A common framework for EMT and collective cell migration

Development (Cambridge)

Volumn 143, Issue 23, 2016, Pages 4291-4300

  Campbell, Kyra ^a,b   Casanova, Jordi ^a,b  

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

Collective migration; EMT; Epithelial; Mesenchymal

Indexed keywords

UVOMORULIN; CADHERIN;

ADHERENS JUNCTION; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL MIGRATION; CELL POLARITY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; HUMAN; METASTASIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; CELL MOTION; CYTOLOGY; EMBRYO DEVELOPMENT; MESENCHYMAL STROMA CELL; MESODERM; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CELL ADHESION; CELL MOVEMENT; EMBRYONIC DEVELOPMENT; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MESENCHYMAL STROMAL CELLS; MESODERM; NEOPLASM METASTASIS; NEOPLASMS;

EID: 85002169871     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.139071     Document Type: Article

References (100)

1. Aceto, N., Bardia, A., Miyamoto, D. T., Donaldson, M. C., Wittner, B. S., Spencer, J. A., Yu, M., Pely, A., Engstrom, A., Zhu, H. et al. (2014). Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158, 1110-1122.
2. Acloque, H., Adams, M. S., Fishwick, K., Bronner-Fraser, M. and Nieto, M. A. (2009). Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J. Clin. Invest. 119, 1438-1449.
3. Ahlstrom, J. D. and Erickson, C. A. (2009). The neural crest epithelialmesenchymal transition in 4D: a ‘tail’ of multiple non-obligatory cellular mechanisms. Development 136, 1801-1812.
4. Arnoux, V., Côme, C., Kusewitt, D. F., Hudson, L. G. and Savagner, P. (2005). Cutaneous wound reepithelialization. In Rise and Fall of Epithelial Phenotype: Concepts of Epithelial-Mesenchymal Transition (ed. P. Savagner), pp. 111-134.
5. Boston, MA: Springer US., Bahri, S., Wang, S., Conder, R., Choy, J., Vlachos, S., Dong, K., Merino, C., Sigrist, S., Molnar, C., Yang, X. et al. (2010). The leading edge during dorsal closure as a model for epithelial plasticity: Pak is required for recruitment of the Scribble complex and septate junction formation. Development 137, 2023-2032.
6. Barrallo-Gimeno, A. and Nieto, M. A. (2005). The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132, 3151-3161.
7. Batlle, E., Sancho, E., Francı́, C., Dominguez, D., Monfar, M., Baulida, J. and Garcı́a De Herreros A. (2000). The transcription factor snail is a repressor of Ecadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89.
8. Baum, B. and Georgiou, M. (2011). Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J. Cell Biol. 192, 907-917.
9. Bertet, C., Sulak, L. and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
10. Berx, G. and van Roy, F. (2009). Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb. Perspect. Biol. 1, a003129.
11. Blankenship, J. T., Backovic, S. T., Sanny, J. S. P., Weitz, O. and Zallen, J. A. (2006). Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 11, 459-470.
12. Brown, N. H. (2011). Extracellular matrix in development: insights from mechanisms conserved between invertebrates and vertebrates. Cold Spring Harb. Perspect. Biol. 3, a005082.
13. Cai, D., Chen, S.-C., Prasad, M., He, L., Wang, X., Choesmel-Cadamuro, V., Sawyer, J. K., Danuser, G. and Montell, D. J. (2014). Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 157, 1146-1159.
14. Campbell, K. and Casanova, J. (2015). A role for E-cadherin in ensuring cohesive migration of a heterogeneous population of non-epithelial cells. Nat. Commun. 6, 7998.
