Fellow travellers: Emergent properties of collective cell migration

EMBO Reports

Volumn 13, Issue 11, 2012, Pages 984-991

  Rorth, Pernille ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

collective cell movement; dynamics; guidance; mechanics; rotation

Indexed keywords

CANCER CELL; CELL ADHESION; CELL CONTACT; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL ADHESION; CELL COMMUNICATION; CELL MOVEMENT; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; ROTATION;

EID: 84868711769     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2012.149     Document Type: Review

References (86)

1. Rørth P (2009) Collective cell migration. Annu Rev Cell Dev Biol 25: 407-429
2. Weijer CJ (2009) Collective cell migration in development. J Cell Sci 122: 3215-3223
3. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10: 445-457
4. Friedl P, Locker J, Sahai E, Segall JE (2012) Classifying collective cancer cell invasion. Nat Cell Biol 14: 777-783
5. du Roure O, Saez A, Buguin A, Austin RH, Chavrier P, Silberzan P, Ladoux B (2005) Force mapping in epithelial cell migration. Proc Natl Acad Sci USA 102: 2390-2395 (Pubitemid 40279386)
6. Haga H, Irahara C, Kobayashi R, Nakagaki T, Kawabata K (2005) Collective movement of epithelial cells on a collagen gel substrate. Biophys J 88: 2250-2256 (Pubitemid 40976231)
7. Vitorino P, Meyer T (2008) Modular control of endothelial sheet migration. Genes Dev 22: 3268-3281
8. Teddy JM, Kulesa PM (2004) In vivo evidence for short-And long-range cell communication in cranial neural crest cells. Development 131: 6141-6151 (Pubitemid 40123927)
9. Murase S, Horwitz AF (2004) Directions in cell migration along the rostral migratory stream: the pathway for migration in the brain. Curr Top Dev Biol 61: 135-152 (Pubitemid 39752369)
10. Nam SC et al (2007) Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J Comp Neurol 505: 190-208
11. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9: 893-904 (Pubitemid 47190444)
12. Rørth P (2011) Whence directionality: guidance mechanisms in solitary and collective cell migration. Dev Cell 20: 9-18
13. Rørth P (2007) Collective guidance of collective cell migration. Trends Cell Biol 17: 575-579 (Pubitemid 350138436)
14. Theveneau E, Marchant L, Kuriyama S, Gull M, Moepps B, Parsons M, Mayor R (2010) Collective chemotaxis requires contact-dependent cell polarity. Dev Cell 19: 39-53
15. Kulesa PM, Fraser SE (2000) In ovo time-lapse analysis of chick hindbrain neural crest cell migration shows cell interactions during migration to the branchial arches. Development 127: 1161-1172 (Pubitemid 30179507)
16. Duband JL, Monier F, Delannet M, Newgreen D (1995) Epithelium-mesenchyme transition during neural crest development. Acta Anat (Basel) 154: 63-78 (Pubitemid 26101389)
17. Kasemeier-Kulesa JC, Bradley R, Pasquale EB, Lefcort F, Kulesa PM (2006) Eph/ephrins and N-cadherin coordinate to control the pattern of sympathetic ganglia. Development 133: 4839-4847 (Pubitemid 46085050)
18. Carmona-Fontaine C, Theveneau E, Tzekou A, Tada M, Woods M, Page KM, Parsons M, Lambris JD, Mayor R (2011) Complement fragment C3a controls mutual cell attraction during collective cell migration. Dev Cell 21: 1026-1037
19. Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, Parsons M, Stern CD, Mayor R (2008) Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456: 957-961
20. Kimura K et al (1996) Regulation of myosin phosphatase by Rho and Rho-Associated kinase (Rho-kinase). Science 273: 245-248 (Pubitemid 26285892)
21. Hidalgo-Carcedo C, Hooper S, Chaudhry SI, Williamson P, Harrington K, Leitinger B, Sahai E (2011) 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
22. Omelchenko T, Hall A (2012) Myosin-IXA regulates collective epithelial cell migration by targeting RhoGAP activity to cell-cell junctions. Curr Biol 22: 278-288
23. Block ER, Matela AR, SundarRaj N, Iszkula ER, Klarlund JK (2004) Wounding induces motility in sheets of corneal epithelial cells through loss of spatial constraints: role of heparin-binding epidermal growth factor-like growth factor signaling. J Biol Chem 279: 24307-24312 (Pubitemid 38725293)
24. Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P, Ladoux B, Buguin A, Silberzan P (2007) Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci USA 104: 15988-15993 (Pubitemid 350099346)
25. Reffay M, Petitjean L, Coscoy S, Grasland-Mongrain E, Amblard F, Buguin A, Silberzan P (2011) Orientation and polarity in collectively migrating cell structures: statics and dynamics. Biophys J 100: 2566-2575
26. Gotlieb AI, May LM, Subrahmanyan L, Kalnins VI (1981) Distribution of microtubule organizing centers in migrating sheets of endothelial cells. J Cell Biol 91: 589-594 (Pubitemid 12215650)
27. Etienne-Manneville S, Hall A (2001) Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106: 489-498 (Pubitemid 32786992)
