Combinatorial deployment of F-actin regulators to build complex 3D actin structures in vivo

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Abstract

Despite extensive studies on the actin regulators that direct microfilament dynamics, how these regulators are combinatorially utilized in organismal tissues to generate 3D structures is an unresolved question. Here, we present an in-depth characterization of cortical actin cap dynamics and their regulation in vivo. We identify rapid phases of initiation, expansion, duplication and disassembly and examine the functions of 7 different Actin and/or Nucleator Regulators (ANRPs) in guiding these behaviors. We find ANRPs provide distinct activities in building actin cap morphologies – specifically, while DPod1 is a major regulator of actin intensities, Cortactin is required for continued cortical growth, while Coronin functions in both growth and intensity and is required for Cortactin localization to the cap periphery. Unexpectedly, cortical actin populations recover more rapidly after regulator disruption, suggestive of a deep competition for limited G-actin pools, and we measure in vivo Arp2/3 recruitment efficiencies through an ectopic relocalization strategy. Our results illustrate how the coordination of multiple actin regulators can orchestrate organized and dynamic actin structures in a developmental system.

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All data generated or analyzed during this study are included in the manuscript and supporting files. Transgenic stocks have been made freely available.

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Yi Xie

Biological Sciences, University of Denver, Denver, United States

Competing interests
The authors declare that no competing interests exist.
Rashmi Budhathoki

Biological Sciences, University of Denver, Denver, United States

Competing interests
The authors declare that no competing interests exist.
J Todd Blankenship

Biological Sciences, University of Denver, Denver, United States

For correspondence
jblanke4@du.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8687-9527

Funding

National Institute of General Medical Sciences (R01GM127447)

Yi Xie

National Institute of General Medical Sciences (R01GM126422)

Yi Xie

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.