Nck adaptor proteins link Tks5 to invadopodia actin regulation and ECM degradation

Journal of Cell Science

Volumn 122, Issue 15, 2009, Pages 2727-2740

  Stylli, Stanley S ^a   Stacey, T T I ^a   Verhagen, Anne M ^b   Xu, San San ^a   Pass, Ian ^c   Courtneidge, Sara A ^c   Lock, Peter ^a,d  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c BURNHAM INSTITUTE   (United States)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

ECM degradation; Invadopodia; Nck; Podosome; Src; Tks5

Indexed keywords

ADAPTOR PROTEIN; F ACTIN; MUTANT PROTEIN; NCK PROTEIN; NCK1 PROTEIN; NCK2 PROTEIN; PROTEIN SH2; PROTEIN SH3; PROTEIN TKS5; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER INVASION; CELL ACTIVITY; CELL STRUCTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INVADOPODIA; MEMBRANE COMPONENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CELL SURFACE EXTENSIONS; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOPRECIPITATION; MICE; NEOPLASMS; ONCOGENE PROTEINS; PHOSPHOPROTEINS; RNA, SMALL INTERFERING; SRC HOMOLOGY DOMAINS; TRANSFECTION; TUMOR CELLS, CULTURED;

MAMMALIA;

EID: 69549122682     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.046680     Document Type: Article

References (56)

