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ZO-1 controls endothelial adherens junctions, cell-cell tension, angiogenesis, and barrier formation.


ABSTRACT: Intercellular junctions are crucial for mechanotransduction, but whether tight junctions contribute to the regulation of cell-cell tension and adherens junctions is unknown. Here, we demonstrate that the tight junction protein ZO-1 regulates tension acting on VE-cadherin-based adherens junctions, cell migration, and barrier formation of primary endothelial cells, as well as angiogenesis in vitro and in vivo. ZO-1 depletion led to tight junction disruption, redistribution of active myosin II from junctions to stress fibers, reduced tension on VE-cadherin and loss of junctional mechanotransducers such as vinculin and PAK2, and induced vinculin dissociation from the ?-catenin-VE-cadherin complex. Claudin-5 depletion only mimicked ZO-1 effects on barrier formation, whereas the effects on mechanotransducers were rescued by inhibition of ROCK and phenocopied by JAM-A, JACOP, or p114RhoGEF down-regulation. ZO-1 was required for junctional recruitment of JACOP, which, in turn, recruited p114RhoGEF. ZO-1 is thus a central regulator of VE-cadherin-dependent endothelial junctions that orchestrates the spatial actomyosin organization, tuning cell-cell tension, migration, angiogenesis, and barrier formation.

SUBMITTER: Tornavaca O 

PROVIDER: S-EPMC4362456 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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ZO-1 controls endothelial adherens junctions, cell-cell tension, angiogenesis, and barrier formation.

Tornavaca Olga O   Chia Minghao M   Dufton Neil N   Almagro Lourdes Osuna LO   Conway Daniel E DE   Randi Anna M AM   Schwartz Martin A MA   Matter Karl K   Balda Maria S MS  

The Journal of cell biology 20150309 6


Intercellular junctions are crucial for mechanotransduction, but whether tight junctions contribute to the regulation of cell-cell tension and adherens junctions is unknown. Here, we demonstrate that the tight junction protein ZO-1 regulates tension acting on VE-cadherin-based adherens junctions, cell migration, and barrier formation of primary endothelial cells, as well as angiogenesis in vitro and in vivo. ZO-1 depletion led to tight junction disruption, redistribution of active myosin II from  ...[more]

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