Phosphoinositides in the regulation of actin cortex and cell migration

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 6, 2015, Pages 824-831

  Tsujita, Kazuya ^a   Itoh, Toshiki ^a  

^a KOBE UNIVERSITY   (Japan)

Author keywords

Adhesion energy; Cell migration; Cortical actin; Membrane tension; Phosphoinositide

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; ACTIN; ACTIN BINDING PROTEIN; ADAPTOR PROTEIN; ERM PROTEIN; EZRIN; LAMELLIPODIN; MOESIN; MYOSIN I; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPID; PROTEIN SH3; PROTEIN TYROSINE KINASE; RADIXIN; SORTING NEXIN; SORTING NEXIN 9; TAPP1 PROTEIN; TAPP2 PROTEIN; TKS5 PROTEIN; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; INOSITOL-POLYPHOSPHATE 5-PHOSPHATASE; MEMBRANE PROTEIN; MYOSIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

3T3 CELL LINE; ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL MIGRATION; CELL SHAPE; CELL STRUCTURE; CHEMOTAXIS; ENZYME SUBSTRATE; FOCAL ADHESION; IN VITRO STUDY; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PSEUDOPODIUM; SIGNAL TRANSDUCTION; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; CELL MEMBRANE; CELL MOVEMENT; CELL SHAPE; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MYOSINS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

EID: 84926288127     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.10.011     Document Type: Review

References (86)

