Loss of scar/WAVE complex promotes N-WASP- and FAK-dependent invasion

Current Biology

Volumn 23, Issue 2, 2013, Pages 107-117

  Tang, Haoran ^a   Li, Ang ^a   Bi, Jing ^b   Veltman, Douwe M ^a   Zech, Tobias ^a   Spence, Heather J ^a   Yu, Xinzi ^a   Timpson, Paul ^a   Insall, Robert H ^a   Frame, Margaret C ^b   MacHesky, Laura M ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; FOCAL ADHESION KINASE 1; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PTK2 PROTEIN, HUMAN; WASF1 PROTEIN, HUMAN; WASL PROTEIN, HUMAN; WISKOTT ALDRICH SYNDROME PROTEIN;

ANIMAL; ARTICLE; CELL MOTION; CELL TRANSFORMATION; FOCAL ADHESION; GENE SILENCING; HUMAN; METABOLISM; PHOSPHORYLATION; RAT; TUMOR CELL LINE; TUMOR INVASION;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; FOCAL ADHESION KINASE 1; FOCAL ADHESIONS; GENE KNOCKDOWN TECHNIQUES; HUMANS; NEOPLASM INVASIVENESS; PHOSPHORYLATION; RATS; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 84872684818     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2012.11.059     Document Type: Article

References (43)

