Compressive forces stabilize microtubules in living cells

被引:42
作者
Li, Yuhui [1 ,2 ]
Kucera, Ondrej [1 ,2 ,3 ]
Cuvelier, Damien [4 ,5 ,6 ]
Rutkowski, David M. [7 ]
Deygas, Mathieu [4 ,5 ]
Rai, Dipti [8 ]
Pavlovic, Tonja [8 ]
Vicente, Filipe Nunes [9 ]
Piel, Matthieu [4 ,5 ]
Giannone, Gregory [9 ]
Vavylonis, Dimitrios [7 ]
Akhmanova, Anna [8 ]
Blanchoin, Laurent [1 ,2 ]
Thery, Manuel [1 ,2 ]
机构
[1] Univ Paris, Hop St Louis, Inst Rech St Louis, CytoMorpho Lab,INSERM,CEA,UMRS1160, Paris, France
[2] Univ Grenoble Alpes, Interdisciplinary Res Inst Grenoble, CytoMorpho Lab, CEA,CNRS,INRA,Lab Phyiol Cellulaire & Vegetale, Grenoble, France
[3] South East Technol Univ, Dept Engn Technol, Waterford, Ireland
[4] Inst Curie, UMR144, Paris, France
[5] Inst Pierre Gilles Gennes, Paris, France
[6] Sorbonne Univ, F-75005 Paris, France
[7] Lehigh Univ, Dept Phys, Bethlehem, PA USA
[8] Univ Utrecht, Fac Sci, Dept Biol, Cell Biol Neurobiol & Biophys, Utrecht, Netherlands
[9] Univ Bordeaux, Interdisciplinary Inst Neurosci, CNRS, IINS,UMR 5297, Bordeaux, France
基金
欧洲研究理事会;
关键词
DYNAMIC INSTABILITY; SELF-REPAIR; FILAMENTS; PLATFORM; CLASP2;
D O I
10.1038/s41563-023-01578-1
中图分类号
O64 [物理化学(理论化学)、化学物理学];
学科分类号
070304 ; 081704 ;
摘要
Microtubules respond to mechanical compression by deforming, becoming more stable, which results in CLASP2 recruitment to the distorted shaft-a process crucial for cell migration through confined spaces. Microtubules are cytoskeleton components with unique mechanical and dynamic properties. They are rigid polymers that alternate phases of growth and shrinkage. Nonetheless, the cells can display a subset of stable microtubules, but it is unclear whether microtubule dynamics and mechanical properties are related. Recent in vitro studies suggest that microtubules have mechano-responsive properties, being able to stabilize their lattice by self-repair on physical damage. Here we study how microtubules respond to cycles of compressive forces in living cells and find that microtubules become distorted, less dynamic and more stable. This mechano-stabilization depends on CLASP2, which relocates from the end to the deformed shaft of microtubules. This process seems to be instrumental for cell migration in confined spaces. Overall, these results demonstrate that microtubules in living cells have mechano-responsive properties that allow them to resist and even counteract the forces to which they are subjected, being a central mediator of cellular mechano-responses.
引用
收藏
页码:913 / +
页数:16
相关论文
共 65 条
[1]   CLASP Mediates Microtubule Repair by Restricting Lattice Damage and Regulating Tubulin Incorporation [J].
Aher, Amol ;
Rai, Dipti ;
Schaedel, Laura ;
Gaillard, Jeremie ;
John, Karin ;
Liu, Qingyang ;
Altelaar, Maarten ;
Blanchoin, Laurent ;
Thery, Manuel ;
Akhmanova, Anna .
CURRENT BIOLOGY, 2020, 30 (11) :2175-+
[2]   Evidence for new C-terminally truncated variants of α- and β-tubulins [J].
Aillaud, Chrystelle ;
Bosc, Christophe ;
Saoudi, Yasmina ;
Denarier, Eric ;
Peris, Leticia ;
Sago, Laila ;
Taulet, Nicolas ;
Cieren, Adeline ;
Tort, Olivia ;
Magiera, Maria M. ;
Janke, Carsten ;
Redeker, Virginie ;
Andrieux, Annie ;
Moutin, Marie-Jo .
MOLECULAR BIOLOGY OF THE CELL, 2016, 27 (04) :640-653
[3]   CLASPs are CLIP-115 and-170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts [J].
Akhmanova, A ;
Hoogenraad, CC ;
Drabek, K ;
Stepanova, T ;
Dortland, B ;
Verkerk, T ;
Vermeulen, W ;
Burgering, BM ;
De Zeeuw, CI ;
Grosveld, F ;
Galjart, N .
CELL, 2001, 104 (06) :923-935
[4]   Mechanisms of microtubule organization in differentiated animal cells [J].
Akhmanova, Anna ;
Kapitein, Lukas C. .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2022, 23 (08) :541-558
[5]   Control of microtubule organization and dynamics: two ends in the limelight [J].
Akhmanova, Anna ;
Steinmetz, Michel O. .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2015, 16 (12) :711-726
[6]   The nucleus is an intracellular propagator of tensile forces in NIH 3T3 fibroblasts [J].
Alam, Samer G. ;
Lovett, David ;
Kim, Dae In ;
Roux, Kyle J. ;
Dickinson, Richard B. ;
Lele, Tanmay P. .
JOURNAL OF CELL SCIENCE, 2015, 128 (10) :1901-1911
[7]   A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis [J].
Ambrose, Chris ;
Allard, Jun F. ;
Cytrynbaum, Eric N. ;
Wasteneys, Geoffrey O. .
NATURE COMMUNICATIONS, 2011, 2
[8]   Self-repair promotes microtubule rescue [J].
Aumeier, Charlotte ;
Schaedel, Laura ;
Gaillard, Jeremie ;
John, Karin ;
Blanchoin, Laurent ;
Thery, Manuel .
NATURE CELL BIOLOGY, 2016, 18 (10) :1054-1064
[9]   Robust Method for High-Throughput Surface Patterning of Deformable Substrates [J].
Azioune, Ammar ;
Carpi, Nicolas ;
Fink, Jenny ;
Chehimi, Mohamed M. ;
Cuvelier, Damien ;
Piel, Matthieu .
LANGMUIR, 2011, 27 (12) :7349-7352
[10]   Actin Stress Fibers Response and Adaptation under Stretch [J].
Bernal, Roberto ;
Van Hemelryck, Milenka ;
Gurchenkov, Basile ;
Cuvelier, Damien .
INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 2022, 23 (09)