1. A.G. Clark, O. Wartlick, G. Salbreux, and E.K. Paluch Stresses at the cell surface during animal cell morphogenesis Curr. Biol.:CB 24 2014 R484 R494
2. M.P. Sheetz Cell control by membrane-cytoskeleton adhesion Nat. Rev. Mol. Cell Biol. 2 2001 392 396
3. P.A. Janmey, and U. Lindberg Cytoskeletal regulation: rich in lipids Nat. Rev. Mol. Cell Biol. 5 2004 658 666
4. T. Takenawa, and T. Itoh Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane Biochim. Biophys. Acta 1533 2001 190 206
5. H.L. Yin, and P.A. Janmey Phosphoinositide regulation of the actin cytoskeleton Annu. Rev. Physiol. 65 2003 761 789
6. D. Raucher, T. Stauffer, W. Chen, K. Shen, S. Guo, J.D. York, M.P. Sheetz, and T. Meyer Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion Cell 100 2000 221 228
7. A. Diz-Munoz, M. Krieg, M. Bergert, I. Ibarlucea-Benitez, D.J. Muller, E. Paluch, and C.P. Heisenberg Control of directed cell migration in vivo by membrane-to-cortex attachment PLoS Biol. 8 2010 e1000544
8. R.E. McConnell, and M.J. Tyska Leveraging the membrane-cytoskeleton interface with myosin-1 Trends Cell Biol. 20 2010 418 426
9. N.C. Gauthier, T.A. Masters, and M.P. Sheetz Mechanical feedback between membrane tension and dynamics Trends Cell Biol. 22 2012 527 535
10. A. Diz-Munoz, D.A. Fletcher, and O.D. Weiner Use the force: membrane tension as an organizer of cell shape and motility Trends Cell Biol. 23 2013 47 53
11. R. Nambiar, R.E. McConnell, and M.J. Tyska Control of cell membrane tension by myosin-I Proc. Natl. Acad. Sci. U. S. A. 106 2009 11972 11977
12. Y. Wang, R.I. Litvinov, X. Chen, T.L. Bach, L. Lian, B.G. Petrich, S.J. Monkley, Y. Kanaho, D.R. Critchley, T. Sasaki, M.J. Birnbaum, J.W. Weisel, J. Hartwig, and C.S. Abrams Loss of PIP5KIgamma, unlike other PIP5KI isoforms, impairs the integrity of the membrane cytoskeleton in murine megakaryocytes J. Clin. Invest. 118 2008 812 819
13. R.G. Fehon, A.I. McClatchey, and A. Bretscher Organizing the cell cortex: the role of ERM proteins Nat. Rev. Mol. Cell Biol. 11 2010 276 287
14. K. Hamada, T. Shimizu, T. Matsui, S. Tsukita, and T. Hakoshima Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain EMBO J. 19 2000 4449 4462
15. B.T. Fievet, A. Gautreau, C. Roy, L. Del Maestro, P. Mangeat, D. Louvard, and M. Arpin Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin J. Cell Biol. 164 2004 653 659
16. C. Barret, C. Roy, P. Montcourrier, P. Mangeat, and V. Niggli Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP(2)) binding site in the NH(2)-terminal domain of ezrin correlates with its altered cellular distribution J. Cell Biol. 151 2000 1067 1080
17. J.J. Hao, Y. Liu, M. Kruhlak, K.E. Debell, B.L. Rellahan, and S. Shaw Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane J. Cell Biol. 184 2009 451 462
18. M.J. Brown, R. Nijhara, J.A. Hallam, M. Gignac, K.M. Yamada, S.L. Erlandsen, J. Delon, M. Kruhlak, and S. Shaw Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization Blood 102 2003 3890 3899
19. D. Raucher, and M.P. Sheetz Cell spreading and lamellipodial extension rate is regulated by membrane tension J. Cell Biol. 148 2000 127 136
20. Y. Liu, N.V. Belkina, C. Park, R. Nambiar, S.M. Loughhead, G. Patino-Lopez, K. Ben-Aissa, J.J. Hao, M.J. Kruhlak, H. Qi, U.H. von Andrian, J.H. Kehrl, M.J. Tyska, and S. Shaw Constitutively active ezrin increases membrane tension, slows migration, and impedes endothelial transmigration of lymphocytes in vivo in mice Blood 119 2012 445 453
21. G. Charras, and E. Paluch Blebs lead the way: how to migrate without lamellipodia Nat. Rev. Mol. Cell Biol. 9 2008 730 736
22. S.M. Hayden, J.S. Wolenski, and M.S. Mooseker Binding of brush border myosin I to phospholipid vesicles J. Cell Biol. 111 1990 443 451
23. D.E. Hokanson, and E.M. Ostap Myo1c binds tightly and specifically to phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate Proc. Natl. Acad. Sci. U. S. A. 103 2006 3118 3123
24. D.E. Hokanson, J.M. Laakso, T. Lin, D. Sept, and E.M. Ostap Myo1c binds phosphoinositides through a putative pleckstrin homology domain Mol. Biol. Cell 17 2006 4856 4865
