Diffusible crosslinkers generate directed forces in microtubule networks

Cell
Zdenek LanskyStefan Diez

Abstract

Cytoskeletal remodeling is essential to eukaryotic cell division and morphogenesis. The mechanical forces driving the restructuring are attributed to the action of molecular motors and the dynamics of cytoskeletal filaments, which both consume chemical energy. By contrast, non-enzymatic filament crosslinkers are regarded as mere friction-generating entities. Here, we experimentally demonstrate that diffusible microtubule crosslinkers of the Ase1/PRC1/Map65 family generate directed microtubule sliding when confined between partially overlapping microtubules. The Ase1-generated forces, directly measured by optical tweezers to be in the piconewton-range, were sufficient to antagonize motor-protein driven microtubule sliding. Force generation is quantitatively explained by the entropic expansion of confined Ase1 molecules diffusing within the microtubule overlaps. The thermal motion of crosslinkers is thus harnessed to generate mechanical work analogous to compressed gas propelling a piston in a cylinder. As confinement of diffusible proteins is ubiquitous in cells, the associated entropic forces are likely of importance for cellular mechanics beyond cytoskeletal networks.

References

May 21, 1991·Journal of Theoretical Biology·K Tawada, K Sekimoto
Jul 1, 1985·Proceedings of the National Academy of Sciences of the United States of America·T L Hill
Aug 1, 1994·Biophysical Journal·A J HuntJ Howard
Jul 1, 1993·Biophysical Journal·C S PeskinG F Oster
Jul 10, 2003·Proceedings of the National Academy of Sciences of the United States of America·Roya ZandiWilliam M Gelbart
Feb 4, 2005·Molecular Biology of the Cell·Isabelle LoïodiceP T Tran
May 6, 2005·Nature·Lukas C KapiteinChristoph F Schmidt
Jun 17, 2006·Proceedings of the National Academy of Sciences of the United States of America·Charles L AsburyTrisha N Davis
Jan 8, 2008·Current Opinion in Cell Biology·Amity L Manning, Duane A Compton
Nov 4, 2008·Current Biology : CB·Lukas C KapiteinErwin J G Peterman
Jan 1, 2009·Proceedings of the National Academy of Sciences of the United States of America·Ganhui LanSean X Sun
May 12, 2009·Nature Cell Biology·Gero FinkStefan Diez
May 30, 2009·Proceedings of the National Academy of Sciences of the United States of America·Harold P Erickson
Jan 13, 2010·Current Biology : CB·Erwin J G Peterman, Jonathan M Scholey
Mar 12, 2010·Cellular and Molecular Life Sciences : CMLS·Gul Civelekoglu-Scholey, Jonathan M Scholey
May 5, 2010·The Journal of Cell Biology·Christian Hentrich, Thomas Surrey
Aug 10, 2010·Current Biology : CB·Sean X SunCharles W Wolgemuth
Feb 26, 2011·Science·Johanna RoostaluThomas Surrey
Jun 7, 2011·Biophysical Journal·Felix RuhnowStefan Diez
Jul 19, 2011·Nucleic Acids Research·Robert A FortiesRalf Bundschuh
Sep 6, 2011·Nature Cell Biology·Marcus BraunMarcel E Janson
Mar 7, 2012·Proceedings of the National Academy of Sciences of the United States of America·Xuefei MaRobert S Adelstein
Aug 21, 2012·Nature Cell Biology·Jeanne C StachowiakCarl C Hayden
Apr 24, 2013·Proceedings of the National Academy of Sciences of the United States of America·Vladimir A VolkovEkaterina L Grishchuk
Sep 10, 2014·Proceedings of the National Academy of Sciences of the United States of America·Shane R NelsonDavid M Warshaw

❮ Previous
Next ❯

Citations

Mar 22, 2016·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Marcus BraunStefan Diez
May 12, 2016·Biophysical Journal·Hui-Shun Kuan, Meredith D Betterton
Aug 10, 2016·Current Biology : CB·Thomas H CheffingsMohan K Balasubramanian
Oct 8, 2016·Cell Adhesion & Migration·Mathijs VleugelMarileen Dogterom
Dec 13, 2016·Biology·Jonathan M ScholeyIngrid Brust-Mascher
Mar 11, 2017·Scientific Reports·Nen Saito, Kunihiko Kaneko
Mar 23, 2017·Chemical Society Reviews·H Hess, Jennifer L Ross
May 12, 2017·The Journal of Cell Biology·Scott Forth, Tarun M Kapoor
Jun 3, 2017·Soft Matter·Kasimira T StanhopeJennifer L Ross
Jan 25, 2017·Science Advances·Robert BlackwellMeredith D Betterton
Jul 1, 2017·Nature Cell Biology·Henri G Franquelim, Petra Schwille
Oct 17, 2017·Nature Chemical Biology·Marcus BraunStefan Diez
May 25, 2018·Annual Review of Biophysics·David OriolaJan Brugués
Aug 14, 2018·PLoS Computational Biology·Silke Bergeler, Erwin Frey
Feb 12, 2019·Wiley Interdisciplinary Reviews. Nanomedicine and Nanobiotechnology·Rachel Andorfer, Joshua D Alper
Jul 26, 2019·Biological Reviews of the Cambridge Philosophical Society·Zhen-Yu SheMing-Hui Lu
Oct 29, 2019·Cytoskeleton·Manuel Lera-Ramirez, François J Nédélec
Apr 7, 2020·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Maja Matis
Sep 16, 2019·BMC Biology·Haining ZhouJunlin Teng
Jul 30, 2020·The Journal of Biological Chemistry·Fan ZhengChuanhai Fu
Nov 14, 2015·Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics·S SutradharR Paul
Sep 1, 2017·Soft Matter·Subhadip GhoshDebasish Chaudhuri
Sep 11, 2019·Physical Review. E·Marcel PrelogovićNenad Pavin
Jul 29, 2020·Frontiers in Chemistry·Emilia M GradKerstin G Blank
Sep 26, 2015·Physical Review Letters·D JohannK Kruse
May 28, 2019·Soft Matter·Bianca EdozieJennifer L Ross
Jun 30, 2019·The Journal of Cell Biology·Melissa C PamulaTarun M Kapoor
Jul 28, 2016·Polymers·Jörg SchnaußJosef A Käs
Jun 17, 2020·Journal of Cell Science·Marcus BraunZdenek Lansky
Aug 29, 2020·Physical Review Letters·Harmen Wierenga, Pieter Rein Ten Wolde
Oct 1, 2020·Molecular Biology of the Cell·Ezekiel C ThomasJeffrey K Moore
Nov 26, 2020·Developmental Cell·Nenad Pavin, Iva M Tolić

❮ Previous
Next ❯

Related Concepts

Related Feeds

Cell eTOC

Cell is a scientific journal publishing research across a broad range of disciplines within the life sciences field. Discover the latest research from Cell here.

© 2022 Meta ULC. All rights reserved