Calpain 2 and PTP1B function in a novel pathway with Src to regulate invadopodia dynamics and breast cancer cell invasion

Journal of Cell Biology

Volumn 180, Issue 5, 2008, Pages 957-971

  Cortesio, Christa L ^a,b   Chan, Keefe T ^a,b   Perrin, Benjamin J ^a,b   Burton, Nicholas O ^a,b   Zhang, Sheng ^c   Zhang, Zhong Yin ^c   Huttenlocher, Anna ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN 2; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 1B; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER CELL; CELL INVASION; CELL MOTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

BREAST NEOPLASMS; CALPAIN; CARCINOMA; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MUTATION; NEOPLASM INVASIVENESS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PSEUDOPODIA; SIGNAL TRANSDUCTION;

EID: 40849120593     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200708048     Document Type: Article

References (50)

1. Arregui, C.O., J. Balsamo, and J. Lilien. 1998. Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J. Cell Biol. 143:861-873.
2. Artym, V.V., Y. Zhang, F. Seillier-Moiseiwitsch, K.M. Yamada, and S.C. Mueller. 2006. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 66:3034-3043.
3. Bentires-Alj, M., and B.G. Neel. 2007. Protein-tyrosine phosphatase 1B is required for HER2/Neu-induced breast cancer. Cancer Res. 67:2420-2424.
4. Bhatt, A.K., and A. Huttenlocher. 2003. Dynamic imaging of cell-substrate contacts. Methods Enzymol. 361:337-352.
5. Bjorge, J.D., A. Pang, and D.J. Fujita. 2000. Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J. Biol. Chem. 275:41439-41446.
6. Buccione, R., J.D. Orth, and M.A. McNiven. 2004. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5:647-657.
7. Calle, Y., H.C. Chou, A.J. Thrasher, and G.E. Jones. 2004. Wiskott-Aldrich syndrome protein and the cytoskeletal dynamics of dendritic cells. J. Pathol. 204:460-469.
8. Calle, Y., N.O. Carragher, A.J. Thrasher, and G.E. Jones. 2006. Inhibition of calpain stabilises podosomes and impairs dendritic cell motility. J. Cell Sci. 119:2375-2385.
9. Carragher, N.O., M.A. Westhoff, D. Riley, D.A. Potter, P. Dutt, J.S. Elce, P.A. Greer, and M.C. Frame. 2002. v-Src-induced modulation of the calpain-calpastatin proteolytic system regulates transformation. Mol. Cell. Biol. 22:257-269.
10. Carragher, N.O., B.D. Fonseca, and M.C. Frame. 2004. Calpain activity is generally elevated during transformation but has oncogene-specific biological functions. Neoplasia. 6:53-73.
11. Carragher, N.O., S.M. Walker, L.A. Scott Carragher, F. Harris, T.K. Sawyer, V.G. Brunton, B.W. Ozanne, and M.C. Frame. 2006. Calpain 2 and Src dependence distinguishes mesenchymal and amoeboid modes of tumour cell invasion: a link to integrin function. Oncogene. 25:5726-5740.
12. Chang, B.Y., K.B. Conroy, E.M. Machleder, and C.A. Cartwright. 1998. RACK1, a receptor for activated C kinase and a homolog of the beta subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol. Cell. Biol. 18:3245-3256.
13. Chen, W.T. 1989. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J. Exp. Zool. 251:167-185.
14. Clark, E.S., A.S. Whigham, W.G. Yarbrough, and A.M. Weaver. 2007. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67:4227-4235.
15. Cortesio, C.L., and W. Jiang. 2006. Mannan-binding lectin-associated serine protease 3 cleaves synthetic peptides and insulin-like growth factor-binding protein 5. Arch. Biochem. Biophys. 449:164-170.
16. Ezumi, Y., H. Takayama, and M. Okuma. 1995. Differential regulation of protein-tyrosine phosphatases by integrin alpha IIb beta 3 through cytoskeletal reorganization and tyrosine phosphorylation in human platelets. J. Biol. Chem. 270:11927-11934.
17. Franco, S.J., and A. Huttenlocher. 2005. Regulating cell migration: calpains make the cut. J. Cell Sci. 118:3829-3838.
18. Franco, S., B. Perrin, and A. Huttenlocher. 2004a. Isoform specific function of calpain 2 in regulating membrane protrusion. Exp. Cell Res. 299:179-187.
19. Franco, S.J., M.A. Rodgers, B.J. Perrin, J. Han, D.A. Bennin, D.R. Critchley, and A. Huttenlocher. 2004b. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell Biol. 6:977-983.
20. Frangioni, J.V., A. Oda, M. Smith, E.W. Salzman, and B.G. Neel. 1993. Calpain-catalyzed cleavage and subcellular relocation of protein phosphotyrosine phosphatase 1B (PTP-1B) in human platelets. EMBO J. 12:4843-4856.
21. Gimona, M., and R. Buccione. 2006. Adhesions that mediate invasion. Int. J. Biochem. Cell Biol. 38:1875-1892.
22. Glading, A., D.A. Lauffenburger, and A. Wells. 2002. Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol. 12:46-54.
23. Hernandez, M.V., M.G. Sala, J. Balsamo, J. Lilien, and C.O. Arregui. 2006. ER-bound PTP1B is targeted to newly forming cell-matrix adhesions. J. Cell Sci. 119:1233-1243.
