Division of Cell and Developmental Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia 4072.
Mater Research - The University of Queensland, Woolloongabba, Queensland, Australia 4102.
Mol Biol Cell. 2024 Jan 1;35(1):br3. doi: 10.1091/mbc.E23-08-0337. Epub 2023 Oct 30.
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.
细胞凋亡挤出是一种组织内在的过程,使上皮细胞能够消除不适或多余的细胞。这可以通过早期挤出凋亡细胞来举例说明,这对于维持上皮屏障和防止炎症至关重要。凋亡挤出是一种主动的机械过程,涉及凋亡细胞与其相邻细胞之间的力学转导,以及组织力学的局部变化。在这里,我们报告说,黏附连接(AJs)处预先存在的机械张力决定了凋亡挤出的效果。具体来说,通过过表达磷酸化肌球蛋白 II 调节轻链(MRLC)来增加基础机械张力会损害凋亡挤出。当凋亡细胞或其周围上皮细胞中的张力增加时,就会发生这种情况。此外,我们发现促炎细胞因子 TNFα 会刺激肌球蛋白 II 并增加基础 AJ 张力,从而破坏顶端挤出,导致凋亡细胞在单层中被保留。重要的是,用抑制性 MRLC 突变体或原肌球蛋白抑制剂逆转机械张力足以恢复 TNFα 处理的单层中的凋亡挤出。总之,这些发现表明组织张力的基础水平是凋亡挤出的重要决定因素,病原体因素可能会利用这一因素破坏上皮细胞对凋亡的稳态反应。