Critical role of N-cadherin in myofibroblast invasion and migration in vitro stimulated by colon-cancer-cell-derived TGF-β or wounding

Journal of Cell Science

Volumn 117, Issue 20, 2004, Pages 4691-4703

  De Wever, Olivier ^a   Westbroek, Wendy ^a   Verloes, An ^a   Bloemen, Nele ^a   Bracke, Marc ^a   Gespach, Christian ^b   Bruyneel, Erik ^a   Mareel, Marc ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b HÔPITAL SAINT ANTOINE   (France)

Author keywords

Cross signaling; JNK; Spheroid

Indexed keywords

COLLAGEN TYPE 1; MATRIGEL; NERVE CELL ADHESION MOLECULE; NEUTRALIZING ANTIBODY; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; CANCER CELL; CANCER INVASION; CELL MIGRATION; CELL POLARITY; CELL STIMULATION; COCULTURE; COLON CANCER; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; FILOPODIUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; IN VITRO STUDY; MYOFIBROBLAST; NERVE CELL NETWORK; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SPHEROID CELL; UPREGULATION; WOUND; WOUND HEALING;

ANIMALS; ANTIGENS, CD; CADHERINS; CELL ADHESION MOLECULES; CELL LINE; CELL MOVEMENT; CELL POLARITY; COCULTURE TECHNIQUES; COLONIC NEOPLASMS; CULTURE MEDIA, CONDITIONED; FIBROBLASTS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE CELLS; NEOPLASM INVASIVENESS; PHENOTYPE; RATS; SPHEROIDS, CELLULAR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMALIA;

EID: 7244250188     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01322     Document Type: Article

References (57)