24. Huttenlocher, A., S.P. Palecek, Q. Lu, W. Zhang, R.L. Mellgren, D.A. Lauffenburger, M.H. Ginsberg, and A.F. Horwitz. 1997. Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 272:32719-32722.
25. Julien, S.G., N. Dube, M. Read, J. Penney, M. Paquet, Y. Han, B.P. Kennedy, W.J. Muller, and M.L. Tremblay. 2007. Protein tyrosine phosphatase 1B deficiency or inhibition delays ErbB2-induced mammary tumorigenesis and protects from lung metastasis. Nat. Genet. 39:338-346.
26. Kuchay, S.M., N. Kim, E.A. Grunz, W.P. Fay, and A.H. Chishti. 2007. Double knockouts reveal that protein tyrosine phosphatase 1B is a physiological target of calpain-1 in platelets. Mol. Cell. Biol. 27:6038-6052.
27. Liang, F., S.Y. Lee, J. Liang, D.S. Lawrence, and Z.Y. Zhang. 2005. The role of protein-tyrosine phosphatase 1B in integrin signaling. J. Biol. Chem. 280:24857-24863.
28. Libertini, S.J., B.S. Robinson, N.K. Dhillon, D. Glick, M. George, S. Dandekar, J.P. Gregg, E. Sawai, and M. Mudryj. 2005. Cyclin E both regulates and is regulated by calpain 2, a protease associated with metastatic breast cancer phenotype. Cancer Res. 65:10700-10708.
29. Linder, S. 2007. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17:107-117.
30. Linder, S., and M. Aepfelbacher. 2003. Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 13:376-385.
31. Luxenburg, C., L. Addadi, and B. Geiger. 2006. The molecular dynamics of osteoclast adhesions. Eur. J. Cell Biol. 85:203-211.
32. Marzia, M., R. Chiusaroli, L. Neff, N.Y. Kim, A.H. Chishti, R. Baron, and W.C. Horne. 2006. Calpain is required for normal osteoclast function and is down-regulated by calcitonin. J. Biol. Chem. 281:9745-9754.
33. Mamoune, A., J.H. Luo, D.A. Lauffenburger, and A. Wells. 2003. Calpain-2 as a target for limiting prostate cancer invasion. Cancer Res. 63:4632-4640.
34. Nuzzi, P.A., M.A. Senetar, and A. Huttenlocher. 2007. Asymmetric localization of calpain 2 during neutrophil chemotaxis. Mol. Biol. Cell. 18:795-805.
35. Perrin, B.J., K.J. Amann, and A. Huttenlocher. 2006. Proteolysis of cortactin by calpain regulates membrane protrusion during cell migration. Mol. Biol. Cell. 17:239-250.
36. Peters, G.H., S. Branner, K.B. Moller, J.N. Andersen, and N.P. Moller. 2003. Enzyme kinetic characterization of protein tyrosine phosphatases. Biochimie. 85:527-534.
37. Ruoslahti, E., E.G. Hayman, M. Pierschbacher, and E. Engvall. 1982. Fibronectin: purification, immunochemical properties, and biological activities. Methods Enzymol. 82 Pt A:803-831.
38. Segall, J.E., S. Tyerech, L. Boselli, S. Masseling, J. Helft, A. Chan, J. Jones, and J. Condeelis. 1996. EGF stimulates lamellipod extension in metastatic mammary adenocarcinoma cells by an actin-dependent mechanism. Clin. Exp. Metastasis. 14:61-72.
39. Spinardi, L., and P.C. Marchisio. 2006. Podosomes as smart regulators of cellular adhesion. Eur. J. Cell Biol. 85:191-194.
40. Su, Y., Z. Cui, Z. Li, and E.R. Block. 2006. Calpain-2 regulation of VEGF-mediated angiogenesis. FASEB J. 20:1443-1451.
41. Tarone, G., D. Cirillo, F.G. Giancotti, P.M. Comoglio, and P.C. Marchisio. 1985. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp. Cell Res. 159:141-157.
42. Tatin, F., C. Varon, E. Genot, and V. Moreau. 2006. A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J. Cell Sci. 119:769-781.
43. Tonks, N.K., and S.K. Muthuswamy. 2007. A brake becomes an accelerator: PTP1B-a new therapeutic target for breast cancer. Cancer Cell. 11:214-216.
44. Webb, D.J., K. Donais, L.A. Whitmore, S.M. Thomas, C.E. Turner, J.T. Parsons, and A.F. Horwitz. 2004. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6:154-161.
45. Webb, B.A., L. Jia, R. Eves, and A.S. Mak. 2007. Dissecting the functional domain requirements of cortactin in invadopodia formation. Eur. J. Cell Biol. 86:189-206.
46. Wiener, J.R., B.J. Kerns, E.L. Harvey, M.R. Conaway, J.D. Iglehart, A. Berchuck, and R.C. Bast Jr. 1994. Overexpression of the protein tyrosine phosphatase PTP1B in human breast cancer: association with p185c-erbB-2 protein expression. J. Natl. Cancer Inst. 86:372-378.
47. Xie, L., S.Y. L ee, J.N. Andersen, S. Waters, K. Shen, X.L. Guo, N.P. Moller, J.M. Olefsky, D.S. Lawrence, and Z.Y. Zhang. 2003. Cellular effects of small molecule PTP1B inhibitors on insulin signaling. Biochemistry. 42:12792-12804.
48. Yamaguchi, H., and J. Condeelis. 2007. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta. 1773:642-652.
49. Yamaguchi, H., M. Lorenz, S. Kempiak, C. Sarmiento, S. Coniglio, M. Symons, J. Segall, R. Eddy, H. Miki, T. Takenawa, and J. Condeelis. 2005. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168:441-452.
50. Zamir, E., B.Z. Katz, S. Aota, K.M. Yamada, B. Geiger, and Z. Kam. 1999. Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112:1655-1669.