanics. Here we report that the preexisting mechanical tension at adherens junctions (AJs) conditions the efficacy of apoptotic extrusion. Specifically, increasing baseline mechanical tension by overexpression of a phosphomimetic Myosin II regulatory light chain (MRLC) compromises apoptotic extrusion. This occurs when tension is increased in either the apoptotic cell or its surrounding epithelium. Further, we find that the proinflammatory cytokine, TNFα, stimulates Myosin II and increases baseline AJ tension to disrupt apical extrusion, causing apoptotic cells to be retained in monolayers. Importantly, reversal of mechanical tension with an inhibitory MRLC mutant or tropomyosin inhibitors is sufficient to restore apoptotic extrusion in TNFα-treated monolayers. Together, these findings demonstrate that baseline levels of tissue tension are important determinants of apoptotic extrusion, which can potentially be coopted by pathogenetic factors to disrupt the homeostatic response of epithelia to apoptosis.

Identifiants

pubmed: 37903230
doi: 10.1091/mbc.E23-08-0337
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

br3

Auteurs

Zoya Mann (Z)

Division of Cell and Developmental Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia 4072.

Fayth Lim (F)

Division of Cell and Developmental Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia 4072.

Suzie Verma (S)

Division of Cell and Developmental Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia 4072.

Bageshri N Nanavati (BN)

Division of Cell and Developmental Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia 4072.

Julie M Davies (JM)

Mater Research - The University of Queensland, Woolloongabba, Queensland, Australia 4102.

Jakob Begun (J)

Mater Research - The University of Queensland, Woolloongabba, Queensland, Australia 4102.
Department of Gastroenterology, Mater Hospital Brisbane, South Brisbane, Australia 4101.

Edna C Hardeman (EC)

School of Biomedical Sciences, Faculty of Medicine and Health, Univeristy of New South Wales Sydney, New South Wales, Australia 2052.

Peter W Gunning (PW)

School of Biomedical Sciences, Faculty of Medicine and Health, Univeristy of New South Wales Sydney, New South Wales, Australia 2052.

Deepa Subramanyam (D)

National Centre for Cell Science, Savitribai Phule Pune University, Pune 411007, India.

Alpha S Yap (AS)

Division of Cell and Developmental Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia 4072.

Kinga Duszyc (K)

Division of Cell and Developmental Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia 4072.

Classifications MeSH