1. Abram, C. L., Seals, D. F., Pass, I., Salinsky, D., Maurer, L., Roth, T. M. and Courtneidge, S. A. (2003). The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J. Biol. Chem. 278, 16844-16851.
2. Ago, T., Kuribayashi, F., Hiroaki, H., Takeya, R., Ito, T., Kohda, D. and Sumimoto, H. (2003). Phosphorylation of p47phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc. Natl. Acad. Sci. USA 100, 4474-4479.
3. Alexander, N. R., Branch, K. M., Parekh, A., Clark, E. S., Iwueke, I. C., Guelcher, S. A. and Weaver, A. M. (2008). Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 18, 1295-1299.
4. Artym, V. V., Zhang, Y., Seillier-Moiseiwitsch, F., Yamada, K. M. and Mueller, S. C. (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.
5. Ayala, I., Baldassarre, M., Giacchetti, G., Caldieri, G., Tete, S., Luini, A. and Buccione, R. (2008). Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J. Cell Sci. 121, 369-378.
6. Badowski, C., Pawlak, G., Grichine, A., Chabadel, A., Oddou, C., Jurdic, P., Pfaff, M., Albiges-Rizo, C. and Block, M. R. (2008). Paxillin phosphorylation controls invadopodia/podosomes spatiotemporal organization. Mol. Biol. Cell 19, 633-645.
7. Baldassarre, M., Pompeo, A., Beznoussenko, G., Castaldi, C., Cortellino, S., McNiven, M. A., Luini, A. and Buccione, R. (2003). Dynamin participates in focal extracellular matrix degradation by invasive cells. Mol. Biol. Cell 14, 1074-1084.
8. Basbaum, C. B. and Werb, Z. (1996). Focalized proteolysis: spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr. Opin. Cell Biol. 8, 731-738.
9. Benesch, S., Lommel, S., Steffen, A., Stradal, T. E., Scaplehorn, N., Way, M., Wehland, J. and Rottner, K. (2002). Phosphatidylinositol 4,5-biphosphate (PIP2)-induced vesicle movement depends on N-WASP and involves Nck, WIP, and Grb2. J. Biol. Chem. 277, 37771-37776.
10. Bharti, S., Inoue, H., Bharti, K., Hirsch, D. S., Nie, Z., Yoon, H. Y., Artym, V., Yamada, K. M., Mueller, S. C., Barr, V. A. et al. (2007). Src-dependent phosphorylation of ASAP1 regulates podosomes. Mol. Cell. Biol. 27, 8271-8283.
11. Bladt, F., Aippersbach, E., Gelkop, S., Strasser, G. A., Nash, P., Tafuri, A., Gertler, F. B. and Pawson, T. (2003). The murine Nck SH2/ SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol. Cell. Biol. 23, 4586-4597.
12. Bowden, E. T., Barth, M., Thomas, D., Glazer, R. I. and Mueller, S. C. (1999). An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 18, 4440-4449.
13. Bowden, E. T., Coopman, P. J. and Mueller, S. C. (2001). Invadopodia: unique methods for measurement of extracellular matrix degradation in vitro. Methods Cell Biol. 63, 613-627.
14. Campellone, K. G., Rankin, S., Pawson, T., Kirschner, M. W., Tipper, D. J. and Leong, J. M. (2004). Clustering of Nck by a 12-residue Tir phosphopeptide is sufficient to trigger localized actin assembly. J. Cell Biol. 164, 407-416.
15. Carlier, M. F., Nioche, P., Broutin-L'Hermite, I., Boujemaa, R., Le Clainche, C., Egile, C., Garbay, C., Ducruix, A., Sansonetti, P. and Pantaloni, D. (2000). GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex. J. Biol. Chem. 275, 21946-21952.
16. Chen, W. T., Olden, K., Bernard, B. A. and Chu, F. F. (1984). Expression of transformation-associated protease(s) that degrade fibronectin at cell contact sites. J. Cell Biol. 98, 1546-1555.
17. Chuang, Y. Y., Tran, N. L., Rusk, N., Nakada, M., Berens, M. E. and Symons, M. (2004). Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res. 64, 8271-8275.
18. Clark, E. S., Whigham, A. S., Yarbrough, W. G. and Weaver, A. M. (2007). Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67, 4227-4235.
19. Co, C., Wong, D. T., Gierke, S., Chang, V. and Taunton, J. (2007). Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 128, 901-913.
20. Condeelis, J. and Segall, J. E. (2003). Intravital imaging of cell movement in tumours. Nat. Rev. Cancer 3, 921-930.
21. Frese, S., Schubert, W. D., Findeis, A. C., Marquardt, T., Roske, Y. S., Stradal, T. E. and Heinz, D. W. (2006). The phosphotyrosine peptide binding specificity of Nck1 and Nck2 Src homology 2 domains. J. Biol. Chem. 281, 18236-18245.
22. Friedl, P. and Wolf, K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
23. Friedl, P. and Wolf, K. (2008). Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res. 68, 7247-7249.
24. Frischknecht, F., Moreau, V., Rottger, S., Gonfloni, S., Reckmann, I., Superti-Furga, G. and Way, M. (1999). Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401, 926-929.
25. Garg, P., Verma, R., Nihalani, D., Johnstone, D. B. and Holzman, L. B. (2007). Neph1 cooperates with nephrin to transduce a signal that induces actin polymerization. Mol. Cell. Biol. 27, 8698-8712.
26. Gimona, M., Buccione, R., Courtneidge, S. A. and Linder, S. (2008). Assembly and biological role of podosomes and invadopodia. Curr. Opin. Cell Biol. 20, 235-241.
27. Groemping, Y., Lapouge, K., Smerdon, S. J. and Rittinger, K. (2003). Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113, 343-355.
28. Gruenheid, S., DeVinney, R., Bladt, F., Goosney, D., Gelkop, S., Gish, G. D., Pawson, T. and Finlay, B. B. (2001). Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat. Cell Biol. 3, 856-859.