15. Campbell, K., Whissell, G., Franch-Marro, X., Batlle, E. and Casanova, J. (2011). Specific GATA factors act as conserved inducers of an endodermal-EMT. Dev. Cell 21, 1051-1061.
16. Cano, A., Pérez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F. and Nieto, M. A. (2000). The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83.
17. Carver, E. A., Jiang, R., Lan, Y., Oram, K. F. and Gridley, T. (2001). The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol. Cell. Biol. 21, 8184-8188.
18. Caussinus, E., Colombelli, J. and Affolter, M. (2008). Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation. Curr. Biol. 18, 1727-1734.
19. Cavallaro, U. and Christofori, G. (2004). Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat. Rev. Cancer 4, 118-132.
20. Cheung, K. J. and Ewald, A. J. (2016). A collective route to metastasis: seeding by tumor cell clusters. Science 352, 167-169.
21. Cho, A., Kato, M., Whitwam, T., Kim, J. H. and Montell, D. J. (2016). An atypical tropomyosin in Drosophila with intermediate filament-like properties. Cell Rep. 16, 928-938.
22. Chuai, M., Hughes, D. and Weijer, C. J. (2012). Collective epithelial and mesenchymal cell migration during gastrulation. Curr. Genomics 13, 267-277.
23. Classen, A.-K., Anderson, K. I., Marois, E. and Eaton, S. (2005). Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 9, 805-817.
24. Collins, C. and Nelson, W. J. (2015). Running with neighbors: coordinating cell migration and cell-cell adhesion. Curr. Opin. Cell Biol. 36, 62-70.
25. Davies, J. A. and Garrod, D. R. (1997). Molecular aspects of the epithelial phenotype. BioEssays 19, 699-704.
26. Dumortier, J. G., Martin, S., Meyer, D., Rosa, F. M. and David, N. B. (2012). Collective mesendoderm migration relies on an intrinsic directionality signal transmitted through cell contacts. Proc. Natl. Acad. Sci. USA 109, 16945-16950.
27. Ewald, A. J., Brenot, A., Duong, M., Chan, B. S. and Werb, Z. (2008). Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev. Cell 14, 570-581.
28. Ewald, A. J., Huebner, R. J., Palsdottir, H., Lee, J. K., Perez, M. J., Jorgens, D. M., Tauscher, A. N., Cheung, K. J., Werb, Z. and Auer, M. (2012). Mammary collective cell migration involves transient loss of epithelial features and individual cell migration within the epithelium. J. Cell Sci. 125, 2638-2654.
29. Friedl, P. and Gilmour, D. (2009). Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445-457.
30. Friedl, P. and Wolf, K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
31. Galván, J. A., Zlobec, I., Wartenberg, M., Lugli, A., Gloor, B., Perren, A. and Karamitopoulou, E. (2015). Expression of E-cadherin repressors SNAIL, ZEB1 and ZEB2 by tumour and stromal cells influences tumour-budding phenotype and suggests heterogeneity of stromal cells in pancreatic cancer. Br. J. Cancer 112, 1944-1950.
32. Gompel, N., Cubedo, N., Thisse, C., Thisse, B., Dambly-Chaudiére, C. and Ghysen, A. (2001). Pattern formation in the lateral line of zebrafish. Mech. Dev. 105, 69-77.
33. Grigore, A. D., Jolly, M. K., Jia, D., Farach-Carson, M. C. and Levine, H. (2016). Tumor budding: the name is EMT. Partial EMT. J. Clin. Med. 5, 51.
34. Haeger, A., Wolf, K., Zegers, M. M. and Friedl, P. (2015). Collective cell migration: guidance principles and hierarchies. Trends Cell Biol. 25, 556-566.
35. Hashimoto, K., Fujimoto, H. and Nakatsuji, N. (1987). An ECM substratum allows mouse mesodermal cells isolated from the primitive streak to exhibit motility similar to that inside the embryo and reveals a deficiency in the T/T mutant cells. Development 100, 587-598.
