Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin

Journal of Experimental Medicine

Volumn 204, Issue 12, 2007, Pages 2935-2948

  Leong, Kevin G ^a,c   Niessen, Kyle ^a,c   Kulic, Iva ^a,c   Raouf, Afshin ^b   Eaves, Connie ^b,c   Pollet, Ingrid ^a,c   Karsan, Aly ^a,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; JAGGED1; NOTCH RECEPTOR; TRANSCRIPTION FACTOR SLUG; TUMOR MARKER; UVOMORULIN;

ANOIKIS; ARTICLE; BREAST CANCER; CANCER INHIBITION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; MESENCHYME CELL; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSITIONAL CELL CARCINOMA;

BINDING SITES; BREAST; BREAST NEOPLASMS; CADHERINS; CALCIUM-BINDING PROTEINS; CELL LINE; EPITHELIAL CELLS; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MESODERM; RECEPTOR, NOTCH1; TRANSCRIPTION FACTORS;

EID: 36549010842     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20071082     Document Type: Article

References (57)

1. Mumm, J.S., and R. Kopan. 2000. Notch signaling: from the outside in. Dev. Biol. 228:151-165.
2. Leong, K.G., and A. Karsan. 2006. Recent insights into the role of Notch signaling in tumorigenesis. Blood. 107:2223-2233.
3. Gallahan, D., C. Jhappan, G. Robinson, L. Hennighausen, R. Sharp, E. Kordon, R. Callahan, G. Merlino, and G.H. Smith. 1996. Expression of a truncated Int3 gene in developing secretory mammary epithelium specifically retards lobular differentiation resulting in tumorigenesis. Cancer Res. 56:1775-1785.
4. Hu, C., A. Dievart, M. Lupien, E. Calvo, G. Tremblay, and P. Jolicoeur. 2006. Overexpression of activated murine Notch1 and Notch3 in transgenic mice blocks mammary gland development and induces mammary tumors. Am. J. Pathol. 168:973-990.
5. Callahan, R., and S.E. Egan. 2004. Notch signaling in mammary development and oncogenesis. J. Mammary Gland Biol. Neoplasia. 9:145-163.
6. Parr, C., G. Watkins, and W.G. Jiang. 2004. The possible correlation of Notch-1 and Notch-2 with clinical outcome and tumour clinicopathological parameters in human breast cancer. Int. J. Mol. Med. 14:779-786.
7. Reedijk, M., S. Odorcic, L. Chang, H. Zhang, N. Miller, D.R. McCready, G. Lockwood, and S.E. Egan. 2005. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res. 65:8530-8537.
8. Ayyanan, A., G. Civenni, L. Ciarloni, C. Morel, N. Mueller, K. Lefort, A. Mandinova, W. Raffoul, M. Fiche, G.P. Dotto, and C. Brisken. 2006. Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc. Natl. Acad. Sci. USA. 103:3799-3804.
9. Weijzen, S., P. Rizzo, M. Braid, R. Vaishnav, S.M. Jonkheer, A. Zlobin, B.A. Osborne, S. Gottipati, J.C. Aster, W.C. Hahn, et al. 2002. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat. Med. 8:979-986.
10. Pece, S., M. Serresi, E. Santolini, M. Capra, E. Hulleman, V. Galimberti, S. Zurrida, P. Maisonneuve, G. Viale, and P.P. Di Fiore. 2004. Loss of negative regulation by Numb over Notch is relevant to human breast carcinogenesis. J. Cell Biol. 167:215-221.
11. Stylianou, S., R.B. Clarke, and K. Brennan. 2006. Aberrant activation of notch signaling in human breast cancer. Cancer Res. 66:1517-1525.
12. Vincent-Salomon, A., and J.P. Thiery. 2003. Host microenvironment in breast cancer development: epithelial-mesenchymal transition in breast cancer development. Breast Cancer Res. 5:101-106.