28. Pouthas F, Girard P, Lecaudey V, Ly TB, Gilmour D, Boulin C, Pepperkok R, Reynaud EG (2008) In migrating cells, the Golgi complex and the position of the centrosome depend on geometrical constraints of the substratum. J Cell Sci 121: 2406-2414
29. Thery M, Racine V, Piel M, Pepin A, Dimitrov A, Chen Y, Sibarita JB, Bornens M (2006) Anisotropy of cell adhesive microenvironment governs cell internal organization and orientation of polarity. Proc Natl Acad Sci USA 103: 19771-19776 (Pubitemid 46037506)
30. Dupin I, Camand E, Etienne-Manneville S (2009) Classical cadherins control nucleus and centrosome position and cell polarity. J Cell Biol 185: 779-786
31. Desai RA, Gao L, Raghavan S, Liu WF, Chen CS (2009) Cell polarity triggered by cell-cell adhesion via E-cadherin. J Cell Sci 122: 905-911
32. Farooqui R, Fenteany G (2005) Multiple rows of cells behind an epithelial wound edge extend cryptic lamellipodia to collectively drive cell-sheet movement. J Cell Sci 118: 51-63 (Pubitemid 40277104)
33. Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ, Ruiz SA, Nelson CM, Chen CS (2010) Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci USA 107: 9944-9949
34. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, Kam Z, Geiger B, Bershadsky AD (2001) Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 153: 1175-1186
35. Weber GF, Bjerke MA, DeSimone DW (2012) A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 22: 104-115
36. Trepat X, Fredberg JJ (2011) Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol 21: 638-646
37. Helmke BP, Rosen AB, Davies PF (2003) Mapping mechanical strain of an endogenous cytoskeletal network in living endothelial cells. Biophys J 84: 2691-2699 (Pubitemid 36373589)
38. Wong P, Coulombe PA (2003) Loss of keratin 6 (K6) proteins reveals a function for intermediate filaments during wound repair. J Cell Biol 163: 327-337 (Pubitemid 37363133)
39. Long HA, Boczonadi V, McInroy L, Goldberg M, Määttä A (2006) Periplakin-dependent re-organisation of keratin cytoskeleton and loss of collective migration in keratin-8-downregulated epithelial sheets. J Cell Sci 119: 5147-5159 (Pubitemid 46085193)
40. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, Sahai E (2007) Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9: 1392-1400 (Pubitemid 350201752)
41. Larsen M, Wei C, Yamada KM (2006) Cell and fibronectin dynamics during branching morphogenesis. J Cell Sci 119: 3376-3384 (Pubitemid 44405222)
42. Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z (2008) Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 14: 570-581 (Pubitemid 351479940)
43. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C, Shima DT (2002) Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev 16: 2684-2698
44. Ghabrial AS, Krasnow MA (2006) Social interactions among epithelial cells during tracheal branching morphogenesis. Nature 441: 746-749 (Pubitemid 43865219)
45. Gerhardt H et al (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161: 1163-1177 (Pubitemid 36870177)
46. Yana I et al (2007) Crosstalk between neovessels and mural cells directs the site-specific expression of MT1-MMP to endothelial tip cells. J Cell Sci 120: 1607-1614 (Pubitemid 46831790)
47. del Toro R et al (2010) Identification and functional analysis of endothelial tip cell-enriched genes. Blood 116: 4025-4033
48. Nabeshima K, Inoue T, Shimao Y, Okada Y, Itoh Y, Seiki M, Koono M (2000) Front-cell-specific expression of membrane-type 1 matrix metalloproteinase and gelatinase A during cohort migration of colon carcinoma cells induced by hepatocyte growth factor/scatter factor. Cancer Res 60: 3364-3369 (Pubitemid 30482147)
49. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, Christofori G (2006) Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 9: 261-272
50. Vignjevic D, Schoumacher M, Gavert N, Janssen KP, Jih G, Lae M, Louvard D, Ben-Ze'ev A, Robine S (2007) Fascin, a novel target of beta-catenin-TCF signaling, is expressed at the invasive front of human colon cancer. Cancer Res 67: 6844-6853 (Pubitemid 47105531)
51. McLennan R, Dyson L, Prather KW, Morrison JA, Baker RE, Maini PK, Kulesa PM (2012) Multiscale mechanisms of cell migration during development: theory and experiment. Development 139: 2935-2944
52. Aigouy B, Lepelletier L, Giangrande A (2008) Glial chain migration requires pioneer cells. J Neurosci 28: 11635-11641
53. Haas P, Gilmour D (2006) Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev Cell 10: 673-680
54. Jacinto A, Wood W, Balayo T, Turmaine M, Martinez-Arias A, Martin P (2000) Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr Biol 10: 1420-1426 (Pubitemid 32692871)
55. Jakobsson L et al (2010) Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12: 943-953