1. Abassi, Y. A. and Vuori, K. (2002). Tyrosine 221 in Crk regulates adhesion-dependent membrane localization of Crk and Rac and activation of Rac signaling. EMBO J. 21, 4571-4582.
2. Aberle, H., Schwartz, H., Hoschuetzky, H. and Kemler, R. (1996). Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to α-catenin. J. Biol. Chem. 271, 1520-1526.
3. Adams, C. L. and Nelson, W. J. (1998). Cytomechanics of cadherin-mediated cell-cell adhesion. Curr. Opin. Cell Biol. 10 572-577.
4. André, F., Rigot, V., Remacle-Bonnet, M., Luis, J., Pommier, G. and Marvaldi, J. (1999). Protein kinases C-γ and -δ are involved in insulin-like growth factor I-induced migration of colonic epithelial cells. Gastroenterology 116, 64-77.
5. Balsamo, J., Arregui, C., Leung, T. and Lilien, J. (1998). The nonreceptor protein tyrosin phosphatase PTP1B binds to the cytoplasmic domain of N-cadherin and regulates the cadherin-actin linkage. J. Cell Biol. 143, 523-532.
6. Bennett, B. L., Sasaki, D. T., Murray, B. W., O'Leary, E. C., Sakata, S. T., Xu, W., Leisten, J. C., Motiwala, A., Pierce, S., Satoh, Y. et al. (2001). SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98, 13681-13686.
7. Bhowmick, N. A., Ghiassi, M., Bakin, A., Aakre, M., Lundquist, C. A., Engel, M. E., Arteaga, C. L. and Moses, H. L. (2001). Transforming growth factor-β1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell 12, 27-36.
8. Bracke, M. E., Boterberg, T. and Mareel, M. M. (2001). Chick heart invasion assay. In: Methods in Molecular Medicine, Vol. 58: Metastasis Research Protocols, Vol. 2: Cell Behavior In Vitro and In Vivo (ed. S. A. Brooks and U. Schumacher) pp. 91-102. Totowa, NJ: Humana Press.
9. Carmeliet, P. and Jain, R. K. (2000). Angiogenesis in cancer and other diseases, Nature 407, 249-257.
10. Chicheportiche, Y., Vassalli, P. and Tartakoff, A. M. (1984). Characterization of cytoplasmically oriented Golgi proteins with a monoclonal antibody. J. Cell Biol. 99, 2200-2210.
11. De Wever, O. and Mareel, M. (2003). Role of tissue stroma in cancer cell invasion. J. Pathol. 200, 429-447.
12. De Wever, O., Nguyen, Q.-D., van Hoorde, L., Bracke, M., Bruyneel, E., Gespach, C. and Mareel, M. (2004). Tenascin-C and SF /HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J. 18, 1016-1018.
13. Derynck, R. and Zhang, Y. (2003). Smad-dependent and Smad-independent pathways in TGF-β family signaling. Nature 425 577-584.
14. Derynck, R., Akhurst, R. J. and Balmain, A. (2001). TGF-β signaling in tumor suppression and cancer progression. Nat. Genet. 29, 117-129.
15. Dimanche-Boitrel, M. T., Vakaet, L., Jr, Pujuguet, P., Chauffert, B., Martin, M. S., Hammann, A., van Roy, F., Mareel, M. and Martin, F. (1994). In vivo and in vitro invasiveness of a rat colon cancer cell line maintaining E-cadherin expression. An enhancing role of tumor-associated myofibroblasts. Int. J. Cancer 56, 512-521.
16. Doherty, P. and Walsh, F. S. (1996). CAM-FGF receptor interactions: a model for axonal growth. Mol. Cell. Neurosci. 8 99-111.
17. Ehrlich, J. S., Hansen, M. D. and Nelson, W. J. (2002). Spatio-temporal regulation of Rac1 localization and lamellipodia dynamics during epithelial cell-cell adhesion. Dev. Cell 3, 259-270.
18. Engel, M. E., McDonnell, M. A., Law, B. K. and Moses, H. L. (1999). Interdependent SMAD and JNK signaling in transforming growth factor-β-mediated transcription. J. Biol. Chem. 274, 37413-37420.
19. Fukumura, D., Xavier, R., Sugiura, T., Chen, Y., Park, E.-C., Lu, N., Selig, M., Nielsen, G., Taksir, T., Jain, R. K. et al. (1998). Tumor induction of VEGF promoter activity in stromal cells. Cell 94, 715-725.
20. Goodwin, M., Kovacs, E. M., Thoreson, M. A., Reynolds, A. B. and Yap, A. S. (2003). Minimal mutation of the cytoplasmic tail inhibits the ability of E-cadherin to activate Rac but not phosphatidylinositol 3-kinase. Direct evidence of a role for cadherin-activated Rac signaling in adhesion and contact formation. J. Biol. Chem. 278, 20533-20539.
