Literature DB >> 18463289

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

Ana-Suncana Smith1, Kheya Sengupta, Stefanie Goennenwein, Udo Seifert, Erich Sackmann.   

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.

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Year:  2008        PMID: 18463289      PMCID: PMC2383988          DOI: 10.1073/pnas.0801706105

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  29 in total

1.  Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates.

Authors:  N Q Balaban; U S Schwarz; D Riveline; P Goichberg; G Tzur; I Sabanay; D Mahalu; S Safran; A Bershadsky; L Addadi; B Geiger
Journal:  Nat Cell Biol       Date:  2001-05       Impact factor: 28.824

2.  Growth and shape stability of a biological membrane adhesion complex in the diffusion-mediated regime.

Authors:  V B Shenoy; L B Freund
Journal:  Proc Natl Acad Sci U S A       Date:  2005-02-22       Impact factor: 11.205

3.  Antagonist-induced deadhesion of specifically adhered vesicles.

Authors:  Ana-Suncana Smith; Barbara G Lorz; Udo Seifert; Erich Sackmann
Journal:  Biophys J       Date:  2005-11-04       Impact factor: 4.033

4.  Theory of force regulation by nascent adhesion sites.

Authors:  Robijn Bruinsma
Journal:  Biophys J       Date:  2005-04-22       Impact factor: 4.033

5.  Effective adhesion strength of specifically bound vesicles.

Authors:  Ana-Suncana Smith; Udo Seifert
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2005-06-07

6.  Force-induced adsorption and anisotropic growth of focal adhesions.

Authors:  Achim Besser; Samuel A Safran
Journal:  Biophys J       Date:  2006-03-02       Impact factor: 4.033

7.  Theoretical and experimental studies on cross-bridge migration during cell disaggregation.

Authors:  A Tozeren; K L Sung; S Chien
Journal:  Biophys J       Date:  1989-03       Impact factor: 4.033

8.  Raft partitioning and dynamic behavior of human placental alkaline phosphatase in giant unilamellar vesicles.

Authors:  Nicoletta Kahya; Deborah A Brown; Petra Schwille
Journal:  Biochemistry       Date:  2005-05-24       Impact factor: 3.162

9.  Extracellular matrix controls myosin light chain phosphorylation and cell contractility through modulation of cell shape and cytoskeletal prestress.

Authors:  Thomas R Polte; Gabriel S Eichler; Ning Wang; Donald E Ingber
Journal:  Am J Physiol Cell Physiol       Date:  2004-03       Impact factor: 4.249

10.  Influence of receptor lateral mobility on adhesion strengthening between membranes containing LFA-3 and CD2.

Authors:  P Y Chan; M B Lawrence; M L Dustin; L M Ferguson; D E Golan; T A Springer
Journal:  J Cell Biol       Date:  1991-10       Impact factor: 10.539

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  29 in total

1.  Nucleation and growth of integrin adhesions.

Authors:  Erdinç Atilgan; Ben Ovryn
Journal:  Biophys J       Date:  2009-05-06       Impact factor: 4.033

Review 2.  Probing mechanical principles of focal contacts in cell-matrix adhesion with a coupled stochastic-elastic modelling framework.

Authors:  Huajian Gao; Jin Qian; Bin Chen
Journal:  J R Soc Interface       Date:  2011-06-01       Impact factor: 4.118

3.  Lifetime and strength of periodic bond clusters between elastic media under inclined loading.

Authors:  Jin Qian; Jizeng Wang; Yuan Lin; Huajian Gao
Journal:  Biophys J       Date:  2009-11-04       Impact factor: 4.033

4.  Statistical Mechanics of an Elastically Pinned Membrane: Static Profile and Correlations.

Authors:  Josip Augustin Janeš; Henning Stumpf; Daniel Schmidt; Udo Seifert; Ana-Sunčana Smith
Journal:  Biophys J       Date:  2018-12-08       Impact factor: 4.033

Review 5.  Supported lipid bilayer platforms to probe cell mechanobiology.

Authors:  Roxanne Glazier; Khalid Salaita
Journal:  Biochim Biophys Acta Biomembr       Date:  2017-05-11       Impact factor: 3.747

6.  Specific and reversible DNA-directed self-assembly of oil-in-water emulsion droplets.

Authors:  Maik Hadorn; Eva Boenzli; Kristian T Sørensen; Harold Fellermann; Peter Eggenberger Hotz; Martin M Hanczyc
Journal:  Proc Natl Acad Sci U S A       Date:  2012-11-21       Impact factor: 11.205

7.  Force-induced formation and propagation of adhesion nanodomains in living fungal cells.

Authors:  David Alsteens; Melissa C Garcia; Peter N Lipke; Yves F Dufrêne
Journal:  Proc Natl Acad Sci U S A       Date:  2010-11-08       Impact factor: 11.205

Review 8.  Membrane adhesion and the formation of heterogeneities: biology, biophysics, and biotechnology.

Authors:  V D Gordon; T J O'Halloran; O Shindell
Journal:  Phys Chem Chem Phys       Date:  2015-04-13       Impact factor: 3.676

Review 9.  A conformation-induced oligomerization model for B cell receptor microclustering and signaling.

Authors:  Pavel Tolar; Susan K Pierce
Journal:  Curr Top Microbiol Immunol       Date:  2010       Impact factor: 4.291

10.  Model of SNARE-mediated membrane adhesion kinetics.

Authors:  Jason M Warner; Erdem Karatekin; Ben O'Shaughnessy
Journal:  PLoS One       Date:  2009-08-03       Impact factor: 3.240

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