1. R.H. Insall, and L.M. Machesky Actin dynamics at the leading edge: from simple machinery to complex networks Dev. Cell 17 2009 310 322
2. Z. Chen, D. Borek, S.B. Padrick, T.S. Gomez, Z. Metlagel, A.M. Ismail, J. Umetani, D.D. Billadeau, Z. Otwinowski, and M.K. Rosen Structure and control of the actin regulatory WAVE complex Nature 468 2010 533 538
3. S. Eden, R. Rohatgi, A.V. Podtelejnikov, M. Mann, and M.W. Kirschner Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck Nature 418 2002 790 793
4. A. Gautreau, H.Y. Ho, J. Li, H. Steen, S.P. Gygi, and M.W. Kirschner Purification and architecture of the ubiquitous Wave complex Proc. Natl. Acad. Sci. USA 101 2004 4379 4383
5. A.M. Ismail, S.B. Padrick, B. Chen, J. Umetani, and M.K. Rosen The WAVE regulatory complex is inhibited Nat. Struct. Mol. Biol. 16 2009 561 563
6. A.M. Lebensohn, and M.W. Kirschner Activation of the WAVE complex by coincident signals controls actin assembly Mol. Cell 36 2009 512 524
7. O.D. Weiner, W.A. Marganski, L.F. Wu, S.J. Altschuler, and M.W. Kirschner An actin-based wave generator organizes cell motility PLoS Biol. 5 2007 e221
8. O.D. Weiner, M.C. Rentel, A. Ott, G.E. Brown, M. Jedrychowski, M.B. Yaffe, S.P. Gygi, L.C. Cantley, H.R. Bourne, and M.W. Kirschner Hem-1 complexes are essential for Rac activation, actin polymerization, and myosin regulation during neutrophil chemotaxis PLoS Biol. 4 2006 e38
9. V. Koronakis, P.J. Hume, D. Humphreys, T. Liu, O. Hørning, O.N. Jensen, and E.J. McGhie WAVE regulatory complex activation by cooperating GTPases Arf and Rac1 Proc. Natl. Acad. Sci. USA 108 2011 14449 14454
10. J.M. Silva, E. Ezhkova, J. Silva, S. Heart, M. Castillo, Y. Campos, V. Castro, F. Bonilla, C. Cordon-Cardo, and S.K. Muthuswamy Cyfip1 is a putative invasion suppressor in epithelial cancers Cell 137 2009 1047 1061
11. B. Escobar, G. de Cárcer, G. Fernández-Miranda, A. Cascón, J.J. Bravo-Cordero, M.C. Montoya, M. Robledo, M. Cañamero, and M. Malumbres Brick1 is an essential regulator of actin cytoskeleton required for embryonic development and cell transformation Cancer Res. 70 2010 9349 9359
12. M. Schober, S. Raghavan, M. Nikolova, L. Polak, H.A. Pasolli, H.E. Beggs, L.F. Reichardt, and E. Fuchs Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics J. Cell Biol. 176 2007 667 680
13. M. Toutant, A. Costa, J.M. Studler, G. Kadaré, M. Carnaud, and J.A. Girault Alternative splicing controls the mechanisms of FAK autophosphorylation Mol. Cell. Biol. 22 2002 7731 7743
14. V.G. Brunton, and M.C. Frame Src and focal adhesion kinase as therapeutic targets in cancer Curr. Opin. Pharmacol. 8 2008 427 432
15. M.C. Frame, H. Patel, B. Serrels, D. Lietha, and M.J. Eck The FERM domain: organizing the structure and function of FAK Nat. Rev. Mol. Cell Biol. 11 2010 802 814
16. H. Schägger, W.A. Cramer, and G. von Jagow Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis Anal. Biochem. 217 1994 220 230
17. E. Derivery, J. Fink, D. Martin, A. Houdusse, M. Piel, T.E. Stradal, D. Louvard, and A. Gautreau Free Brick1 is a trimeric precursor in the assembly of a functional wave complex PLoS ONE 3 2008 e2462
18. K. Hotary, X.Y. Li, E. Allen, S.L. Stevens, and S.J. Weiss A cancer cell metalloprotease triad regulates the basement membrane transmigration program Genes Dev. 20 2006 2673 2686
19. X. Yu, and L.M. Machesky Cells assemble invadopodia-like structures and invade into matrigel in a matrix metalloprotease dependent manner in the circular invasion assay PLoS ONE 7 2012 e30605
20. E.H. Van Aken, O. De Wever, L. Van Hoorde, E. Bruyneel, J.J. De Laey, and M.M. Mareel Invasion of retinal pigment epithelial cells: N-cadherin, hepatocyte growth factor, and focal adhesion kinase Invest. Ophthalmol. Vis. Sci. 44 2003 463 472
21. A. Li, J.C. Dawson, M. Forero-Vargas, H.J. Spence, X. Yu, I. König, K. Anderson, and L.M. Machesky The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion Curr. Biol. 20 2010 339 345
22. A.S. Kim, L.T. Kakalis, N. Abdul-Manan, G.A. Liu, and M.K. Rosen Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein Nature 404 2000 151 158
23. D. Yamazaki, T. Fujiwara, S. Suetsugu, and T. Takenawa A novel function of WAVE in lamellipodia: WAVE1 is required for stabilization of lamellipodial protrusions during cell spreading Genes Cells 10 2005 381 392
