N-cadherin signaling potentiates mammary tumor metastasis via enhanced extracellular signal-regulated kinase activation

Cancer Research

Volumn 67, Issue 7, 2007, Pages 3106-3116

  Hulit, James ^a   Suyama, Kimita ^a   Chung, Su ^a   Keren, Rinat ^a   Agiostratidou, Georgia ^a   Shan, Weisong ^b   Dong, Xinyuan ^a   Williams, Terence M ^c   Lisanti, Michael P ^c   Knudsen, Karen ^d   Hazan, Rachel B ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE; NERVE CELL ADHESION MOLECULE; CADHERIN; VIRUS T ANTIGEN;

ANIMAL EXPERIMENT; ARTICLE; BREAST EPITHELIUM; BREAST TUMOR; CONTROLLED STUDY; GENE EXPRESSION; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; BIOSYNTHESIS; CELL MOTION; DRUG ANTAGONISM; ENZYME ACTIVATION; ENZYMOLOGY; EXPERIMENTAL NEOPLASM; FEMALE; GENETICS; LUNG TUMOR; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; UPREGULATION;

ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; LUNG NEOPLASMS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MATRIX METALLOPROTEINASE 9; MICE; PHOSPHORYLATION; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 34248148453     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-3401     Document Type: Article

References (40)

1. Cavallaro U, Christofbri G. Multitasking in tumor progression: signaling functions of cell adhesion molecules. Ann N Y Acad Sci 2004;1014:58-66.
2. Hazan RB, Qiao R, Keren R, Badano I, Suyama K. Cadherin switch in tumor progression. Ann N Y Acad Sci 2004;1014:155-63.
3. Cavallaro U, Schaffhauser B, Christofori G. Cadherins and the tumour progression: is it all in a switch? Cancer Lett 2002;176:123-8.
4. Knudsen KA, Wheelock MJ. Cadherins and the mammary gland. J Cell Biochem 2005:95:488-96.
5. Nagi C, Guttman M, Jaffer S, et al. N-cadherin expression in breast cancer: correlation with an aggressive histologic variant-invasive micropapillary carcinoma Breast Cancer Res Treat 2005:94:225-35.
6. Birchmeier W, Behrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim Biophys Acta 1994;1198:11-26.
7. Islam S, Carey TE, Wolf GT, Wheelock MJ, Johnson KR. Expression of N-cadherin by human squamous carcinoma cells induces a scattered fibroblastic phenotype with disrupted cell-cell adhesion. J Cell Biol 1996;135:1643-54.
8. Nieman MT, Prudoff RS, Johnson KR, Wheelock MJ. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J Cell Biol 1999;147:631-44.
9. Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 2000;148:779-90.
10. Kim JB, Islam S, Kim YJ, et al. N-Cadherin extracellular repeat 4 mediates epithelial to mesenchymal transition and increased motility. J Cell Biol 2000;151:1193-206.
11. Suyama K, Shapiro I, Guttman M, Hazan RB. A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2002;2:301-14.
12. Hazan RB, Kang L, Whooley BP, Borgen PI. N-cadherin promotes adhesion between invasive breast cancer cells and the stroma. Cell Adhes Commun 1997;4:399-411.
13. Tran NL, Nagle RB, Cress AE, Heimark RL. N-Cadherin expression in human prostate carcinoma cell lines. An epithelial-mesenchymal transformation mediating adhesion with stromal cells. Am J Pathol 1999;155:787-98.
14. Qi J, Chen N, Wang J, Siu CH. Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the β-catenin signaling pathway. Mol Biol Cell 2005;16:4386-97.
15. Dilworth SM. Polyoma virus middle T antigen and its role in identifying cancer-related molecules. Nat Rev Cancer 2002;2:951-6.
16. Lin EY, Jones JG, Li P, et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 2003;163:2113-26.
17. Hutchinson JN, Muller WJ. Transgenic mouse models of human breast cancer. Oncogene 2000:19:130-7.
18. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;12:954-61.
19. Maglione JE, Moghanaki D, Young LJ, et al. Transgenic polyoma middle-T mice model premalignant mammary disease. Cancer Res 2001;61:8298-305.
20. Knudsen KA, Sauer C, Johnson KR, Wheelock MJ. Effect of N-cadherin misexpression by the mammary epithelium in mice. J Cell Biochem 2005;95:1093-107.
21. Bozdagi O, Shan W, Tanaka H, Benson DL, Huntley GW. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 2000;28:245-59.
22. Borowsky AD, Namba R, Young LJ, et al. Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior. Clin Exp Metastasis 2005;22:47-59.
23. Muraoka-Cook RS, Kurokawa H, Koh Y, et al. Conditional overexpression of active transforming growth factor β1 in vivo accelerates metastases of transgenic mammary tumors. Cancer Res 2004;64:9002-11.
24. Albini A, Iwamoto Y, Heinman HK, et al. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987;47:3239-45.
25. Dunant N, Ballmer-Hofer K. Signalling by Src family kinases: lessons learnt from DNA tumour viruses. Cell Signal 1997;9:385-93.
26. Westermarck J, Kahari VM. Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J 1999;13:781-92.
27. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006;25:9-34.
28. Hiratsuka S, Nakamura K, Iwai S, et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2002;2:289-300.
29. Olson MW, Bernardo MM, Pietila M, et al. Characterization of the monomeric and dimeric forms of latent and active matrix metalloproteinase-9. Differential rates for activation by stromelysin 1. J Biol Chem 2000;275:2661-8.
30. Mohammadi M, Froum S, Hamby JM, et al. Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J 1998;17:5896-904.
31. Koziczak M, Holbro T, Hynes NE. Blocking of FGFR signaling inhibits breast cancer cell proliferation through downregulation of D-type cyclins. Oncogene 2004;23:3501-8.
32. Hatta K, Takagi S, Fujisawa H, Takeichi M. Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev Biol 1987;120:215-27.
33. Hatta K, Takeichi M. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 1986;320:447-9.
34. Alexander NR, Tran NL, Rekapally H, et al. N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1. Cancer Res 2006;66:3365-9.
35. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995;80:179-85.
36. Schaeffer HJ, Weber MJ. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol 1999;19:2435-44.
37. Cuevas BD, Winter-Vann AM, Johnson NL, Johnson GL. MEKK1 controls matrix degradation and tumor cell dissemination during metastasis of polyoma middle-T driven mammary cancer. Oncogene 2006;25:4998-5010.
38. McCawley LJ, Li S, Wattenberg EV, Hudson LG. Sustained activation of the mitogen-activated protein kinase pathway. A mechanism underlying receptor tyrosine kinase specificity for matrix metalloproteinase-9 induction and cell migration. J Biol Chem 1999;274:4347-53.
39. Murphy LO, MacKeigan JP, Blenis J. A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration. Mol Cell Biol 2004;24:144-53.
40. Sternlicht MD, Lochter A, Sympson CJ, et al. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 1999;98:137-46.