Differential Rac1 signalling by guanine nucleotide exchange factors implicates FLII in regulating Rac1-driven cell migration

Nature Communications

Volumn 7, Issue , 2016, Pages

  Marei, Hadir ^a   Carpy, Alejandro ^b   Woroniuk, Anna ^a   Vennin, Claire ^c   White, Gavin ^a   Timpson, Paul ^c   Macek, Boris ^b   Malliri, Angeliki ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS AND CELL COMPONENTS; GENE EXPRESSION; MOTILITY; PHENOTYPE; PROTEIN; TUMOR;

ACTIN; CARRIER PROTEIN; FLII PROTEIN, MOUSE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PREX1 PROTEIN, MOUSE; RAC1 PROTEIN; TIAM1 PROTEIN, MOUSE;

ANIMAL; CELL LINE; CELL MOTION; GENETICS; HUMAN; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CARRIER PROTEINS; CELL LINE; CELL MOVEMENT; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICE; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84958559692     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10664     Document Type: Article

References (70)

1. Geiger, T. R. & Peeper, D. S. Metastasis mechanisms. Biochim. Biophys. Acta 1796, 293-308 (2009).
2. Yilmaz, M. & Christofori, G. Mechanisms of motility in metastasizing cells. Mol. Cancer Res. 8, 629-642 (2010).
3. Parri, M. & Chiarugi, P. Rac and Rho GTPases in cancer cell motility control. Cell Commun. Signal. 8, 23 (2010).
4. Lauffenburger, D. A. & Horwitz, A. F. Cell migration: a physically integrated molecular process. Cell 84, 359-369 (1996).
5. Malliri, A. & Collard, J. G. Role of Rho-family proteins in cell adhesion and cancer. Curr. Opin. Cell Biol. 15, 583-589 (2003).
6. Mack, N. A., Whalley, H. J., Castillo-Lluva, S. & Malliri, A. The diverse roles of Rac signaling in tumorigenesis. Cell Cycle 10, 1571-1581 (2011).
7. Williamson, R. C. et al. Coronin-1C and RCC2 guide mesenchymal migration by trafficking Rac1 and controlling GEF exposure. J. Cell Sci. 127, 4292-4307 (2014).
8. Braun, A. et al. Rac1 and Aurora A regulate MCAK to polarize microtubule growth in migrating endothelial cells. J. Cell Biol. 206, 97-112 (2014).
9. Miki, H., Yamaguchi, H., Suetsugu, S. & Takenawa, T. IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408, 732-735 (2000).
10. Takenawa, T. & Miki, H. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114, 1801-1809 (2001).
11. Johnston, S. A., Bramble, J. P., Yeung, C. L., Mendes, P. M. & Machesky, L. M. Arp2/3 complex activity in filopodia of spreading cells. BMC. Cell. Biol. 9, 65 (2008).
12. Price, L. S., Leng, J., Schwartz, M. A. & Bokoch, G. M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 9, 1863-1871 (1998).
13. Rottner, K., Hall, A. & Small, J. V. Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol. 9, 640-648 (1999).
14. Hordijk, P. L. et al. Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 278, 1464-1466 (1997).
15. Nola, S. et al. Ajuba is required for Rac activation and maintenance of E-cadherin adhesion. J. Cell Biol. 195, 855-871 (2011).
16. Dawson, J. C., Bruche, S., Spence, H. J., Braga, V. M. & Machesky, L. M. Mtss1 promotes cell-cell junction assembly and stability through the small GTPase Rac1. PLoS ONE 7, e31141 (2012).
17. Jin, G. et al. Biomechanical regulation of matrix metalloproteinase-9 in cultured chondrocytes. J. Orthop. Res. 18, 899-908 (2000).
18. Westermarck, J. & Kahari, V. M. Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 13, 781-792 (1999).
19. Lozano, E., Betson, M. & Braga, V. M. Tumor progression: small GTPases and loss of cell-cell adhesion. Bioessays 25, 452-463 (2003).
20. Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629-635 (2002).
21. Sander, E. E. & Collard, J. G. Rho-like GTPases: their role in epithelial cell-cell adhesion and invasion. Eur. J. Cancer. 35, 1905-1911 (1999).
22. Zhou, K. et al. Guanine nucleotide exchange factors regulate specificity of downstream signaling from Rac and Cdc42. J. Biol. Chem. 273, 16782-16786 (1998).
