The Csk-binding protein PAG regulates PDGF-induced Src mitogenic signaling via GM1

Journal of Cell Biology

Volumn 182, Issue 3, 2008, Pages 603-614

  Veracini, Laurence ^a   Simon, Valérie ^a   Richard, Véronique ^a   Schraven, Burkhart ^b   Horejsi, Vaclav ^c   Roche, Serge ^a   Benistant, Christine ^a  

^a UNIV MONTPELLIER   (France)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GANGLIOSIDE GM1; PHOSPHOPROTEIN ASSOCIATED WITH GLYCOSPHINGOLIPID ENRICHED MICRODOMAIN; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE; SIALIDASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CAVEOLA; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CAVEOLAE; DNA; G(M1) GANGLIOSIDE; HUMANS; MEMBRANE PROTEINS; MICE; MITOGENS; MODELS, BIOLOGICAL; NEURAMINIDASE; NIH 3T3 CELLS; PHOSPHOPROTEINS; PLATELET-DERIVED GROWTH FACTOR; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 49749096806     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200705102     Document Type: Article

References (45)

1. Baumeister, U., R. Funke, K. Ebnet, H. Vorschmitt, S. Koch, and D. Vestweber. 2005. Association of Csk to VE-cadherin and inhibition of cell proliferation. EMBO J. 24:1686-1695.
2. Bénistant, C., J. Bourgaux, H. Chapuis, N. Mottet, S. Roche, and J. Bali. 2001. The C-terminal Src kinase is a tumour antigen in human carcinoma. Cancer Res. 61:1415-1420.
3. Boggon, T.J., and M.J. Eck. 2004. Structure and regulation of Src family kinases. Oncogene. 23:7918-7927.
4. Boureux, A., O. Furstoss, V. Simon, and S. Roche. 2005. c-Abl tyrosine kinase regulates a Rac/JNK and a Rac/Nox pathway for DNA synthesis and c-myc expression induced by growth factors. J. Cell Sci. 118:3717-3726.
5. Brdicka, T., D. Pavlistova, A. Leo, E. Bruyns, V. Korinek, P. Angelisova, J. Scherer, A. Shevchenko, I. Hilgert, J. Cerny, et al. 2000. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J. Exp. Med. 191:1591-1604.
6. Bromann, P.A., H. Korkaya, and S.A. Courtneidge. 2004. The interplay between Src family kinases and receptor tyrosine kinases. Oncogene. 23:7957-7968.
7. Broome, M.A., and S.A. Courtneidge. 2000. No requirement for src family kinases for PDGF signaling in fibroblasts expressing SV40 large T antigen. Oncogene. 19:2867-2869.
8. Choudhury, A., D.L. Marks, K.M. Proctor, G.W. Gould, and R.E. Pagano. 2006. Regulation of caveolar endocytosis by syntaxin 6-dependent delivery of membrane components to the cell surface. Nat. Cell Biol. 8:317-328.
9. Couet, J., S. Li, T. Okamoto, T. Ikezu, and M.P. Lisanti. 1997. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 272:6525-6533.
10. Da Silva, J.S., T. Hasegawa, T. Miyagi, C.G. Dotti, and J. Abad-Rodriguez. 2005. Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat. Neurosci. 8:606-615.
11. Frame, M.C. 2004. Newest findings on the oldest oncogene; how activated src does it. J. Cell Sci. 117:989-998.
12. Franco, M., O. Furstoss, V. Simon, C. Benistant, W.J. Hong, and S. Roche. 2006. The adaptor protein Tom1L1 is a negative regulator of Src mitogenic signaling induced by growth factors. Mol. Biol. Cell. 26:1932-1947.
13. Furstoss, O., K. Dorey, V. Simon, D. Barilla, G. Superti-Furga, and S. Roche. 2002. c-Abl is an effector of Src for growth factor-induced c-myc expression and DNA synthesis. EMBO J. 21:514-524.
14. Galbiati, F., D. Volonte, J.A. Engelman, G. Watanabe, R. Burk, R.G. Pestell, and M.P. Lisanti. 1998. Targeted downregulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J. 17:6633-6648.
15. Greaves, J., and L.H. Chamberlain. 2007. Palmitoylation-dependent protein sorting. J. Cell Biol. 176:249-254.
16. Herbst, R.S., M. Fukuoka, and J. Baselga. 2004. Gefitinib-a novel targeted approach to treating cancer. Nat. Rev. Cancer. 4:956-965.
17. Horejsi, V. 2005. Lipid rafts and their roles in T-cell activation. Microbes Infect. 7:310-316.
18. Horejsi, V., W. Zhang, and B. Schraven. 2004. Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat. Rev. Immunol. 4:603-616.
19. Imamoto, A., and P. Soriano. 1993. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell. 73:1117-1124.
20. Ingley, E., J.R. Schneider, C.J. Payne, D.J. McCarthy, K.W. Harder, M.L. Hibbs, and S.P. Klinken. 2006. Csk-binding protein mediates sequential enzymatic down-regulation and degradation of Lyn in erythropoietin-stimulated cells. J. Biol. Chem. 281:31920-31929.
21. Janes, P.W., S.C. Ley, and A.I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147:447-461.
22. Jiang, L.Q., X. Feng, W. Zhou, P.G. Knyazev, A. Ullrich, and Z. Chen. 2006. Csk-binding protein (Cbp) negatively regulates epidermal growth factor-induced cell transformation by controlling Src activation. Oncogene. 25:5495-5506.