13. Timmerman, L.A., J. Grego-Bessa, A. Raya, E. Bertran, J.M. Perez-Pomares, J. Diez, S. Aranda, S. Palomo, F. McCormick, J.C. Izpisua-Belmonte, and J.L. de la Pompa. 2004. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18:99-115.
14. Noseda, M., G. McLean, K. Niessen, L. Chang, I. Pollet, R. Montpetit, R. Shahidi, K. Dorovini-Zis, L. Li, B. Beckstead, et al. 2004. Notch activation results in phenotypic and functional changes consistent with endothelial-to-mesenchymal transformation. Circ. Res. 94:910-917.
15. Come, C., V. Arnoux, F. Bibeau, and P. Savagner. 2004. Roles of the transcription factors snail and slug during mammary morphogenesis and breast carcinoma progression. J. Mammary Gland Biol. Neoplasia. 9:183-193.
16. Martin, T.A., A. Goyal, G. Watkins, and W.G. Jiang. 2005. Expression of the transcription factors snail, slug, and twist and their clinical signifi-cance in human breast cancer. Ann. Surg. Oncol. 12:488-496.
17. Rhodes, D.R., J. Yu, K. Shanker, N. Deshpande, R. Varambally, D. Ghosh, T. Barrette, A. Pandey, and A.M. Chinnaiyan. 2004. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia. 6:1-6.
18. Iso, T., L. Kedes, and Y. Hamamori. 2003. HES and HERP families: multiple effectors of the Notch signaling pathway. J. Cell. Physiol. 194:237-255.
19. van de Wetering, M., N. Barker, I.C. Harkes, M. van der Heyden, N.J. Dijk, A. Hollestelle, J.G. Klijn, H. Clevers, and M. Schutte. 2001. Mutant E-cadherin breast cancer cells do not display constitutive Wnt signaling. Cancer Res. 61:278-284.
20. Imatani, A., and R. Callahan. 2000. Identification of a novel NOTCH-4/INT-3 RNA species encoding an activated gene product in certain human tumor cell lines. Oncogene. 19:223-231.
21. Small, D., D. Kovalenko, D. Kacer, L. Liaw, M. Landriscina, C. Di Serio, I. Prudovsky, and T. Maciag. 2001. Soluble Jagged 1 represses the function of its transmembrane form to induce the formation of the Src-dependent chord-like phenotype. J. Biol. Chem. 276:32022-32030.
22. Marambaud, P., J. Shioi, G. Serban, A. Georgakopoulos, S. Sarner, V. Nagy, L. Baki, P. Wen, S. Efthimiopoulos, Z. Shao, et al. 2002. A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J. 21:1948-1956.
23. Zavadil, J., L. Cermak, N. Soto-Nieves, and E.P. Bottinger. 2004. Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J. 23:1155-1165.
24. Krebs, L.T., Y. Xue, C.R. Norton, J.R. Shutter, M. Maguire, J.P. Sundberg, D. Gallahan, V. Closson, J. Kitajewski, R. Callahan, et al. 2000. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 14:1343-1352.
25. Leong, K.G., X. Hu, L. Li, M. Noseda, B. Larrivee, C. Hull, L. Hood, F. Wong, and A. Karsan. 2002. Activated Notch4 inhibits angiogenesis: role of beta 1-integrin activation. Mol. Cell. Biol. 22:2830-2841.
26. Zeng, Q., S. Li, D.B. Chepeha, T.J. Giordano, J. Li, H. Zhang, P.J. Polverini, J. Nor, J. Kitajewski, and C.Y. Wang. 2005. Crosstalk between tumor and endothelial cells promotes tumor angiogenesis by MAPK activation of Notch signaling. Cancer Cell. 8:13-23.
27. Hatsell, S., T. Rowlands, M. Hiremath, and P. Cowin. 2003. Beta-catenin and Tcfs in mammary development and cancer. J. Mammary Gland Biol. Neoplasia. 8:145-158.
