Collagen I-mediated up-regulation of N-cadherin requires cooperative signals from integrins and discoidin domain receptor

Journal of Cell Biology

Volumn 180, Issue 6, 2008, Pages 1277-1289

  Shintani, Yasushi ^a   Fukumoto, Yuri ^b   Chaika, Nina ^a   Svoboda, Robert ^a   Wheelock, Margaret J ^a,b   Johnson, Keith R ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; DISCOIDIN; FIBRONECTIN; FOCAL ADHESION KINASE; INTEGRIN; NERVE CELL ADHESION MOLECULE; PROTEIN TYROSINE KINASE;

ARTICLE; CANCER CELL CULTURE; CELL ADHESION; CONTROLLED STUDY; HUMAN; HUMAN CELL; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; UPREGULATION;

CADHERINS; CELL ADHESION; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; COLLAGEN TYPE I; CRK-ASSOCIATED SUBSTRATE PROTEIN; EPITHELIAL CELLS; FOCAL ADHESION KINASE 2; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; INTEGRIN ALPHA2BETA1; MESODERM; NEOPLASM INVASIVENESS; RAP1 GTP-BINDING PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 41549155540     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200708137     Document Type: Article

References (83)

1. Affolter, M., S. Bellusci, N. Itoh, B. Shilo, J.P. Thiery, and Z. Werb. 2003. Tube or not tube: remodeling epithelial tissues by branching morphogenesis. Dev. Cell. 4:11-18.
2. Armstrong, T., G. Packham, L.B. Murphy, A.C. Bateman, J.A. Conti, D.R. Fine, C.D. Johnson, R.C. Benyon, and J.P. Iredale. 2004. Type I collagen promotes the malignant phenotype of pancreatic ductal adenocarcinoma. Clin. Cancer Res. 10:7427-7437.
3. Arthur, W.T., L.A. Quilliam, and J.A. Cooper. 2004. Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J. Cell Biol. 167:111-122.
4. Bachem, M.G., M. Schunemann, M. Ramadani, M. Siech, H. Beger, A. Buck, S. Zhou, A. Schmid-Kotsas, and G. Adler. 2005. Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology. 128:907-921.
5. Barrios-Rodiles, M., K.R. Brown, B. Ozdamar, R. Bose, Z. Liu, R.S. Donovan, F. Shinjo, Y. Liu, J. Dembowy, I.W. Taylor, et al. 2005. High-throughput mapping of a dynamic signaling network in mammalian cells. Science. 307:1621-1625.
6. Baumgart, M., E. Heinmoller, O. Horstmann, H. Becker, and B.M. Ghadimi. 2005. The genetic basis of sporadic pancreatic cancer. Cell. Oncol. 27:3-13.
7. Blaukat, A., I. Ivankovic-Dikic, E. Gronroos, F. Dolfi, G. Tokiwa, K. Vuori, and I. Dikic. 1999. Adaptor proteins Grb2 and Crk couple Pyk2 with activation of specific mitogen-activated protein kinase cascades. J. Biol. Chem. 274:14893-14901.
8. Bogoyevitch, M.A., and B. Kobe. 2006. Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol. Mol. Biol. Rev. 70:1061-1095.
9. Bos, J.L. 2005. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17:123-128.
10. Caron, E., A.J. Self, and A. Hall. 2000. The GTPase Rap1 controls functional activation of macrophage integrin alphaMbeta2 by LPS and other inflammatory mediators. Curr. Biol. 10:974-978.
11. Cavallaro, U., B. Schaffhauser, and G. Christofori. 2002. Cadherins and the tumour progression: is it all in a switch? Cancer Lett. 176:123-128.
12. Chodniewicz, D., and R.L. Klemke. 2004. Regulation of integrin-mediated cellular responses through assembly of a CAS/Crk scaffold. Biochim. Biophys. Acta. 1692:63-76.
13. Cordes, N., J. Seidler, R. Durzok, H. Geinitz, and C. Brakebusch. 2006. beta1-integrin-mediated signaling essentially contributes to cell survival after radiation-induced genotoxic injury. Oncogene. 25:1378-1390.
14. De Wever, O., W. Westbroek, A. Verloes, N. Bloemen, M. Bracke, C. Gespach, E. Bruyneel, and M. Mareel. 2004. Critical role of N-cadherin in myofibroblast invasion and migration in vitro stimulated by colon-cancer-cell- derived TGF- { beta } or wounding. J. Cell Sci. 117:4691-4703.
15. Defilippi, P., P. Di Stefano, and S. Cabodi. 2006. p130CAS: a versatile scaffold in signaling networks. Trends Cell Biol. 16:257-263.
