Physical forces during collective cell migration

被引:899
作者
Trepat, Xavier [1 ,2 ,3 ]
Wasserman, Michael R. [1 ]
Angelini, Thomas E. [4 ]
Millet, Emil [1 ]
Weitz, David A. [4 ]
Butler, James P. [1 ,5 ]
Fredberg, Jeffrey J. [1 ]
机构
[1] Harvard Univ, Sch Publ Hlth, Program Mol & Integrat Physiol Sci, Boston, MA 02115 USA
[2] Univ Barcelona, Unitat Biofis & Bioengn, Inst Bioengn Catalonia, E-08036 Barcelona, Spain
[3] Ciber Enfermedades Respiratorias, Barcelona 08036, Spain
[4] Harvard Univ, Sch Engn & Appl Sci, Cambridge, MA 02138 USA
[5] Harvard Univ, Dept Med, Sch Med, Boston, MA 02115 USA
关键词
FOCAL ADHESIONS; GRANULAR MATTER; BEAD PACKS; MORPHOGENESIS; SHEETS; ACTIN; FLUCTUATIONS; FIBROBLASTS; MICROSCOPY; DIVERSITY;
D O I
10.1038/NPHYS1269
中图分类号
O4 [物理学];
学科分类号
0702 ;
摘要
Fundamental biological processes including morphogenesis, tissue repair and tumour metastasis require collective cell motions(1-3), and to drive these motions cells exert traction forces on their surroundings(4). Current understanding emphasizes that these traction forces arise mainly in 'leader cells' at the front edge of the advancing cell sheet(5-9). Our data are contrary to that assumption and show for the first time by direct measurement that traction forces driving collective cell migration arise predominately many cell rows behind the leading front edge and extend across enormous distances. Traction fluctuations are anomalous, moreover, exhibiting broad non-Gaussian distributions characterized by exponential tails(10-12). Taken together, these unexpected findings demonstrate that although the leader cell may have a pivotal role in local cell guidance, physical forces that it generates are but a small part of a global tug-of-war involving cells well back from the leading edge.
引用
收藏
页码:426 / 430
页数:5
相关论文
共 39 条
[1]   Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts [J].
Beningo, KA ;
Dembo, M ;
Kaverina, I ;
Small, JV ;
Wang, YL .
JOURNAL OF CELL BIOLOGY, 2001, 153 (04) :881-887
[2]   Sheet migration by wounded monolayers as an emergent property of single-cell dynamics [J].
Bindschadler, Michael ;
McGrath, James L. .
JOURNAL OF CELL SCIENCE, 2007, 120 (05) :876-884
[3]   Traction fields, moments, and strain energy that cells exert on their surroundings [J].
Butler, JP ;
Tolic-Norrelykke, IM ;
Fabry, B ;
Fredberg, JJ .
AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, 2002, 282 (03) :C595-C605
[4]   Model for force fluctuations in bead packs [J].
Coppersmith, SN ;
Liu, C ;
Majumdar, S ;
Narayan, O ;
Witten, TA .
PHYSICAL REVIEW E, 1996, 53 (05) :4673-4685
[5]   Spatio-temporal analysis of eukaryotic cell motility by improved force cytometry [J].
del Alamo, Juan C. ;
Meili, Ruedi ;
Alonso-Latorre, Baldomero ;
Rodriguez-Rodriguez, Javier ;
Aliseda, Alberto ;
Firtel, Richard A. ;
Lasheras, Juan C. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (33) :13343-13348
[6]   Stresses at the cell-to-substrate interface during locomotion of fibroblasts [J].
Dembo, M ;
Wang, YL .
BIOPHYSICAL JOURNAL, 1999, 76 (04) :2307-2316
[7]   Force mapping in epithelial cell migration [J].
du Roure, O ;
Saez, A ;
Buguin, A ;
Austin, RH ;
Chavrier, P ;
Silberzan, P ;
Ladoux, B .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (07) :2390-2395
[8]   Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement [J].
Farooqui, R ;
Fenteany, G .
JOURNAL OF CELL SCIENCE, 2005, 118 (01) :51-63
[9]   Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets [J].
Fenteany, G ;
Janmey, PA ;
Stossel, TP .
CURRENT BIOLOGY, 2000, 10 (14) :831-838
[10]   Collective cell migration in morphogenesis and cancer [J].
Friedl, P ;
Hegerfeldt, Y ;
Tusch, M .
INTERNATIONAL JOURNAL OF DEVELOPMENTAL BIOLOGY, 2004, 48 (5-6) :441-449