36. Hatta, K. and Takeichi, M. (1986). Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320, 447-449.
37. Hava, D., Forster, U., Matsuda, M., Cui, S., Link, B. A., Eichhorst, J., Wiesner, B., Chitnis, A. and Abdelilah-Seyfried, S. (2009). Apical membrane maturation and cellular rosette formation during morphogenesis of the zebrafish lateral line. J. Cell Sci. 122, 687-695.
38. Hay, E. D. (2005). The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev. Dyn. 233, 706-720.
39. Hazan, R. B., Qiao, R., Keren, R., Badano, I. and Suyama, K. (2004). Cadherin switch in tumor progression. Ann. N. Y. Acad. Sci. 1014, 155-163.
40. Huber, M. A., Kraut, N. and Beug, H. (2005). Molecular requirements for epithelialmesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17, 548-558.
41. Jacinto, A., Wood, W., Woolner, S., Hiley, C., Turner, L., Wilson, C., Martinez-Arias, A. and Martin, P. (2002). Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr. Biol. 12, 1245-1250.
42. Jaźwińska, A., Ribeiro, C. and Affolter, M. (2003). Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat. Cell Biol. 5, 895-901.
43. Jolly, M. K., Boareto, M., Huang, B., Jia, D., Lu, M., Ben-Jacob, E., Onuchic, J. N. and Levine, H. (2015). Implications of the hybrid epithelial/mesenchymal phenotype in metastasis. Front. Oncol. 5, 155.
44. Kardash, E., Reichman-Fried, M., Maitre, J. L., Boldajipour, B., Papusheva, E., Messerschmidt, E. M., Heisenberg, C. P. and Raz, E. (2010). A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat. Cell Biol. 12, 47-53; sup pp 41-11.
45. Kowalczyk, A. P. and Nanes, B. A. (2012). Adherens junction turnover: regulating adhesion through cadherin endocytosis, degradation, and recycling. Subcell. Biochem. 60, 197-222.
46. Kulesa, P. M. and Gammill, L. S. (2010). Neural crest migration: patterns, phases and signals. Dev. Biol. 344, 566-568.
47. Lamouille, S., Xu, J. and Derynck, R. (2014). Molecular mechanisms of epithelialmesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196.
48. Lebreton, G. and Casanova, J. (2014). Specification of leading and trailing cell features during collective migration in the Drosophila trachea. J. Cell Sci. 127, 465-474.
49. Lecuit, T. (2004). Junctions and vesicular trafficking during Drosophila cellularization. J. Cell Sci. 117, 3427-3433.
50. Leptin, M. (1991). twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev. 5, 1568-1576.
51. Li, W. and Kang, Y. (2016). Probing the fifty shades of EMT in metastasis. Trends Cancer 2, 65-67.
52. Lim, J. and Thiery, J. P. (2011). Alternative path to EMT: regulation of apicobasal polarity in Drosophila. Dev. Cell 21, 983-984.
53. Mayor, R. and Etienne-Manneville, S. (2016). The front and rear of collective cell migration. Nat. Rev. Mol. Cell Biol. 17, 97-109.
54. Montero, J.-A., Carvalho, L., Wilsch-Brauninger, M., Kilian, B., Mustafa, C. and Heisenberg, C.-P. (2005). Shield formation at the onset of zebrafish gastrulation. Development 132, 1187-1198.
55. Nakatsuji, N., Snow, M. H. and Wylie, C. C. (1986). Cinemicrographic study of the cell movement in the primitive-streak-stage mouse embryo. J. Embryol. Exp. Morphol. 96, 99-109.
56. Nakaya, Y. and Sheng, G. (2008). Epithelial to mesenchymal transition during gastrulation: an embryological view. Dev. Growth Differ. 50, 755-766.
57. Nakaya, Y., Sukowati, E.W., Wu, Y. and Sheng, G. (2008). RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 10, 765-775.
