A molecular mechanotransduction pathway regulates collective migration of epithelial cells

Nature Cell Biology

Volumn 17, Issue 3, 2015, Pages 276-287

  Das, Tamal ^a,b   Safferling, Kai ^b   Rausch, Sebastian ^a,b   Grabe, Niels ^b   Boehm, Heike ^a,b   Spatz, Joachim P ^a,b  

^a MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MERLIN; MYOSIN ADENOSINE TRIPHOSPHATASE; RAC1 PROTEIN; RAC1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL INTERACTION; CELL JUNCTION; CELL MIGRATION; CELL MOTION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; LAMELLIPODIUM; MECHANOTRANSDUCTION; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SKIN EPITHELIUM; ACTIN FILAMENT; ANIMAL; CELL ADHESION; CELL COMMUNICATION; CELL LINE; DOG; FLOW KINETICS; GENE EXPRESSION REGULATION; GENETICS; KERATINOCYTE; MDCK CELL LINE; METABOLISM; PSEUDOPODIUM; TIME LAPSE IMAGING; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; ACTOMYOSIN; ANIMALS; CELL ADHESION; CELL COMMUNICATION; CELL LINE; CELL MOVEMENT; DOGS; GENE EXPRESSION REGULATION; HUMANS; INTERCELLULAR JUNCTIONS; KERATINOCYTES; MADIN DARBY CANINE KIDNEY CELLS; MECHANOTRANSDUCTION, CELLULAR; NEUROFIBROMIN 2; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; RHEOLOGY; TIME-LAPSE IMAGING;

EID: 84923805975     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3115     Document Type: Article

References (63)

