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Research Article

Dynamic force sensing of filamin revealed in single-molecule experiments

Lorenz Rognoni, Johannes Stigler, Benjamin Pelz, Jari Ylänne, and Matthias Rief
PNAS November 27, 2012 109 (48) 19679-19684; https://doi.org/10.1073/pnas.1211274109
Lorenz Rognoni
aPhysik Department E22, Technische Universität München, 85748 Garching, Germany;
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Johannes Stigler
aPhysik Department E22, Technische Universität München, 85748 Garching, Germany;
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Benjamin Pelz
aPhysik Department E22, Technische Universität München, 85748 Garching, Germany;
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Jari Ylänne
bDepartment of Biological and Environmental Science and Nanoscience Center, University of Jyväskylä, FI-40014 Jyväskylä, Finland; and
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Matthias Rief
aPhysik Department E22, Technische Universität München, 85748 Garching, Germany;
cMunich Center for Integrated Protein Science, 81377 München, Germany
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  • For correspondence: mrief@ph.tum.de
  1. Edited by James A. Spudich, Stanford University School of Medicine, Stanford, CA, and approved October 15, 2012 (received for review July 2, 2012)

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Abstract

Mechanical forces are important signals for cell response and development, but detailed molecular mechanisms of force sensing are largely unexplored. The cytoskeletal protein filamin is a key connecting element between the cytoskeleton and transmembrane complexes such as integrins or the von Willebrand receptor glycoprotein Ib. Here, we show using single-molecule mechanical measurements that the recently reported Ig domain pair 20–21 of human filamin A acts as an autoinhibited force-activatable mechanosensor. We developed a mechanical single-molecule competition assay that allows online observation of binding events of target peptides in solution to the strained domain pair. We find that filamin force sensing is a highly dynamic process occurring in rapid equilibrium that increases the affinity to the target peptides by up to a factor of 17 between 2 and 5 pN. The equilibrium mechanism we find here can offer a general scheme for cellular force sensing.

  • optical tweezers
  • mechanosensing

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: mrief{at}ph.tum.de.
  • Author contributions: L.R. and M.R. designed research; L.R. performed research; J.S. and B.P. contributed new reagents/analytic tools; L.R., J.Y., and M.R. analyzed data; and L.R., J.Y., and M.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1211274109/-/DCSupplemental.

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Filamin is a dynamic cellular force sensor
Lorenz Rognoni, Johannes Stigler, Benjamin Pelz, Jari Ylänne, Matthias Rief
Proceedings of the National Academy of Sciences Nov 2012, 109 (48) 19679-19684; DOI: 10.1073/pnas.1211274109

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Filamin is a dynamic cellular force sensor
Lorenz Rognoni, Johannes Stigler, Benjamin Pelz, Jari Ylänne, Matthias Rief
Proceedings of the National Academy of Sciences Nov 2012, 109 (48) 19679-19684; DOI: 10.1073/pnas.1211274109
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