Force-induced growth of adhesion domains is controlled by receptor mobility

*II. Institut für Theoretische Physik II, Universität Stuttgart, Pfaffenwaldring 57/III, D-70550 Stuttgart, Germany;
^†Institut für Theoretische Physik I, Universität Erlangen-Nürnberg, Staudtstrasse 7, D-91058 Erlangen, Germany;
^§Institut für Bio- und Nanosysteme-4: Biomechanik, Forschungszentrum Jülich, Leo Brand Strasse, D-52425 Jülich, Germany;
^¶Centre de Recherche en Matière Condensée et Nanosciences, Centre National de la Recherche Scientifique, Campus de Luminy, Case 913, F-13288 Marseille Cedex 9, France; and
^‖E22 Institut für Biophysik, Technische Universität München, James Franck Strasse, D-85748 Garching, Germany

Communicated by L. B. Freund, Brown University, Providence, RI, March 10, 2008 (received for review October 13, 2007)

Abstract

In living cells, adhesion structures have the astonishing ability to grow and strengthen under force. Despite the rising evidence of the importance of this phenomenon, little is known about the underlying mechanism. Here, we show that force-induced adhesion-strengthening can occur purely because of the thermodynamic response to the elastic deformation of the membrane, even in the absence of the actively regulated cytoskeleton of the cell, which was hitherto deemed necessary. We impose pN-forces on two fluid membranes, locally pre-adhered by RGD-integrin binding. One of the binding partners is always mobile whereas the mobility of the other can be switched on or off. Immediate passive strengthening of adhesion structures occurs in both cases. When both binding partners are mobile, strengthening is aided by lateral movement of intact bonds as a transient response to force-induced membrane-deformation. By extending our microinterferometric technique to the suboptical regime, we show that the adhesion, as well as the resistance to force-induced de-adhesion, is greatly enhanced when both, rather than only one, of the binding partners are mobile. We formulate a theory that explains our observations by linking the macroscopic shape deformation with the microscopic formation of bonds, which further elucidates the importance of receptor mobility. We propose this fast passive response to be the first-recognition that triggers signaling events leading to mechanosensing in living cells.

Footnotes

^‡To whom correspondence should be addressed. E-mail: smith{at}theo2.physik.uni-stuttgart.de
Author contributions: A.-S.S., K.S., U.S., and E.S. designed research; A.-S.S. and S.G. performed research; A.-S.S. and K.S. analyzed data; and A.-S.S. and K.S. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/cgi/content/full/0801706105/DCSupplemental.