4.8 Article

Septins mediate a microtubule-actin crosstalk that enables actin growth on microtubules

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2202803119

Keywords

septins; actin; microtubules; growth cones; actin-microtubule crosstalk

Funding

  1. NIH [5 R35 GM136337-03, 5 R35 GM 140832-02]
  2. Pennsylvania Department of Health CURE grant [SAP 4100085747]

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Cellular morphogenesis and processes such as cell division and migration require the coordination of the microtubule and actin cytoskeletons. This study shows that septins mediate microtubule-actin crosstalk by coupling actin polymerization to microtubule lattices.
Cellular morphogenesis and processes such as cell division and migration require the coordination of the microtubule and actin cytoskeletons. Microtubule-actin crosstalk is poorly understood and largely regarded as the capture and regulation of microtubules by actin. Septins are filamentous guanosine-5'-triphosphate (GTP) binding proteins, which comprise the fourth component of the cytoskeleton along microtubules, actin, and intermediate filaments. Here, we report that septins mediate microtubule-actin crosstalk by coupling actin polymerization to microtubule lattices. Superresolution and platinum replica electron microscopy (PREM) show that septins localize to overlapping microtubules and actin filaments in the growth cones of neurons and non-neuronal cells. We demonstrate that recombinant septin complexes directly crosslink microtubules and actin filaments into hybrid bundles. In vitro reconstitution assays reveal that microtubule-bound septins capture and align stable actin filaments with microtubules. Strikingly, septins enable the capture and polymerization of growing actin filaments on microtubule lattices. In neuronal growth cones, septins are required for the maintenance of the peripheral actin network that fans out from microtubules. These findings show that septins directly mediate microtubule interactions with actin filaments, and reveal a mechanism of microtubule-templated actin growth with broader significance for the self-organization of the cytoskeleton and cellular morphogenesis.

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