16. Feltes, C.M., A. Kudo, O. Blaschuk, and S.W. Byers. 2002. An alternatively spliced cadherin-11 enhances human breast cancer cell invasion. Cancer Res. 62:6688-6697.
17. Grignani, F., T. Kinsella, A. Mencarelli, M. Valtieri, D. Riganelli, L. Lanfrancone, C. Peschle, G.P. Nolan, and P.G. Pelicci. 1998. High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res. 58:14-19.
18. Grunert, S., M. Jechlinger, and H. Beug. 2003. Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat. Rev. Mol. Cell Biol. 4:657-665.
19. Grzesiak, J.J., and M. Bouvet. 2006. The alpha2beta1 integrin mediates the malignant phenotype on type I collagen in pancreatic cancer cell lines. Br. J. Cancer. 94:1311-1319.
20. Guo, W., and F.G. Giancotti. 2004. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5:816-826.
21. Hazan, R.B., G.R. Phillips, R.F. Qiao, L. Norton, and S.A. Aaronson. 2000. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J. Cell Biol. 148:779-790.
22. Herrmann, C., G. Horn, M. Spaargaren, and A. Wittinghofer. 1996. Differential interaction of the ras family GTP-binding proteins H-Ras, Rap1A, and R-Ras with the putative effector molecules Raf kinase and Ral-guanine nucleotide exchange factor. J. Biol. Chem. 271:6794-6800.
23. Hulit, J., K. Suyama, S. Chung, R. Keren, G. Agiostratidou, W. Shan, X. Dong, T.M. Williams, M.P. Lisanti, K. Knudsen, and R.B. Hazan. 2007. N-cadherin signaling potentiates mammary tumor metastasis via enhanced extracellular signal-regulated kinase activation. Cancer Res. 67:3106-3116.
24. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687.
25. Imamura, T., H. Iguchi, T. Manabe, G. Ohshio, T. Yoshimura, Z.H. Wang, H. Suwa, S. Ishigami, and M. Imamura. 1995. Quantitative analysis of collagen and collagen subtypes I, III, and V in human pancreatic cancer, tumor-associated chronic pancreatitis, and alcoholic chronic pancreatitis. Pancreas. 11:357-364.
26. Ireton, R.C., M.A. Davis, J. van Hengel, D.J. Mariner, K. Barnes, M.A. Thoreson, P.Z. Anastasiadis, L. Matrisian, L.M. Bundy, L. Sealy, et al. 2002. A novel role for p120 catenin in E-cadherin function. J. Cell Biol. 159:465-476.
27. Islam, S., T.E. Carey, G.T. Wolf, M.J. Wheelock, and K.R. Johnson. 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.
28. Johnson, K.R., J.E. Lewis, D. Li, J. Wahl, A.P. Soler, K.A. Knudsen, and M.J. Wheelock. 1993. P- and E-cadherin are in separate complexes in cells expressing both cadherins. Exp. Cell Res. 207:252-260.
29. Johnson, E., C.S. Theisen, K.R. Johnson, and M.J. Wheelock. 2004. R-cadherin influences cell motility via Rho family GTPases. J. Biol. Chem. 279:31041-31049.
30. Keating, D.T., D.M. Sadlier, A. Patricelli, S.M. Smith, D. Walls, J.J. Egan, and P.P. Doran. 2006. Microarray identifies ADAM family members as key responders to TGF-beta1 in alveolar epithelial cells. Respir. Res. 7:114.
31. Kirsch, K., M. Kensinger, H. Hanafusa, and A. August. 2002. A p130CAS tyrosine phosphorylated substrate domain decoy disrupts v-crk signaling. BMC Cell Biol. 3:18.
32. Knox, A.L., and N.H. Brown. 2002. Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science. 295:1285-1288.
33. Koenig, A., C. Mueller, C. Hasel, G. Adler, and A. Menke. 2006. Collagen type I induces disruption of E-cadherin-mediated cell-cell contacts and promotes proliferation of pancreatic carcinoma cells. Cancer Res. 66:4662-4671.
34. Kooistra, M.R., N. Dube, and J.L. Bos. 2007. Rap1: a key regulator in cell-cell junction formation. J. Cell Sci. 120:17-22.
35. Lee, J.G., and E.P. Kay. 2 006. FGF-2-mediated signal transduction during endothelial mesenchymal transformation in corneal endothelial cells. Exp. Eye Res. 83:1309-1316.
36. Lee, J.M., S. Dedhar, R. Kalluri, and E.W. Thompson. 2006. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172:973-981.
37. Linder, S., E. Castanos-Velez, A. von Rosen, and P. Biberfeld. 2001. Immunohistochemical expression of extracellular matrix proteins and adhesion molecules in pancreatic carcinoma. Hepatogastroenterology. 48:1321-1327.
