E-cadherin-dependent growth suppression is mediated by the cyclin- dependent kinase inhibitor p27(KIP1)

Journal of Cell Biology

Volumn 142, Issue 2, 1998, Pages 557-571

  St Croix, Brad ^a,c   Sheehan, Capucine ^a   Rak, Janusz W ^a   Fłorenes, Vivi Ann ^a   Slingerland, Joyce M ^a,b   Kerbel, Robert S ^a  

^a SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^b DEPARTMENT OF RADIATION ONCOLOGY   (Canada)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Cyclin D; E cadherin; Epidermal growth factor receptor; Kip1; P27

Indexed keywords

CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN P27; RETINOBLASTOMA PROTEIN; UVOMORULIN;

ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL CONTACT; CELL FUNCTION; CELL PROLIFERATION; GROWTH INHIBITION; PRIORITY JOURNAL; PROTEIN BINDING; RETINOBLASTOMA; SURVIVAL RATE;

ANIMALS; CADHERINS; CELL ADHESION; CELL CYCLE PROTEINS; CELL DIVISION; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; ENZYME INHIBITORS; FEMALE; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NEUTRALIZATION TESTS; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN; TRANSFECTION; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

EID: 0032572526     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.2.557     Document Type: Article

References (86)

1. Aberle, H., H. Schwartz, and R. Kemler. 1996. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J. Cell Biochem. 61:514-523.
2. Agrawal, D., P. Hauser, F. McPherson, F. Dong, A. Garcia, and W.J. Pledger. 1996. Repression of p27kip1 synthesis by platelet-derived growth factor in BALB/c 3T3 cells. Mol. Cell Biol. 16:4327-4336.
3. Alessandrini, A., D.S. Chiaur, and M. Pagano. 1997. Regulation of the cyclin-dependent kinase inhibitor p27 by degradation and phosphorylation. Leukemia. 11:342-345.
4. 3H]thymidine-labeled spheroids. Demonstration that some non-labeled cells have S and G2 DNA content. Cell Tissue Kinet. 16:237-246.
5. Aoki, J., M. Umeda, K. Takio, K. Titani, H. Utsumi, M. Sasaki, and K. Inoue. 1991. Neural cell adhesion molecule mediates contact-dependent inhibition of growth of near-diploid mouse fibroblast cell line m5S/1M. J. Cell Biol. 115:1751-1761.
6. Assoian, R.K. 1997. Anchorage-dependent cell cycle progression. J. Cell Biol. 136:1-4.
7. Balsamo, J., T. Leung, H. Ernst, M.K. Zanin, S. Hoffman, and J. Lilien. 1996. Regulated binding of PTP1B-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of beta-catenin. J. Cell Biol. 134:801-813.
8. Becker, K.F., M.J. Atkinson, U. Reich, I. Becker, H. Nekarda, J.R. Siewert, and H. Hofler. 1994. E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res. 54:3845-3852.
9. Bohrens, J., J.P. von Kries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of β-catenin with the transcription factor LEF-1. Nature. 382:638-642.
10. Berx, G., A.M. Cleton-Jansen, K. Strumane, W.J. de Leeuw, F. Nollet, F. Van Roy, and C. Cornelisse. 1996. E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene. 13:1919-1925.
11. Bjorge, J.D., T.O. Chan, M. Antczak, H.J. Kung, and D.J. Fujita. 1990. Activated type I phosphatidylinositol kinase is associated with the epidermal growth factor (EGF) receptor following EGF stimulation. Proc. Natl. Acad. Sci. USA. 87:3816-3820.