25. A. Honda, M. Nogami, T. Yokozeki, M. Yamazaki, H. Nakamura, H. Watanabe, K. Kawamoto, K. Nakayama, A.J. Morris, M.A. Frohman, and Y. Kanaho Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation Cell 99 1999 521 532
26. M. Kisseleva, Y. Feng, M. Ward, C. Song, R.A. Anderson, and G.D. Longmore The LIM protein Ajuba regulates phosphatidylinositol 4,5-bisphosphate levels in migrating cells through an interaction with and activation of PIPKI alpha Mol. Cell. Biol. 25 2005 3956 3966
27. T. Golub, and P. Caroni PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility J. Cell Biol. 169 2005 151 165
28. S. Choi, N. Thapa, A.C. Hedman, Z. Li, D.B. Sacks, and R.A. Anderson IQGAP1 is a novel phosphatidylinositol 4,5 bisphosphate effector in regulation of directional cell migration EMBO J. 32 2013 2617 2630
29. T. Takenawa, and S. Suetsugu The WASP-WAVE protein network: connecting the membrane to the cytoskeleton Nat. Rev. Mol. Cell Biol. 8 2007 37 48
30. R. Rohatgi, H.Y. Ho, and M.W. Kirschner Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4, 5-bisphosphate J. Cell Biol. 150 2000 1299 1310
31. R. Rohatgi, L. Ma, H. Miki, M. Lopez, T. Kirchhausen, T. Takenawa, and M.W. Kirschner The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly Cell 97 1999 221 231
32. H.Y. Ho, R. Rohatgi, A.M. Lebensohn, M. Le, J. Li, S.P. Gygi, and M.W. Kirschner Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex Cell 118 2004 203 216
33. K. Takano, K. Toyooka, and S. Suetsugu EFC/F-BAR proteins and the N-WASP-WIP complex induce membrane curvature-dependent actin polymerization EMBO J. 27 2008 2817 2828
34. S.B. Padrick, H.C. Cheng, A.M. Ismail, S.C. Panchal, L.K. Doolittle, S. Kim, B.M. Skehan, J. Umetani, C.A. Brautigam, J.M. Leong, and M.K. Rosen Hierarchical regulation of WASP/WAVE proteins Mol. Cell 32 2008 426 438
35. C. Le Clainche, D. Schlaepfer, A. Ferrari, M. Klingauf, K. Grohmanova, A. Veligodskiy, D. Didry, D. Le, C. Egile, M.F. Carlier, and R. Kroschewski IQGAP1 stimulates actin assembly through the N-WASP-Arp2/3 pathway J. Biol. Chem. 282 2007 426 435
36. R.H. Insall, and O.D. Weiner PIP3, PIP2, and cell movement - similar messages, different meanings? Dev. Cell 1 2001 743 747
37. N. Thapa, Y. Sun, M. Schramp, S. Choi, K. Ling, and R.A. Anderson Phosphoinositide signaling regulates the exocyst complex and polarized integrin trafficking in directionally migrating cells Dev. Cell 22 2012 116 130
38. Y. Sun, K. Ling, M.P. Wagoner, and R.A. Anderson Type I gamma phosphatidylinositol phosphate kinase is required for EGF-stimulated directional cell migration J. Cell Biol. 178 2007 297 308
39. M.A. Lokuta, M.A. Senetar, D.A. Bennin, P.A. Nuzzi, K.T. Chan, V.L. Ott, and A. Huttenlocher Type Igamma PIP kinase is a novel uropod component that regulates rear retraction during neutrophil chemotaxis Mol. Biol. Cell 18 2007 5069 5080
40. R.A. Lacalle, R.M. Peregil, J.P. Albar, E. Merino, A.C. Martinez, I. Merida, and S. Manes Type I phosphatidylinositol 4-phosphate 5-kinase controls neutrophil polarity and directional movement J. Cell Biol. 179 2007 1539 1553
41. W. Xu, P. Wang, B. Petri, Y. Zhang, W. Tang, L. Sun, H. Kress, T. Mann, Y. Shi, P. Kubes, and D. Wu Integrin-induced PIP5K1C kinase polarization regulates neutrophil polarization, directionality, and in vivo infiltration Immunity 33 2010 340 350
42. J.M. Serrador, J.L. Alonso-Lebrero, M.A. del Pozo, H. Furthmayr, R. Schwartz-Albiez, J. Calvo, F. Lozano, and F. Sanchez-Madrid Moesin interacts with the cytoplasmic region of intercellular adhesion molecule-3 and is redistributed to the uropod of T lymphocytes during cell polarization J. Cell Biol. 138 1997 1409 1423
43. J.H. Lee, T. Katakai, T. Hara, H. Gonda, M. Sugai, and A. Shimizu Roles of p-ERM and Rho-ROCK signaling in lymphocyte polarity and uropod formation J. Cell Biol. 167 2004 327 337
44. A.B. Jaffe, and A. Hall Rho GTPases: biochemistry and biology Annu. Rev. Cell Dev. Biol. 21 2005 247 269
45. K. Riento, and A.J. Ridley Rocks: multifunctional kinases in cell behaviour Nat. Rev. Mol. Cell Biol. 4 2003 446 456