38. Liu, Y. 2004. Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J. Am. Soc. Nephrol. 15:1-12.
39. Maeda, M., K.R. Johnson, and M.J. Wheelock. 2005. Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J. Cell Sci. 118:873-887.
40. McNamee, H.P., D.E. Ingber, and M.A. Schwartz. 1993. Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J. Cell Biol. 121:673-678.
41. Menke, A., C. Philippi, R. Vogelmann, B. Seidel, M.P. Lutz, G. Adler, and D. Wedlich. 2001. Down-regulation of E-cadherin gene expression by collagen type I and type III in pancreatic cancer cell lines. Cancer Res. 61:3508-3517.
42. Miranti, C.K., and J.S. Brugge. 2002. Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4:E83-E90.
43. Moustakas, A., and C.H. Heldin. 2005. Non-Smad TGF-beta signals. J. Cell Sci. 118:3573-3584.
44. Nieman, M.T., R.S. Prudoff, K.R. Johnson, and M.J. Wheelock. 1999. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J. Cell Biol. 147:631-644.
45. Orr, A.W., and J.E. Murphy-Ullrich. 2004. Regulation of endothelial cell function BY FAK and PYK2. Front. Biosci. 9:1254-1266.
46. Ozdamar, B., R. Bose, M. Barrios-Rodiles, H.R. Wang, Y. Zhang, and J.L. Wrana. 2005. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science. 307:1603-1609.
47. Park, S.Y., H.K. Avraham, and S. Avraham. 2004. RAFTK/Pyk2 activation is mediated by trans-acting autophosphorylation in a Src-independent manner. J. Biol. Chem. 279:33315-33322.
48. Pishvaian, M.J., C.M. Feltes, P. Thompson, M.J. Bussemakers, J.A. Schalken, and S.W. Byers. 1999. Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res. 59:947-952.
49. Price, L.S., A. Hajdo-Milasinovic, J. Zhao, F.J. Zwartkruis, J.G. Collard, and J.L. Bos. 2004. Rap1 regulates E-cadherin-mediated cell-cell adhesion. J. Biol. Chem. 279:35127-35132.
50. Radisky, D.C., D.D. Levy, L.E. Littlepage, H. Liu, C.M. Nelson, J.E. Fata, D. Leake, E.L. Godden, D.G. Albertson, M.A. Nieto, et al. 2005. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature. 436:123-127.
51. Reedquist, K.A., E. Ross, E.A. Koop, R.M. Wolthuis, F.J. Zwartkruis, Y. van Kooyk, M. Salmon, C.D. Buckley, and J.L. Bos. 2000. The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J. Cell Biol. 148:1151-1158.
52. Ross, K.R., D.A. Corey, J.M. Dunn, and T.J. Kelley. 2007. SMAD3 expression is regulated by mitogen-activated protein kinase kinase-1 in epithelial and smooth muscle cells. Cell. Signal. 19:923-931.
53. Sander, E.E., S. van Delft, J.P. ten Klooster, T. Reid, R.A. van der Kammen, F. Michiels, and J.G. Collard. 1998. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143:1385-1398.
54. Saoncella, S., F. Echtermeyer, F. Denhez, J.K. Nowlen, D.F. Mosher, S.D. Robinson, R.O. Hynes, and P.F. Goetinck. 1999. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl. Acad. Sci. USA. 96:2805-2810.
55. Savagner, P. 2001. Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays. 23:912-923.
56. Schaller, M.D., C.A. Borgman, B.S. Cobb, R.R. Vines, A.B. Reynolds, and J.T. Parsons. 1992. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA. 89:5192-5196.
57. Schlaepfer, D.D., and T. Hunter. 1998. Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell Biol. 8:151-157.
58. Shi, Y., and J. Massague. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 113:685-700.
59. 2-terminal kinase 1 and up-regulating N-Cadherin expression. Cancer Res. 66:11745-11753.
60. Shintani, Y., M.J. Wheelock, and K.R. Johnson. 2006b. PI3K-Rac1-JNK signaling mediates collagen I-induced cell scattering and up-regulation of N-cadherin expression in mouse mammary epithelial cells. Mol. Biol. Cell. 17:2963-2975.
61. Shintani, Y., Y. Fukumoto, P.M. Grandgenett, M.A. Hollingsworth, M.J. Wheelock, and K.R. Johnson. 2008a. ADH-1 suppresses N-cadherin-dependent pancreatic cancer progression. Int. J. Cancer. 122:71-77.
62. Shintani, Y., M. Maeda, N. Chaika, K.R. Johnson, and M.J. Wheelock. 2008b. Collagen I Promotes EMT in Lung Cancer Cells via TGF-beta3 Signaling. Am. J. Respir. Cell Mol. Biol. 38:95-104.