24. J.R. Ryu, A. Echarri, R. Li, and A.M. Pendergast Regulation of cell-cell adhesion by Abi/Diaphanous complexes Mol. Cell. Biol. 29 2009 1735 1748
25. X. Wu, S. Suetsugu, L.A. Cooper, T. Takenawa, and J.L. Guan Focal adhesion kinase regulation of N-WASP subcellular localization and function J. Biol. Chem. 279 2004 9565 9576
26. Y. Wang, and M.A. McNiven Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex J. Cell Biol. 196 2012 375 385
27. M. Gimona, R. Buccione, S.A. Courtneidge, and S. Linder Assembly and biological role of podosomes and invadopodia Curr. Opin. Cell Biol. 20 2008 235 241
28. M. Schoumacher, R.D. Goldman, D. Louvard, and D.M. Vignjevic Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia J. Cell Biol. 189 2010 541 556
29. T. Igishi, S. Fukuhara, V. Patel, B.Z. Katz, K.M. Yamada, and J.S. Gutkind Divergent signaling pathways link focal adhesion kinase to mitogen-activated protein kinase cascades. Evidence for a role of paxillin in c-Jun NH(2)-terminal kinase activation J. Biol. Chem. 274 1999 30738 30746
30. V. Bouchard, M.J. Demers, S. Thibodeau, V. Laquerre, N. Fujita, T. Tsuruo, J.F. Beaulieu, R. Gauthier, A. Vézina, L. Villeneuve, and P.H. Vachon Fak/Src signaling in human intestinal epithelial cell survival and anoikis: differentiation state-specific uncoupling with the PI3-K/Akt-1 and MEK/Erk pathways J. Cell. Physiol. 212 2007 717 728
31. G.H. Ashton, J.P. Morton, K. Myant, T.J. Phesse, R.A. Ridgway, V. Marsh, J.A. Wilkins, D. Athineos, V. Muncan, and R. Kemp Focal adhesion kinase is required for intestinal regeneration and tumorigenesis downstream of Wnt/c-Myc signaling Dev. Cell 19 2010 259 269
32. Y. Sonoda, S. Watanabe, Y. Matsumoto, E. Aizu-Yokota, and T. Kasahara FAK is the upstream signal protein of the phosphatidylinositol 3-kinase-Akt survival pathway in hydrogen peroxide-induced apoptosis of a human glioblastoma cell line J. Biol. Chem. 274 1999 10566 10570
33. D. Yamamoto, Y. Sonoda, M. Hasegawa, M. Funakoshi-Tago, E. Aizu-Yokota, and T. Kasahara FAK overexpression upregulates cyclin D3 and enhances cell proliferation via the PKC and PI3-kinase-Akt pathways Cell. Signal. 15 2003 575 583
34. H.J. Spence, P. Timpson, H.R. Tang, R.H. Insall, and L.M. Machesky Scar/WAVE3 contributes to motility and plasticity of lamellipodial dynamics but not invasion in three dimensions Biochem. J. 448 2012 35 42
35. D.M. Veltman, J.S. King, L.M. Machesky, and R.H. Insall SCAR knockouts in Dictyostelium: WASP assumes SCAR's position and upstream regulators in pseudopods J. Cell Biol. 198 2012 501 508
36. X.D. Ren, W.B. Kiosses, D.J. Sieg, C.A. Otey, D.D. Schlaepfer, and M.A. Schwartz Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover J. Cell Sci. 113 2000 3673 3678
37. B. Serrels, A. Serrels, V.G. Brunton, M. Holt, G.W. McLean, C.H. Gray, G.E. Jones, and M.C. Frame Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex Nat. Cell Biol. 9 2007 1046 1056
38. X. Yu, T. Zech, L. McDonald, E.G. Gonzalez, A. Li, I. Macpherson, J.P. Schwarz, H. Spence, K. Futó, and P. Timpson N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods J. Cell Biol. 199 2012 527 544
39. P. Timpson, E.J. McGhee, Z. Erami, M. Nobis, J.A. Quinn, M. Edward, and K.I. Anderson Organotypic collagen I assay: a malleable platform to assess cell behaviour in a 3-dimensional context J. Vis. Exp. 2011 e3089
40. C. Lu, X.Y. Li, Y. Hu, R.G. Rowe, and S.J. Weiss MT1-MMP controls human mesenchymal stem cell trafficking and differentiation Blood 115 2010 221 229
41. K. Sakai, T. Kurokawa, Y. Furui, Y. Kuronuma, M. Sekiguchi, J. Ando, Y. Inagaki, W. Tang, M. Nakata, and Y. Fujita-Yamaguchi Invasion of carcinoma cells into reconstituted type I collagen gels: visual real-time analysis by time-lapse microscopy Biosci. Trends 5 2011 10 16
42. V. Sanz-Moreno, G. Gadea, J. Ahn, H. Paterson, P. Marra, S. Pinner, E. Sahai, and C.J. Marshall Rac activation and inactivation control plasticity of tumor cell movement Cell 135 2008 510 523
43. V.V. Artym, Y. Zhang, F. Seillier-Moiseiwitsch, K.M. Yamada, and S.C. Mueller Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function Cancer Res. 66 2006 3034 3043