A Trio-Rac1-Pak1 signalling axis drives invadopodia disassembly

Nature Cell Biology

Volumn 16, Issue 6, 2014, Pages 571-583

  Moshfegh, Yasmin ^a   Bravo Cordero, Jose Javier ^a   Miskolci, Veronika ^a   Condeelis, John ^a   Hodgson, Louis ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; P21 ACTIVATED KINASE 1; RAC1 PROTEIN; TRIO GUANINE NUCLEOTIDE EXCHANGE FACTOR; UNCLASSIFIED DRUG; CTTN PROTEIN, HUMAN; NERVE PROTEIN; P21 ACTIVATED KINASE; PAK1 PROTEIN, HUMAN; PAK1 PROTEIN, RAT; PROTEIN SERINE THREONINE KINASE; RAC1 PROTEIN, HUMAN; RAC1 PROTEIN, RAT; TRIO PROTEIN, HUMAN; TRIO PROTEIN, RAT;

ANIMAL CELL; ARTICLE; BIOSENSOR; BREAST CANCER CELL LINE; BREAST CARCINOMA; CELL INVASION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; INVADOPODIUM; NONHUMAN; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TUMOR INVASION; ANIMAL; BREAST TUMOR; CELL MOTION; CELL SURFACE; ENZYMOLOGY; EXTRACELLULAR MATRIX; FEMALE; GENETIC PROCEDURES; GENETIC TRANSFECTION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; TIME; TUMOR CELL LINE;

ANIMALS; BIOSENSING TECHNIQUES; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURFACE EXTENSIONS; CORTACTIN; EXTRACELLULAR MATRIX; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; NEOPLASM INVASIVENESS; NERVE TISSUE PROTEINS; P21-ACTIVATED KINASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RAC1 GTP-BINDING PROTEIN; RATS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84901836960     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2972     Document Type: Article

References (70)