28. Wong, A.S., and B.M. Gumbiner. 2003. Adhesion-independent mechanism for suppression of tumor cell invasion by E-cadherin. J. Cell Biol. 161:1191-1203.
29. Tripathi, M.K., S. Misra, S.V. Khedkar, N. Hamilton, C. Irvin-Wilson, C. Sharan, L. Sealy, and G. Chaudhuri. 2005. Regulation of BRCA2 gene expression by the SLUG repressor protein in human breast cells. J. Biol. Chem. 280:17163-17171.
30. Bachman, K.E., B.H. Park, I. Rhee, H. Rajagopalan, J.G. Herman, S.B. Baylin, K.W. Kinzler, and B. Vogelstein. 2003. Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell. 3:89-95.
31. Berx, G., K. Staes, J. van Hengel, F. Molemans, M.J. Bussemakers, A. van Bokhoven, and F. van Roy. 1995. Cloning and characterization of the human invasion suppressor gene E-cadherin (CDH1). Genomics. 26:281-289.
32. Cameron, E.E., K.E. Bachman, S. Myohanen, J.G. Herman, and S.B. Baylin. 1999. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet. 21:103-107.
33. MacKenzie, F., P. Duriez, F. Wong, M. Noseda, and A. Karsan. 2004. Notch4 inhibits endothelial apoptosis via RBP-Jkappa-dependent and -independent pathways. J. Biol. Chem. 279:11657-11663.
34. Zweidler-McKay, P.A., Y. He, L. Xu, C.G. Rodriguez, F.G. Karnell, A.C. Carpenter, J.C. Aster, D. Allman, and W.S. Pear. 2005. Notch signaling is a potent inducer of growth arrest and apoptosis in a wide range of B cell malignancies. Blood. 106:3898-3906.
35. Weng, A.P., A.A. Ferrando, W. Lee, J.P. Morris IV, L.B. Silverman, C. Sanchez-Irizarry, S.C. Blacklow, A.T. Look, and J.C. Aster. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 306:269-271.
36. Santagata, S., F. Demichelis, A. Riva, S. Varambally, M.D. Hofer, J.L. Kutok, R. Kim, J. Tang, J.E. Montie, A.M. Chinnaiyan, et al. 2004. JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res. 64:6854-6857.
37. Parker, B.S., P. Argani, B.P. Cook, H. Liangfeng, S.D. Chartrand, M. Zhang, S. Saha, A. Bardelli, Y. Jiang, T.B. St Martin, et al. 2004. Alterations in vascular gene expression in invasive breast carcinoma. Cancer Res. 64:7857-7866.
38. Wu, W.S., S. Heinrichs, D. Xu, S.P. Garrison, G.P. Zambetti, J.M. Adams, and A.T. Look. 2005. Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell. 123:641-653.
39. Mungamuri, S.K., X. Yang, A.D. Thor, and K. Somasundaram. 2006. Survival signaling by Notch1: mammalian target of rapamycin (mTOR)-dependent inhibition of p53. Cancer Res. 66:4715-4724.
40. Androutsellis-Theotokis, A., R.R. Leker, F. Soldner, D.J. Hoeppner, R. Ravin, S.W. Poser, M.A. Rueger, S.K. Bae, R. Kittappa, and R.D. McKay. 2006. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature. 442:823-826.
41. Bermejo-Rodriguez, C., M. Perez-Caro, P.A. Perez-Mancera, M. Sanchez-Beato, M.A. Piris, and I. Sanchez-Garcia. 2006. Mouse cDNA microarray analysis uncovers Slug targets in mouse embryonic fibroblasts. Genomics. 87:113-118.
42. Weng, Z., M. Xin, L. Pablo, D. Grueneberg, M. Hagel, G. Bain, T. Muller, and J. Papkoff. 2002. Protection against anoikis and down-regulation of cadherin expression by a regulatable beta-catenin protein. J. Biol. Chem. 277:18677-18686.
43. Conacci-Sorrell, M., I. Simcha, T. Ben-Yedidia, J. Blechman, P. Savagner, and A. Ben-Zéev. 2003. Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of β-catenin signaling, Slug, and MAPK. J. Cell Biol. 163:847-857.
