Modeling the roles of cohesotaxis, cell-intercalation, and tissue geometry in collective cell migration of Xenopus mesendoderm

Author:

Comlekoglu Tien12ORCID,Dzamba Bette J.1,Pacheco Gustavo G.1ORCID,Shook David R.1ORCID,Sego T. J.3ORCID,Glazier James A.4ORCID,Peirce Shayn M.2ORCID,DeSimone Douglas W.1ORCID

Affiliation:

1. University of Virginia 1 Department of Cell Biology , , Charlottesville, VA 22908 , USA

2. University of Virginia 2 Department of Biomedical Engineering , , Charlottesville, VA 22903 , USA

3. University of Florida 3 Department of Medicine , , Gainesville, FL 32610 , USA

4. The Biocomplexity Institute, Indiana University 4 Department of Intelligent Systems Engineering and , Bloomington, IN 47408 , USA

Abstract

ABSTRACT Collectively migrating Xenopus mesendoderm cells are arranged into leader and follower rows with distinct adhesive properties and protrusive behaviors. In vivo, leading row mesendoderm cells extend polarized protrusions and migrate along a fibronectin matrix assembled by blastocoel roof cells. Traction stresses generated at the leading row result in the pulling forward of attached follower row cells. Mesendoderm explants removed from embryos provide an experimentally tractable system for characterizing collective cell movements and behaviors, yet the cellular mechanisms responsible for this mode of migration remain elusive. We introduce a novel agent-based computational model of migrating mesendoderm in the Cellular-Potts computational framework to investigate the respective contributions of multiple parameters specific to the behaviors of leader and follower row cells. Sensitivity analyses identify cohesotaxis, tissue geometry, and cell intercalation as key parameters affecting the migration velocity of collectively migrating cells. The model predicts that cohesotaxis and tissue geometry in combination promote cooperative migration of leader cells resulting in increased migration velocity of the collective. Radial intercalation of cells towards the substrate is an additional mechanism contributing to an increase in migratory speed of the tissue. Model outcomes are validated experimentally using mesendoderm tissue explants.

Funder

National Institutes of Health

University of Virginia

Publisher

The Company of Biologists

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1. First person – Tien Comlekoglu;Biology Open;2024-08-15

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