The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway

Nature Cell Biology

Volumn 8, Issue 8, 2006, Pages 815-825

  Noren, Nicole K ^a   Foos, Gabriele ^a   Hauser, Craig A ^a   Pasquale, Elena B ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; CRK LIKE PROTEIN; EPHRIN B2 FC FUSION PROTEIN; EPHRIN RECEPTOR B4; GELATINASE A; HYBRID PROTEIN; IMATINIB; MATRIX METALLOPROTEINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER CELL; CANCER INHIBITION; CANCER INVASION; CARCINOGENICITY; CELL MOTILITY; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENETIC TRANSFECTION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; IN VIVO STUDY; MOUSE; NONHUMAN; NUDE MOUSE; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR SPHEROID; TUMOR XENOGRAFT; ZYMOGRAPHY;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; EPHRIN-B2; FEMALE; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; MAMMARY NEOPLASMS, EXPERIMENTAL; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM TRANSPLANTATION; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-ABL; PROTO-ONCOGENE PROTEINS C-CRK; PYRIMIDINES; RECEPTOR, EPHB4; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 33746646032     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1438     Document Type: Article

References (50)

1. Batlle, E. et al. EphB receptor activity suppresses colorectal cancer progression. Nature 435, 1126-1130 (2005).
2. Jubb, A. M. et al. EphB2 is a prognostic factor in colorectal cancer. Clin. Cancer Res. 11, 5181-5187 (2005).
3. Guo, D. L. et al. Reduced expression of EphB2 that parallels invasion and metastasis in colorectal tumours. Carcinogenesis 27, 454-464 (2006).
4. Huusko, P. et al. Nonsense-mediated decay microarray analysis identifies mutations of EPHB2 in human prostate cancer. Nature Genet. 36, 979-983 (2004).
5. Pasquale, E. B. Eph receptor signalling casts a wide net on cell behaviour. Nature Rev. Mol. Cell Biol. 6, 462-475 (2005).
6. Noblitt, L. W. et al. Decreased tumorigenic potential of EphA2-overexpressing breast cancer cells following treatment with adenoviral vectors that express EphrinA1. Cancer Gene Ther. 11, 757-766 (2004).
7. Zelinski, D. P., Zantek, N. D., Stewart, J. C., Irizarry, A. R. & Kinch, M. S. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res. 61, 2301-2306 (2001).
8. Liu, W. et al. Effects of overexpression of ephrin-B2 on tumour growth in human colorectal cancer. Br. J. Cancer 90, 1620-1626 (2004).
9. Berclaz, G. et al. Expression of the receptor protein tyrosine kinase myk-1-htk in normal and malignant mammary epithelium. Biochem. Biophys. Res. Commun. 226, 869-875 (1996).
10. Liu, W. et al. Coexpression of ephrin-Bs and their receptors in colon carcinoma. Cancer 94, 934-939 (2002).
11. Wu, Q. et al. Expression of Ephb2 and Ephb4 in breast carcinoma. Pathol. Oncol. Res. 10, 26-33 (2004).
12. Xia, G. et al. Up-regulation of EphB4 in mesothelioma and its biological significance. Clin. Cancer Res. 11, 4305-4315 (2005).
13. Noren, N. K., Lu, M., Freeman, A. L., Koolpe, M. & Pasquale, E. B. Interplay between EphB4 on tumor cells and vascular ephrin-B2 regulates tumor growth. Proc. Natl Acad. Sci. USA 101, 5583-5588 (2004).
14. Nikolova, Z., Djonov, V., Zuercher, G., Andres, A. C. & Ziemiecki, A. Cell-type specific and estrogen dependent expression of the receptor tyrosine kinase EphB4 and its ligand ephrin-B2 during mammary gland morphogenesis. J. Cell Sci. 111, 2741-2751 (1998).
15. Sellappan, S. et al. Lineage infidelity of MDA-MB-435 cells: Expression of melanocyte proteins in a breast cancer cell line. Cancer Res. 64, 3479-3485 (2004).
16. Feller, S. M. Crk family adaptors-signalling complex formation and biological roles. Oncogene 20, 6348-6371 (2001).
17. Gorre, M. E. et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293, 876-880 (2001).
18. Chodniewicz, D. & Klemke, R. L. Regulation of integrin-mediated cellular responses through assembly of a CAS-Crk scaffold. Biochim. Biophys. Acta 1692, 63-76 (2004).
19. Spencer, K. S., Graus-Porta, D., Leng, J., Hynes, N. E. & Klemke, R. L. ErbB2 is necessary for induction of carcinoma cell invasion by ErbB family receptor tyrosine kinases. J. Cell Biol. 148, 385-397 (2000).
20. Kelm, J. M., Timmins, N. E., Brown, C. J., Fussenegger, M. & Nielsen, L. K. Method for generation of homogeneous multicellular tumor spheroids applicable to a wide variety of cell types. Biotechnol. Bioeng. 83, 173-180 (2003).
21. Duffy, M. J., Maguire, T. M., Hill, A., McDermott, E. & O'Higgins, N. Metalloproteinases: Role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res. 2, 252-257 (2000).