58. Nandadasa, S., Tao, Q., Menon, N. R., Heasman, J. and Wylie, C. (2009). N-and E-cadherins in Xenopus are specifically required in the neural and non-neural ectoderm, respectively, for F-actin assembly and morphogenetic movements. Development 136, 1327-1338.
59. Navarro, P., Lozano, E. and Cano, A. (1993). Expression of E-or P-cadherin is not sufficient to modify the morphology and the tumorigenic behavior of murine spindle carcinoma cells. Possible involvement of plakoglobin. J. Cell Sci. 105, 923-934.
60. Niessen, C. M. and Gottardi, C. J. (2008). Molecular components of the adherens junction. Biochim. Biophy. Acta 1778, 562-571.
61. Nieto, M. A. (2011). The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell Dev. Biol. 27, 347-376.
62. Nieto, M. A., Huang, R. Y.-J., Jackson, R. A. and Thiery, J. P. (2016). Emt: 2016. Cell 166, 21-45.
63. Niewiadomska, P., Godt, D. and Tepass, U. (1999). DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J. Cell Biol. 144, 533-547.
64. Oda, H. and Tsukita, S. (2001). Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J. Cell Sci. 114, 493-501.
65. Oda, H., Tsukita, S. and Takeichi, M. (1998). Dynamic behavior of the cadherinbased cell-cell adhesion system during Drosophila gastrulation. Dev. Biol. 203, 435-450.
66. Ohkubo, T. and Ozawa, M. (2004). The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J. Cell Sci. 117, 1675-1685.
67. Pastor-Pareja, J. C., Grawe, F., Martín-Blanco, E. and Garcia-Bellído, A. (2004). Invasive cell behavior during Drosophila imaginal disc eversion is mediated by the JNK signaling cascade. Dev. Cell 7, 387-399.
68. Peinado, H., Olmeda, D. and Cano, A. (2007). Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer 7, 415-428.
69. Pinheiro, E. M. and Montell, D. J. (2004). Requirement for Par-6 and Bazooka in Drosophila border cell migration. Development 131, 5243-5251.
70. Revenu, C. and Gilmour, D. (2009). EMT 2.0: shaping epithelia through collective migration. Curr. Opin. Genet. Dev. 19, 338-342.
71. Revenu, C., Streichan, S., Dona, E., Lecaudey, V., Hufnagel, L. and Gilmour, D. (2014). Quantitative cell polarity imaging defines leader-to-follower transitions during collective migration and the key role of microtubule-dependent adherens junction formation. Development 141, 1282-1291.
72. Rodriguez, F. J., Lewis-Tuffin, L. J. and Anastasiadis, P. Z. (2012). E-cadherin’s dark side: possible role in tumor progression. Biochim. Biophys. Acta 1826, 23-31.
73. Rørth, P. (2009). Collective cell migration. Annu. Rev. Cell Dev. Biol. 25, 407-429.
74. Rørth, P. (2012). Fellow travellers: emergent properties of collective cell migration. EMBO Rep. 13, 984-991.
75. Sandmann, T., Girardot, C., Brehme, M., Tongprasit, W., Stolc, V. and Furlong, E. E. (2007). A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev. 21, 436-449.
76. Scarpa, E. and Mayor, R. (2016). Collective cell migration in development. J. Cell Biol. 212, 143-155.
77. Schafer, G., Narasimha, M., Vogelsang, E. and Leptin, M. (2014). Cadherin switching during the formation and differentiation of the Drosophila mesoderm–implications for epithelial-to-mesenchymal transitions. J. Cell Sci. 127, 1511-1522.
78. Schulte, J., Weidig, M., Balzer, P., Richter, P., Franz, M., Junker, K., Gajda, M., Friedrich, K., Wunderlich, H., Östman, A., et al. (2012). Expression of the Ecadherin repressors Snail, Slug and Zeb1 in urothelial carcinoma of the urinary bladder: relation to stromal fibroblast activation and invasive behaviour of carcinoma cells. Histochem. Cell Biol. 138, 847-860.
