Cells Respond to Mechanical Stress by Rapid Disassembly of Caveolae

被引:667
作者
Sinha, Bidisha [2 ,3 ]
Koester, Darius [2 ,3 ]
Ruez, Richard [1 ,4 ]
Gonnord, Pauline [1 ,4 ]
Bastiani, Michele [8 ,9 ]
Abankwa, Daniel [8 ,9 ]
Stan, Radu V. [10 ]
Butler-Browne, Gillian [11 ]
Vedie, Benoit [12 ]
Johannes, Ludger [1 ,4 ]
Morone, Nobuhiro [13 ]
Parton, Robert G. [8 ,9 ]
Raposo, Graca [1 ,5 ,6 ]
Sens, Pierre [7 ]
Lamaze, Christophe [1 ,4 ]
Nassoy, Pierre [2 ,3 ]
机构
[1] CNRS UMR144, F-75248 Paris 05, France
[2] Univ Paris 06, CNRS UMR168, F-75248 Paris 05, France
[3] Inst Curie, Ctr Rech, Chim Phys Lab, F-75248 Paris 05, France
[4] Inst Curie, Ctr Rech, Lab Traf Signalisat & Ciblage Intracellulaires, F-75248 Paris 05, France
[5] PICT IBiSA Inst Curie, F-75248 Paris 05, France
[6] Inst Curie, Ctr Rech, Lab Struct & Compartiments Membranaires, F-75248 Paris 05, France
[7] ESPCI, CNRS UMR 7083, F-75231 Paris 05, France
[8] Univ Queensland, Inst Mol Biosci, Brisbane, Qld 4072, Australia
[9] Ctr Microscopy & Microanal, Brisbane, Qld 4072, Australia
[10] Dartmouth Med Sch, Lebanon, NH 03756 USA
[11] UM76 UPMC, Hop La Pitie Salpetriere, Inst Myol, CNRS AIM,Inserm U974,UMR7215, F-75651 Paris 13, France
[12] Hop Europeen Georges Pompidou, Biochim Lab, F-75015 Paris, France
[13] Natl Ctr Neurol & Psychiat, Natl Inst Neurosci, Dept Ultrastruct Res, Kodaira, Tokyo 1878502, Japan
基金
英国医学研究理事会; 澳大利亚研究理事会;
关键词
SIGNAL-REGULATED KINASE; MEMBRANE TENSION; DEPENDENT ACTIVATION; ENDOTHELIAL-CELLS; IN-VITRO; PROTEIN; ENDOCYTOSIS; MUTATIONS; MUSCLE; GENE;
D O I
10.1016/j.cell.2010.12.031
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
The functions of caveolae, the characteristic plasma membrane invaginations, remain debated. Their abundance in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by osmotic swelling or by uniaxial stretching results in a rapid disappearance of caveolae, in a reduced caveolin/Cavin1 interaction, and in an increase of free caveolins at the plasma membrane. Tether-pulling force measurements in cells and in plasma membrane spheres demonstrate that caveola flattening and disassembly is the primary actin-and ATP-independent cell response that buffers membrane tension surges during mechanical stress. Conversely, stress release leads to complete caveola reassembly in an actin-and ATP-dependent process. The absence of a functional caveola reservoir in myotubes from muscular dystrophic patients enhanced membrane fragility under mechanical stress. Our findings support a new role for caveolae as a physiological membrane reservoir that quickly accommodates sudden and acute mechanical stresses.
引用
收藏
页码:402 / 413
页数:12
相关论文
共 51 条
  • [1] A novel switch region regulates H-ras membrane orientation and signal output
    Abankwa, Daniel
    Hanzal-Bayer, Michael
    Ariotti, Nicolas
    Plowman, Sarah J.
    Gorfe, Alemayehu A.
    Parton, Robert G.
    McCammon, J. Andrew
    Hancock, John F.
    [J]. EMBO JOURNAL, 2008, 27 (05) : 727 - 735
  • [2] Chronic shear induces caveolae formation and alters ERK and Akt responses in endothelial cells
    Boyd, NL
    Park, H
    Yi, H
    Boo, YC
    Sorescu, GP
    Sykes, M
    Jo, H
    [J]. AMERICAN JOURNAL OF PHYSIOLOGY-HEART AND CIRCULATORY PHYSIOLOGY, 2003, 285 (03): : H1113 - H1122
  • [3] Geometric control of cell life and death
    Chen, CS
    Mrksich, M
    Huang, S
    Whitesides, GM
    Ingber, DE
    [J]. SCIENCE, 1997, 276 (5317) : 1425 - 1428
  • [4] Coalescence of membrane tethers:: experiments, theory, and applications
    Cuvelier, D
    Derényi, I
    Bassereau, P
    Nassoy, P
    [J]. BIOPHYSICAL JOURNAL, 2005, 88 (04) : 2714 - 2726
  • [5] Keratin mutations of epidermolysis bullosa simplex alter the kinetics of stress response to osmotic shock
    D'Alessandro, M
    Russell, D
    Morley, SM
    Davies, AM
    Lane, EB
    [J]. JOURNAL OF CELL SCIENCE, 2002, 115 (22) : 4341 - 4351
  • [6] Regulation of endocytosis, exocytosis, and shape by membrane tension
    Dai, J
    Sheetz, MP
    [J]. COLD SPRING HARBOR SYMPOSIA ON QUANTITATIVE BIOLOGY, 1995, 60 : 567 - 571
  • [7] Membrane tether formation from blebbing cells
    Dai, JW
    Sheetz, MP
    [J]. BIOPHYSICAL JOURNAL, 1999, 77 (06) : 3363 - 3370
  • [8] Dai JW, 1998, J NEUROSCI, V18, P6681
  • [9] The secretion-coupled endocytosis correlates with membrane tension changes in RBL 2H3 cells
    Dai, JW
    TingBeall, HP
    Sheetz, MP
    [J]. JOURNAL OF GENERAL PHYSIOLOGY, 1997, 110 (01) : 1 - 10
  • [10] A practical guide to giant vesicles. Probing the membrane nanoregime via optical microscopy
    Dimova, Rumiana
    Aranda, Said
    Bezlyepkina, Natalya
    Nikolov, Vesselin
    Riske, Karin A.
    Lipowsky, Reinhard
    [J]. JOURNAL OF PHYSICS-CONDENSED MATTER, 2006, 18 (28) : S1151 - S1176