1. Rorth, P. Fellow travellers: emergent properties of collective cell migration. EMBO Rep. 13, 984-991 (2012
2. Friedl, P. & Gilmour, D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445-457 (2009
3. Friedl, P., Locker, J., Sahai, E. & Segall, J. E. Classifying collective cancer cell invasion. Nat. Cell Biol. 14, 777-783 (2012
4. Ramel, D., Wang, X. B., Laflamme, C., Montell, D. J. & Emery, G. Rab11 regulates cell-cell communication during collective cell movements. Nat. Cell Biol. 15, 317-324 (2013
5. Theveneau, E., et al. Chase-And-run between adjacent cell populations promotes directional collective migration. Nat. Cell Biol. 15, 763 (2013
6. Simpson, K. J., et al. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat. Cell Biol. 10, 1027-1038 (2008
7. Poujade, M., et al. Collective migration of an epithelial monolayer in response to a model wound. Proc. Natl Acad. Sci. USA 104, 15988-15993 (2007
8. Angelini, T. E., Hannezo, E., Trepat, X., Fredberg, J. J. & Weitz, D. A. Cell Migration Driven by Cooperative Substrate Deformation Patterns. Phys. Rev. Lett. 104, 168104 (2010
9. Petitjean, L., et al. Velocity Fields in a Collectively Migrating Epithelium. Biophys. J. 98, 1790-1800 (2010
10. Gaggioli, C., et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 9, 1392-1400 (2007
11. Xu, N., Keung, B. & Myat, M. M. Rho GTPase controls invagination and cohesive migration of the Drosophila salivary gland through Crumbs and Rho-kinase. Dev. Biol. 321, 88-100 (2008
12. Wang, X. B., He, L., Wu, Y. I., Hahn, K. M. & Montell, D. J. Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat. Cell. Biol. 12, 591-597 (2010
13. Hidalgo-Carcedo, C., et al. Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat. Cell Biol. 13, 49-58 (2011
14. Ng, M. R., Besser, A., Danuser, G. & Brugge, J. S. Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility. J. Cell Biol. 199, 545-563 (2012
15. Reffay, M., et al. Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells. Nat. Cell Biol. 16, 217-223 (2014
16. Peglion, F., Llense, F. & Etienne-Manneville, S. Adherens junction treadmilling during collective migration. Nat. Cell Biol. 16, 639-651 (2014
17. Tambe, D. T., et al. Collective cell guidance by cooperative intercellular forces. Nat. Mater. 10, 469-475 (2011
18. Trepat, X., et al. Physical forces during collective cell migration. Nat. Phys. 5, 426-430 (2009
19. Angelini, T. E., et al. Glass-like dynamics of collective cell migration. Proc. Natl Acad. Sci. USA 108, 4714-4719 (2011
20. Dupont, S., et al. Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 (2011
21. Bernascone, I. & Martin-Belmonte, F. Crossroads of Wnt and Hippo in epithelial tissues. Trends Cell Biol. 23, 380-389 (2013
22. Bosveld, F., et al. Mechanical control of morphogenesis by Fat/Dachsous/Four-Jointed planar cell polarity pathway. Science 336, 724-727 (2012
23. Fehon, R. G., McClatchey, A. I. & Bretscher, A. Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11, 276-287 (2010
24. Hamaratoglu, F., et al. The tumour-suppressor genes NF2/Merlin and expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat. Cell Biol. 8, 27-36 (2006
25. Li, W., Cooper, J., Karajannis, M. A. & Giancotti, F. G. Merlin: a tumour suppressor with functions at the cell cortex and in the nucleus. EMBO Rep. 13, 204-215 (2012
26. Cole, B. K., Curto, M., Chan, A. W. & McClatchey, A. I. Localization to the cortical cytoskeleton is necessary for Nf2/Merlin-dependent epidermal growth factor receptor silencing. Mol. Cell Biol. 28, 1274-1284 (2008
27. Wozniak, M. A. & Chen, C. S. Mechanotransduction in development: a growing role for contractility. Nat. Rev. Mol. Cell Biol. 10, 34-43 (2009
28. Vogel, V. & Sheetz, M. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7, 265-275 (2006
29. Tse, J. M., et al. Mechanical compression drives cancer cells toward invasive phenotype. Proc. Natl Acad. Sci. USA 109, 911-916 (2012
30. Serra-Picamal, X., et al. Mechanical waves during tissue expansion. Nat. Phys. 8, 628-634 (2012
31. Yi, C. L., et al. A Tight junction-Associated merlin-Angiomotin complex Mediates Merlin's regulation of mitogenic signaling and tumor suppressive functions. Cancer Cell 19, 527-540 (2011
32. Lallemand, D., Saint-Amaux, A. L. & Giovannini, M. Tumor-suppression functions of merlin are independent of its role as an organizer of the actin cytoskeleton in Schwann cells. J. Cell Sci. 122, 4141-4149 (2009
33. Machacek, M., et al. Coordination of Rho GTPase activities during cell protrusion. Nature 461, 99-103 (2009
34. Wu, Y. I., et al. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461, 104-108 (2009