56. Arima S et al (2011) Angiogenic morphogenesis driven by dynamic and heterogeneous collective endothelial cell movement. Development 138: 4763-4776
57. Hellstrom M et al (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445: 776-780 (Pubitemid 46279716)
58. Siekmann AF, Lawson ND (2007) Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445: 781-784 (Pubitemid 46279717)
59. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD, Thurston G (2006) Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444: 1032-1037 (Pubitemid 46018516)
60. Ridgway J et al (2006) Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444: 1083-1087 (Pubitemid 46018529)
61. Ghabrial A, Luschnig S, Metzstein MM, Krasnow MA (2003) Branching morphogenesis of the Drosophila tracheal system. Annu Rev Cell Dev Biol 19: 623-647 (Pubitemid 37487363)
62. Caussinus E, Colombelli J, Affolter M (2008) Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation. Curr Biol 18: 1727-1734
63. Prasad M, Montell DJ (2007) Cellular and molecular mechanisms of border cell migration analyzed using time-lapse live-cell imaging. Dev Cell 12: 997-1005 (Pubitemid 46805918)
64. Bianco A, Poukkula M, Cliffe A, Mathieu J, Luque CM, Fulga TA, Rørth P (2007) Two distinct modes of guidance signalling during collective migration of border cells. Nature 448: 362-365 (Pubitemid 47080343)
65. Wang X, He L, Wu YI, Hahn KM, Montell DJ (2010) Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat Cell Biol 12: 591-597
66. Inaki M, Vishnu S, Cliffe A, Rørth P (2012) Effective guidance of collective migration based on differences in cell states. Proc Natl Acad Sci USA 109: 2027-2032
67. Pearson GW, Hunter T (2007) Real-time imaging reveals that noninvasive mammary epithelial acini can contain motile cells. J Cell Biol 179: 1555-1567
68. Haigo SL, Bilder D (2011) Global tissue revolutions in a morphogenetic movement controlling elongation. Science 331: 1071-1074
69. Tanner K, Mori H, Mroue R, Bruni-Cardoso A, Bissell MJ (2012) Coherent angular motion in the establishment of multicellular architecture of glandular tissues. Proc Natl Acad Sci USA 109: 1973-1978
70. Brangwynne C, Huang S, Parker KK, Ingber DE, Ostuni E (2000) Symmetry breaking in cultured mammalian cells. In Vitro Cell Dev Biol Anim 36: 563-565 (Pubitemid 32112884)
71. Huang S, Brangwynne CP, Parker KK, Ingber DE (2005) Symmetry-breaking in mammalian cell cohort migration during tissue pattern formation: role of random-walk persistence. Cell Motil Cytoskeleton 61: 201-213 (Pubitemid 41060777)
72. O'Brien LE, Zegers MM, Mostov KE (2002) Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3: 531-537 (Pubitemid 34733434)
73. Ferrari A, Veligodskiy A, Berge U, Lucas MS, Kroschewski R (2008) ROCK-mediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation. J Cell Sci 121: 3649-3663
74. Marmaras A, Berge U, Ferrari A, Kurtcuoglu V, Poulikakos D, Kroschewski R (2010) A mathematical method for the 3D analysis of rotating deformable systems applied on lumen-forming MDCK cell aggregates. Cytoskeleton (Hoboken) 67: 224-240
75. Escudero LM, Bischoff M, Freeman M (2007) Myosin II regulates complex cellular arrangement and epithelial architecture in Drosophila. Dev Cell 13: 717-729 (Pubitemid 350011984)
76. Yang N, Inaki M, Cliffe A, Rørth P (2012) Microtubules and Lis-1/NudE/dynein regulate invasive cell-on-cell migration in Drosophila. PLoS ONE 7: e40632
77. Klein TJ, Mlodzik M (2005) Planar cell polarization: an emerging model points in the right direction. Annu Rev Cell Dev Biol 21: 155-176 (Pubitemid 41740631)
78. Roszko I, Sawada A, Solnica-Krezel L (2009) Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin Cell Dev Biol 20: 986-997
79. Viktorinova I, Konig T, Schlichting K, Dahmann C (2009) The cadherin Fat2 is required for planar cell polarity in the Drosophila ovary. Development 136: 4123-4132
80. Bertet C, Sulak L, Lecuit T (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429: 667-671 (Pubitemid 38812319)
81. Skoglund P, Keller R (2010) Integration of planar cell polarity and ECM signaling in elongation of the vertebrate body plan. Curr Opin Cell Biol 22: 589-596
82. Blankenship JT, Backovic ST, Sanny JS, Weitz O, Zallen JA (2006) Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell 11: 459-470 (Pubitemid 44430903)
83. Rauzi M, Lenne PF, Lecuit T (2010) Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468: 1110-1114
84. Fernandez-Gonzalez R, Zallen JA (2011) Oscillatory behaviours and hierarchical assembly of contractile structures in intercalating cells. Phys Biol 8: 045005
85. Heath JP (1996) Epithelial cell migration in the intestine. Cell Biol Int 20: 139-146 (Pubitemid 26132259)
86. Nelson SA et al (2012) Tumorigenic fragments of APC cause dominant defects in directional cell migration in multiple model systems. Dis Model Mech [Epub ahead of print] doi: 10.1242/dmm.008607