SH3YL1 regulates dorsal ruffle formation by a novel phosphoinositide-binding domain

Journal of Cell Biology

Volumn 193, Issue 5, 2011, Pages 901-916

  Hasegawa, Junya ^a   Tokuda, Emi ^a   Tenno, Takeshi ^a   Tsujita, Kazuya ^a   Sawai, Haruko ^a   Hiroaki, Hidekazu ^a   Takenawa, Tadaomi ^a   Itoh, Toshiki ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID BINDING PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; SH3 DOMAIN CONTAINING YSC84 LIKE 1; SRC HOMOLOGY 2 CONTAINING INOSITOL 5 PHOSPHATASE 2; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; MEMBRANE STRUCTURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS;

ANIMALS; CARRIER PROTEINS; CELL MEMBRANE STRUCTURES; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; HELA CELLS; HUMANS; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

MAMMALIA;

EID: 79959418683     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201012161     Document Type: Article

References (53)

1. Aoki, N., K. Ito, and M. Ito. 2000. A novel mouse gene, Sh3yl1, is expressed in the anagen hair follicle. J. Invest. Dermatol. 114:1050-1056.
2. Araki, N., M.T. Johnson, and J.A. Swanson. 1996. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. Cell Biol. 135:1249-1260.
3. Bhatia, V.K., K.L. Madsen, P.Y. Bolinger, A. Kunding, P. Hedegård, U. Gether, and D. Stamou. 2009. Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J. 28:3303-3314.
4. Buccione, R., J.D. Orth, and M.A. McNiven. 2004. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5:647-657.
5. Buschman, M.D., P.A. Bromann, P. Cejudo-Martin, F. Wen, I. Pass, and S.A. Courtneidge. 2009. The novel adaptor protein Tks4 (SH3PXD2B) is required for functional podosome formation. Mol. Biol. Cell. 20:1302-1311.
6. Dewar, H., D.T. Warren, F.C. Gardiner, C.G. Gourlay, N. Satish, M.R. Richardson, P.D. Andrews, and K.R. Ayscough. 2002. Novel proteins linking the actin cytoskeleton to the endocytic machinery in Saccharomyces cerevisiae. Mol. Biol. Cell. 13:3646-3661.
7. Dharmawardhane, S., A. Schürmann, M.A. Sells, J. Chernoff, S.L. Schmid, and G.M. Bokoch. 2000. Regulation of macropinocytosis by p21-activated kinase-1. Mol. Biol. Cell. 11:3341-3352.
8. Dowrick, P., P. Kenworthy, B. McCann, and R. Warn. 1993. Circular ruffle formation and closure lead to macropinocytosis in hepatocyte growth factor/ scatter factor-treated cells. Eur. J. Cell Biol. 61:44-53.
9. Dyson, J.M., C.J. O'Malley, J. Becanovic, A.D. Munday, M.C. Berndt, I.D. Coghill, H.H. Nandurkar, L.M. Ooms, and C.A. Mitchell. 2001. The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin. J. Cell Biol. 155:1065- 1079.
10. Ebina, T., H. Toh, and Y. Kuroda. 2009. Loop-length-dependent SVM prediction of domain linkers for high-throughput structural proteomics. Biopolymers. 92:1-8.
11. Emanuelsson, O., S. Brunak, G. von Heijne, and H. Nielsen. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953-971.
12. Farsad, K., N. Ringstad, K. Takei, S.R. Floyd, K. Rose, and P. De Camilli. 2001. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155:193-200.
13. Ford, M.G., I.G. Mills, B.J. Peter, Y. Vallis, G.J. Praefcke, P.R. Evans, and H.T. McMahon. 2002. Curvature of clathrin-coated pits driven by epsin. Nature. 419:361-366.
14. Foster, F.M., C.J. Traer, S.M. Abraham, and M.J. Fry. 2003. The phosphoinositide (PI) 3-kinase family. J. Cell Sci. 116:3037-3040.
