Mechanical Intercellular Communication via Matrix‐Borne Cell Force Transmission During Vascular Network Formation

Intercellular communication is critical to the formation and homeostatic function of all tissues. Previous work has shown that cells can communicate mechanically via the transmission of cell‐generated forces through their surrounding extracellular matrix, but this process is not well understood. Her...

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Bibliographic Details
Published in:	Advanced science Vol. 11; no. 3; pp. e2306210 - n/a
Main Authors:	Davidson, Christopher D., Midekssa, Firaol S., DePalma, Samuel J., Kamen, Jordan L., Wang, William Y., Jayco, Danica Kristen P., Wieger, Megan E., Baker, Brendon M.
Format:	Journal Article
Language:	English
Published:	Germany John Wiley & Sons, Inc 01-01-2024 Wiley
Subjects:	Biocompatible Materials calcium signaling Cell adhesion & migration Cell Communication Communication electrospinning Endothelial Cells Endothelium Extracellular Matrix fibrous matrices focal adhesion kinase focal adhesions force transmission Hydrogels Hypotheses Ligands mechanical communication Mechanical properties mechanosensitive ion channels Piezo1 Tissue Engineering Topography TRPV4 vasculogenic assembly vasculogenic assembly endothelial cells focal adhesions calcium signaling Piezo1 mechanosensitive ion channels electrospinning focal adhesion kinase TRPV4 force transmission fibrous matrices mechanical communication extracellular matrix
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Summary:	Intercellular communication is critical to the formation and homeostatic function of all tissues. Previous work has shown that cells can communicate mechanically via the transmission of cell‐generated forces through their surrounding extracellular matrix, but this process is not well understood. Here, mechanically defined, synthetic electrospun fibrous matrices are utilized in conjunction with a microfabrication‐based cell patterning approach to examine mechanical intercellular communication (MIC) between endothelial cells (ECs) during their assembly into interconnected multicellular networks. It is found that cell force‐mediated matrix displacements in deformable fibrous matrices underly directional extension and migration of neighboring ECs toward each other prior to the formation of stable cell‐cell connections enriched with vascular endothelial cadherin (VE‐cadherin). A critical role is also identified for calcium signaling mediated by focal adhesion kinase and mechanosensitive ion channels in MIC that extends to multicellular assembly of 3D vessel‐like networks when ECs are embedded within fibrin hydrogels. These results illustrate a role for cell‐generated forces and ECM mechanical properties in multicellular assembly of capillary‐like EC networks and motivates the design of biomaterials that promote MIC for vascular tissue engineering. This work describes how endothelial cells (ECs) utilize mechanical intercellular communication (MIC) during vasculogenic assembly into capillary‐like, multicellular networks. Mechanically permissive matrices and EC actomyosin activity enable long‐range force transmission to direct cell migration and subsequent cell‐cell contact formation. In particular, focal adhesion signaling and stretch‐induced activation of ion channels (Piezo1/TRPV4) are critical to EC MIC and vasculogenic assembly.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	2198-3844 2198-3844
DOI:	10.1002/advs.202306210