63. Tanaka, S., and H. Hanafusa. 1998. Guanine-nucleotide exchange protein C3G activates JNK1 by a ras-independent mechanism. JNK1 activation inhibited by kinase negative forms of MLK3 and DLK mixed lineage kinases. J. Biol. Chem. 273:1281-1284.
64. ten Dijke, P., and C.S. Hill. 2004. New insights into TGF-beta-Smad signalling. Trends Biochem. Sci. 29:265-273.
65. Thiery, J.P. 2002. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer. 2:442-454.
66. Thiery, J.P. 2003. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15:740-746.
67. Thiery, J.P., and J.P. Sleeman. 2006. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7:131-142.
68. Tomita, K., A. van Bokhoven, G.J. van Leenders, E.T. Ruijter, C.F. Jansen, M.J. Bussemakers, and J.A. Schalken. 2000. Cadherin switching in human prostate cancer progression. Cancer Res. 60:3650-3654.
69. Vogel, W., C. Brakebusch, R. Fassler, F. Alves, F. Ruggiero, and T. Pawson. 2000. Discoidin domain receptor 1 is activated independently of beta(1) integrin. J. Biol. Chem. 275:5779-5784.
70. Vogel, W.F., R. Abdulhussein, and C.E. Ford. 2006. Sensing extracellular matrix: an update on discoidin domain receptor function. Cell. Signal. 18:1108-1116.
71. Wahl, J.K. III, Y.J. Kim, J.M. Cullen, K.R. Johnson, and M.J. Wheelock. 2003. N-cadherin-catenin complexes form prior to cleavage of the proregion and transport to the plasma membrane. J. Biol. Chem. 278:17269-17276.
72. Wang, L., Y. Pan, and J.L. Dai. 2004. Evidence of MKK4 pro-oncogenic activity in breast and pancreatic tumors. Oncogene. 23:5978-5985.
73. Wilcox-Adelman, S.A., F. Denhez, and P.F. Goetinck. 2002. Syndecan-4 modulates focal adhesion kinase phosphorylation. J. Biol. Chem. 277:32970-32977.
74. Yajnik, V., C. Paulding, R. Sordella, A.I. McClatchey, M. Saito, D.C. Wahrer, P. Reynolds, D.W. Bell, R. Lake, S. van den Heuvel, et al. 2003. DOCK4, a GTPase activator, is disrupted during tumorigenesis. Cell. 112:673-684.
75. Yamanari, H., T. Suganuma, T. Iwamura, N. Kitamura, S. Taniguchi, and T. Setoguchi. 1994. Extracellular matrix components regulating glandular differentiation and the formation of basal lamina of a human pancreatic cancer cell line in vitro. Exp. Cell Res. 211:175-182.
76. Yano, H., Y. Mazaki, K. Kurokawa, S.K. Hanks, M. Matsuda, and H. Sabe. 2004. Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J. Cell Biol. 166:283-295.
77. Zavadil, J., and E.P. Bottinger. 2005. TGF-beta and epithelial-to- mesenchymal transitions. Oncogene. 24:5764-5774.
78. Zeisberg, M., G. Bonner, Y. Maeshima, P. Colorado, G.A. Muller, F. Strutz, and R. Kalluri. 2001. Renal fibrosis: collagen composition and assembly regulates epithelial-mesenchymal transdifferentiation. Am. J. Pathol. 159:1313-1321.
79. Zeisberg, M., Y. Maeshima, B. Mosterman, and R. Kalluri. 2002. Renal fibrosis. Extracellular matrix microenvironment regulates migratory behavior of activated tubular epithelial cells. Am. J. Pathol. 160:2001-2008.
80. Zhang, G., K.A. Kernan, S.J. Collins, X. Cai, J.M. Lopez-Guisa, J.L. Degen, Y. Shvil, and A.A. Eddy. 2007. Plasmin(ogen) promotes renal interstitial fibrosis by promoting epithelial-to-mesenchymal transition: role of plasmin-activated signals. J. Am. Soc. Nephrol. 18:846-859.
81. Zhang, L., L. Chenwei, R. Mahmood, K. van Golen, J. Greenson, G. Li, N.J. D'Silva, X. Li, C.F. Burant, C.D. Logsdon, and D.M. Simeone. 2006. Identification of a putative tumor suppressor gene Rap1GAP in pancreatic cancer. Cancer Res. 66:898-906.
82. Zheng, C., J. Xiang, T. Hunter, and A. Lin. 1999. The JNKK2-JNK1 fusion protein acts as a constitutively active c-Jun kinase that stimulates c-Jun transcription activity. J. Biol. Chem. 274:28966-28971.
83. Zoltan-Jones, A., L. Huang, S. Ghatak, and B.P. Toole. 2003. Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J. Biol. Chem. 278:45801-45810.