29. Hashimoto, S., Onodera, Y., Hashimoto, A., Tanaka, M., Hamaguchi, M., Yamada, A. and Sabe, H. (2004). Requirement for Arf6 in breast cancer invasive activities. Proc. Natl. Acad. Sci. USA 101, 6647-6652.
30. I, S. T., Nie, Z., Stewart, A., Najdovska, M., Hall, N. E., He, H., Randazzo, P. A. and Lock, P. (2004). ARAP3 is transiently tyrosine phosphorylated in cells attaching to fibronectin and inhibits cell spreading in a RhoGAP-dependent manner. J. Cell Sci. 117, 6071-6084.
31. Jones, N., Blasutig, I. M., Eremina, V., Ruston, J. M., Bladt, F., Li, H., Huang, H., Larose, L., Li, S. S., Takano, T. et al. (2006). Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440, 818-823.
32. Karathanassis, D., Stahelin, R. V., Bravo, J., Perisic, O., Pacold, C. M., Cho, W. and Williams, R. L. (2002). Binding of the PX domain of p47(phox) to phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction. EMBO J. 21, 5057-5068.
33. Linder, S. (2007). The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17, 107-117.
34. Lock, P., Abram, C. L., Gibson, T. and Courtneidge, S. A. (1998). A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J. 17, 4346-4357.
35. Maher, P. A. (2000). Disruption of cell-substrate adhesion activates the protein tyrosine kinase pp60(c-src). Exp. Cell Res. 260, 189-198.
36. Mitra, S. K. and Schlaepfer, D. D. (2006). Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18, 516-523.
37. Mizutani, K., Miki, H., He, H., Maruta, H. and Takenawa, T. (2002). Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res. 62, 669-674.
38. Moreau, V., Frischknecht, F., Reckmann, I., Vincentelli, R., Rabut, G., Stewart, D. and Way, M. (2000). A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat. Cell Biol. 2, 441-448.
39. Nollau, P. and Mayer, B. J. (2001). Profiling the global tyrosine phosphorylation state by Src homology 2 domain binding. Proc. Natl. Acad. Sci. USA 98, 13531-13536.
40. Oikawa, T., Itoh, T. and Takenawa, T. (2008). Sequential signals toward podosome formation in NIH-src cells. J. Cell Biol. 182, 157-169.
41. Onodera, Y., Hashimoto, S., Hashimoto, A., Morishige, M., Mazaki, Y., Yamada, A., Ogawa, E., Adachi, M., Sakurai, T., Manabe, T. et al. (2005). Expression of AMAP1, an ArfGAP, provides novel targets to inhibit breast cancer invasive activities. EMBO J. 24, 963-973.
42. Rivera, G. M., Briceno, C. A., Takeshima, F., Snapper, S. B. and Mayer, B. J. (2004). Inducible clustering of membrane-targeted SH3 domains of the adaptor protein Nck triggers localized actin polymerization. Curr. Biol. 14, 11-22.
43. Rohatgi, R., Nollau, P., Ho, H. Y., Kirschner, M. W. and Mayer, B. J. (2001). Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 276, 26448-26452.
44. Scaplehorn, N., Holmstrom, A., Moreau, V., Frischknecht, F., Reckmann, I. and Way, M. (2002). Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr. Biol. 12, 740-745.
45. Seals, D. F., Azucena, E. F., Jr, Pass, I., Tesfay, L., Gordon, R., Woodrow, M., Resau, J. H. and Courtneidge, S. A. (2005). The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 7, 155-165.
46. Songyang, Z., Shoelson, S. E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W. G., King, F., Roberts, T., Ratnofsky, S., Lechleider, R. J. et al. (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778.
47. Songyang, Z., Shoelson, S. E., McGlade, J., Olivier, P., Pawson, T., Bustelo, X. R., Barbacid, M., Sabe, H., Hanafusa, H., Yi, T. et al. (1994). Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/ fes, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14, 2777-2785.
48. Symons, M. (2008). Cell biology: watching the first steps of podosome formation. Curr. Biol. 18, R925-R927.
49. Tague, S. E., Muralidharan, V. and D'Souza-Schorey, C. (2004). ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc. Natl. Acad. Sci. USA 101, 9671-9676.
50. Tehrani, S., Tomasevic, N., Weed, S., Sakowicz, R. and Cooper, J. A. (2007). Src phosphorylation of cortactin enhances actin assembly. Proc. Natl. Acad. Sci. USA 104, 11933-11938.
51. Thompson, O., Kleino, I., Crimaldi, L., Gimona, M., Saksela, K. and Winder, S. J. (2008). Dystroglycan, Tks5 and Src mediated assembly of podosomes in myoblasts. PLoS ONE 3, e3638.
52. Verhagen, A. M., Ekert, P. G., Pakusch, M., Silke, J., Connolly, L. M., Reid, G. E., Moritz, R. L., Simpson, R. J. and Vaux, D. L. (2000). Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102, 43-53.
53. Verma, R., Kovari, I., Soofi, A., Nihalani, D., Patrie, K. and Holzman, L. B. (2006). Nephrin ectodomain engagement results in Src kinase activation, nephrin phosphorylation, Nck recruitment, and actin polymerization. J. Clin. Invest. 116, 1346-1359.
54. Weaver, A. M. (2006). Invadopodia: specialized cell structures for cancer invasion. Clin. Exp. Metastasis 23, 97-105.
55. Woodring, P. J., Meisenhelder, J., Johnson, S. A., Zhou, G. L., Field, J., Shah, K., Bladt, F., Pawson, T., Niki, M., Pandolfi, P. P. et al. (2004). c-Abl phosphorylates Dok1 to promote filopodia during cell spreading. J. Cell Biol. 165, 493-503.
56. Yamaguchi, H., Lorenz, M., Kempiak, S., Sarmiento, C., Coniglio, S., Symons, M., Segall, J., Eddy, R., Miki, H., Takenawa, T. et al. (2005). Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441-452.