Steering cell migration by alternating blebs and actin-rich protrusions

Diz-Muñoz, Alba and Romanczuk, Pawel and Yu, Weimiao and Bergert, Martin and Ivanovitch, Kenzo D and Salbreux, Guillame and Heisenberg, Carl-Philipp and Paluch, Ewa K (2016) Steering cell migration by alternating blebs and actin-rich protrusions. BMC Biology, 14 (1). Article number: 74 . ISSN 1741-7007

[img] Text
s12915-016-0294-x.pdf - Published Version
Available under License Creative Commons Attribution.
[IST-2016-695-v1+1]
Download (1831Kb)
Official URL: http://dx.doi.org/10.1186/s12915-016-0294-x

Abstract

Background: High directional persistence is often assumed to enhance the efficiency of chemotactic migration. Yet, cells in vivo usually display meandering trajectories with relatively low directional persistence, and the control and function of directional persistence during cell migration in three-dimensional environments are poorly understood. Results: Here, we use mesendoderm progenitors migrating during zebrafish gastrulation as a model system to investigate the control of directional persistence during migration in vivo. We show that progenitor cells alternate persistent run phases with tumble phases that result in cell reorientation. Runs are characterized by the formation of directed actin-rich protrusions and tumbles by enhanced blebbing. Increasing the proportion of actin-rich protrusions or blebs leads to longer or shorter run phases, respectively. Importantly, both reducing and increasing run phases result in larger spatial dispersion of the cells, indicative of reduced migration precision. A physical model quantitatively recapitulating the migratory behavior of mesendoderm progenitors indicates that the ratio of tumbling to run times, and thus the specific degree of directional persistence of migration, are critical for optimizing migration precision. Conclusions: Together, our experiments and model provide mechanistic insight into the control of migration directionality for cells moving in three-dimensional environments that combine different protrusion types, whereby the proportion of blebs to actin-rich protrusions determines the directional persistence and precision of movement by regulating the ratio of tumbling to run times.

Item Type: Article
DOI: 10.1186/s12915-016-0294-x
Uncontrolled Keywords: Bleb, cell migration, Persistence, Actin-rich protrusion, Directionality, Protrusion orientation, Run and tumble
Subjects: 500 Science > 570 Life sciences; biology > 572 Biochemistry
500 Science > 570 Life sciences; biology > 576 Genetics and evolution
Research Group: Heisenberg Group
SWORD Depositor: Sword Import User
Depositing User: Sword Import User
Date Deposited: 05 Dec 2016 15:13
Last Modified: 30 Aug 2017 14:42
URI: https://repository.ist.ac.at/id/eprint/695

Actions (login required)

View Item View Item