23. Krause, S. A. et al. Functional specialisation of yeast Rho1 GTP exchange factors. J. Cell. Sci. 125, 2721-2731 (2012).
24. Connolly, B. A., Rice, J., Feig, L. A. & Buchsbaum, R. J. Tiam1-IRSp53 complex formation directs specificity of rac-mediated actin cytoskeleton regulation. Mol. Cell. Biol. 25, 4602-4614 (2005).
25. Rajagopal, S. et al. Scaffold proteins IRSp53 and spinophilin regulate localized Rac activation by T-lymphocyte invasion and metastasis protein 1 (TIAM1). J. Biol. Chem. 285, 18060-18071 (2010).
26. Manser, E. et al. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell. 1, 183-192 (1998).
27. Buchsbaum, R. J., Connolly, B. A. & Feig, L. A. Interaction of Rac exchange factors Tiam1 and Ras-GRF1 with a scaffold for the p38 mitogen-activated protein kinase cascade. Mol. Cell. Biol. 22, 4073-4085 (2002).
28. Buchsbaum, R. J., Connolly, B. A. & Feig, L. A. Regulation of p70 S6 kinase by complex formation between the Rac guanine nucleotide exchange factor (Rac-GEF) Tiam1 and the scaffold spinophilin. J. Biol. Chem. 278, 18833-18841 (2003).
29. Sander, E. E., ten Klooster, J. P., van Delft, S., van der Kammen, R. A. & Collard, J. G. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147, 1009-1022 (1999).
30. Uhlenbrock, K. et al. The RacGEF Tiam1 inhibits migration and invasion of metastatic melanoma via a novel adhesive mechanism. J. Cell. Sci. 117, 4863-4871 (2004).
31. Campbell, A. D. et al. P-Rex1 cooperates with PDGFRbeta to drive cellular migration in 3D microenvironments. PLoS ONE 8, e53982 (2013).
32. Lindsay, C. R. et al. P-Rex1 is required for efficient melanoblast migration and melanoma metastasis. Nat. Commun. 2, 555 (2011).
33. Qin, J. et al. Upregulation of PIP3-dependent Rac exchanger 1 (P-Rex1) promotes prostate cancer metastasis. Oncogene 28, 1853-1863 (2009).
34. Nie, B., Cheng, N., Dinauer, M. C. & Ye, R. D. Characterization of P-Rex1 for its role in fMet-Leu-Phe-induced superoxide production in reconstituted COS(phox) cells. Cell. Signal. 22, 770-782 (2010).
35. Tolias, K. F. et al. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45, 525-538 (2005).
36. Gloeckner, C. J., Boldt, K., Schumacher, A., Roepman, R. & Ueffing, M. A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics 7, 4228-4234 (2007).
37. Gloeckner, C. J., Boldt, K., Schumacher, A. & Ueffing, M. Tandem affinity purification of protein complexes from mammalian cells by the Strep/FLAG (SF)-TAP tag. Methods Mol. Biol. 564, 359-372 (2009).
38. Gloeckner, C. J., Boldt, K. & Ueffing, M. Strep/FLAG tandem affinity purification (SF-TAP) to study protein interactions. Curr. Protoc. Protein Sci. 57, 19 20.1-19.20.19 (2009).
39. Ong, S. E. et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386 (2002).
40. Ong, S. E. & Mann, M. Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262 (2005).
41. Prasad, T. S., Kandasamy, K. & Pandey, A. Human protein reference database and human proteinpedia as discovery tools for systems biology. Methods Mol. Biol. 577, 67-79 (2009).
42. Kandasamy, K. et al. NetPath: a public resource of curated signal transduction pathways. Genome Biol. 11, R3 (2010).
43. McDowall, M. D., Scott, M. S. & Barton, G. J. PIPs: human protein-protein interaction prediction database. Nucleic Acids Res. 37, D651-D656 (2009).
44. Scott, M. S. & Barton, G. J. Probabilistic prediction and ranking of human protein-protein interactions. BMC Bioinformatics 8, 239 (2007).
45. Mann, M. Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 7, 952-958 (2006).
46. Davy, D. A., Campbell, H. D., Fountain, S., de Jong, D. & Crouch, M. F. The flightless I protein colocalizes with actin- and microtubule-based structures in motile Swiss 3T3 fibroblasts: evidence for the involvement of PI 3-kinase and Ras-related small GTPases. J. Cell Sci. 114, 549-562 (2001).