35. Fenteany, G., Janmey, P. A. & Stossel, T. P. Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr. Biol. 10, 831-838 (2000
36. Okada, T., Lopez-Lago, M. & Giancotti, F. G. Merlin/NF-2 mediates contact inhibition of growth by suppressing recruitment of Rac to the plasma membrane. J. Cell Biol. 171, 361-371 (2005
37. Guo, L., Moon, C., Niehaus, K., Zheng, Y. & Ratner, N. Rac1 Controls Schwann Cell Myelination through cAMP and NF2/merlin. J. Neurosci. 32, 17251-17261 (2012
38. Gladden, A. B., Hebert, A. M., Schneeberger, E. E. & McClatchey, A. I. The NF2 tumor suppressor, Merlin, regulates epidermal development through the establishment of a junctional polarity complex. Dev. Cell 19, 727-739 (2010
39. Hebert, A. M., DuBoff, B., Casaletto, J. B., Gladden, A. B. & McClatchey, A. I. Merlin/ERM proteins establish cortical asymmetry and centrosome position. Genes Dev. 26, 2709-2723 (2012
40. Flaiz, C., Kaempchen, K., Matthies, C. & Hanemann, C. O. Actin-rich protrusions and nonlocalized GTPase activation in Merlin-deficient schwannomas. J. Neuropathol. Exp. Neurol. 66, 608-616 (2007
41. Shaw, R. J., et al. The Nf2 tumor suppressor, merlin, functions in Rac-dependent signaling. Dev. Cell 1, 63-72 (2001
42. Farooqui, R. & Fenteany, G. Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J. Cell Sci. 118, 51-63 (2005
43. Schubert, R. A., Dodd, I. B., Egan, J. B. & Shearwin, K. E. Cro's role in the CI-Cro bistable switch is critical for lambda's transition from lysogeny to lytic development. Genes Dev. 21, 2461-2472 (2007
44. Huang, B., et al. The three-way switch operation of Rac1/RhoA GTPase-based circuit controlling amoeboid-hybrid-mesenchymal transition. Sci. Rep. 4, 6449 (2014
45. Saito, K., Ozawa, Y., Hibino, K. & Ohta, Y. FilGAP, a Rho/Rho-Associated protein kinase-regulated GTPase-Activating protein for Rac, controls tumor cell migration. Mol. Biol. Cell 23, 4739-4750 (2012
46. Sanz-Moreno, V., et al. Rac activation and inactivation control plasticity of tumor cell movement. Cell 135, 510-523 (2008
47. Alfthan, K., Heiska, L., Gronholm, M., Renkema, G. H. & Carpen, O. Cyclic AMPdependent protein kinase phosphorylates merlin at serine 518 independently of p21-Activated kinase and promotes merlin-ezrin heterodimerization. J. Biol. Chem. 279, 18559-18566 (2004
48. Jin, H. C., Sperka, T., Herrlich, P. & Morrison, H. Tumorigenic transformation by CPI-17 through inhibition of a merlin phosphatase. Nature 442, 576-579 (2006
49. Safferling, K., et al. Wound healing revised: a novel reepithelialization mechanism revealed by in vitro and in silico models. J. Cell Biol. 203, 691-709 (2013
50. Trepat, X. & Fredberg, J. J. Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol. 21, 638-646 (2011
51. Lukeman, R., Li, Y. X. & Edelstein-Keshet, L. Inferring individual rules from collective behavior. Proc. Natl Acad. Sci. USA 107, 12576-12580 (2010
52. Sumino, Y., et al. Large-scale vortex lattice emerging from collectively moving microtubules. Nature 483, 448-452 (2012
53. Yates, C. A., et al. Inherent noise can facilitate coherence in collective swarm motion. Proc. Natl Acad. Sci. USA 106, 5464-5469 (2009
54. Fang, X. F., et al. The SOX2 response program in glioblastoma multiforme: an integrated ChIP-seq, expression microarray, and microRNA analysis. BMC Genomics 12, 11 (2011
55. Dang, I., et al. Inhibitory signalling to the Arp2/3 complex steers cell migration. Nature 503, 281-284 (2013
56. Jungbauer, S., Gao, H. J., Spatz, J. P. & Kemkemer, R. Two characteristic regimes in frequency-dependent dynamic reorientation of fibroblasts on cyclically stretched substrates. Biophys. J. 95, 3470-3478 (2008
57. Harris, A. R. & Charras, G. T. Experimental validation of atomic force microscopybased cell elasticity measurements. Nanotechnology 22, 345102 (2011
58. Grashoff, C., et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266 (2010
59. Feder, T. J., BrustMascher, I., Slattery, J. P., Baird, B. & Webb, W. W. Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys. J. 70, 2767-2773 (1996
60. Das, T., Maiti, T. K. & Chakraborty, S. Augmented stress-responsive characteristics of cell lines in narrow confinements. Integr. Biol. 3, 684-695 (2011
61. Rausch, S., et al. Polarizing cytoskeletal tension to induce leader cell formation during collective cell migration. Biointerphases 8, 32 (2013
62. Tseng, Q., et al. Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proc. Natl Acad. Sci. USA 109, 1506-1511 (2012
63. Tambe, D. T., et al. Monolayer stress microscopy: limitations, artifacts, and accuracy of recovered intercellular stresses. PLoS ONE 8, e55172 (2013