46. A. Bretscher, K. Edwards, and R.G. Fehon ERM proteins and merlin: integrators at the cell cortex Nat. Rev. Mol. Cell Biol. 3 2002 586 599
47. S. Funamoto, R. Meili, S. Lee, L. Parry, and R.A. Firtel Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis Cell 109 2002 611 623
48. D. Wessels, D.F. Lusche, S. Kuhl, P. Heid, and D.R. Soll PTEN plays a role in the suppression of lateral pseudopod formation during Dictyostelium motility and chemotaxis J. Cell Sci. 120 2007 2517 2531
49. J. van Rheenen, X. Song, W. van Roosmalen, M. Cammer, X. Chen, V. Desmarais, S.C. Yip, J.M. Backer, R.J. Eddy, and J.S. Condeelis EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells J. Cell Biol. 179 2007 1247 1259
50. K. Tsujita, T. Itoh, A. Kondo, M. Oyama, H. Kozuka-Hata, Y. Irino, J. Hasegawa, and T. Takenawa Proteome of acidic phospholipid-binding proteins: spatial and temporal regulation of Coronin 1A by phosphoinositides J. Biol. Chem. 285 2010 6781 6789
51. R. Meili, C. Ellsworth, S. Lee, T.B. Reddy, H. Ma, and R.A. Firtel Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium EMBO J. 18 1999 2092 2105
52. J.M. Haugh, F. Codazzi, M. Teruel, and T. Meyer Spatial sensing in fibroblasts mediated by 3' phosphoinositides J. Cell Biol. 151 2000 1269 1280
53. G. Servant, O.D. Weiner, P. Herzmark, T. Balla, J.W. Sedat, and H.R. Bourne Polarization of chemoattractant receptor signaling during neutrophil chemotaxis Science 287 2000 1037 1040
54. T. Sasaki, J. Irie-Sasaki, R.G. Jones, A.J. Oliveira-dos-Santos, W.L. Stanford, B. Bolon, A. Wakeham, A. Itie, D. Bouchard, I. Kozieradzki, N. Joza, T.W. Mak, P.S. Ohashi, A. Suzuki, and J.M. Penninger Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration Science 287 2000 1040 1046
55. E. Hirsch, V.L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M.P. Wymann Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation Science 287 2000 1049 1053
56. S. Funamoto, K. Milan, R. Meili, and R.A. Firtel Role of phosphatidylinositol 3' kinase and a downstream pleckstrin homology domain-containing protein in controlling chemotaxis in Dictyostelium J. Cell Biol. 153 2001 795 810
57. N. Andrew, and R.H. Insall Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions Nat. Cell Biol. 9 2007 193 200
58. O. Hoeller, and R.R. Kay Chemotaxis in the absence of PIP3 gradients Curr. Biol.:CB 17 2007 813 817
59. Y. Kunisaki, A. Nishikimi, Y. Tanaka, R. Takii, M. Noda, A. Inayoshi, K. Watanabe, F. Sanematsu, T. Sasazuki, T. Sasaki, and Y. Fukui DOCK2 is a Rac activator that regulates motility and polarity during neutrophil chemotaxis J. Cell Biol. 174 2006 647 652
60. H.C. Welch, W.J. Coadwell, C.D. Ellson, G.J. Ferguson, S.R. Andrews, H. Erdjument-Bromage, P. Tempst, P.T. Hawkins, and L.R. Stephens P-Rex1, a PtdIns(3,4,5)P3- and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac Cell 108 2002 809 821
61. S. Yoshii, M. Tanaka, Y. Otsuki, D.Y. Wang, R.J. Guo, Y. Zhu, R. Takeda, H. Hanai, E. Kaneko, and H. Sugimura alphaPIX nucleotide exchange factor is activated by interaction with phosphatidylinositol 3-kinase Oncogene 18 1999 5680 5690
62. S.K. Yoo, Q. Deng, P.J. Cavnar, Y.I. Wu, K.M. Hahn, and A. Huttenlocher Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish Dev. Cell 18 2010 226 236
63. E.S. Welf, S. Ahmed, H.E. Johnson, A.T. Melvin, and J.M. Haugh Migrating fibroblasts reorient directionality by a metastable, PI3K-dependent mechanism J. Cell Biol. 197 2012 105 114
64. T. Shibata, M. Nishikawa, S. Matsuoka, and M. Ueda Modeling the self-organized phosphatidylinositol lipid signaling system in chemotactic cells using quantitative image analysis J. Cell Sci. 125 2012 5138 5150
65. Y. Arai, T. Shibata, S. Matsuoka, M.J. Sato, T. Yanagida, and M. Ueda Self-organization of the phosphatidylinositol lipids signaling system for random cell migration Proc. Natl. Acad. Sci. U. S. A. 107 2010 12399 12404
66. R.H. Insall Understanding eukaryotic chemotaxis: a pseudopod-centred view Nat. Rev. Mol. Cell Biol. 11 2010 453 458
