Rho mediates endocytosis of epidermal growth factor receptor through phosphorylation of endophilin A1 by Rho-kinase

Genes to Cells

Volumn 10, Issue 10, 2005, Pages 973-987

  Kaneko, Takako ^a   Maeda, Akio ^a,b   Takefuji, Mikito ^a   Aoyama, Hiroki ^a   Nakayama, Masanori ^a   Kawabata, Saeko ^a   Kawano, Yoji ^a   Iwamatsu, Akihiro ^c   Amano, Mutsuki ^a   Kaibuchi, Kozo ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c KIRIN BREWERY CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; CLATHRIN; ENDOPHILIN; ENDOPHILIN A1; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; LIGAND; PROTEIN CIN85; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; THREONINE; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME SUBSTRATE; INTERNALIZATION; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

ACYLTRANSFERASES; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CATTLE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOCYTOSIS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; PC12 CELLS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RHOA GTP-BINDING PROTEIN; TRANSFECTION;

EID: 26044447158     PISSN: 13569597     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2005.00895.x     Document Type: Article

References (67)

1. Amano, M., Ito, M., Kimura, K., et al. (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
2. Amano, M., Chihara, K., Kimura, K., et al. (1997) Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275, 1308-1311.
3. Amano, M., Chihara, K., Nakamura, N., et al. (1999) The COOH terminus of Rho-kinase negatively regulates rho-kinase activity. J. Biol. Chem. 274, 32418-32424.
4. Borinstein, S.C., Hyatt, M.A., Sykes, V.W., et al. (2000) SETA is a multifunctional adapter protein with three SH3 domains that binds Grb2, Cbl, and the novel SB1 proteins. Cell Signal 12, 769-779.
5. Bresnick, A.R., Wolff-Long, V.L., Baumann, O. & Pollard, T.D. (1995) Phosphorylation on threonine-18 of the regulatory light chain dissociates the ATPase and motor properties of smooth muscle myosin II. Biochemistry 34, 12576-12583.
6. Burridge, K. & Wennerberg, K. (2004) Rho and Rac take center stage. Cell 116, 167-179.
7. Di Fiore, P.P. & De Camilli, P. (2001) Endocytosis and signaling: an inseparable partnership. Cell 106, 1-4.
8. Dikic, I. (2003) Mechanisms controlling EGF receptor endocytosis and degradation. Biochem. Soc. Trans. 31, 1178-1181.
9. Dikic, I. & Giordano, S. (2003) Negative receptor signalling. Curr. Opin. Cell Biol. 15, 128-135.
10. Etienne-Manneville, S. & Hall, A. (2002) Rho GTPases in cell biology. Nature 420, 629-635.
11. Fabian-Fine, R., Verstreken, P., Hiesinger, P.R., et al. (2003) Endophilin promotes a late step in endocytosis at glial invaginations in Drosophila photoreceptor terminals. J. Neurosci. 23, 10732-10744.
12. Fukata, Y., Oshiro, N., Kinoshita, N., et al. (1999) Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J. Cell Biol. 145, 347-361.
13. Gad, H., Ringstad, N., Low, P., et al. (2000) Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27, 301-312.
14. Giachino, C., Lantelme, E., Lanzetti, L., Saccone, S., et al. (1997) A novel SH3-containing human gene family preferentially expressed in the central nervous system. Genomics 41, 427-434.
15. Goto, H., Kosako, H., Tanabe, K., et al. (1998) Phosphorylation of vimentin by Rho-associated kinase at a unique amino-terminal site that is specifically phosphorylated during cytokinesis. J. Biol. Chem. 273, 11728-11736.
16. Gout, I., Middleton, G., Adu, J., et al. (2000) Negative regulation of PI 3-kinase by Ruk, a novel adaptor protein. EMBO J. 19, 4015-4025.
17. Govek, E.E., Newey, S.E. & Van Aelst, L. (2005) The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1-49.