15. Gaidarov, I., M.E. Smith, J. Domin, and J.H. Keen. 2001. The class II phosphoinositide 3-kinase C2alpha is activated by clathrin and regulates clathrin-mediated membrane trafficking. Mol. Cell. 7:443-449.
16. Gallop, J.L., C.C. Jao, H.M. Kent, P.J. Butler, P.R. Evans, R. Langen, and H.T. McMahon. 2006. Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25:2898-2910.
17. Gewinner, C., Z.C. Wang, A. Richardson, J. Teruya-Feldstein, D. Etemadmoghadam, D. Bowtell, J. Barretina, W.M. Lin, L. Rameh, L. Salmena, et al. 2009. Evidence that inositol polyphosphate 4-phosphatase type II is a tumor suppressor that inhibits PI3K signaling. Cancer Cell. 16:115-125.
18. Gray, A., H. Olsson, I.H. Batty, L. Priganica, and C. Peter Downes. 2003. Nonradioactive methods for the assay of phosphoinositide 3-kinases and phosphoinositide phosphatases and selective detection of signaling lipids in cell and tissue extracts. Anal. Biochem. 313:234-245.
19. Heath, R.J., and R.H. Insall. 2008. F-BAR domains: multifunctional regulators of membrane curvature. J. Cell Sci. 121:1951-1954.
20. Hogan, A., Y. Yakubchyk, J. Chabot, C. Obagi, E. Daher, K. Maekawa, and S.H. Gee. 2004. The phosphoinositol 3,4-bisphosphate-binding protein TAPP1 interacts with syntrophins and regulates actin cytoskeletal organization. J. Biol. Chem. 279:53717-53724.
21. Ishihara, H., T. Sasaoka, H. Hori, T. Wada, H. Hirai, T. Haruta, W.J. Langlois, and M. Kobayashi. 1999. Molecular cloning of rat SH2-containing inositol phosphatase 2 (SHIP2) and its role in the regulation of insulin signaling. Biochem. Biophys. Res. Commun. 260:265-272.
22. Itoh, T., and P. De Camilli. 2006. BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta. 1761:897-912.
23. Itoh, T., and T. Takenawa. 2002. Phosphoinositide-binding domains: functional units for temporal and spatial regulation of intracellular signalling. Cell. Signal. 14:733-743.
24. Itoh, T., K.S. Erdmann, A. Roux, B. Habermann, H. Werner, and P. De Camilli. 2005. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell. 9:791- 804.
25. Juncker, A.S., H. Willenbrock, G. Von Heijne, S. Brunak, H. Nielsen, and A. Krogh. 2003. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12:1652-1662.
26. Kamioka, Y., S. Fukuhara, H. Sawa, K. Nagashima, M. Masuda, M. Matsuda, and N. Mochizuki. 2004. A novel dynamin-associating molecule, forminbinding protein 17, induces tubular membrane invaginations and participates in endocytosis. J. Biol. Chem. 279:40091-40099.
27. Kang, H., C. Freund, J.S. Duke-Cohan, A. Musacchio, G. Wagner, and C.E. Rudd. 2000. SH3 domain recognition of a proline-independent tyrosinebased RKxxYxxY motif in immune cell adaptor SKAP55. EMBO J. 19:2889-2899.
28. Krueger, E.W., J.D. Orth, H. Cao, and M.A. McNiven. 2003. A dynamin-cortactin-Arp2/3 complex mediates actin reorganization in growth factor-stimulated cells. Mol. Biol. Cell. 14:1085-1096.
29. Lanzetti, L., A. Palamidessi, L. Areces, G. Scita, and P.P. Di Fiore. 2004. Rab5 is a signalling GTPase involved in actin remodelling by receptor tyrosine kinases. Nature. 429:309-314.
30. Lee, E., M. Marcucci, L. Daniell, M. Pypaert, O.A. Weisz, G.C. Ochoa, K. Farsad, M.R. Wenk, and P. De Camilli. 2002. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science. 297:1193-1196.
31. Legg, J.A., G. Bompard, J. Dawson, H.L. Morris, N. Andrew, L. Cooper, S.A. Johnston, G. Tramountanis, and L.M. Machesky. 2007. N-WASP involvement in dorsal ruffle formation in mouse embryonic fibroblasts. Mol. Biol. Cell. 18:678-687.