12. Bottazzi, M.E., and R.K. Assoian. 1997. The extracellular matrix and mitogenic growth factors control G1 phase cyclins and cyclin-dependent kinase inhibitors. Trends Cell Biol. 7:348-352.
13. Brady-Kalnay, S.M., A.J. Flint, and N.K. Tonks. 1993. Homophilic binding of PTPμ, a receptor-type protein tyrosine phosphatase, can mediate cell-cell aggregation. J. Cell Biol. 122:961-972.
14. Bullions, L.C., D.A. Notterman, L.S. Chung, and A.J. Levine. 1997. Expression of wild-type alpha-catenin protein in cells with a mutant alpha-catenin gene restores both growth regulation and tumor suppressor activities. Mol. Cell Biol. 17:4501-4508.
15. Kip1 for restriction point control of the fibroblast cell cycle. Science. 272: 877-880.
16. Diehl, J.A., F. Zindy, and C.J. Sherr. 1997. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11:957-972.
17. Dimanche-Boitrel, M.T., P. Genne, O. Duchamp, and B. Chauffert. 1994. Confluence dependent resistance (CDR) to doxorubicin and E-cadherin expression in murine mammary cells. Cancer Lett. 85:173-176.
18. Fagotto, F., N. Funayama, U. Gluck, and B.M. Gumbiner. 1996. Binding to cadherins antagonizes the signaling activity of beta-catenin during axis formation in Xenopus. J. Cell Biol. 132:1105-1114.
19. Freyer, J.P., and R.M. Sutherland. 1980. Selective dissociation and characterization of cells from different regions of multicell tumor spheroids. Cancer Res. 40:3956-3965.
20. Gaits, F., R.Y. Li, A. Ragab, J.M. Ragab-Thomas, and H. Chap. 1995. Increase in receptor-like protein tyrosine phosphatase activity and expression level on density-dependent growth arrest of endothelial cells. Biochem. J. 311:97-103.
21. Gebbink, M.F., G.C. Zondag, G.M. Koningstein, E. Feiken, R.W. Wubbolts, and W.H. Moolenaar. 1995. Cell surface expression of receptor protein tyrosine phosphatase RPTP mu is regulated by cell-cell contact. J. Cell Biol. 131:251-260.
22. Helmlinger, G., P.A. Netti, H.C. Lichtenbeld, R.J. Melder, and R.K. Jain. 1997. Solid stress inhibits the growth of multicellular tumor spheroids. Nat. Biotechnol. 15:778-783.
23. Hengst, L., V. Dulic, J.M. Slingerland, E. Lees, and S.I. Reed. 1994. A cell cycle-regulated inhibitor of cyclin-dependent kinases. Proc. Natl. Acad. Sci. USA. 91:5291-5295.
24. Kip1 accumulation during the cell cycle. Science. 271:1861-1864.
25. Hermiston, M.L., M.H. Wong, and J.I. Gordon. 1996. Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev. 10:985-996.
26. Hermiston, M.L., and J.I. Gordon. 1995a. In vivo analysis of cadherin function in the mouse intestinal epithelium: essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death. J. Cell Biol. 129: 489-506.
27. Hermiston, M.L., and J.I. Gordon. 1995b. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science. 270: 1203-1207.
28. Hoschuetzky, H., H. Aberle, and R. Kemler. 1994. Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127:1375-1380.
29. Huang, F., S. Hsu, Z. Yan, S. Winawer, and E. Friedman. 1994. The capacity for growth stimulation by TGF beta 1 seen only in advanced colon cancers cannot be ascribed to mutations in APC, DCC, p53 or ras. Oncogene. 9:3701-3706.
30. Huber, O., R. Korn, J. McLaughlin, M. Ohsugi, B.G. Herrmann, and R. Kemler. 1996. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59:3-10.
31. Irani, K., Y. Xia, J.L. Zweier, S.J. Sollott, C.J. Der, E.R. Fearon, M. Sundaresan, T. Finkel, and P.J. Goldschmidt-Clermont. 1997. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science. 275:1649-1652.
