Phosphatidylinositol 5-phosphate regulates invasion through binding and activation of Tiam1

Nature Communications

Volumn 5, Issue , 2014, Pages

  Viaud, Julien ^a   Lagarrigue, Frédéric ^a   Ramel, Damien ^a   Allart, Sophie ^b   Chicanne, Gaëtan ^a   Ceccato, Laurie ^a   Courilleau, Delphine ^a   Xuereb, Jean Marie ^a   Pertz, Olivier ^c   Payrastre, Bernard ^a,d   Gaits Iacovoni, Frédérique ^a  

^a University Hospital of Toulouse   (France)

^b France   (France)

^c UNIVERSITY OF BASEL   (Switzerland)

^d TOULOUSE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL ENZYME; INITIATION FACTOR; IPGD PROTEIN; PHOSPHATASE; PHOSPHATE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 5 PHOSPHATE; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; TIAM1 PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; FIBROBLAST GROWTH FACTOR 1; GUANINE NUCLEOTIDE EXCHANGE FACTOR; IPGD PROTEIN, SHIGELLA FLEXNERI; PHOSPHATIDYLINOSITOL 5-PHOSPHATE; POLYPHOSPHOINOSITIDE; PROTEIN CDC42; RAC1 PROTEIN, HUMAN; TIAM1 PROTEIN, HUMAN;

BACTERIUM; CELL ORGANELLE; LIPID; MEMBRANE; PATHOLOGY; PHOSPHATASE; PHYSIOLOGICAL RESPONSE; PROTEIN;

ARTICLE; CELL INVASION; CONTROLLED STUDY; CYTOSKELETON; GENE ACTIVATION; GENE ACTIVITY; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; HUMAN; LARGE CELL LYMPHOMA; METABOLISM; PATHOGENICITY; PATHOLOGY; SHIGELLA FLEXNERI; TUMOR INVASION;

ACTINS; BACTERIAL PROTEINS; CDC42 GTP-BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 1; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; LYMPHOMA, LARGE-CELL, ANAPLASTIC; NEOPLASM INVASIVENESS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHORIC MONOESTER HYDROLASES; RAC1 GTP-BINDING PROTEIN; SHIGELLA FLEXNERI;

EID: 84902160158     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5080     Document Type: Article

References (62)