79. Shamir, E. R. and Ewald, A. J. (2015). Adhesion in mammary development: novel roles for E-cadherin in individual and collective cell migration. Curr. Top. Dev. Biol. 112, 353-382.
80. Shamir, E. R., Pappalardo, E., Jorgens, D. M., Coutinho, K., Tsai, W.-T., Aziz, K., Auer, M., Tran, P. T., Bader, J. S. and Ewald, A. J. (2014). Twist1-induced dissemination preserves epithelial identity and requires E-cadherin. J. Cell Biol. 204, 839-856.
81. Shaye, D. D., Casanova, J. and Llimargas, M. (2008). Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat. Cell Biol. 10, 964-970.
82. Shook, D. and Keller, R. (2003). Mechanisms, mechanics and function of epithelialmesenchymal transitions in early development. Mech. Dev. 120, 1351-1383.
83. Strumane, K., Berx, G. and Van Roy, F. (2004). Cadherins in cancer. Handbook Exp. Pharmacol. 165, 69-103.
84. Supatto, W., McMahon, A., Fraser, S. E. and Stathopoulos, A. (2009). Quantitative imaging of collective cell migration during Drosophila gastrulation: multiphoton microscopy and computational analysis. Nat. Protoc. 4, 1397-1412.
85. Szabó, A. and Mayor, R. (2015). Cell traction in collective cell migration and morphogenesis: the chase and run mechanism. Cell Adh. Migr. 9, 380-383.
86. Taneyhill, L. A. (2008). To adhere or not to adhere: the role of Cadherins in neural crest cell development. Cell Adh. Migr. 2, 223-230.
87. Tepass, U. and Hartenstein, V. (1994). The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161, 563-596.
88. Tepass, U., Tanentzapf, G., Ward, R. and Fehon, R. (2001). Epithelial cell polarity and cell junctions in Drosophila. Annu. Rev. Genet. 35, 747-784.
89. Theveneau, E. and Mayor, R. (2011). Can mesenchymal cells undergo collective cell migration? The case of the neural crest. Cell Adh. Migr. 5, 490-498.
90. Theveneau, E. and Mayor, R. (2012). Cadherins in collective cell migration of mesenchymal cells. Curr. Opin. Cell Biol. 24, 677-684.
91. Theveneau, E. and Mayor, R. (2013). Collective cell migration of epithelial and mesenchymal cells. Cell. Mol. Life Sci. 70, 3481-3492.
92. Theveneau, E., Marchant, L., Kuriyama, S., Gull, M., Moepps, B., Parsons, M. and Mayor, R. (2010). Collective chemotaxis requires contact-dependent cell polarity. Dev. Cell 19, 39-53.
93. Thiery, J. P., Acloque, H., Huang, R. Y. J. and Nieto, M. A. (2009). Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890.
94. West, J. J. and Harris, T. J. (2016). Cadherin trafficking for tissue morphogenesis: control and consequences. Traffic.
95. Williams, M., Burdsal, G., Periasamy, A., Lewandoski, M. and Sutherland, A. (2012). Mouse primitive streak forms in situ by initiation of epithelial to mesenchymal transition without migration of a cell population. Dev. Dyn. 241, 270-283.
96. Wood, W., Jacinto, A., Grose, R., Woolner, S., Gale, J., Wilson, C. and Martin, P. (2002). Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 4, 907-912.
97. Ye, X. and Weinberg, R. A. (2015). Epithelial-mesenchymal plasticity: a central regulator of cancer progression. Trends Cell Biol. 25, 675-686.
98. Yu, M., Bardia, A., Wittner, B. S., Stott, S. L., Smas, M. E., Ting, D. T., Isakoff, S. J., Ciciliano, J. C., Wells, M. N., Shah, A. M. et al. (2013). Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580-584.
99. Zallen, J. A. (2007). Planar polarity and tissue morphogenesis. Cell 129, 1051-1063.
100. Zohn, I. E., Li, Y., Skolnik, E. Y., Anderson, K. V., Han, J. and Niswander, L. (2006). p38 and a p38-interacting protein are critical for downregulation of E-cadherin during mouse gastrulation. Cell 125, 957-969.