32. Johnson, J.P. 1991. Cell adhesion molecules of the immunoglobulin supergene family and their role in malignant transformation and progression to metastatic disease. Cancer Metastasis Rev. 10:11-22.
33. Jothy, S., S.B. Munro, L. LeDuy, D. McClure, and O.W. Blaschuk. 1995. Adhesion or anti-adhesion in cancer: what matters more? Cancer Metastasis Rev. 14:363-376.
34. Juliano, R.L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J. Cell Biol. 120:577-585.
35. Kanal, Y., A. Ochiai, T. Shibata, T. Oyama, S. Ushijima, S. Akimoto, and S. Hirohashi. 1995. c-erbB-2 gene product directly associates with beta-catenin and plakoglobin. Biochem. Biophys. Res. Commun. 208:1067-1072.
36. Kandikonda, S., D. Oda, R. Niederman, and B.C. Sorkin. 1996. Cadherin-mediated adhesion is required for normal growth regulation of human gingival epithelial cells. Cell Adhes. Commun. 4:13-24.
37. Kato, A., H. Takahashi, Y. Takahashi, and H. Matsushime. 1997. Inactivation of the cyclin D-dependent kinase in the rat fibroblast cell line, 3Y1, induced by contact inhibition. J. Biol. Chem. 272:8065-8070.
38. Kato, J.Y., M. Matsuoka, K. Polyak, J. Massague, and C.J. Sherr. 1994. Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell. 79:487-496.
39. Kawada, M., S. Yamagoe, Y. Murakami, K. Suzuki, S. Mizuno, and Y. Uehara. 1997. Induction of p27Kip1 degradation and anchorage independence by Ras through the MAP kinase signaling pathway. Oncogene. 15:629-637.
40. Kobayashi, H., S. Man, S.J. Kapitain, B.A. Teicher, and R.S. Kerbel. 1993. Acquired multicellular-mediated resistance to alkylating agents in cancer. Proc. Natl. Acad. Sci. USA. 90:3294-3298.
41. Kypta, R.M., H. Su, and L.F. Reichardt. 1996. Association between a transmembrane protein tyrosine phosphatase and the cadherin-catenin complex. J. Cell Biol. 134:1519-1529.
42. Lichtner, R.B., and V. Schirrmacher. 1990. Cellular distribution and biological activity of epidermal growth factor receptors in A431 cells are influenced by cell-cell contact. J. Cell Physiol. 144:303-312.
43. Mandal, M., D. Bandyopadhyay, T.M. Goepfert, and R. Kumar. 1998. Interferon-induces expression of cyclin-dependent kinase-inhibitors p21WAF1 and p27Kip1 that prevent activation of cyclin-dependent kinase by CDK-activating kinase (CAK). Oncogene. 16:217-225.
44. Mansbridge, J.N., R. Knuchel, A.M. Knapp, and R.M. Sutherland. 1992. Importance of tyrosine phosphatases in the effects of cell-cell contact and microenvironments on EGF-stimulated tyrosine phosphorylation. J. Cell Physiol. 151:433-442.
45. Meredith, J.E.J., and M.A. Schwartz. 1997. Integrins, adhesion and apoptosis. Trends Cell Biol. 7:146-151.
46. Miyaki, M., K. Tanaka, R. Kikuchi-Yanoshita, M. Muraoka, M. Konishi, and M. Takeichi. 1995. Increased cell-substratum adhesion, and decreased gelatinase secretion and cell growth, induced by E-cadherin transfection of human colon carcinoma cells. Oncogene. 11:2547-2552.
47. Molenaar, M., M. van de Wetering, M. Oosterwegel, J. Peterson-Maduro, S. Godsave, V. Korinek, J. Roose, O. Destree, and H. Clevers. 1996. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell. 86:391-399.
48. Morgan, D.O. 1995. Principles of CDK regulation. Nature. 374:131-134.
49. kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell. 85: 707-720.