44. Liu, S., G. Dontu, and M.S. Wicha. 2005. Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res. 7:86-95.
45. Stingl, J., C.J. Eaves, I. Zandieh, and J.T. Emerman. 2001. Characterization of bipotent mammary epithelial progenitor cells in normal adult human breast tissue. Breast Cancer Res. Treat. 67:93-109.
46. van't Veer, L.J., H. Dai, M.J. van de Vijver, Y.D. He, A.A. Hart, M. Mao, H.L. Peterse, K. van der Kooy, M.J. Marton, A.T. Witteveen, et al. 2002. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 415:530-536.
47. Zhao, H., A. Langerod, Y. Ji, K.W. Nowels, J.M. Nesland, R. Tibshirani, I.K. Bukholm, R. Karesen, D. Botstein, A.L. Borresen-Dale, and S.S. Jeffrey. 2004. Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol. Biol. Cell. 15:2523-2536.
48. Giordano, T.J., D.G. Thomas, R. Kuick, M. Lizyness, D.E. Misek, A.L. Smith, D. Sanders, R.T. Aljundi, P.G. Gauger, N.W. Thompson, et al. 2003. Distinct transcriptional profiles of adrenocortical tumors uncovered by DNA microarray analysis. Am. J. Pathol. 162:521-531.
49. Freije, W.A., F.E. Castro-Vargas, Z. Fang, S. Horvath, T. Cloughesy, L.M. Liau, P.S. Mischel, and S.F. Nelson. 2004. Gene expression profiling of gliomas strongly predicts survival. Cancer Res. 64:6503-6510.
50. Jain, S., M.A. Watson, M.K. DeBenedetti, Y. Hiraki, J.F. Moley, and J. Milbrandt. 2004. Expression profiles provide insights into early malignant potential and skeletal abnormalities in multiple endocrine neoplasia type 2B syndrome tumors. Cancer Res. 64:3907-3913.
51. Chen, X., S.Y. Leung, S.T. Yuen, K.M. Chu, J. Ji, R. Li, A.S. Chan, S. Law, O.G. Troyanskaya, J. Wong, et al. 2003. Variation in gene expression patterns in human gastric cancers. Mol. Biol. Cell. 14:3208-3215.
52. Garber, M.E., O.G. Troyanskaya, K. Schluens, S. Petersen, Z. Thaesler, M. Pacyna-Gengelbach, M. van de Rijn, G.D. Rosen, C.M. Perou, R.I. Whyte, et al. 2001. Diversity of gene expression in adenocarcinoma of the lung. Proc. Natl. Acad. Sci. USA. 98:13784-13789.
53. Schaner, M.E., D.T. Ross, G. Ciaravino, T. Sorlie, O. Troyanskaya, M. Diehn, Y.C. Wang, G.E. Duran, T.L. Sikic, S. Caldeira, et al. 2003. Gene expression patterns in ovarian carcinomas. Mol. Biol. Cell. 14:4376-4386.
54. Higgins, J.P., R. Shinghal, H. Gill, J.H. Reese, M. Terris, R.J. Cohen, M. Fero, J.R. Pollack, M. van de Rijn, and J.D. Brooks. 2003. Gene expression patterns in renal cell carcinoma assessed by complementary DNA microarray. Am. J. Pathol. 162:925-932.
55. Frierson, H.F., Jr., A.K. El-Naggar, J.B. Welsh, L.M. Sapinoso, A.I. Su, J. Cheng, T. Saku, C.A. Moskaluk, and G.M. Hampton. 2002. Large scale molecular analysis identifies genes with altered expression in salivary adenoid cystic carcinoma. Am. J. Pathol. 161:1315-1323.
56. Linn, S.C., R.B. West, J.R. Pollack, S. Zhu, T. Hernandez-Boussard, T.O. Nielsen, B.P. Rubin, R. Patel, J.R. Goldblum, D. Siegmund, et al. 2003. Gene expression patterns and gene copy number changes in dermatofibrosarcoma protuberans. Am. J. Pathol. 163:2383-2395.
57. Segal, N.H., P. Pavlidis, W.S. Noble, C.R. Antonescu, A. Viale, U.V. Wesley, K. Busam, H. Gallardo, D. DeSantis, M.F. Brennan, et al. 2003. Classification of clear-cell sarcoma as a subtype of melanoma by genomic profiling. J. Clin. Oncol. 21:1775-1781.