18. Guichet, A., Wucherpfennig, T., Dudu, V., et al. (2002) Essential role of endophilin A in synaptic vesicle budding at the Drosophila neuromuscular junction. EMBO J. 21, 1661-1672.
19. Haugh, J.M., Schooler, K., Wells, A., Wiley, H.S. & Lauffenburger, D.A. (1999) Effect of epidermal growth factor receptor internalization on regulation of the phospholipase C-gamma1 signaling pathway. J. Biol. Chem. 274, 8958-8965.
20. de Heuvel, E., Bell, A.W., Ramjaun, A.R., et al. (1997) Identification of the major synaptojanin-binding proteins in brain. J. Biol. Chem. 272, 8710-8716.
21. Hill, E., van Der Kaay, J., Downes, C.P. & Smythe, E. (2001) The role of dynamin and its binding partners in coated pit invagination and scission. J. Cell Biol. 152, 309-323.
22. Hrboticky, N., Feldmeer, T., Essler, M., Wiedemann, A. & Aepfelbacher, M. (2002) Involvement of the GTPase Rho in the cellular uptake of low density lipoprotein by human skin fibroblasts. Biochem. Biophys. Acta 1580, 123-132.
23. Huang, S.S., Lokeshwar, V.B. & Huang, J.S. (1988) Modulation of the epidermal growth factor receptor by brain-derived growth factor in Swiss mouse 3T3 cells. J. Cell Biochem. 36, 209-221.
24. Huttner, W.B. & Schmidt, A.A. (2002) Membrane curvature: a case of endofeelin. Trends Cell Biol. 12, 155-158.
25. Ishizaki, T., Maekawa, M., Fujisawa, K., et al. (1996) The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J. 15, 1885-1893.
26. Iwamatsu, A. (1992) S-carboxymethylation of proteins transferred onto polyvinylidene difluoride membranes followed by in situ protease digestion and amino acid microsequencing. Electrophoresis 13, 142-147.
27. Jensen, O.N., Podtelejnikov, A. & Mann, M. (1996) Delayed extraction improves specificity in database searches by matrix-assisted laser desorption/ionization peptide maps. Rapid Commun. Mass Spectrom. 10, 1371-1378.
28. Joazeiro, C.A., Wing, S.S., Huang, H., et al. (1999) The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286, 309-312.
29. Kaibuchi, K., Kuroda, S. & Amano, M. (1999) Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68, 459-486.
30. Kamisoyama, H., Araki, Y. & Ikebe, M. (1994) Mutagenesis of the phosphorylation site (serine 19) of smooth muscle myosin regulatory light chain and its effects on the properties of myosin. Biochemistry 33, 840-847.
31. Kawano, Y., Fukata, Y., Oshiro, N., et al. (1999) Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147, 1023-1038.
32. Kimura, K., Ito, M., Amano, M., et al. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
33. Lamaze, C., Chuang, T.H., Terlecky, L.J., Bokoch, G.M. & Schmid, S.L. (1996) Regulation of receptor-mediated endocytosis by Rho and Rac. Nature 382, 177-179.
34. Leung, T., Manser, E., Tan, L. & Lim, L. (1995) A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 270, 29051-29054.
35. Levkowitz, G., Waterman, H., Ettenberg, S.A., et al. (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4, 1029-1040.
36. + and phorbol esters synergistically inhibit internalization of epidermal growth factor in pancreatic acini. Biochem. J. 223, 893-900.
37. Matsui, T., Amano, M., Yamamoto, T., et al. (1996) Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J. 15, 2208-2216.
38. Matsuura, Y., Possee, R.D., Overton, H.A. & Bishop, D.H. (1987) Baculovirus expression vectors: the requirements for high level expression of proteins, including glycoproteins. J. Gen. Virol. 68 (Pt 5), 1233-1250.
39. Meng, W., Numazaki, M., Takeuchi, K., et al. (2004) DIP (mDia interacting protein) is a key molecule regulating Rho and Rac in a Src-dependent manner. EMBO J. 23, 760-771.
40. Micheva, K.D., Ramjaun, A.R., Kay, B.K. & McPherson, P.S. (1997) SH3 domain-dependent interactions of endophilin with amphiphysin. FEBS Lett. 414, 308-312.