22. Koolpe, M., Burgess, R., Dail, M. & Pasquale, E. B. EphB receptor-binding peptides identified by phage display enable design of an antagonist with ephrin-like affinity. J. Biol. Chem. 280, 17301-17311 (2005).
23. Lamorte, L., Royal, I., Naujokas, M. & Park, M. Crk adapter proteins promote an epithelial-mesenchymal-like transition and are required for HGF-mediated cell spreading and breakdown of epithelial adherens junctions. Mol. Biol. Cell 13, 1449-1461 (2002).
24. Kain, K. H. & Klemke, R. L. Inhibition of cell migration by Abl family tyrosine kinases through uncoupling of Crk-CAS complexes. J. Biol. Chem. 276, 16185-16192 (2001).
25. Kain, K. H., Gooch, S. & Klemke, R. L. Cytoplasmic c-Abl provides a molecular 'Rheostat' controlling carcinoma cell survival and invasion. Oncogene 22, 6071-6080 (2003).
26. Frasca, F., Vigneri, P., Vella, V., Vigneri, R. & Wang, J. Y. Tyrosine kinase inhibitor STI571 enhances thyroid cancer cell motile response to hepatocyte growth factor. Oncogene 20, 3845-3856 (2001).
27. Woodring, P. J., Hunter, T. & Wang, J. Y. Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases. J. Cell Sci. 116, 2613-2626 (2003).
28. Truong, T., Sun, G., Doorly, M., Wang, J. Y. & Schwartz, M. A. Modulation of DNA damage-induced apoptosis by cell adhesion is independently mediated by p53 and c-Abl. Proc. Natl Acad. Sci. U S A 100, 10281-10286 (2003).
29. Harbott, L. K. & Nobes, C. D. A key role for Abl family kinases in EphA receptor-mediated growth cone collapse. Mol. Cell. Neurosci. 30, 1-11 (2005).
30. Plattner, R., Kadlec, L., DeMali, K. A., Kazlauskas, A. & Pendergast, A. M. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev. 13, 2400-2411 (1999).
31. Furstoss, O. et al. c-Abl is an effector of Src for growth factor-induced c-myc expression and DNA synthesis. EMBO J. 21, 514-524 (2002).
32. Zukerberg, L. R. et al. Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 26, 633-646 (2000).
33. Moresco, E. M., Donaldson, S., Williamson, A. & Koleske, A. J. Integrin-mediated dendrite branch maintenance requires Abelson (Abl) family kinases. J. Neurosci. 25, 6105-6118 (2005).
34. Yu, H. H., Zisch, A. H., Dodelet, V. C. & Pasquale, E. B. Multiple signaling interactions of Abl and Arg kinases with the EphB2 receptor. Oncogene 20, 3995-4006 (2001).
35. Zou, X. & Calame, K. Signaling pathways activated by oncogenic forms of Abl tyrosine kinase. J. Biol. Chem. 274, 18141-18144 (1999).
36. Hantschel, O. & Superti-Furga, G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nature Rev. Mol. Cell Biol. 5, 33-44 (2004).
37. Plattner, R. & Pendergast, A. M. Activation and signaling of the Abl tyrosine kinase: Bidirectional link with phosphoinositide signaling. Cell Cycle 2, 273-274 (2003).
38. Sini, P., Cannas, A., Koleske, A. J., Di Fiore, P. P. & Scita, G. Abl-dependent tyrosine phosphorylation of Sos-1 mediates growth-factor-induced Rac activation. Nature Cell Biol. 6, 268-274 (2004).
39. Takino, T. et al. Tyrosine phosphorylation of the CrkII adaptor protein modulates cell migration. J. Cell Sci. 116, 3145-3155 (2003).
40. Shin, I., Kim, S., Song, H., Kim, H. R. & Moon, A. H-Ras-specific activation of Rac-MKK3/6-p38 pathway: Its critical role in invasion and migration of breast epithelial cells. J. Biol. Chem. 280, 14675-14683 (2005).
41. Yang, C., Liu, Y., Leskow, F. C., Weaver, V. M. & Kazanietz, M. G. Rac-GAP-dependent inhibition of breast cancer cell proliferation by β2-chimerin. J. Biol. Chem. 280, 24363-24370 (2005).
42. Depaepe, V. et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 435, 1244-1250 (2005).
43. Miao, H. et al. Activation of EphA receptor tyrosine kinase inhibits the Ras-MAPK pathway. Nature Cell Biol. 3, 527-530 (2001).
44. Dohn, M., Jiang, J. Y. & Chen, X. B. Receptor tyrosine kinase EphA2 is regulated by p53-family proteins and induces apoptosis. Oncogene 20, 6503-6515 (2001).
45. Lawrenson, I. D. et al. Ephrin-A5 induces rounding, blebbing and de-adhesion of EphA3-expressing 293T and melanoma cells by CrkII and Rho-mediated signalling. J. Cell Sci. 115, 1059-1072 (2002).
46. Nagashima, K. et al. Adaptor protein Crk is required for ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells. Mol. Biol. Cell 13, 4231-4242 (2002).
47. Barrios, A. et al. Eph/Ephrin signaling regulates the mesenchymal-to-epithelial transition of the paraxial mesoderm during somite morphogenesis. Curr. Biol. 13, 1571-82 (2003).
48. Miao, H. et al. EphA kinase activation regulates HGF-induced epithelial branching morphogenesis. J. Cell Biol. 162, 1281-1292 (2003).
49. Xia, G. et al. EphB4 expression and biological significance in prostate cancer. Cancer Res. 65, 4623-4632 (2005).
50. Druker, B. J. et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nature Med. 2, 561-566 (1996).