1. Fidler, I. J. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 3, 453-458 (2003). (Pubitemid 37328849)
2. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
3. Comen, E. A. Tracking the seed and tending the soil: evolving concepts in metastatic breast cancer. Discov. Med. 14, 97-104 (2012).
4. Thiery, J. P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442-454 (2002).
5. Linder, S., Wiesner, C. & Himmel, M. Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 27, 185-211 (2011).
6. Murphy, D. A. & Courtneidge, S. A. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426 (2011).
7. Coopman, P. J., Do, M. T., Thompson, E. W. & Mueller, S. C. Phagocytosis of cross-linked gelatin matrix by human breast carcinoma cells correlates with their invasive capacity. Clin. Cancer Res. 4, 507-515 (1998). (Pubitemid 28122770)
8. Oser, M. et al. Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J. Cell Biol. 186, 571-587 (2009).
9. Struckhoff, A. P., Rana, M. K. & Worthylake, R. A. RhoA can lead the way in tumor cell invasion and metastasis. Front. Biosci. 16, 1915-1926 (2011).
10. Bravo-Cordero, J. J. et al. A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia. Curr. Biol. 21, 635-644 (2011).
11. Jaffe, A. B. & Hall, A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269 (2005). (Pubitemid 41740635)
12. Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629-635 (2002). (Pubitemid 36764489)
13. Yamaguchi, H. et al. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441-452 (2005). (Pubitemid 40205066)
14. Sakurai-Yageta, M. et al. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J. Cell Biol. 181, 985-998 (2008). (Pubitemid 351846831)
15. Keely, P. J., Westwick, J. K., Whitehead, I. P., Der, C. J. & Parise, L. V. Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. Nature 390, 632-636 (1997). (Pubitemid 28016201)
16. Sahai, E. & Marshall, C. J. RHO-GTPases and cancer. Nat. Rev. Cancer 2, 133-142 (2002).
17. Baugher, P. J., Krishnamoorthy, L., Price, J. E. & Dharmawardhane, S. F. Rac1 and Rac3 isoform activation is involved in the invasive and metastatic phenotype of human breast cancer cells. Breast Cancer Res. 7, R965-R974 (2005).
18. Sun, D., Xu, D. & Zhang, B. Rac signaling in tumorigenesis and as target for anticancer drug development. Drug Resist. Updates 9, 274-287 (2006). (Pubitemid 46357635)
19. Vega, F. M. & Ridley, A. J. Rho GTPases in cancer cell biology. FEBS Lett. 582, 2093-2101 (2008).
20. Barrio-Real, L. & Kazanietz, M. G. Rho GEFs and cancer: linking gene expression and metastatic dissemination. Sci. Signal. 5, pe43 (2012).
21. Fritz, G., Just, I. & Kaina, B. Rho GTPases are over-expressed in human tumors. Int. J. Cancer 81, 682-687 (1999). (Pubitemid 29214373)
22. Nakahara, H. et al. Involvement of Cdc42 and Rac small G proteins in invadopodia formation of RPMI7951 cells. Genes Cells 8, 1019-1027 (2003). (Pubitemid 38072277)
23. Pignatelli, J., Tumbarello, D. A., Schmidt, R. P. & Turner, C. E. Hic-5 promotes invadopodia formation and invasion during TGF-beta-induced epithelial-mesenchymal transition. J. Cell Biol. 197, 421-437 (2012).
24. Li, A. et al. Activated mutant NRas(Q61K) drives aberrant melanocyte signaling, survival, and invasiveness via a Rac1-dependent mechanism. J. Invest. Dermatol. 132, 2610-2621 (2012).
25. Kwiatkowska, A. et al. The small GTPase RhoG mediates glioblastoma cell invasion. Mol. Cancer 11, 65 (2012).
26. Kraynov, V. S. et al. Localized Rac activation dynamics visualized in living cells. Science 290, 333-337 (2000).
27. Wu, Y. I. et al. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461, 104-108 (2009).
28. El-Sibai, M. et al. RhoA/ROCK-mediated switching between Cdc42-and Rac1-dependent protrusion in MTLn3 carcinoma cells. Exp. Cell Res. 314, 1540-1552 (2008).
29. Cailleau, R., Young, R., Olive, M. & Reeves, W. J. Jr Breast tumor cell lines from pleural effusions. J. Natl Cancer Inst. 53, 661-674 (1974).
30. Lasfargues, E. Y., Coutinho, W. G. & Redfield, E. S. Isolation of two human tumor epithelial cell lines from solid breast carcinomas. J. Natl Cancer Inst. 61, 967-978 (1978). (Pubitemid 9042085)
31. Littlewood-Evans, A. J. et al. The osteoclast-associated protease cathepsin K is expressed in human breast carcinoma. Cancer Res. 57, 5386-5390 (1997). (Pubitemid 27516378)
32. Tait, L., Soule, H. D. & Russo, J. Ultrastructural and immunocytochemical characterization of an immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50, 6087-6094 (1990). (Pubitemid 20331425)
33. Pertz, O., Hodgson, L., Klemke, R. L. & Hahn, K. M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440, 1069-1072 (2006).
34. Itoh, R. E. et al. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell Biol. 22, 6582-6591 (2002).
35. Nakamura, T., Kurokawa, K., Kiyokawa, E. & Matsuda, M. Analysis of the spatiotemporal activation of rho GTPases using Raichu probes. Methods Enzymol. 406, 315-332 (2006). (Pubitemid 43207449)
36. Lei, M. et al. Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 102, 387-397 (2000).
37. Rossman, K. L., Der, C. J. & Sondek, J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180 (2005). (Pubitemid 40215811)
38. Machacek, M. et al. Coordination of Rho GTPase activities during cell protrusion. Nature 461, 99-103 (2009).
39. Desmarais, V. et al. N-WASP and cortactin are involved in invadopodium-dependent chemotaxis to EGF in breast tumor cells. Cell Motil. Cytoskeleton. 66, 303-316 (2009).
