Plexin-B2 orchestrates collective stem cell dynamics via actomyosin contractility, cytoskeletal tension and adhesion

Chrystian Junqueira Alves, Rafael Dariolli, Jonathan Haydak, Sangjo Kang, Theodore Hannah, Robert J. Wiener, Stefanie DeFronzo, Rut Tejero, Gabriele L. Gusella, Aarthi Ramakrishnan, Rodrigo Alves Dias, Alexandre Wojcinski, Santosh Kesari, Li Shen, Eric A. Sobie, José Paulo Rodrigues Furtado de Mendonça, Evren U. Azeloglu, Hongyan Zou () and Roland H. Friedel ()
Additional contact information
Chrystian Junqueira Alves: Icahn School of Medicine at Mount Sinai
Rafael Dariolli: Icahn School of Medicine at Mount Sinai
Jonathan Haydak: Icahn School of Medicine at Mount Sinai
Sangjo Kang: Icahn School of Medicine at Mount Sinai
Theodore Hannah: Icahn School of Medicine at Mount Sinai
Robert J. Wiener: Icahn School of Medicine at Mount Sinai
Stefanie DeFronzo: Icahn School of Medicine at Mount Sinai
Rut Tejero: Icahn School of Medicine at Mount Sinai
Gabriele L. Gusella: Icahn School of Medicine at Mount Sinai
Aarthi Ramakrishnan: Icahn School of Medicine at Mount Sinai
Rodrigo Alves Dias: Federal University of Juiz de Fora
Alexandre Wojcinski: Pacific Neuroscience Institute and John Wayne Cancer Institute at Providence Saint John’s Health Center
Santosh Kesari: Pacific Neuroscience Institute and John Wayne Cancer Institute at Providence Saint John’s Health Center
Li Shen: Icahn School of Medicine at Mount Sinai
Eric A. Sobie: Icahn School of Medicine at Mount Sinai
José Paulo Rodrigues Furtado de Mendonça: Federal University of Juiz de Fora
Evren U. Azeloglu: Icahn School of Medicine at Mount Sinai
Hongyan Zou: Icahn School of Medicine at Mount Sinai
Roland H. Friedel: Icahn School of Medicine at Mount Sinai

Nature Communications, 2021, vol. 12, issue 1, 1-23

Abstract: Abstract During morphogenesis, molecular mechanisms that orchestrate biomechanical dynamics across cells remain unclear. Here, we show a role of guidance receptor Plexin-B2 in organizing actomyosin network and adhesion complexes during multicellular development of human embryonic stem cells and neuroprogenitor cells. Plexin-B2 manipulations affect actomyosin contractility, leading to changes in cell stiffness and cytoskeletal tension, as well as cell-cell and cell-matrix adhesion. We have delineated the functional domains of Plexin-B2, RAP1/2 effectors, and the signaling association with ERK1/2, calcium activation, and YAP mechanosensor, thus providing a mechanistic link between Plexin-B2-mediated cytoskeletal tension and stem cell physiology. Plexin-B2-deficient stem cells exhibit premature lineage commitment, and a balanced level of Plexin-B2 activity is critical for maintaining cytoarchitectural integrity of the developing neuroepithelium, as modeled in cerebral organoids. Our studies thus establish a significant function of Plexin-B2 in orchestrating cytoskeletal tension and cell-cell/cell-matrix adhesion, therefore solidifying the importance of collective cell mechanics in governing stem cell physiology and tissue morphogenesis.

Date: 2021
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DOI: 10.1038/s41467-021-26296-7

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