32. Lemmon, M.A. 2008. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9:99-111.
33. Liu, Y.W., M.C. Surka, T. Schroeter, V. Lukiyanchuk, and S.L. Schmid. 2008. Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells. Mol. Biol. Cell. 19:5347-5359.
34. Mayer, B.J., and R. Gupta. 1998. Functions of SH2 and SH3 domains. Curr. Top. Microbiol. Immunol. 228:1-22.
35. McMahon, H.T., and J.L. Gallop. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature. 438:590-596.
36. Mellström, K., C.H. Heldin, and B. Westermark. 1988. Induction of circular membrane ruffling on human fibroblasts by platelet-derived growth factor. Exp. Cell Res. 177:347-359.
37. Oikawa, T., T. Itoh, and T. Takenawa. 2008. Sequential signals toward podosome formation in NIH-src cells. J. Cell Biol. 182:157-169.
38. Orth, J.D., and M.A. McNiven. 2006. Get off my back! Rapid receptor internalization through circular dorsal ruffles. Cancer Res. 66:11094-11096.
39. Palamidessi, A., E. Frittoli, M. Garré, M. Faretta, M. Mione, I. Testa, A. Diaspro, L. Lanzetti, G. Scita, and P.P. Di Fiore. 2008. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell. 134:135-147.
40. Riedl, J., A.H. Crevenna, K. Kessenbrock, J.H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T.A. Holak, Z. Werb, et al. 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods. 5:605-607.
41. Ringstad, N., Y. Nemoto, and P. De Camilli. 1997. The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc. Natl. Acad. Sci. USA. 94:8569-8574.
42. Robertson, A.S., E.G. Allwood, A.P. Smith, F.C. Gardiner, R. Costa, S.J. Winder, and K.R. Ayscough. 2009. The WASP homologue Las17 activates the novel actin-regulatory activity of Ysc84 to promote endocytosis in yeast. Mol. Biol. Cell. 20:1618-1628.
43. Sasaki, J., S. Kofuji, R. Itoh, T. Momiyama, K. Takayama, H. Murakami, S. Chida, Y. Tsuya, S. Takasuga, S. Eguchi, et al. 2010. The PtdIns(3,4)P(2) phosphatase INPP4A is a suppressor of excitotoxic neuronal death. Nature. 465:497-501.
44. Schlunck, G., H. Damke, W.B. Kiosses, N. Rusk, M.H. Symons, C.M. Waterman-Storer, S.L. Schmid, and M.A. Schwartz. 2004. Modulation of Rac localization and function by dynamin. Mol. Biol. Cell. 15:256-267.
45. Sindić, A., A. Aleksandrova, A.P. Fields, S. Volinia, and H. Banfić. 2001. Presence and activation of nuclear phosphoinositide 3-kinase C2beta during compensatory liver growth. J. Biol. Chem. 276:17754-17761.
46. Suetsugu, S., D. Yamazaki, S. Kurisu, and T. Takenawa. 2003. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell. 5:595-609.
47. Suyama, M., and O. Ohara. 2003. DomCut: prediction of inter-domain linker regions in amino acid sequences. Bioinformatics. 19:673-674.
48. Swanson, J.A., and C. Watts. 1995. Macropinocytosis. Trends Cell Biol. 5:424- 428.
49. Takei, K., V.I. Slepnev, V. Haucke, and P. De Camilli. 1999. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1:33-39.
50. Tsujita, K., S. Suetsugu, N. Sasaki, M. Furutani, T. Oikawa, and T. Takenawa. 2006. Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 172:269-279.
51. Warn, R., D. Brown, P. Dowrick, A. Prescott, and A. Warn. 1993. Cytoskeletal changes associated with cell motility. Symp. Soc. Exp. Biol. 47:325-338.
52. Xie, J., I. Vandenbroere, and I. Pirson. 2008. SHIP2 associates with intersectin and recruits it to the plasma membrane in response to EGF. FEBS Lett. 582:3011-3017.
53. Yarar, D., C.M. Waterman-Storer, and S.L. Schmid. 2007. SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev. Cell. 13:43-56.