1. Di Paolo, G. & De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (2006).
2. Payrastre, B. et al. Phosphoinositides: key players in cell signalling, in time and space. Cell Signal. 13, 377-387 (2001).
3. Lemmon, M. A. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111 (2008).
4. McCrea, H. J. & De Camilli, P. Mutations in phosphoinositide metabolizing enzymes and human disease. Physiology (Bethesda) 24, 8-16 (2009).
5. Pendaries, C., Tronchere, H., Plantavid, M. & Payrastre, B. Phosphoinositide signaling disorders in human diseases. FEBS Lett. 546, 25-31 (2003).
6. Viaud, J., Boal, F., Tronchere, H., Gaits-Iacovoni, F. & Payrastre, B. Phosphatidylinositol 5-phosphate: A nuclear stress lipid and a tuner of membranes and cytoskeleton dynamics. Bioessays 36, 260-272 (2013).
7. Grainger, D. L., Tavelis, C., Ryan, A. J. & Hinchliffe, K. A. The emerging role of PtdIns5P: another signalling phosphoinositide takes its place. Biochem. Soc. Trans. 40, 257-261 (2012).
8. Gozani, O. et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114, 99-111 (2003).
9. Jones, D. R. et al. Nuclear PtdIns5P as a transducer of stress signaling: an in vivo role for PIP4Kbeta. Mol. Cell. 23, 685-695 (2006).
10. Ramel, D. et al. Shigella flexneri infection generates the lipid PI5P to alter endocytosis and prevent termination of EGFR signaling. Sci. Signal. 4, ra61 (2011).
11. Sarkes, D. & Rameh, L. E. A novel HPLC-based approach makes possible the spatial characterization of cellular PtdIns5P and other phosphoinositides. Biochem. J. 428, 375-384 (2010).
12. Mason, D. et al. Alteration of epithelial structure and function associated with PtdIns(4, 5)P2 degradation by a bacterial phosphatase. J. Gen. Physiol. 129, 267-283 (2007).
13. Niebuhr, K. et al. Conversion of PtdIns(4, 5)P2 into PtdIns(5)P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J. 21, 5069-5078 (2002).
14. Pendaries, C. et al. PtdIns5P activates the host cell PI3-kinase/Akt pathway during Shigella flexneri infection. EMBO J. 25, 1024-1034 (2006).
15. Oppelt, A. et al. Production of phosphatidylinositol 5-phosphate via PIKfyve and MTMR3 regulates cell migration. EMBO Rep. 14, 57-64 (2013).
16. Sbrissa, D., Ikonomov, O. C., Filios, C., Delvecchio, K. & Shisheva, A. Functional dissociation between PIKfyve-synthesized PtdIns5P and PtdIns(3, 5)P2 by means of the PIKfyve inhibitor YM201636. Am. J. Physiol. Cell Physiol. 303, C436-C446 (2012).
17. Sbrissa, D., Ikonomov, O. C., Strakova, J. & Shisheva, A. Role for a novel signaling intermediate, phosphatidylinositol 5-phosphate, in insulin-regulated F-actin stress fiber breakdown and GLUT4 translocation. Endocrinology 145, 4853-4865 (2004).
18. Colomba, A. et al. Activation of Rac1 and the exchange factor Vav3 are involved in NPM-ALK signaling in anaplastic large cell lymphomas. Oncogene 27, 2728-2736 (2008).
19. Colomba, A. et al. inhibition of Rac controls NPM-ALK-dependent lymphoma development and dissemination. Blood Cancer J 1, e21 (2011).
20. Lagarrigue, F. et al. Matrix metalloproteinase-9 is upregulated in nucleophosmin-anaplastic lymphoma kinase-positive anaplastic lymphomas ans activated at the cell surface by the chaperone heat shock protein 90 to promote cell invasion. Cancer Res. 70, 6978-6987 (2010).
21. Dupuis-Coronas, S. et al. The nucleophosmin-anaplastic lymphoma kinase oncogene interacts, activates, and uses the kinase PIKfyve to increase invasiveness. J. Biol. Chem. 286, 32105-32114 (2011).
22. Hall, A. Rho GTPases and the actin cytoskeleton. Science 279, 509-514 (1998).
23. Heasman, S. J. & Ridley, A. J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701 (2008).
24. Chicanne, G. et al. A novel mass assay to quantify the bioactive lipid PtdIns3P in various biological samples. Biochem. J. 447, 17-23 (2012).
25. 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).
26. Pelish, H. E. et al. Secramine inhibits Cdc42-dependent functions in cells and Cdc42 activation in vitro. Nat. Chem. Biol. 2, 39-46 (2006).
27. Haugsten, E. M., Oppelt, A. & Wesche, J. Phosphatidylinositol 5-phosphate is a second messenger important for cell migration. Commun. Integr. Biol. 6, e25446 (2013).
28. Coronas, S. et al. Elevated levels of PtdIns5P in NPM-ALK transformed cells: implication of PIKfyve. Biochem. Biophys. Res. Commun. 372, 351-355 (2008).
29. Vigil, D., Cherfils, J., Rossman, K. L. & Der, C. J. Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat. Rev. Cancer 10, 842-857 (2010).
30. Lazer, G. & Katzav, S. Guanine nucleotide exchange factors for RhoGTPases: good therapeutic targets for cancer therapy? Cell Signal. 23, 969-979 (2011).