40. Stylli, S. S. et al. Nck adaptor proteins link Tks5 to invadopodia actin regulation and ECM degradation. J. Cell Sci. 122, 2727-2740 (2009).
41. Whale, A., Hashim, F. N., Fram, S., Jones, G. E. & Wells, C. M. Signalling to cancer cell invasion through PAK family kinases. Front. Biosci. 16, 849-864 (2011).
42. Vidal, C., Geny, B., Melle, J., Jandrot-Perrus, M. & Fontenay-Roupie, M. Cdc42/Rac1-dependent activation of the p21-activated kinase (PAK) regulates human platelet lamellipodia spreading: implication of the cortical-actin binding protein cortactin. Blood 100, 4462-4469 (2002). (Pubitemid 35429686)
43. Webb, B. A. et al. Phosphorylation of cortactin by p21-activated kinase. Arch. Biochem. Biophys. 456, 183-193 (2006). (Pubitemid 44880282)
44. Webb, B. A. et al. PAK1 induces podosome formation in A7r5 vascular smooth muscle cells in a PAK-interacting exchange factor-dependent manner. Am. J. Physiol. Cell Physiol. 289, C898-C907 (2005). (Pubitemid 41361646)
45. Ayala, I. et al. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J. Cell Sci. 121, 369-378 (2008). (Pubitemid 351356708)
46. Gao, Y., Dickerson, J. B., Guo, F., Zheng, J. & Zheng, Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl Acad. Sci. USA 101, 7618-7623 (2004). (Pubitemid 38658078)
47. Ferri, N., Corsini, A., Bottino, P., Clerici, F. & Contini, A. Virtual screening approach for the identification of new Rac1 inhibitors. J. Med. Chem. 52, 4087-4090 (2009).
48. Stam, J. C. et al. Targeting of Tiam1 to the plasma membrane requires the cooperative function of the N-terminal pleckstrin homology domain and an adjacent protein interaction domain. J. Biol. Chem. 272, 28447-28454 (1997). (Pubitemid 27517792)
49. Van Rijssel, J., Hoogenboezem, M., Wester, L., Hordijk, P. L. & Van Buul, J. D. The N-terminal DH-PH domain of Trio induces cell spreading and migration by regulating lamellipodia dynamics in a Rac1-dependent fashion. PLoS ONE 7, e29912 (2012).
50. Debreceni, B. et al. Mechanisms of guanine nucleotide exchange and Rac-mediated signaling revealed by a dominant negative trio mutant. J. Biol. Chem. 279, 3777-3786 (2004). (Pubitemid 38140622)
51. Bowden, E. T., Barth, M., Thomas, D., Glazer, R. I. & Mueller, S. C. An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 18, 4440-4449 (1999). (Pubitemid 29396652)
52. Manabe, R., Kovalenko, M., Webb, D. J. & Horwitz, A. R. GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J. Cell Sci. 115, 1497-1510 (2002). (Pubitemid 34428707)
53. Frank, S. R. & Hansen, S. H. The PIX-GIT complex: a G protein signaling cassette in control of cell shape. Semin. Cell. Dev. Biol. 19, 234-244 (2008).
54. Sarmiento, C. et al. WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J. Cell Biol. 180, 1245-1260 (2008). (Pubitemid 351468478)
55. Manser, E. et al. Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell Biol. 17, 1129-1143 (1997). (Pubitemid 27097342)
56. Frost, J. A., Khokhlatchev, A., Stippec, S., White, M. A. & Cobb, M. H. Differential effects of PAK1-activating mutations reveal activity-dependent and-independent effects on cytoskeletal regulation. J. Biol. Chem. 273, 28191-28198 (1998). (Pubitemid 28496117)
57. Kiosses, W. B., Daniels, R. H., Otey, C., Bokoch, G. M. & Schwartz, M. A. A role for p21-activated kinase in endothelial cell migration. J. Cell Biol. 147, 831-844 (1999).
58. Chan, K. T., Cortesio, C. L. & Huttenlocher, A. FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. J. Cell Biol. 185, 357-370 (2009).
59. Cortesio, C. L. et al. Calpain 2 and PTP1B function in a novel pathway with Src to regulate invadopodia dynamics and breast cancer cell invasion. J. Cell Biol. 180, 957-971 (2008). (Pubitemid 351398422)
60. Van Rijssel, J. & van Buul, J. D. The many faces of the guanine-nucleotide exchange factor trio. Cell Adh. Migr. 6, 482-487 (2012).
61. Wen, P. Y. & Kesari, S. Malignant gliomas in adults. N. Engl. J. Med. 359, 492-507 (2008).
62. Bravo-Cordero, J. J., Hodgson, L. & Condeelis, J. Directed cell invasion and migration during metastasis. Curr. Opin. Cell Biol. 24, 277-283 (2012).
63. Lee, K. et al. Matrix compliance regulates Rac1b localization, NADPH oxidase assembly, and epithelial-mesenchymal transition. Mol. Biol. Cell 23, 4097-4108 (2012).
64. Gringel, A. et al. PAK4 and alphaPIX determine podosome size and number in macrophages through localized actin regulation. J. Cell Physiol. 209, 568-579 (2006). (Pubitemid 44484648)
65. Newsome, T. P., Scaplehorn, N. & Way, M. SRC mediates a switch from microtubule-to actin-based motility of vaccinia virus. Science 306, 124-129 (2004). (Pubitemid 39451954)
66. Rizzo, M. A., Springer, G. H., Granada, B. & Piston, D. W. An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449 (2004). (Pubitemid 38451376)
67. Nagai, T. et al. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90 (2002). (Pubitemid 34044921)
68. Beaty, B. T. et al. β1 integrin regulates Arg to promote invadopodial maturation and matrix degradation. Mol. Biol. Cell 24, 1661-1675 (2013).
69. Chen, W. T. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J. Exp. Zool. 251, 167-185 (1989).
70. Yip, S. C. et al. The distinct roles of Ras and Rac in PI 3-kinase-dependent protrusion during EGF-stimulated cell migration. J. Cell Sci. 120, 3138-3146 (2007).