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Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo

François B. Robin, Jonathan B. Michaux, William M. McFadden, Edwin M. Munro
doi: https://doi.org/10.1101/076356
François B. Robin
1Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago IL, 60637
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Jonathan B. Michaux
1Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago IL, 60637
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William M. McFadden
3Biophysics Program, University of Chicago, Chicago IL, 60637
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Edwin M. Munro
1Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago IL, 60637
2Committee on Development, Regeneration and Stem Cell Biology, University of Chicago, Chicago IL, 60637
3Biophysics Program, University of Chicago, Chicago IL, 60637
4Institute for Biophysical Dynamics, University of Chicago, Chicago IL, 60637
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  • For correspondence: emunro@uchicago.edu
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Abstract

Pulsed actomyosin contractility underlies diverse modes of tissue morphogenesis, but the mechanisms that generate pulsed contractions are still poorly understood. Here, we combine quantitative imaging with genetic perturbations and mathematical modeling to identify a core mechanism for pulsed contractility in early C. elegans embryos. We show that pulsed accumulation of actomyosin is governed almost entirely by local control of assembly and disassembly downstream of RhoA. Pulsed activation and inactivation of RhoA precedes, respectively, the accumulation and disappearance of actomyosin, and persists in the near complete absence of Myosin II. Autocatalytic activation of RhoA underlies rapid pulse initiation, while delayed accumulation of the RhoA GTPase activating proteins (GAPs) RGA-3/4 provides negative feedback to terminate each pulse. Mathematical models, tightly constrained by our experiments, confirm that this combination of positive and negative feedback is sufficient to generate locally pulsatile RhoA dynamics and reproduce the observed waveform of RhoA activation and RGA-3/4 accumulation. We propose that excitable RhoA dynamics are a common driver for pulsed contractility that can be tuned or coupled to actomyosin dynamics in different ways to produce a diversity of morphogenetic outcomes.

  • Abbreviations List

    AB
    anterior blastomere in the two-cell stage C. elegans embryo
    AHPH
    active RhoA binding domain of Anillin
    GAP
    GTPase Activating Protein
    NMY-2
    non-muscle myosin heavy chain
    P0
    one-cell C.elegans embryo, or zygote
    TIRF
    total internal reflection
    UTR
    F-actin binding domain of Utrophin
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    Posted September 21, 2016.
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    Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo
    François B. Robin, Jonathan B. Michaux, William M. McFadden, Edwin M. Munro
    bioRxiv 076356; doi: https://doi.org/10.1101/076356
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    Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo
    François B. Robin, Jonathan B. Michaux, William M. McFadden, Edwin M. Munro
    bioRxiv 076356; doi: https://doi.org/10.1101/076356

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