67. M. Nishio, K. Watanabe, J. Sasaki, C. Taya, S. Takasuga, R. Iizuka, T. Balla, M. Yamazaki, H. Watanabe, R. Itoh, S. Kuroda, Y. Horie, I. Forster, T.W. Mak, H. Yonekawa, J.M. Penninger, Y. Kanaho, A. Suzuki, and T. Sasaki Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1 Nat. Cell Biol. 9 2007 36 44
68. S. Dowler, R.A. Currie, D.G. Campbell, M. Deak, G. Kular, C.P. Downes, and D.R. Alessi Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities Biochem. J. 351 2000 19 31
69. A. Hogan, Y. Yakubchyk, J. Chabot, C. Obagi, E. Daher, K. Maekawa, and S.H. Gee The phosphoinositol 3,4-bisphosphate-binding protein TAPP1 interacts with syntrophins and regulates actin cytoskeletal organization J. Biol. Chem. 279 2004 53717 53724
70. J. Hasegawa, E. Tokuda, T. Tenno, K. Tsujita, H. Sawai, H. Hiroaki, T. Takenawa, and T. Itoh SH3YL1 regulates dorsal ruffle formation by a novel phosphoinositide-binding domain J. Cell Biol. 193 2011 901 916
71. W.A. Kimber, L. Trinkle-Mulcahy, P.C. Cheung, M. Deak, L.J. Marsden, A. Kieloch, S. Watt, R.T. Javier, A. Gray, C.P. Downes, J.M. Lucocq, and D.R. Alessi Evidence that the tandem-pleckstrin-homology-domain-containing protein TAPP1 interacts with Ptd(3,4)P2 and the multi-PDZ-domain-containing protein MUPP1 in vivo Biochem. J. 361 2002 525 536
72. W.A. Kimber, M. Deak, A.R. Prescott, and D.R. Alessi Interaction of the protein tyrosine phosphatase PTPL1 with the PtdIns(3,4)P2-binding adaptor protein TAPP1 Biochem. J. 376 2003 525 535
73. M. Krause, J.D. Leslie, M. Stewart, E.M. Lafuente, F. Valderrama, R. Jagannathan, G.A. Strasser, D.A. Rubinson, H. Liu, M. Way, M.B. Yaffe, V.A. Boussiotis, and F.B. Gertler Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics Dev. Cell 7 2004 571 583
74. M. Krause, E.W. Dent, J.E. Bear, J.J. Loureiro, and F.B. Gertler Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration Annu. Rev. Cell Dev. Biol. 19 2003 541 564
75. E.M. Lafuente, A.A. van Puijenbroek, M. Krause, C.V. Carman, G.J. Freeman, A. Berezovskaya, E. Constantine, T.A. Springer, F.B. Gertler, and V.A. Boussiotis RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion Dev. Cell 7 2004 585 595
76. A.L. Law, A. Vehlow, M. Kotini, L. Dodgson, D. Soong, E. Theveneau, C. Bodo, E. Taylor, C. Navarro, U. Perera, M. Michael, G.A. Dunn, D. Bennett, R. Mayor, and M. Krause Lamellipodin and the Scar/WAVE complex cooperate to promote cell migration in vivo J. Cell Biol. 203 2013 673 689
77. Y.H. Bae, Z. Ding, T. Das, A. Wells, F. Gertler, and P. Roy Profilin1 regulates PI(3,4)P2 and lamellipodin accumulation at the leading edge thus influencing motility of MDA-MB-231 cells Proc. Natl. Acad. Sci. U. S. A. 107 2010 21547 21552
78. D. Yarar, C.M. Waterman-Storer, and S.L. Schmid SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis Dev. Cell 13 2007 43 56
79. L.F. Seet, and W. Hong The Phox (PX) domain proteins and membrane traffic Biochim. Biophys. Acta 1761 2006 878 896
80. F. Kanai, H. Liu, S.J. Field, H. Akbary, T. Matsuo, G.E. Brown, L.C. Cantley, and M.B. Yaffe The PX domains of p47phox and p40phox bind to lipid products of PI(3)K Nat. Cell Biol. 3 2001 675 678
81. T. Oikawa, T. Itoh, and T. Takenawa Sequential signals toward podosome formation in NIH-src cells J. Cell Biol. 182 2008 157 169
82. D. Yarar, M.C. Surka, M.C. Leonard, and S.L. Schmid SNX9 activities are regulated by multiple phosphoinositides through both PX and BAR domains Traffic 9 2008 133 146
83. Y. Posor, M. Eichhorn-Gruenig, D. Puchkov, J. Schoneberg, A. Ullrich, A. Lampe, R. Muller, S. Zarbakhsh, F. Gulluni, E. Hirsch, M. Krauss, C. Schultz, J. Schmoranzer, F. Noe, and V. Haucke Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate Nature 499 2013 233 237
84. P. Lock, C.L. Abram, T. Gibson, and S.A. Courtneidge 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 1998 4346 4357
85. D.F. Seals, E.F. Azucena Jr., I. Pass, L. Tesfay, R. Gordon, M. Woodrow, J.H. Resau, and S.A. Courtneidge The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells Cancer Cell 7 2005 155 165
86. V.P. Sharma, R. Eddy, D. Entenberg, M. Kai, F.B. Gertler, and J. Condeelis Tks5 and SHIP2 regulate invadopodium maturation, but not initiation, in breast carcinoma cells Curr. Biol.:CB 23 2013 2079 2089