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Non-channel mechanosensors working at focal adhesion-stress fiber complex

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Abstract

Mechanosensitive ion channels (MSCs) have long been the only established molecular class of cell mechanosensors; however, in the last decade, a variety of non-channel type mechanosensor molecules have been identified. Many of them are focal adhesion-associated proteins that include integrin, talin, and actin. Mechanosensors must be non-soluble molecules firmly interacting with relatively rigid cellular structures such as membranes (in terms of lateral stiffness), cytoskeletons, and adhesion structures. The partner of MSCs is the membrane in which MSC proteins efficiently transduce changes in the membrane tension into conformational changes that lead to channel opening. By contrast, the integrin, talin, and actin filament form a linear complex of which both ends are typically anchored to the extracellular matrices via integrins. Upon cell deformation by forces, this structure turns out to be a portion that efficiently transduces the generated stress into conformational changes of composite molecules, leading to the activation of integrin (catch bond with extracellular matrices) and talin (unfolding to induce vinculin bindings). Importantly, this structure also serves as an “active” mechanosensor to detect substrate rigidity by pulling the substrate with contraction of actin stress fibers (SFs), which may induce talin unfolding and an activation of MSCs in the vicinity of integrins. A recent study demonstrates that the actin filament acts as a mechanosensor with unique characteristics; the filament behaves as a negative tension sensor in which increased torsional fluctuations by tension decrease accelerate ADF/cofilin binding, leading to filament disruption. Here, we review the latest progress in the study of those non-channel mechanosensors and discuss their activation mechanisms and physiological roles.

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Abbreviations

AJ:

Adherens junction

ECM:

Extracellular matrix

FA:

Focal adhesion

HUVEC:

Human umbilical vein endothelial cell

MSC:

Mechanosensitive ion channel

MSCCa :

Ca2+-permeable mechanosensitive ion channel

VBS:

Vinculin-binding site

SF:

Stress fiber

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Acknowledgments

This work was supported by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (to K.H., H.T., and M.S.), a grant from the Japan Space Forum (to H.T. and M.S.), and a Seed Grant from MBI (to MS).

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Authors and Affiliations

  1. Mechanobiology Institute, National University of Singapore, 117411, Singapore, Singapore

    Hiroaki Hirata & Masahiro Sokabe

  2. Department of Physiology, Nagoya University Graduate School of Medicine, Nagoya, 466-8550, Japan

    Hitoshi Tatsumi

  3. Mechanobiology Laboratory, Nagoya University Graduate School of Medicine, 65 Tsurumai, Showa-ku, Nagoya, Aichi, 466-8550, Japan

    Kimihide Hayakawa & Masahiro Sokabe

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  1. Hiroaki Hirata
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  2. Hitoshi Tatsumi
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  3. Kimihide Hayakawa
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Correspondence to Masahiro Sokabe.

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Hirata, H., Tatsumi, H., Hayakawa, K. et al. Non-channel mechanosensors working at focal adhesion-stress fiber complex. Pflugers Arch - Eur J Physiol 467, 141–155 (2015). https://doi.org/10.1007/s00424-014-1558-3

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