The C-terminus of ephrin-B1 regulates metalloproteinase secretion and invasion of cancer cells

Journal of Cell Science

Volumn 120, Issue 13, 2007, Pages 2179-2189

  Tanaka, Masamitsu ^a   Sasaki, Kazuki ^a,b   Kamata, Reiko ^a   Sakai, Ryuichi ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

Eph; Ephrin; Metalloproteinase; Secretion

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; EPHRIN B1; EPHRIN RECEPTOR B2; GUANOSINE TRIPHOSPHATASE; METALLOPROTEINASE; NEUTROPHIL COLLAGENASE;

ANIMAL CELL; ARTICLE; CANCER CELL; CANCER INVASION; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EXOCYTOSIS; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HYPOTHESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTOR 1; ENZYME ACTIVATION; EPHRIN-B1; EXOCYTOSIS; GENE EXPRESSION REGULATION, NEOPLASTIC; GUANOSINE TRIPHOSPHATE; HUMANS; MATRIX METALLOPROTEINASE 8; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; U937 CELLS;

EID: 34447538273     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.008607     Document Type: Article

References (50)

1. Akedo, H., Shinkai, K., Mukai, M., Mori, Y., Tateishi, R., Tanaka, K., Yamamoto, R. and Morishita, T. (1986). Interaction of rat ascites hepatoma cells with cultured mesothelial cell layers: a model for tumor invasion. Cancer Res. 46, 2416-2422.
2. Amour, A., Knight, C. G., Webster, A., Slocombe, M., Stephens, P. E., Knauper, V., Docherty A. J. F. and Murphy, G. (2000). The in vitro activity of ADAM-10 is inhibited by TIMP-1 and TIMP-3. FEBS Lett. 473, 275-279.
3. Batlle, E., Henderson, J. T., Beghtel, H., Van den Born, M., Sancho, E., Huls, G., Meeldijk, J., Robertson, J., Van de Wetering, M., Pawson, T. et al. (2002). Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111, 251-263.
4. Batlle, E., Bacani, J., Begthel, H., Jonkheer, S., Gregorieff, A., Van den Born, M., Malats, N., Sancho, E., Boon, E., Pawson, T. et al. (2005). EphB receptor activity suppresses colorectal cancer progression. Nature 435, 1126-1130.
5. Blits-Huizinga, C., Nelersa, C., Malhotra, A. and Liebl, D. (2004). Ephrins and their receptors: binding versus biology. IUBMB Life 56, 257-265.
6. Bong, Y. S., Park, Y. H., Lee, H. S., Mood, K., Ishimura, A. and Daar, I. O. (2004). Tyr-298 in ephrin-B1 is critical for an interaction with the Grb4 adaptor protein. Biochem. J. 377, 499-507.
7. Brew, K., Dinakarpandian, D. and Nagase, H. (2000). Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochem. Biophys. Acta 1477, 267-283.
8. Castellvi, J., Garcia, A., De la Torre, J., Hernandez, J., Gil, A., Xercavins, J. and Cajal, S. R. (2006). EphrinB expression in epithelial ovarian neoplasms correlates with tumor differentiation and angiogenesis. Hum. Pathol. 37, 883-889.
9. Chinni, S. R., Sivalogan, S., Dong, Z., Trindade Filho, J. C., Deng, X., Bonfil, R. D. and Cher, M. L. (2006). CXCL12/CXCR4 signaling activates Akt-1 and MMP-9 expression in prostate cancer cells: the role of Bone microenvironment-associated CXCL12. Prostate 66, 32-48.
10. Cowan, C. A. and Henkemeyer, M. (2001). The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413, 174-179.
11. Dell'Angelica, E. C., Puertollano, R., Mullins, C., Aguilar, R. C., Vargas, J.D., Hartnell, L. M. and Bonifacino, J.S. (2000). GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J. Cell Biol. 149, 81-93.
12. Donaldson, J. G. (2005). Arfs, phosphoinositides and membrane traffic. Biochem. Soc. Trans. 33, 1276-1278.
13. Georgakopoulos, A., Litterst, C., Ghersi, E., Baki, L., Xu, C. J., Serban, G. and Robakis, N. K. (2006). Metalloproteinase/Presenilin1 processing of ephrinB regulates EphB-induced Src phosphorylation and signaling. EMBO J. 25, 1242-1252.
