ZO-1 interacts with YB-1 in endothelial cells to regulate stress granule formation during angiogenesis

Yassine El Bakkouri, Rony Chidiac, Chantal Delisle, Jeanne Corriveau, Gael Cagnone, Vanda Gaonac’h-Lovejoy, Ashley Chin, Éric Lécuyer, Stephane Angers, Jean-Sébastien Joyal, Ivan Topisirovic, Laura Hulea, Alexandre Dubrac and Jean-Philippe Gratton ()
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Yassine El Bakkouri: Université de Montréal
Rony Chidiac: Université de Montréal
Chantal Delisle: Université de Montréal
Jeanne Corriveau: Université de Montréal
Gael Cagnone: Centre Hospitalier Universitaire Sainte-Justine Research Center
Vanda Gaonac’h-Lovejoy: Université de Montréal
Ashley Chin: Institut de recherches cliniques de Montréal (IRCM)
Éric Lécuyer: Institut de recherches cliniques de Montréal (IRCM)
Stephane Angers: University of Toronto
Jean-Sébastien Joyal: Centre Hospitalier Universitaire Sainte-Justine Research Center
Ivan Topisirovic: McGill University
Laura Hulea: Université de Montréal
Alexandre Dubrac: Centre Hospitalier Universitaire Sainte-Justine Research Center
Jean-Philippe Gratton: Université de Montréal

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract Zonula occludens-1 (ZO-1) is involved in the regulation of cell-cell junctions between endothelial cells (ECs). Here we identify the ZO-1 protein interactome and uncover ZO-1 interactions with RNA-binding proteins that are part of stress granules (SGs). Downregulation of ZO-1 increased SG formation in response to stress and protected ECs from cellular insults. The ZO-1 interactome uncovered an association between ZO-1 and Y-box binding protein 1 (YB-1), a constituent of SGs. Arsenite treatment of ECs decreased the interaction between ZO-1 and YB-1, and drove SG assembly. YB-1 expression is essential for SG formation and for the cytoprotective effects induced by ZO-1 downregulation. In the developing retinal vascular plexus of newborn mice, ECs at the front of growing vessels express less ZO-1 but display more YB-1-positive granules than ECs located in the vascular plexus. Endothelial-specific deletion of ZO-1 in mice at post-natal day 7 markedly increased the presence of YB-1-positive granules in ECs of retinal blood vessels, altered tip EC morphology and vascular patterning, resulting in aberrant endothelial proliferation, and arrest in the expansion of the retinal vasculature. Our findings suggest that, through its interaction with YB-1, ZO-1 controls SG formation and the response of ECs to stress during angiogenesis.

Date: 2024
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DOI: 10.1038/s41467-024-48852-7

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