21. Hall, D. M. S. and Brooks, S. A. (2001). In vitro invasion assay using Matrigel. In Methods in Molecular Medicine, Vol. 58: Metastasis Research Protocols, Vol. 2: Cell Behavior In Vito and In Vivo (ed. S. A. Brooks and U. Schumacher), pp. 61-70. Totowa, NJ: Humana Press.
22. Hazan, R. B., Phillips, G. R., Fang Qiao, R., Norton, L. and Aaronson, S. A. (2000). Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J. Cell Biol. 148, 779-790.
23. Hocevar, B. A., Brown, T. L. and Howe, P. H. (1999). TGF-β induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J. 18, 1345-1356.
24. Huang, C., Rajfur, Z., Borchers, C., Schaller, M. D. and Jacobson, K. (2003). JNK phosphorylates paxillin and regulates cell migration. Nature 424, 219-223.
25. Huynh-Do, U., Vindis, C., Liu, H., Cerretti, D. P., McGrew, J. T., Enriquez, M., Chen, J. and Daniel, T. O. (2002). Ephrin-B1 transduces signals to activate integrin-mediated migration, attachment and angiogenesis. J. Cell Sci. 115, 3073-3081.
26. Islam, S., Carey, T. E., Wolf, G. T., Wheelock, M. J. and Johnson, K. R. (1996). Expression of N-cadherin by human squamous carcinoma cells induces a scattered fibroblastic phenotype with disrupted cell-cell adhesion. J. Cell Biol. 135, 1643-1654.
27. Kim, J.-B., Islam, S., Kim, Y. J., Prudoff, R. S., Sass, K. M., Wheelock, M. J. and Johnson, K. R. (2000). N-Cadherin extracellular repeat 4 mediates epithetial to mesenchymal transition and increased motility. J. Cell Biol. 151, 1193-1206.
28. Ko, K. S., Arora, P. D. and McCulloch, C. A. G. (2001). Cadherins mediate intercellular mechanical signaling in fibroblasts by activation of stretch-sensitive calcium-permeable channels. J. Biol. Chem. 276, 35967-35977.
29. Kovacs, E. M., Ali, R. G., McCormack, A. J. and Yap, A. S. (2002). E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 277, 6708-6718.
30. Lambert, M., Choquet, D. and Mège, R.-M. (2002). Dynamics of ligand-induced, Rac1-dependent anchoring of cadherins to the actin cytoskeleton. J. Cell Biol. 157, 469-479.
31. Li, B., Paradies, N. E. and Brackenbury, R. W. (1997). Isolation and characterization of the promoter region of the chicken N-cadherin gene. Gene 191, 7-13.
32. Liotta, L. A. and Kohn, E. C. (2001). The microenvironment of the tumour-host interface. Nature 411, 375-379.
33. Mbalaviele, G., Chen, H., Boyce, B. F., Mundy, G. R. and Yoneda, T. (1995). The role of cadherin in the generation of multinucleated osteoclasts from mononuclear precursors in murine marrow. J. Clin. Invest. 95, 2757-2765.
34. Mège, R. M., Goudou, D., Diaz, C., Nicolet, M., Garcia, L., Geraud, G. and Rieger, R (1992). N-cadherin and N-CAM in myoblast fusion: compared localisation and effect of blockade by peptides and antibodies. J. Cell Sci. 103, 897-906.
35. Minden, A., Lin, A., Claret, F, X., Abo, A. and Karin, M. (1995). Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81, 1147-1157.
36. Mulder, K. M. (2000). Role of Ras and Mapks in TGFβ signaling. Cytokine Growth Factor Rev. 11, 23-35.
37. Nawrocki-Raby, B., Gilles, C., Polette, M., Bruyneel, E., Laronze, J.-Y., Bonnet, N., Foidart, J.-M., Mareel, M. and Birembaut, P. (2003). Upregulation of MMPs by soluble E-cadherin in human lung tumor cells. Int. J. Cancer 105, 790-795.
38. Nobes, C. D. and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
39. Noë, V., Willems, J., Vandekerckhove, J., van Roy, F., Bruyneel, E. and Mareel, M. (1999). Inhibition of adhesion and induction of epithelial cell invasion by HAV-containing E-cadherin-specific peptides. J. Cell Sci. 112, 127-135.
40. Noren, N. K., Arthur, W. T. and Burridge, K. (2003). Cadherin engagement inhibits RhoA via p190RhoGAP. J. Biol. Chem. 278, 13615-13618.
