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Multicomponent regulation of actin barbed end assembly by twinfilin, formin and capping protein

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  • Heidi Ulrichs

    (Emory University
    Emory University)

  • Ignas Gaska

    (Emory University
    Emory University)

  • Shashank Shekhar

    (Emory University
    Emory University)

Abstract

Cells control actin assembly by regulating reactions at actin filament barbed ends. Formins accelerate elongation, capping protein (CP) arrests growth and twinfilin promotes depolymerization at barbed ends. How these distinct activities get integrated within a shared cytoplasm is unclear. Using microfluidics-assisted TIRF microscopy, we find that formin, CP and twinfilin can simultaneously bind filament barbed ends. Three‑color, single-molecule experiments reveal that twinfilin cannot bind barbed ends occupied by formin unless CP is present. This trimeric complex is short-lived (~1 s), and results in dissociation of CP by twinfilin, promoting formin-based elongation. Thus, the depolymerase twinfilin acts as a pro-formin pro-polymerization factor when both CP and formin are present. While one twinfilin binding event is sufficient to displace CP from the barbed-end trimeric complex, ~31 twinfilin binding events are required to remove CP from a CP-capped barbed end. Our findings establish a paradigm where polymerases, depolymerases and cappers together tune actin assembly.

Suggested Citation

  • Heidi Ulrichs & Ignas Gaska & Shashank Shekhar, 2023. "Multicomponent regulation of actin barbed end assembly by twinfilin, formin and capping protein," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39655-3
    DOI: 10.1038/s41467-023-39655-3
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    References listed on IDEAS

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    1. Johanna Funk & Felipe Merino & Matthias Schaks & Klemens Rottner & Stefan Raunser & Peter Bieling, 2021. "A barbed end interference mechanism reveals how capping protein promotes nucleation in branched actin networks," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. Shashank Shekhar & Mikael Kerleau & Sonja Kühn & Julien Pernier & Guillaume Romet-Lemonne & Antoine Jégou & Marie-France Carlier, 2015. "Formin and capping protein together embrace the actin filament in a ménage à trois," Nature Communications, Nature, vol. 6(1), pages 1-12, December.
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