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Talin and vinculin combine their activities to trigger actin assembly

Author

Listed:
  • Hong Wang

    (Institute for Integrative Biology of the Cell (I2BC)
    University of Freiburg
    University of Freiburg)

  • Rayan Said

    (Institute for Integrative Biology of the Cell (I2BC))

  • Clémence Nguyen-Vigouroux

    (Institute for Integrative Biology of the Cell (I2BC))

  • Véronique Henriot

    (Institute for Integrative Biology of the Cell (I2BC))

  • Peter Gebhardt

    (University of Freiburg)

  • Julien Pernier

    (Institute for Integrative Biology of the Cell (I2BC))

  • Robert Grosse

    (University of Freiburg
    University of Freiburg)

  • Christophe Le Clainche

    (Institute for Integrative Biology of the Cell (I2BC))

Abstract

Focal adhesions (FAs) strengthen their link with the actin cytoskeleton to resist force. Talin-vinculin association could reinforce actin anchoring to FAs by controlling actin polymerization. However, the actin polymerization activity of the talin-vinculin complex is not known because it requires the reconstitution of the mechanical and biochemical activation steps that control the association of talin and vinculin. By combining kinetic and binding assays with single actin filament observations in TIRF microscopy, we show that the association of talin and vinculin mutants, mimicking mechanically stretched talin and activated vinculin, triggers a sequential mechanism in which filaments are nucleated, capped and released to elongate. In agreement with these observations, FRAP experiments in cells co-expressing the same constitutive mutants of talin and vinculin revealed accelerated growth of stress fibers. Our findings suggest a versatile mechanism for the regulation of actin assembly in FAs subjected to various combinations of biochemical and mechanical cues.

Suggested Citation

  • Hong Wang & Rayan Said & Clémence Nguyen-Vigouroux & Véronique Henriot & Peter Gebhardt & Julien Pernier & Robert Grosse & Christophe Le Clainche, 2024. "Talin and vinculin combine their activities to trigger actin assembly," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53859-1
    DOI: 10.1038/s41467-024-53859-1
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    References listed on IDEAS

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    1. Mingxi Yao & Benjamin T. Goult & Benjamin Klapholz & Xian Hu & Christopher P. Toseland & Yingjian Guo & Peiwen Cong & Michael P. Sheetz & Jie Yan, 2016. "The mechanical response of talin," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    2. Clémence Vigouroux & Véronique Henriot & Christophe Le Clainche, 2020. "Talin dissociates from RIAM and associates to vinculin sequentially in response to the actomyosin force," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Jun Yang & Liang Zhu & Hao Zhang & Jamila Hirbawi & Koichi Fukuda & Pallavi Dwivedi & Jianmin Liu & Tatiana Byzova & Edward F. Plow & Jinhua Wu & Jun Qin, 2014. "Conformational activation of talin by RIAM triggers integrin-mediated cell adhesion," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    4. Carsten Grashoff & Brenton D. Hoffman & Michael D. Brenner & Ruobo Zhou & Maddy Parsons & Michael T. Yang & Mark A. McLean & Stephen G. Sligar & Christopher S. Chen & Taekjip Ha & Martin A. Schwartz, 2010. "Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics," Nature, Nature, vol. 466(7303), pages 263-266, July.
    5. Constantina Bakolitsa & Daniel M. Cohen & Laurie A. Bankston & Andrey A. Bobkov & Gregory W. Cadwell & Lisa Jennings & David R. Critchley & Susan W. Craig & Robert C. Liddington, 2004. "Structural basis for vinculin activation at sites of cell adhesion," Nature, Nature, vol. 430(6999), pages 583-586, July.
    6. Paul Atherton & Ben Stutchbury & De-Yao Wang & Devina Jethwa & Ricky Tsang & Eugenia Meiler-Rodriguez & Pengbo Wang & Neil Bate & Roy Zent & Igor L. Barsukov & Benjamin T. Goult & David R. Critchley &, 2015. "Vinculin controls talin engagement with the actomyosin machinery," Nature Communications, Nature, vol. 6(1), pages 1-12, December.
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