41. Oktay, M., Wary, K. K., Dans, M., Birge, R. B. and Giancotti, F. G. (1999). Integrin-mediated activation of focal adhesion kinase is required for signaling to Jun NH2-terminal kinase and progression through the G1 phase of the cell cycle. J Cell Biol. 145 1461-1469.
42. Olaso, E., Salado, C., Egilegor, E., Gutierrez, V., Santisteban, A., Sancho-Bru, P., Friedman, S. L. and Vidal-Vanaclocha, F. (2003). Proangiogenic role of tumor-activated hepatic stellate cells in experimental melanoma metastasis. Hepatology 37, 674-685.
43. Opdenakker, G. and van Damme, J. (1992). Chemotactic factors, passive invasion and metastasis of cancer cells. Immunol. Today 13, 463-464.
44. Postlethwaite, A. E., Keski-Oja, J., Moses, H. L. and Kang, A. H. (1987). Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor β. J. Exp. Med. 165 251-256.
45. Riehl, R., Johnson, K., Bradley, R., Grunwald, G. B., Cornel, E., Lilienbaum, A. and Holt, C. E. (1996). Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17, 837-848.
46. Roni, V., Habeler, W., Parenti, A., Indraccolo, S., Gola, E., Tosello, V., Cortivo, R., Abatangelo, G., Chieco-Bianchi, L. and Amadori, A. (2003). Recruitment of human umbilical vein endothelial cells and human primary fibroblasts into experimental tumors growing in SCID mice. Exp. Cell Res. 287, 28-38.
47. Sawhney, R. K. and Howard, J. (2002). Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels. J. Cell Biol. 157, 1083-1091.
48. Suriano, G., Oliveira, C., Ferreira, P., Machado, J. C., Bordin, M. C., de Wever, O., Bruyneel, E. A., Moguilevsky, N., Grehan, N., Porter, T. R. et al. (2003). Identification of CDH1 germline missense mutations associated with functional inactivation of the E-cadherin protein in young gastric cancer probands. Hum. Mol. Genet. 12, 575-582.
49. Tang, L., Hung, C. P. and Schuman, E. M. (1998). A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation. Neuron 20, 1165-1175.
50. Van Aken, E. H., Papeleu, P., de Potter, P., Bruyneel, E., Philippé, J., Seregard, S., Kvanta, A., de Laey, J.-J. and Mareel, M. M. (2002). Structure and function of the N-cadherin /catenin complex in retinoblastoma. Invest. Ophthalmol. Vis. Sci. 43, 595-602.
51. Van Aken, E. H., de Wever, O., van Hoorde, L., Bruyneel, E., de Laey, J.-J. and Mareel, M. M. (2003). Invasion of retinal pigment epithelial cells: N-cadherin, hepatocyte growth factor, and focal adhesion kinase. Invest. Opthalmol. Vis. Sci. 44, 463-472.
52. Van Hoorde, L., Braet, K. and Mareel, M. (1999). The N-cadherin/catenin complex in colon fibroblasts and myofibroblasts. Cell Adhesion Commun. 7, 139-150.
53. Vermeulen, S. J., Bruyneel, E. A., Bracke, M. E., de Bruyne, G. K., Vennekens, K. M., Vieminckx, K. L., Berx, G. J., van Roy, F. M. and Mareel, M. M. (1995). Transition from the noninvasive to the invasive phenotype and loss of α-catenin in human colon cancer cells. Cancer Res. 55, 4722-4728.
54. Willems, J., Bruyneel, E., Noë, V., Slegers, H., Zwijsen, A., Mège, R.-M. and Mareel, M. (1995). Cadherin-dependent cell aggregation is affected by decapeptide derived from rat extracellular super-oxide dismutase. FEBS Lett. 363, 289-292.
55. Williams, E., Williams, G., Gour, B. J., Blaschuk, O. W. and Doherty, P. (2000). A novel family of cyclic peptide antagonists suggests that N-cadherin specificity is determined by amino acids that flank the HAV motif. J. Biol. Chem. 275, 4007-4012.
56. Yang, W., Arii, S., Mori, A., Furumoto, K., Nakao, T., Isobe, N., Murata, T., Onodera, H. and Imamura, M. (2001). sFlt-1 gene-transfected fibroblasts: a wound-specific gene therapy inhibits local cancer recurrence. Cancer Res. 61, 7840-7845.
57. Yu, Q. and Stamenkovic, I. (2000). Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis. Genes Dev. 14, 163-176.