14. Hashimoto, G., Aoki, T., Nakamura, H., Tanzawa, K. and Okada, Y. (2001). Inhibition of ADAMTS4 (aggrecanase-1) by tissue inhibitors of metalloproteinases (TIMP-1, 2, 3 and 4). FEBS Lett. 494, 192-195.
15. Hattori, M., Osterfield, M. and Flanagan, J. G. (2000). Regulated cleavage of a contact-mediated axon repellent. Science 289, 1360-1365.
16. Holmberg, J., Genander, M., Halford, M. M., Anneren, C., Sondell, M., Chumley, M. J., Silvany, R. E., Henkemeyer, M. and Frisen, J. (2006). EphB receptors coordinate migration and proliferation in the intestinal stem cell niche. Cell 125, 1151-1263.
17. Huynh-Do, U., Vindis, C., Liu, H., Cerretti, D. P., NcGrew, J. T., Enriquez, M., Chen, J. and Daniel, T. O. (2002). Ephrin-B1 transduces signals to active integrin-mediated migration, attachment and angiogenesis. J. Cell Sci. 115, 3073-3081.
18. Janes, F. W., Saha, N., Barton, W. A., Kolev, M. V., Wimmer-Kleikamp, S. H., Nievergall, E., Blobel, C. P., Himanen, J. P., Lackmann, M. and Nikolov, D. B. (2005). Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 123, 291-304.
19. Kataoka, H., Tanaka, M., Kanamori, M., Yoshii, S., Ihara, M., Wang, Y. J., Song, J. P., Li, Z. Y., Arai, H., Otuki, Y. et al. (2002). Expression profile of EFNB1, EFNB2, two ligands of EPHB2 in human gastric cancer. J. Cancer Res. Clin. Oncol. 128, 343-348.
20. Kawano, K., Iwamura, T., Yamarari, H., Seo, Y., Suganuma, T. and Chijiiwa, K. (2004). Establishment and characterization of a novel human pancreatic cancer cell line (SUIT-4) metastasizing to lymph nodes and lungs in nude mice. Oncology 66, 458-467.
21. Klein, R. (2004). Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr. Opin. Cell Biol. 16, 580-589.
22. Lee, H. S., Bong, Y. S., Moore, K. B., Soria, K., Moody, S. A. and Daar, I. O. (2005). Dishevelled mediates ephrinB1 signalling in the eye field through the planar cell polarity pathway. Nat. Cell Biol. 8, 55-63.
23. Lin, D., Gish, G. D., Songyang, Z. and Powson, T. (1999). The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J. Biol. Chem. 274, 3726-3733.
24. Lint, F. V. and Libert, C. (2006). Matrix metalloproteinase-8: cleavage can be decisive. Cytokine Growth Factor Rev. 17, 217-223.
25. Marston, D. J., Dickinson, S. and Nobes, C. D. (2003). Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat. Cell Biol. 5, 879-888.
26. Meyer, S., Hafner, C., Guba, M., Flegel, S., Geissler, E. K., Becker, B., Koehl, G., Orso, E., Landthaler, M. and Vogt, T. (2005). Ephrin-B2 overexpression enhances integrin-mediated ECM-attachment and migration of B16 melanoma cells. Int. J. Oncol. 27, 1197-1206.
27. Murai, K. K. and Pasquale, E. B. (2003). Ephective signaling: forward, reverse and crosstalk. J. Cell Sci. 116, 2823-2832.
28. Nakada, M., Drake, K. L., Nakada, S., Niska, J. A. and Berens, M. E. (2006). Ephrin-B3 ligand promotes glioma invasion through activation of Rac1. Cancer Res. 66, 8492-8500.
29. Niu, T. K., Pfeifer, A. C., Lippincott-Schwartz, J. and Jackson, C. L. (2005). Dynamics of GBF1, a Brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol. Biol. Cell 16, 1213-1222.
30. Parker, M., Roberts, R., Enriquez, M., Zhao, X., Takahashi, T., Pat, C., Daniel, T. and Chen, J. (2004). Reverse endocytosis of transmembrane ephrin-B ligands via a clathrin-mediated pathway. Biochem. Biophys. Res. Commun. 323, 17-23.
31. Pascall, J. C. and Brown, K. D. (2004). Intramembrane cleavage of ephrinB3 by the human rhomboid family protease, RHBDL2. Biochem. Biophys. Res. Commun. 317, 244-252.
32. Poliakov, A., Cotrina, M. and Wilkinson, D. G. (2004). Diverse roles of Eph receptors end ephrins in the regulation of cell migration and tissue assembly. Dev. Cell 7, 465-480.
33. Raymond, L., Eck, S., Mollmark, J., Hays, E., Tomek, I., Kantor, S., Elliott, S. and Vincenti, M. (2006). Interleukin-1 beta induction of matrix metalloproteinase-1 transcription in chondrocytes requires ERK-dependent activation of CCAAT enhancer-binding protein-beta. J. Cell. Physiol. 207, 683-688.