50. Navarro, P., M. Gomez, A. Pizarro, C. Gamallo, M. Quintanilla, and A. Cano. 1991. A role for the E-cadherin cell-cell adhesion molecule during tumor progression of mouse epidermal carcinogenesis. J. Cell Biol. 115:517-533.
51. Nederman, T., J. Carlsson, and K. Kuoppa. 1988. Penetration of substances into tumour tissue. Model studies using saccharides, thymidine and thymidine-5′-triphosphate in cellular spheroids. Cancer Chemother. Pharmacol. 22:21-25.
52. Ostman, A., Q. Yang, and N.K. Tonks. 1994. Expression of DEP-1, a receptor-like protein-tyrosine-phosphatase, is enhanced with increasing cell density. Proc. Natl. Acad. Sci. USA. 91:9680-9684.
53. Pagano, M., S.W. Tam, A.M. Theodoras, P. Beer-Romero, G. Del Sal, V. Chau, P.R. Yew, G.F. Draetta, and M. Rolfe. 1995. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science. 269:682-685.
54. Pallen, C.J., and P.H. Tong. 1991. Elevation of membrane tyrosine phosphatase activity in density-dependent growth-arrested fibroblasts. Proc. Natl. Acad. Sci. USA. 88:6996-7000.
55. Papkoff, J. 1997. Regulation of complexed and free catenin pools by distinct mechanisms. Differential effects of Wnt-1 and v-Src. J. Biol. Chem. 272: 4536-4543.
56. 1. Cancer Res. 56:3666-3669.
57. Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev. 8:9-22.
58. Rivard, N., G. L'Allemain, J. Bartek, and J. Pouyssegur. 1996. Abrogation of p27Kip1 by cDNA antisense suppresses quiescence (G0 state) in fibroblasts. J. Biol. Chem. 271:18337-18341.
59. Rodriguez-Viciana, P., P.H. Warne, R. Dhand, B. Vanhaesebroeck, I. Gout, M.J. Fry, M.D. Waterfield, and J. Downward. 1994. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature. 370:527-532.
60. Rodriguez-Viciana, P., P.H. Warne, A. Khwaja, B.M. Marte, D. Pappin, P. Das, M.D. Waterfield, A. Ridley, and J. Downward. 1997. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell. 89:457-467.
61. Rubinfeld, B., B. Souza, I. Albert, O. Muller, S.H. Chamberlain, F.R. Masiarz, S. Munemitsu, and P. Polakis. 1993. Association of the APC gene product with beta-catenin. Science. 262:1731-1734.
62. INK4B-cdk4 complexes, and inhibits cyclin D1-cdk4 association in human mammary epithelial cells. Mol. Cell Biol. 17:2458-2467.
63. Shankland, S.J., J. Pippin, M. Flanagan, S.R. Coats, M. Nangaku, K.L. Gordon, J.M. Roberts, W.G. Couser, and R.J. Johnson. 1997. Mesangial cell proliferation mediated by PDGF and bFGF is determined by levels of the cyclin kinase inhibitor p27Kip1. Kidney Int. 51:1088-1099.
64. Sheaff, R.J., M. Groudine, M. Gordon, J.M. Roberts, and B.E. Clurman. 1997. Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 11:1464-1478.
65. Sherr, C.J. 1995. D-type cyclins. Trends. Biochem. Sci. 20:187-190.
66. 1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
67. Shibamoto, S., M. Hayakawa, K. Takeuchi, T. Hori, N. Oku, K. Miyazawa, N. Kitamura, M. Takeichi, and F. Ito. 1994. Tyrosine phosphorylation of beta-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhes. Commun. 1:295-305.
68. Shibata, T., A. Ochiai, Y. Kanai, S. Akimoto, M. Gotoh, N. Yasui, R. Machinami, and S. Hirohashi. 1996. Dominant negative inhibition of the association between beta-catenin and c-erbB-2 by N-terminally deleted beta-catenin suppresses the invasion and metastasis of cancer cells. Oncogene. 13: 883-889.