23. Kabayama, K., T. Sato, K. Saito, N. Loberto, A. Prinetti, S. Sonnino, M. Kinjo, Y. Igarashi, and J. Inokuchi. 2007. Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc. Natl. Acad. Sci. USA. 104:13678-13683.
24. Kawabuchi, M., Y. Satomi, T. Takao, Y. Shimonishi, S. Nada, K. Nagai, A. Tarakhovsky, and M. Okada. 2000. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature. 404:999-1003.
25. Kovalenko, M., L. Ronnstrand, C.H. Heldin, M. Loubtchenkov, A. Gazit, A. Levitzki, and F.D. Bohmer. 1997. Phosphorylation site-specific inhibition of platelet-derived growth factor beta-receptor autophosphorylation by the receptor blocking tyrphostin AG1296. Biochemistry. 36:6260-6269.
26. Lee, H., D. Volonte, F. Galbiati, P. Iyengar, D.M. Lublin, D.B. Bregman, M.T. Wilson, R. Campos-Gonzalez, B. Bouzahzah, R.G. Pestell, et al. 2000. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol. Endocrinol. 14:1750-1775.
27. Li, S., J. Couet, and M.P. Lisanti. 1996. Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J. Biol. Chem. 271:29182-29190.
28. Martin, G.S. 2001. The hunting of the Src. Nat. Rev. Mol. Cell Biol. 2:467-475.
29. Mitsuda, T., K. Furukawa, S. Fukumoto, H. Miyazaki, T. Urano, and K. Furukawa. 2002. Overexpression of ganglioside GM1 results in the dispersion of platelet-derived growth factor receptor from glycolipid-enriched microdomains and in the suppression of cell growth signals. J. Biol. Chem. 277:11239-11246.
30. Mutoh, T., A. Tokuda, T. Miyadai, M. Hamaguchi, and N. Fujiki. 1995. Ganglioside GM1 binds to the Trk protein and regulates receptor function. Proc. Natl. Acad. Sci. USA. 92:5087-5091.
31. Nada, S., T. Yagi, H. Takeda, T. Tokunaga, H. Nakagawa, Y. Ikawa, M. Okada, and S. Aizawa. 1993. Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell. 73:1125-1135.
32. Niu, G., K.L. Wright, Y. Ma, G.M. Wright, M. Huang, R. Irby, J. Briggs, J. Karras, W.D. Cress, D. Pardoll, et al. 2005. Role of Stat3 in regulating p53 expression and function. Mol. Cell. Biol. 25:7432-7440.
33. Oneyama, C., T. Hikita, K. Enya, M.W. Dobenecker, K. Saito, S. Nada, A. Tarakhovsky, and M. Okada. 2008. The lipid raft-anchored adaptor protein cbp controls the oncogenic potential of c-Src. Mol. Cell. 30:426-436.
34. Papini, N., L. Anastasia, C. Tringali, G. Croci, R. Bresciani, K. Yamaguchi, T. Miyagi, A. Preti, A. Prinetti, S. Prioni, et al. 2004. The plasma membrane-associated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J. Biol. Chem. 279:16989-16995.
35. Pike, L.J. 2005. Growth factor receptors, lipid rafts and caveolae: An evolving story. Biochim. Biophys. Acta. 1746:260-273.
36. Sharma, D.K., J.C. Brown, A. Choudhury, T.E. Peterson, E. Holicky, D.L. Marks, R. Simari, R.G. Parton, and R.E. Pagano. 2004. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol. Biol. Cell. 15:3114-3122.
37. Shima, T., S. Nada, and M. Okada. 2003. Transmembrane phosphoprotein Cbp senses cell adhesion signaling mediated by Src family kinase in lipid rafts. Proc. Natl. Acad. Sci. USA. 100:14897-14902.
38. Smida, M., A. Posevitz-Fejfar, V. Horejsi, B. Schraven, and J.A. Lindquist. 2007. A novel negative regulatory function of PAG: blocking Ras activation. Blood. 110:596-615.
39. Solheim, S.A., K.M. Torgersen, K. Tasken, and T. Berge. 2008. Regulation of FynT function by dual domain docking on PAG/Cbp. J. Biol. Chem. 283:2773-2783.
40. Tauzin, S., H. Ding, K. Khatib, I. Ahmad, D. Burdevet, G. van Echten-Deckert, J.A. Lindquist, B. Schraven, N.U. Din, B. Borisch, and D.C. Hoessli. 2008. Oncogenic association of the Cbp/PAG adaptor protein with the Lyn tyrosine kinase in human B-NHL rafts. Blood. 111:2310-2320.
41. Uittenbogaard, A., and E.J. Smart. 2000. Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J. Biol. Chem. 275:25595-25599.
42. Veracini, L., M. Franco, A. Boureux, V. Simon, S. Roche, and C. Benistant. 2006. Two distinct pools of Src family tyrosine kinases regulate PDGF-induced DNA synthesis and actin dorsal ruffles. J. Cell Sci. 119:2921-2934.
43. Wang, Y., K. Yamaguchi, T. Wada, K. Hata, X. Zhao, T. Fujimoto, and T. Miyagi. 2002. A close association of the ganglioside-specific sialidase Neu3 with caveolin in membrane microdomains. J. Biol. Chem. 277:26252-26259.
44. Yew, P.R., and A.J. Berk. 1992. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature. 357:82-85.
45. Zhao, M., J.A. Janas, M. Niki, P.P. Pandolfi, and L. Van Aelst. 2006. Dok-1 independently attenuates Ras/mitogen-activated protein kinase and Src/c-myc pathways to inhibit platelet-derived growth factor-induced mitogenesis. Mol. Cell. Biol. 26:2479-2489.