Collective cell migration: A mechanistic perspective

Physiology

Volumn 28, Issue 6, 2013, Pages 370-379

  Vedula, Sri Ram Krishna ^a   Ravasio, Andrea ^a   Lim, Chwee Teck ^a,b   Ladou, Benoit ^a,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CELL ADHESION; CELL COMMUNICATION; CELL MOTION; COMPUTER SIMULATION; HUMAN; REVIEW; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; TUMOR INVASION; WOUND HEALING;

ANIMALS; CELL ADHESION; CELL COMMUNICATION; CELL MOVEMENT; COMPUTER SIMULATION; HUMANS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; WOUND HEALING;

EID: 84887076354     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00033.2013     Document Type: Review

References (77)

1. Abercrombie M, Heaysman JE. Observations on the social behaviour of cells in tissue culture. I. Speed of movement of chick heart fibroblasts in relation to their mutual contacts. Exp Cell Res 5: 111-131, 1953.
2. Angelini TE, Hannezo E, Trepat X, Fredberg JJ, Weitz DA. Cell migration driven by cooperative substrate deformation patterns. Phys Rev letters 104: 168104, 2010.
3. Angelini TE, Hannezo E, Trepat X, Marquez M, Fredberg JJ, Weitz DA. Glass-like dynamics of collective cell migration. Proc Natl Acad Sci USA 108: 4714-4719, 2011.
4. Anon E, Serra-Picamal X, Hersen P, Gauthier NC, Sheetz MP, Trepat X, Ladoux B. Cell crawling mediates collective cell migration to close undamaged epithelial gaps. Proc Natl Acad Sci USA 109: 10891-10896, 2012.
5. Ashby WJ, Zijlstra A. Established and novel methods of interrogating two-dimensional cell migration. Integr Biol (Camb) 4: 1338-1350, 2012.
6. Bazazi S, Buhl J, Hale JJ, Anstey ML, Sword GA, Simpson SJ, Couzin ID. Collective motion and cannibalism in locust migratory bands. Curr Biol 18: 735-739, 2008.
7. Bianco A, Poukkula M, Cliffe A, Mathieu J, Luque CM, Fulga TA, Rorth P. Two distinct modes of guidance signalling during collective migration of border cells. Nature 448: 362-365, 2007.
8. Blair DL, Neicu T, Kudrolli A. Vortices in vibrated granular rods. Phys Rev E Stat Nonlin Soft Matter Phys 67: 031303, 2003.
9. Butler JP, Tolic-Norrelykke IM, Fabry B, Fred-berg JJ. Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol Cell Physiol 282: C595-C605, 2002.
10. Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, Parsons M, Stern CD, Mayor R. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456: 957-961, 2008.
11. Caussinus E, Colombelli J, Affolter M. Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation. Curr Biol 18: 1727-1734, 2008.
12. Chaté H, Ginelli F, Grégoire G, Peruani F, Raynaud F. Modeling collective motion: variations on the Vicsek model. Eur Phys J B 64: 451-456, 2008.
13. De R, Zemel A, Safran SA. Dynamics of cell orientation. Nat Phys 3: 655-659, 2007.
14. Dembo M, Wang YL. Stresses at the cell-to-substrate interface during locomotion of fibro-blasts. Biophys J 76: 2307-2316, 1999.
15. Douezan S, Guevorkian K, Naouar R, Dufour S, Cuvelier D, Brochard-Wyart F. Spreading dynamics and wetting transition of cellular aggregates. Proc Natl Acad Sci USA 108: 7315-7320, 2011.
16. Doxzen K, Vedula SR, Leong MC, Hirata H, Gov NS, Kabla AJ, Ladoux B, Lim CT. Guidance of collective cell migration by substrate geometry. Integr Biol 5: 1026-1035, 2013.
17. Doyle AD, Wang FW, Matsumoto K, Yamada KM. One-dimensional topography underlies three-dimensional fibrillar cell migration. J Cell Biol 184: 481-490, 2009.
18. Du Roure O, Saez A, Buguin A, Austin RH, Chavrier P, Silberzan P, Ladoux B. Force mapping in epithelial cell migration. Proc Natl Acad Sci USA 102: 2390-2395, 2005.
19. Duchek P, Rorth P. Guidance of cell migration by EGF receptor signaling during Drosophila oo-genesis. Science 291: 131-133, 2001.
20. Duchek P, Somogyi K, Jekely G, Beccari S, Rorth P. Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107: 17-26, 2001.
21. 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.
22. Friedl P, Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nature Rev 10: 445-457, 2009.
