Mechanical forces play crucial roles in a variety
of cell behaviors, including morphogenesis, proliferation and migration. A remarkable
force dependent event across these cell responses is orchestrated dynamics (scrap
and built) of actin cytoskeletons, though the underlying mechanisms are largely
unknown. Actin filaments (AFs) are typically associated with myosin to form a contractile
machinery like stress fibers (SFs). SFs are strengthened with tension while disrupted
with tension release, suggesting that SFs sense tension and transduce it into
their dynamics. We hypothesized that, when SF tension is released, the major SF
component AFs would be disrupted by an actin depolymerizing factor (ADF).
ADF/cofilin is an actin-modulating protein ubiquitously distributed in
eukaryotes and one of the likely candidates to drive SF disruption in response
to tension-release. To test this hypothesis, we placed single AFs under tension
using optical tweezers. When AFs were tensed, cofilin severing of AFs was
largely inhibited in comparison with relaxed AFs. Single molecular imaging revealed
that the cofilin binding rate was decreased when AFs were tensed, indicating
that tension in an AF retards cofilin binding. An AF has a double helix
structure and cofilin binding makes it more twisted, implying that cofilin
binding rate increases when the AF helix is in a more twisted structure. As we found
that torsional fluctuations of single AFs were decreased with tension, it was suggested
that AFs convert tension negatively into their torsional fluctuations to retard
cofilin activity, thus working as a negative tension sensor to disrupt AFs with
cofilin.