69. Shiozaki, H., T. Kadowaki, Y. Doki, M. Inoue, S. Tamura, H. Oka, T. Iwazawa, S. Matsui, K. Shimaya, and M. Takeichi. 1995. Effect of epidermal growth factor on cadherin-mediated adhesion in a human oesophageal cancer cell line. Br. J. Cancer. 71:250-258.
70. Slingerland, J.M., L. Hengst, C.-H. Pan, D. Alexander, M.R. Stampfer, and S.I. Reed. 1994. A novel inhibitor of cyclin-Cdk activity detected in transforming growth factor β-arrested epithelial cells. Mol. Cell. Biol. 14:3683-3694.
71. Sorby, M., and A. Ostman. 1996. Protein-tyrosine phosphatase-mediated decrease of epidermal growth factor and platelet-derived growth factor receptor tyrosine phosphorylation in high cell density cultures. J. Biol. Chem. 271: 10963-10966.
72. Kip1 on adhesion-dependent resistance of tumor cells to anticancer agents. Nat. Med. 2:1204-1210.
73. St. Croix, B., J.W. Rak, S. Kapitain, C. Sheehan, C.H. Graham, and R.S. Kerbel. 1996b. Reversal by hyaluronidase of adhesion-dependent multicellular drug resistance in mammary carcinoma cells. J. Natl. Cancer Inst. 88:1285-1296.
74. St. Croix, B., and R.S. Kerbel. 1997. Cell adhesion and drug resistance in cancer. Curr. Opin. Oncol. 9:549-556.
75. Stappert, J., and R. Kemler. 1994. A short core region of E-cadherin is essential for catenin binding and is highly phosphorylated. Cell Adhes. Commun. 2:319-327.
76. Su, L.K., B. Vogelstein, and K.W. Kinzler. 1993. Association of the APC tumor suppressor protein with catenins. Science. 262:1734-1737.
77. Takahashi, K., and K. Suzuki. 1996. Density-dependent inhibition of growth involves prevention of EGF receptor activation by E-cadherin-mediated cell-cell adhesion. Exp. Cell Res. 226:214-222.
78. Takeda, H., A. Nagafuchi, S. Yonemura, S. Tsukita, J. Behrens, and W. Birchmeier. 1995. V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and beta catenin is not required for the shift. J. Cell Biol. 131:1839-1847.
79. Takuwa, N., and Y. Takuwa. 1997. Ras activity late in G1 phase required for p27kip1 downregulation, passage through the restriction point, and entry into S phase in growth factor-stimulated NIH 3T3 fibroblasts. Mol. Cell Biol. 17:5348-5358.
80. Vestweber, D., and R. Kemler. 1985. Identification of a putative cell adhesion domain of uvomorulin. EMBO (Eur. Mol. Biol. Organ.) J. 4:3393-3398.
81. Kip1. EMBO (Eur. Mol. Biol. Organ.) J. 16:5334-5344.
82. Vleminckx, K., L. Vakaet, Jr., M. Mareel, W. Fiers, and F. Van Roy. 1991. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell. 66:107-119.
83. Wang, H., Z. Lian, M.M. Lerch, Z. Chen, W. Xie, and A. Ullrich. 1996. Characterization of PCP-2, a novel receptor protein tyrosine phosphatase of the MAM domain family. Oncogene. 12:2555-2562.
84. Watabe, M., A. Nagafuchi, S. Tsukita, and M. Takeichi. 1994. Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line. J. Cell Biol. 127:247-256.
85. Watanabe, Y., S.W. Lee, M. Detmar, I. Ajioka, and H.F. Dvorak. 1997. Vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) delays and induces escape from senescence in human dermal microvascular endothelial cells. Oncogene. 14:2025-2032.
86. Winston, J., F. Dong, and W.J. Pledger. 1996. Differential modulation of G1 cyclins and the Cdk inhibitor p27kip1 by platelet-derived growth factor and plasma factors in density-arrested fibroblasts. J. Biol. Chem. 271:11253-11260.