31. Cook, D. R., Rossman, K. L. & Der, C. J. Rho guanine nucleotide exchange factors: regulators of Rho GTPase activity in development and disease. Oncogene doi:10.1038/onc.2013.362 (2013).
32. Lim, M. S. et al. The proteomic signature of NPM/ALK reveals deregulation of multiple cellular pathways. Blood 114, 1585-1595 (2009).
33. Malliri, A. et al. Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours. Nature 417, 867-871 (2002).
34. Mertens, A. E., Roovers, R. C. & Collard, J. G. Regulation of Tiam1-Rac signalling. FEBS Lett. 546, 11-16 (2003).
35. Michiels, F. et al. Regulated membrane localization of Tiam1, mediated by the NH2-terminal pleckstrin homology domain, is Required for Rac-dependent membrane ruffling and C-Jun NH2-terminal kinase activation. J. Cell Biol. 137, 387-398 (1997).
36. Baumeister, M. A. et al. Loss of phosphatidylinositol 3-phosphate binding by the C-terminal Tiam-1 pleckstrin homology domain prevents in vivo Rac1 activation without affecting membrane targeting. J. Biol. Chem. 278, 11457-11464 (2003).
37. Fleming, I. N., Gray, A. & Downes, C. P. Regulation of the Rac1-specific exchange factor Tiam1 involves both phosphoinositide 3-kinase-dependent and-independent components. Biochem. J. 351, 173-182 (2000).
38. Robbe, K., Otto-Bruc, A., Chardin, P. & Antonny, B. Dissociation of GDP dissociation inhibitor and membrane translocation are required for efficient activation of Rac by the Dbl homology-pleckstrin homology region of Tiam. J. Biol. Chem. 278, 4756-4762 (2003).
39. Malecka, K. A., Szentpetery, Z. & Peterson, J. R. Synergistic activation of p21-activated kinase 1 by phosphatidylinositol 4, 5-bisphosphate and Rho GTPases. J. Biol. Chem. 288, 8887-8897 (2013).
40. Thery, M. Micropatterning as a tool to decipher cell morphogenesis and functions. J. Cell Sci. 123, 4201-4213 (2010).
41. Soderberg, O. et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000 (2006).
42. Palamidessi, A. et al. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. cell 134, 135-147 (2008).
43. Yoshizaki, H. et al. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J. Cell Biol. 162, 223-232 (2003).
44. Suetsugu, S., Yamazaki, D., Kurisu, S. & Takenawa, T. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell 5, 595-609 (2003).
45. Buccione, R., Orth, J. D. & McNiven, M. A. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5, 647-657 (2004).
46. Block, M. R. et al. Podosome-type adhesions and focal adhesions, so alike yet so different. Eur. J. Cell Biol. 87, 491-506 (2008).
47. Linder, S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell. Biol. 17, 107-117 (2007).
48. 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).
49. Joffre, C. et al. A direct role for Met endocytosis in tumorigenesis. Nat. Cell Biol. 13, 827-837 (2011).
50. Viaud, J., Gaits-Iacovoni, F. & Payrastre, B. Regulation of the DH-PH tandem of guanine nucleotide exchange factor for Rho GTPases by phosphoinositides. Adv. Biol. Regul. 52, 303-314 (2012).
51. Palfy, M., Remenyi, A. & Korcsmaros, T. Endosomal crosstalk: meeting points for signaling pathways. Trends Cell Biol. 22, 447-456 (2012).
52. Miroshnychenko, D., Dubrovska, A., Maliuta, S., Telegeev, G. & Aspenstrom, P. Novel role of pleckstrin homology domain of the Bcr-Abl protein: analysis of protein-protein and protein-lipid interactions. Exp. Cell Res. 316, 530-542 (2010).
53. Kalluri, R. & Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401 (2006).
54. Saltel, F. et al. Invadosomes: intriguing structures with promise. Eur. J. Cell Biol. 90, 100-107 (2011).
55. Garcia-Mata, R. et al. Analysis of activated GAPs and GEFs in cell lysates. Methods Enzymol. 406, 425-437 (2006).
56. Lamant, L. et al. Establishment of a novel anaplastic large-cell lymphoma-cell line (COST) from a 'small-cell variant' of ALCL. Leukemia 18, 1693-1698 (2004).
57. Sirven, A. et al. Enhanced transgene expression in cord blood CD34(+)-derived hematopoietic cells, including developing T cells and NOD/SCID mouse repopulating cells, following transduction with modified trip lentiviral vectors. Mol. Ther. 3, 438-448 (2001).
58. Benard, V. & Bokoch, G. M. Assay of Cdc42, Rac, and Rho GTPase activation by affinity methods. Methods Enzymol. 345, 349-359 (2002).
59. Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917 (1959).
60. Dowler, S., Kular, G. & Alessi, D. R. Protein lipid overlay assay. Sci. STKE 2002, pl6 (2002).
61. Strochlic, T. I., Viaud, J., Rennefahrt, U. E., Anastassiadis, T. & Peterson, J. R. Phosphoinositides are essential coactivators for p21-activated kinase 1. Mol. Cell 40, 493-500 (2010).
62. Bowden, E. T., Coopman, P. J. & Mueller, S. C. Invadopodia: unique methods for measurement of extracellular matrix degradation in vitro. Methods Cell Biol. 63, 613-627 (2001).