Formin 3 stabilizes the cytoskeleton of Drosophila tendon cells, thus enabling them to resist muscle tensile forces

TL;DR

Formin 3 helps stabilize Drosophila tendon cells' cytoskeleton, allowing them to resist muscle tension.

Contribution

This study identifies Formin 3 as a key stabilizer of cytoskeletal arrays in tendon cells under muscle tension.

Findings

form3 mutants show stretched tendon cells and muscle retraction due to destabilized cytoskeletal arrays.

Form3 is localized along actin and microtubule arrays, suggesting a role in co-bundling these structures.

Disrupted cytoskeletal arrays in form3 mutants reveal insights into inverted formins' function.

Abstract

The cytoskeleton of Drosophila tendon cells features specialized F-actin and microtubule arrays that endow these cells with resistance to the tensile forces exerted by the attached muscles. In a forward genetic screen for mutants with neuromuscular junction and muscle morphology phenotypes in larvae, we identified formin 3 (form3) as a crucial component for stabilizing these cytoskeletal arrays under muscle tension. form3 mutants exhibit severely stretched tendon cells in contact with directly attached larval body wall muscles, leading to muscle retraction and rounding. Both the actomyosin and microtubule arrays are expanded likewise in these mutants and can separate laterally in extreme cases. Analysis of a natively HA-tagged, functional version of Form3 reveals that Form3 is distributed along the length of these cytoskeletal arrays. Based on our findings and existing data on vertebrate and Caenorhabditis elegans orthologs of form3, we propose that the primary function of Form3 in this context is to co-bundle actin filaments and microtubules, thus maximizing the rigidity of these cytoskeletal structures against muscle tensile forces.

Highlighted Article:
The disrupted cytoskeletal arrays within tendon cells in formin 3 mutants, along with the mid-filament localization of Formin 3, provide further insight into the specific actions of inverted formins.

Figures