34. Reuben, P. M. and Cheung, H. S. (2006). Regulation of matrix metalloproteinase (MMP) gene expression by protein kinases. Front. Biosci. 11, 1199-1215.
35. Sasaki, K., Sato, K., Akiyama, Y., Yanagihara, K., Oka, M. and Yamaguchi, K. (2002). Peptidomics-based approach reveals the secretion of the 29-residue COOH-terminal fragment of the putative tumor suppressor protein DMBT1 from pancreatic adenocarcinoma cell lines. Cancer Res. 62, 4894-4898.
36. Sawicki, G., Leon, H., Sawicka, J., Sariahmetoglu, M., Schulze, C. J., Scott, P. G., Szczesna-Cordary, D. and Schulz, R. (2005). Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury. Circulation 112, 544-552.
37. Siller-Lopez, F., Garcia-Banuelos, J., Hasty, K. A., Segura, J., Ramos-Marquez, M., Qoronfleh, M. W., Aguilar-Cordova, E. and Armendariz-Borunda, J. (2000). Truncated active matrix metalloproteinase-8 gene expression in HepG2 cells is active against native type 1 collagen. J. Hepatol. 33, 758-763.
38. Stadlemann, S., Pollheimer, J., Moser, P. L., Raggi, A., Amberger, A., Margreiter, R., Offner, F. A., Mikuz, G., Dirnhofer, S. and Moch, H. (2003). Cytokine-regulated expression of collagenase-2 (MMP-8) is involved in the progression of ovarian cancer. Eur. J. Cancer 39, 2499-2505.
39. Sternlicht, M. D. and Werb, Z. (2001). How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17, 463-516.
40. Tamaki, H. and Yamashina, S. (2002). The stack of the Golgi apparatus. Arch. Histol. Cytol. 65, 209-218.
41. Tanaka, M., Kamo, T., Ota, S. and Sugimura, H. (2003). Association of dishevelled with Eph tyrosine kinase receptor and epbrin mediates cell repulsion. EMBO J. 22, 947-858.
42. Tanaka, M., Ohashi, R., Nakamura, R., Shinmura, K., Kamo, T., Sakai, R. and Sugimura, H. (2004). Tiam1 mediates neurite outgrowth induced by ephrin-B1 and EphA2. EMBO J. 23, 1075-1088.
43. Tanaka, M., Kamata, R. and Sakai, R. (2005). Phosphorylation of ephrin-B1 via the interaction with claudin following cell-cell contact formation. EMBO J. 24, 3700-3711.
44. Tomita, T., Tanaka, S., Morohashi, Y. and Iwatsubo, T. (2006). Presenilin-dependent intramembrane cleavage of ephrin-B1. Mol. Neurodegener. 1, 2.
45. Varelias, A., Koblar, S. A., Cowled, P. A., Carter, C. D. and Clayer, M. (2002). Human osteosarcoma express specific ephrin profiles: implications for tumorigenicity and prognosis. Cancer 95, 862-869.
46. Wahlgren, J., Maisi, P., Sorsa, T., Sutinen, M., Tervahartiala, T., Pirila, E., Teronen, O., Hietanen, J., Tjaderhane, L. and Salo, T. (2001). Expression and induction of collagenases (MMP-8 and -13) in plasma cells and associated with bone-destructive lesions. J. Pathol. 194, 217-224.
47. Woo, J. H., Park, J. W., Lee, S. H., Kim, Y. H., Lee, I. K., Gabrielson, E., Lee, S. H., Lee, H. J., Kho, Y. H. and Won, T. K. (2003). Dykellic acid inhibits phorbol myristate acetate-induced matrix metalloproteinase-9 expression by inhibiting nuclear factor kappa B transcriptional activity. Cancer Res. 63, 3430-3434.
48. Yu, W. H., Eoessner, J. F., McNeish, J. D. and Stamenkovic, I. (2007). CD44 anchors the assembly of matrilysin/MMP-7 with heparin-binding epidermal growth factor precursor and ErbB4 and regulates female reproductive organ remodeling. Genes Dev. 16, 307-323.
49. Zeeh, J. C., Zeghouf, M., Grauffel, C., Guilbert, B., Martin, E., Dejaegere, A. and Cherfils, J. (2006). Dual specificity of the interfacial inhibitor Brefeldin A for Arf proteins and Sec7 domains. J. Biol. Chem. 281, 11805-11814.
50. Zimmer, M., Palmer, A., Kohler, J. and Klein, R. (2003). EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat. Cell Biol. 5, 869-878.