47. Kopecki, Z., O'Neill, G. M., Arkell, R. M. & Cowin, A. J. Regulation of focal adhesions by flightless i involves inhibition of paxillin phosphorylation via a Rac1-dependent pathway. J. Invest. Dermatol. 131, 1450-1459 (2011).
48. Silacci, P. et al. Gelsolin superfamily proteins: key regulators of cellular functions. Cell. Mol. Life Sci. 61, 2614-2623 (2004).
49. Kobe, B. & Kajava, A. V. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11, 725-732 (2001).
50. Kobe, B. & Deisenhofer, J. Proteins with leucine-rich repeats. Curr. Opin. Struct. Biol. 5, 409-416 (1995).
51. Liu, Y. T. & Yin, H. L. Identification of the binding partners for flightless I, a novel protein bridging the leucine-rich repeat and the gelsolin superfamilies. J. Biol. Chem. 273, 7920-7927 (1998).
52. Lee, Y. H., Campbell, H. D. & Stallcup, M. R. Developmentally essential protein flightless I is a nuclear receptor coactivator with actin binding activity. Mol. Cell. Biol. 24, 2103-2117 (2004).
53. Cowin, A. J. et al. Flightless I deficiency enhances wound repair by increasing cell migration and proliferation. J. Pathol. 211, 572-581 (2007).
54. Lin, C. H., Waters, J. M., Powell, B. C., Arkell, R. M. & Cowin, A. J. Decreased expression of Flightless I, a gelsolin family member and developmental regulator, in early-gestation fetal wounds improves healing. Mamm. Genome 22, 341-352 (2011).
55. Kopecki, Z., Arkell, R., Powell, B. C. & Cowin, A. J. Flightless I regulates hemidesmosome formation and integrin-mediated cellular adhesion and migration during wound repair. J. Invest. Dermatol. 129, 2031-2045 (2009).
56. Mohammad, I. et al. Flightless I is a focal adhesion-associated actin-capping protein that regulates cell migration. FASEB J. 26, 3260-3272 (2012).
57. Totsukawa, G. et al. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150, 797-806 (2000).
58. Even-Faitelson, L., Rosenberg, M. & Ravid, S. PAK1 regulates myosin II-B phosphorylation, filament assembly, localization and cell chemotaxis. Cell. Signal. 17, 1137-1148 (2005).
59. Shibata, K. et al. Rac1 regulates myosin II phosphorylation through regulation of myosin light chain phosphatase. J. Cell. Physiol. 230, 1352-1364 (2014).
60. Nobis, M. et al. Intravital FLIM-FRET imaging reveals dasatinib-induced spatial control of src in pancreatic cancer. Cancer Res. 73, 4674-4686 (2013).
61. Cicchi, R. et al. Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy. J Biophotonics 3, 34-43 (2010).
62. Fukata, M. et al. Cdc42 and Rac1 regulate the interaction of IQGAP1 with beta-catenin. J. Biol. Chem. 274, 26044-26050 (1999).
63. Kuroda, S. et al. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science 281, 832-835 (1998).
64. Fukata, M. et al. Involvement of IQGAP1, an effector of Rac1 and Cdc42 GTPases, in cell-cell dissociation during cell scattering. Mol. Cell. Biol. 21, 2165-2183 (2001).
65. Goshima, M. et al. Characterization of a novel Ras-binding protein Ce-FLI-1 comprising leucine-rich repeats and gelsolin-like domains. Biochem. Biophys. Res. Commun. 257, 111-116 (1999).
66. Adams, D. H. et al. Gender specific effects on the actin-remodelling protein Flightless I and TGF-beta1 contribute to impaired wound healing in aged skin. Int. J. Biochem. Cell Biol. 40, 1555-1569 (2008).
67. Arora, P. D., Wang, Y., Bresnick, A., Janmey, P. A. & McCulloch, C. A. Flightless I interacts with NMMIIA to promote cell extension formation, which enables collagen remodeling. Mol. Biol. Cell 26, 2279-2297 (2015).
68. Bonnans, C., Chou, J. & Werb, Z. Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 15, 786-801 (2014).
69. Timpson, P. et al. Organotypic collagen I assay: a malleable platform to assess cell behaviour in a 3-dimensional context. J. Vis. Exp. 56, e3089 (2011).
70. Huo, C. W. et al. High mammographic density is associated with an increase in stromal collagen and immune cells within the mammary epithelium. Breast Cancer Res. 17, 79 (2015).