23. Friedl P, Noble PB, Walton PA, Laird DW, Chau-vin PJ, Tabah RJ, Black M, Zanker KS. Migration of coordinated cell clusters in mesenchymal and epithelial cancer explants in vitro. Cancer Res 55: 4557-4560, 1995.
24. Friedl P, Wolf K. Plasticity of cell migration: a mul-tiscale tuning model. J Cell Biol 188: 11-19, 2010.
25. Gail MH, Boone CW. The locomotion of mouse fibroblasts in tissue culture. Biophys J 10: 980- 993, 1970.
26. Ghassemi S, Meacci G, Liu S, Gondarenko AA, Mathur A, Roca-Cusachs P, Sheetz MP, Hone J. Cells test substrate rigidity by local contractions on submicrometer pillars. Proc Natl Acad Sci USA 109: 5328-5333, 2012.
27. Gonzalez-Rodriguez D, Guevorkian K, Douezan S, Brochard-Wyart F. Soft matter models of developing tissues and tumors. Science 338: 910-917, 2012.
28. Gov NS. Traction forces during collective cell motion. Hfsp J 3: 223-227, 2009.
29. Haas P, Gilmour D. Chemokine signaling mediates self-organizing tissue migration in the ze-brafish lateral line. Dev Cell 10: 673-680, 2006.
30. Huang S, Brangwynne CP, Parker KK, Ingber DE. Symmetry-breaking in mammalian cell cohort migration during tissue pattern formation: role of random-walk persistence. Cell Motil Cytoskele-ton 61: 201-213, 2005.
31. Kabla AJ. Collective cell migration: leadership, invasion and segregation. J R Soc Interface 9: 3268-3278, 2012.
32. Keller R. Cell migration during gastrulation. Curr Opin Cell Biol 17: 533-541, 2005.
33. Khalil AA, Friedl P. Determinants of leader cells in collective cell migration. Integr Biol 2: 568-574, 2010.
34. Kim JH, Dooling LJ, Asthagiri AR. Intercellular mechanotransduction during multicellular mor-phodynamics. J Royal Soc Interface 7: S341-S350, 2010.
35. Ladoux B, Nicolas A. Physically based principles of cell adhesion mechanosensitivity in tissues. Rep Prog Phys 75: 116601, 2012.
36. Le Digabel J, Ghibaudo M, Trichet L, Richert A, Ladoux B. Microfabricated substrates as a tool to study cell mechanotransduction. Med Biol Eng Comput 48: 965-976, 2010.
37. Lecaudey V, Cakan-Akdogan G, Norton WH, Gilmour D. Dynamic Fgf signaling couples morphogenesis and migration in the zebrafish lateral line primordium. Development (Cambridge) 135: 2695-2705, 2008.
38. Lecaudey V, Gilmour D. Organizing moving groups during morphogenesis. Curr Opin Cell Biol 18: 102-107, 2006.
39. Leong MC, Vedula SRK, Lim CT, Ladoux B. Geometrical constraints and physical crowding direct collective migration of fibroblasts. Commun In-tegr Biol 6: e23197, 2013.
40. Martin P. Wound healing: aiming for perfect skin regeneration. Science 276: 75-81, 1997.
41. Mayor R, Carmona-Fontaine C. Keeping in touch with contact inhibition of locomotion. Trends Cell Biol 20: 319-328, 2010.
42. Mertz AF, Banerjee S, Che Y, German GK, Xu Y, Hyland C, Marchetti MC, Horsley V, Dufresne ER. Scaling of traction forces with the size of cohesive cell colonies. Phys Rev Lett 108: 198101, 2012.
43. Miller N, Gerlai R. From schooling to shoaling: patterns of collective motion in zebrafish (Danio rerio). PLos One 7: e48865, 2012.
44. Nagy M, Akos Z, Biro D, Vicsek T. Hierarchical group dynamics in pigeon flocks. Nature 464: 890-893, 2010.
45. Nedelec FJ, Surrey T, Maggs AC, Leibler S. Self-organization of microtubules and motors. Nature 389: 305-308, 1997.
46. Nelson CM, Inman JL, Bissell MJ. Three-dimensional lithographically defined organotypic tissue arrays for quantitative analysis of morphogenesis and neoplastic progression. Nat Protoc 3: 674-678, 2008.
47. Nelson CM, Tien J. Microstructured extracellular matrices in tissue engineering and development. Curr Opin Biotechnol 17: 518-523, 2006.
48. Omelchenko T, Vasiliev JM, Gelfand IM, Feder HH, Bonder EM. Rho-dependent formation of epithelial "leader" cells during wound healing. Proc Natl Acad Sci USA 100: 10788-10793, 2003.
49. Ostuni E, Kane R, Chen CS, Ingber DE, White-sides GM. Patterning mammalian cells using elas-tomeric membranes. Langmuir 16: 7811-7819, 2000.
50. Petitjean L, Reffay M, Grasland-Mongrain E, Pou-jade M, Ladoux B, Buguin A, Silberzan P. Velocity fields in a collectively migrating epithelium. Bio-phys J 98: 1790-1800, 2010.
51. Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P, Ladoux B, Buguin A, Silberzan P. Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci USA 104: 15988-15993, 2007.
52. Ramel D, Wang X, Laflamme C, Montell DJ, Emery G. Rab11 regulates cell-cell communication during collective cell movements. Nat Cell Biol 15: 317-324, 2013.
53. Reffay M, Petitjean L, Coscoy S, Grasland-Mongrain E, Amblard F, Buguin A, Silberzan P. Orientation and polarity in collectively migrating cell structures: statics and dynamics. Biophys J 100: 2566-2575, 2011.
54. Rosen P, Misfeldt DS. Cell density determines epithelial migration in culture. Proc Natl Acad Sci USA 77: 4760-4763, 1980.
55. Schaller V, Weber C, Semmrich C, Frey E, Bausch AR. Polar patterns of driven filaments. Nature 467: 73-77, 2010.
56. Segrè PN, Herbolzheimer E, Chaikin PM. Long-range correlations in sedimentation. Phys Rev Lett 79: 2574-2577, 1997.
57. Sheetz MP, Felsenfeld D, Galbraith CG, Choquet D. Cell migration as a five-step cycle. Biochem Soc Symp 65: 233-243, 1999.
58. Sheetz MP, Felsenfeld DP, Galbraith CG. Cell migration: regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol 8: 51-54, 1998.
59. Sumino Y, Nagai KH, Shitaka Y, Tanaka D, Yo-shikawa K, Chate H, Oiwa K. Large-scale vortex lattice emerging from collectively moving micro-tubules. Nature 483: 448-452, 2012.
60. Tambe DT, Hardin CC, Angelini TE, Rajendran K, Park CY, Serra-Picamal X, Zhou EHH, Zaman MH, Butler JP, Weitz DA, Fredberg JJ, Trepat X. Collective cell guidance by cooperative intercellular forces. Nat Mat 10: 469-475, 2011.
61. Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci USA 100: 1484-1489, 2003.
62. Tanner K, Mori H, Mroue R, Bruni-Cardoso A, Bissell MJ. Coherent angular motion in the establishment of multicellular architecture of glandular tissues. Proc Natl Acad Sci USA 109: 1973-1978, 2012.
63. Thery M. Micropatterning as a tool to decipher cell morphogenesis and functions. J Cell Sci 123: 4201-4213, 2010.
64. Theveneau E, Steventon B, Scarpa E, Garcia S, Trepat X, Streit A, Mayor R. Chase-and-run between adjacent cell populations promotes directional collective migration. Nat Cell Biol 15: 763-772, 2013.
65. Trepat X, Wasserman MR, Angelini TE, Millet E, Weitz DA, Butler JP, Fredberg JJ. Physical forces during collective cell migration. Nature Phys 5: 426-430, 2009.
66. Trichet L, Le Digabel J, Hawkins RJ, Vedula SR, Gupta M, Ribrault C, Hersen P, Voituriez R, Ladoux B. Evidence of a large-scale mechano-sensing mechanism for cellular adaptation to substrate stiffness. Proc Natl Acad Sci USA 109: 6933-6938, 2012.
67. Vedula SRK, Leong MC, Lai TL, Hersen P, Kabla AJ, Lim CT, Ladoux B. Emerging modes of collective cell migration induced by geometrical constraints. Proc Natl Acad Sci USA 109: 12974-12979, 2012.
68. Vicsek T, Czirok A, Ben-Jacob E, Cohen II, Shochet O. Novel type of phase transition in a system of self-driven particles. Phys Rev Lett 75: 1226-1229, 1995.
69. Vicsek T, Zafeiris A. Collective motion. Phys Rep 517: 71-140, 2012.
70. Vogel V, Sheetz M. Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-275, 2006.
71. Voituriez R, Joanny JF, Prost J. Generic phase diagram of active polar films. Phys Rev Lett 96: 028102, 2006.
72. Wan LQ, Ronaldson K, Park M, Taylor G, Zhang Y, Gimble JM, Vunjak-Novakovic G. Micropat-terned mammalian cells exhibit phenotype-specific left-right asymmetry. Proc Natl Acad Sci USA 108: 12295-12300, 2011.
73. Wang X, He L, Wu YI, Hahn KM, Montell DJ. Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat Cell Biol 12: 591-597, 2010.
74. Weber GF, Bjerke MA, DeSimone DW. A mecha-noresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 22: 104-115, 2012.
75. Weijer CJ. Collective cell migration in development. J Cell Sci 122: 3215-3223, 2009.
76. Yarrow JC, Perlman ZE, Westwood NJ, Mitchison TJ. A high-throughput cell migration assay using scratch wound healing, a comparison of image-based readout methods. BMC Biotechnol 4: 21, 2004.
77. Zordan MD, Mill CP, Riese 2nd DJ, Leary JF. A high throughput, interactive imaging, bright-field wound healing assay. Cytometry A 79: 227-232, 2011.