Rectified random cell motility as a mechanism for embryo elongation

Author:

Regev Ido12,Guevorkian Karine345,Gupta Anupam16,Pourquié Olivier4,Mahadevan L.17ORCID

Affiliation:

1. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA

2. Department of Solar Energy and Environmental Physics, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus 84990, Israel

3. Institut de Génétique et de Biologie Moléculaire et Cellulaire, Université de Strasbourg, CNRS, Inserm, Illkirch, France

4. Harvard Medical School, Department of Genetics, Brigham and Women's Hospital, Department of Pathology, Boston, MA 02115, USA

5. Institut Curie, Université PSL, Sorbonne Université, CNRS UMR168, Laboratoire Physico-Chimie Curie, 75005 Paris, France

6. Department of Physics, Indian Institute of Technology Hyderabad, Telangana 502285, India

7. Department of Physics and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA

Abstract

ABSTRACT The body of vertebrate embryos forms by posterior elongation from a terminal growth zone called the tail bud. The tail bud is a source of highly motile cells that eventually constitute the presomitic mesoderm (PSM), a tissue that plays an important role in elongation movements. PSM cells establish an anterior-posterior cell motility gradient that parallels a gradient associated with the degradation of a specific cellular signal (FGF) known to be implicated in cell motility. Here, we combine the electroporation of fluorescent reporters in the PSM with time-lapse imaging in the chicken embryo to quantify cell diffusive movements along the motility gradient. We show that a simple microscopic model for random cell motility induced by FGF activity along with geometric confinement leads to rectified tissue elongation consistent with our observations. A continuum analog of the microscopic model leads to a macroscopic mechano-chemical model for tissue extension that couples FGF activity-induced cell motility and tissue rheology, and is consistent with the experimentally observed speed and extent of elongation. Together, our experimental observations and theoretical models explain how the continuous addition of cells at the tail bud combined with lateral confinement can be converted into oriented movement and drive body elongation.

Funder

Agence Nationale de la Recherche

Human Frontier Science Program

Schlumberger Foundation

National Institutes of Health

Publisher

The Company of Biologists

Subject

Developmental Biology,Molecular Biology

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