41. Narita, T., Amano, F., Yoshizaki, K., et al. (2001) Assignment of SH3KBP1 to human chromosome band Xp22.1-->p21.3 by in situ hybridization. Cytogenet. Cell Genet. 93, 133-134.
42. Petrelli, A., Gilestro, G.F., Lanzardo, S., et al. (2002) The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature 416, 187-190.
43. Raftopoulou, M. & Hall, A. (2004) Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23-32.
44. Reutens, A.T. & Begley, C.G. (2002) Endophilin-1: a multifunctional protein. Int. J. Biochem. Cell Biol. 34, 1173-1177.
45. Riento, K. & Ridley, A.J. (2003) Rocks: multifunctional kinases in cell behaviour. Nature Rev. Mol. Cell Biol. 4, 446-456.
46. Ringstad, N., Nemoto, Y. & De Camilli, P. (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.
47. Ringstad, N., Gad, H., Low, P., et al. (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24, 143-154.
48. Scales, S.J. & Scheller, R.H. (1999) Lipid membranes shape up. Nature 401, 123-124.
49. Schmidt, A., Wolde, M., Thiele, C., et al. (1999) Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401, 133-141.
50. Schuske, K.R., Richmond, J.E., Matthies, D.S., et al. (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40, 749-762.
51. Simpson, F., Hussain, N.K., Qualmann, B., et al. (1999) SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nature Cell Biol. 1, 119-124.
52. Slepnev, V.I. & De Camilli, P. (2000) Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nature Rev. Neurosci. 1, 161-172.
53. Soubeyran, P., Kowanetz, K., Szymkiewicz, I., Langdon, W.Y. & Dikic, I. (2002) Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416, 183-187.
54. Sparks, A.B., Rider, J.E., Hoffman, N.G., et al. (1996) Distinct ligand preferences of Src homology 3 domains from Src,Yes, Abl, Cortactin, p53bp2, PLCgamma, Crk, and Grb2. Proc. Natl. Acad. Sci. USA 93, 1540-1544.
55. Sweeney, H.L., Yang, Z., Zhi, G., Stull, J.T. & Trybus, K.M. (1994) Charge replacement near the phosphorylatable serine of the myosin regulatory light chain mimics aspects of phosphorylation. Proc. Natl. Acad. Sci. USA 91, 1490-1494.
56. Symons, M. & Rusk, N. (2003) Control of vesicular trafficking by Rho GTPases. Curr. Biol. 13, R409-R418.
57. Szymkiewicz, I., Kowanetz, K., Soubeyran, P., et al. (2002) CIN85 participates in Cbl-b-mediated down-regulation of receptor tyrosine kinases. J. Biol. Chem. 277, 39666-39672.
58. Take, H., Watanabe, S., Takeda, K., Yu, Z.X., Iwata, N. & Kajigaya, S. (2000) Cloning and characterization of a novel adaptor protein, CIN85, that interacts with c-Cbl. Biochem. Biophys. Res. Commun. 268, 321-328.
59. Thien, C.B. & Langdon, W.Y. (2001) Cbl: many adaptations to regulate protein tyrosine kinases. Nature Rev. Mol. Cell Biol. 2, 294-307.
60. Torrey, T., Kim, W., Morse, H.C. 3rd & Kozak, C.A. (1998) Cloning, expression and genetic mapping of the mouse SH3 domain protein, SH3D2B. Mamm. Genome 9, 74-75.
61. Uehata, M., Ishizaki, T., Satoh, H., et al. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
62. Van Aelst, L. & D'Souza-Schorey, C. (1997) Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322.
63. Verstreken, P., Kjaerulff, O., Lloyd, T.E., et al. (2002) Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109, 101-112.
64. Verstreken, P., Koh, T.W., Schulze, K.L., et al. (2003) Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40, 733-748.
65. Vieira, A.V., Lamaze, C. & Schmid, S.L. (1996) Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274, 2086-2089.
66. Waterman, H. & Yarden, Y. (2001) Molecular mechanisms underlying endocytosis and sorting of ErbB receptor tyrosine kinases. FEBS Lett. 490, 142-152.
67. Wilde, A., Beattie, E.C., Lem, L., et al. (1999) EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell 96, 677-687.