Keratins coordinate tissue spreading by balancing spreading forces with tissue material properties

Nature Communications, vol. 17

Abstract

Abstract For tissues to spread, they must deform while staying intact. How spreading tissues balance flexibility with integrity is not yet well understood. Here, we show that keratin intermediate filaments adapt tissue mechanical resilience to the stresses arising in epithelial tissues during spreading. By analyzing the expansion of the enveloping cell layer (EVL) over the yolk cell in zebrafish embryos in vivo, we find that keratin network maturation in EVL cells is promoted by stresses building up within the spreading tissue. Through genetic interference and tissue rheology experiments, complemented by a vertex model with mechanochemical feedback, we demonstrate that stress-induced keratin network maturation in the EVL increases tissue viscosity, to prevent tissue rupture. Further, keratins are required in the yolk cell for mechanosensitive actomyosin network contraction and flow, the forces pulling the EVL. These dual mechanosensitive functions of keratins enable a balance between pulling force production and EVL mechanical resilience, ensuring uniform and robust tissue spreading.

Authors 6

1. Suyash Naik

   Institute of Science and Technology Austria

   Affiliation as printed

   Institute of Science and Technology Austria (ISTA), Klosterneuburg, Austria

2. Yann-Edwin Keta Aachen Lorentz Institute for Theoretical Physics

   Leiden University · Centre National de la Recherche Scientifique · Université Paris Cité · Université Paris Sciences et Lettres · Sorbonne Université · Physique et Mécanique des Milieux Hétérogènes · ESPCI Paris

   Affiliation as printed

   Laboratoire de Physique et Mécanique des Milieux Hétérogènes (PMMH), UMR 7636 CNRS, ESPCI Paris - PSL, Sorbonne Université, Université Paris Cité, Paris, France

   Lorentz Institute for Theoretical Physics, LION, Leiden University, Leiden, The Netherlands

3. Kornelija Pranjic-Ferscha

   Institute of Science and Technology Austria

   Affiliation as printed

   Institute of Science and Technology Austria (ISTA), Klosterneuburg, Austria

4. Édouard Hannezo

   Institute of Science and Technology Austria

   Affiliation as printed

   Institute of Science and Technology Austria (ISTA), Klosterneuburg, Austria

5. Silke Henkes Aachen Lorentz Institute for Theoretical Physics

   Leiden University

   Affiliation as printed

   Lorentz Institute for Theoretical Physics, LION, Leiden University, Leiden, The Netherlands. shenkes@lorentz.leidenuniv.nl

6. Carl‐Philipp Heisenberg

   Institute of Science and Technology Austria

   Affiliation as printed

   Institute of Science and Technology Austria (ISTA), Klosterneuburg, Austria. heisenberg@ist.ac.at