Mechanosensation of Tight Junctions Depends on ZO-1 Phase Separation and Flow.

Cornelia Schwayer, Shayan Shamipour, Kornelija Pranjic-Ferscha, Alexandra Schauer, Maria Balda, Masazumi Tada, Karl Matter, Carl-Philipp Heisenberg

Cell 2019 Oct 31

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Cell-cell junctions respond to mechanical forces by changing their organization and function. To gain insight into the mechanochemical basis underlying junction mechanosensitivity, we analyzed tight junction (TJ) formation between the enveloping cell layer (EVL) and the yolk syncytial layer (YSL) in the gastrulating zebrafish embryo. We found that the accumulation of Zonula Occludens-1 (ZO-1) at TJs closely scales with tension of the adjacent actomyosin network, revealing that these junctions are mechanosensitive. Actomyosin tension triggers ZO-1 junctional accumulation by driving retrograde actomyosin flow within the YSL, which transports non-junctional ZO-1 clusters toward the TJ. Non-junctional ZO-1 clusters form by phase separation, and direct actin binding of ZO-1 is required for stable incorporation of retrogradely flowing ZO-1 clusters into TJs. If the formation and/or junctional incorporation of ZO-1 clusters is impaired, then TJs lose their mechanosensitivity, and consequently, EVL-YSL movement is delayed. Thus, phase separation and flow of non-junctional ZO-1 confer mechanosensitivity to TJs. Copyright © 2019 Elsevier Inc. All rights reserved.

Citation

Cornelia Schwayer, Shayan Shamipour, Kornelija Pranjic-Ferscha, Alexandra Schauer, Maria Balda, Masazumi Tada, Karl Matter, Carl-Philipp Heisenberg. Mechanosensation of Tight Junctions Depends on ZO-1 Phase Separation and Flow. Cell. 2019 Oct 31;179(4):937-952.e18