Molecular networks in FGF signaling: Flotillin-1 and Cbl-associated protein compete for the binding to fibroblast growth factor receptor substrate 2

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Tomasovic, Ana ^a,b   Traub, Stephanie ^b   Tikkanen, Ritva ^a,b  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FLOTILLIN 1; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOTYROSINE; TYROSINE; CBL ASSOCIATED PROTEIN, CAP; CBL-ASSOCIATED PROTEIN, CAP; CYTOSKELETON PROTEIN; FIBROBLAST GROWTH FACTOR; FLOTILLINS; FRS2 PROTEIN, HUMAN; MEMBRANE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SORBIN HOMOLOGY DOMAIN; ANIMAL; BINDING COMPETITION; CHEMISTRY; GENE SILENCING; GENETICS; HELA CELL; METABOLISM; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BINDING, COMPETITIVE; CYTOSKELETAL PROTEINS; FIBROBLAST GROWTH FACTORS; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84855335580     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029739     Document Type: Article

References (52)

1. Kouhara H, Hadari YR, Spivak-Kroizman T, Schilling J, Bar-Sagi D, et al. (1997) A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89: 693-702.
2. Meakin SO, MacDonald JI, Gryz EA, Kubu CJ, Verdi JM, (1999) The signaling adapter FRS-2 competes with Shc for binding to the nerve growth factor receptor TrkA. A model for discriminating proliferation and differentiation. J Biol Chem 274: 9861-9870.
3. Rabin SJ, Cleghon V, Kaplan DR, (1993) SNT, a differentiation-specific target of neurotrophic factor-induced tyrosine kinase activity in neurons and PC12 cells. Mol Cell Biol 13: 2203-2213.
4. Gotoh N, (2008) Regulation of growth factor signaling by FRS2 family docking/scaffold adaptor proteins. Cancer Sci 99: 1319-1325.
5. Ong SH, Guy GR, Hadari YR, Laks S, Gotoh N, et al. (2000) FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors. Mol Cell Biol 20: 979-989.
6. Xu H, Lee KW, Goldfarb M, (1998) Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J Biol Chem 273: 17987-17990.
7. McDougall K, Kubu C, Verdi JM, Meakin SO, (2001) Developmental expression patterns of the signaling adapters FRS-2 and FRS-3 during early embryogenesis. Mech Dev 103: 145-148.
8. Gotoh N, Manova K, Tanaka S, Murohashi M, Hadari Y, et al. (2005) The docking protein FRS2alpha is an essential component of multiple fibroblast growth factor responses during early mouse development. Mol Cell Biol 25: 4105-4116.
9. Hadari YR, Gotoh N, Kouhara H, Lax I, Schlessinger J, (2001) Critical role for the docking-protein FRS2 alpha in FGF receptor-mediated signal transduction pathways. Proc Natl Acad Sci U S A 98: 8578-8583.
10. Gotoh N, Laks S, Nakashima M, Lax I, Schlessinger J, (2004) FRS2 family docking proteins with overlapping roles in activation of MAP kinase have distinct spatial-temporal patterns of expression of their transcripts. FEBS Lett 564: 14-18.
11. Dixon SJ, MacDonald JI, Robinson KN, Kubu CJ, Meakin SO, (2006) Trk receptor binding and neurotrophin/fibroblast growth factor (FGF)-dependent activation of the FGF receptor substrate (FRS)-3. Biochim Biophys Acta 1763: 366-380.
12. Kurokawa K, Iwashita T, Murakami H, Hayashi H, Kawai K, et al. (2001) Identification of SNT/FRS2 docking site on RET receptor tyrosine kinase and its role for signal transduction. Oncogene 20: 1929-1938.
13. Melillo RM, Santoro M, Ong SH, Billaud M, Fusco A, et al. (2001) Docking protein FRS2 links the protein tyrosine kinase RET and its oncogenic forms with the mitogen-activated protein kinase signaling cascade. Mol Cell Biol 21: 4177-4187.
14. Lax I, Wong A, Lamothe B, Lee A, Frost A, et al. (2002) The docking protein FRS2alpha controls a MAP kinase-mediated negative feedback mechanism for signaling by FGF receptors. Mol Cell 10: 709-719.
15. Wu Y, Chen Z, Ullrich A, (2003) EGFR and FGFR signaling through FRS2 is subject to negative feedback control by ERK1/2. Biol Chem 384: 1215-1226.
16. Kao S, Jaiswal RK, Kolch W, Landreth GE, (2001) Identification of the mechanisms regulating the differential activation of the mapk cascade by epidermal growth factor and nerve growth factor in PC12 cells. J Biol Chem 276: 18169-18177.
17. Xu H, Goldfarb M, (2001) Multiple effector domains within SNT1 coordinate ERK activation and neuronal differentiation of PC12 cells. J Biol Chem 276: 13049-13056.
18. Delahaye L, Rocchi S, Van Obberghen E, (2000) Potential involvement of FRS2 in insulin signaling. Endocrinology 141: 621-628.
19. Hadari YR, Kouhara H, Lax I, Schlessinger J, (1998) Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol Cell Biol 18: 3966-3973.
20. Ong SH, Hadari YR, Gotoh N, Guy GR, Schlessinger J, et al. (2001) Stimulation of phosphatidylinositol 3-kinase by fibroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins. Proc Natl Acad Sci U S A 98: 6074-6079.
21. Babuke T, Tikkanen R, (2007) Dissecting the molecular function of reggie/flotillin proteins. Eur J Cell Biol 86: 525-532.
22. Morrow IC, Parton RG, (2005) Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6: 725-740.
23. Morrow IC, Rea S, Martin S, Prior IA, Prohaska R, et al. (2002) Flotillin-1/reggie-2 traffics to surface raft domains via a novel golgi-independent pathway. Identification of a novel membrane targeting domain and a role for palmitoylation. J Biol Chem 277: 48834-48841.
24. Neumann-Giesen C, Falkenbach B, Beicht P, Claasen S, Luers G, et al. (2004) Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem J 378: 509-518.
25. Babuke T, Ruonala M, Meister M, Amaddii M, Genzler C, et al. (2009) Hetero-oligomerization of reggie-1/flotillin-2 and reggie-2/flotillin-1 is required for their endocytosis. Cell Signal 21: 1287-1297.
26. Baumann CA, Ribon V, Kanzaki M, Thurmond DC, Mora S, et al. (2000) CAP defines a second signalling pathway required for insulin-stimulated glucose transport. Nature 407: 202-207.
27. Neumann-Giesen C, Fernow I, Amaddii M, Tikkanen R, (2007) Role of EGF-induced tyrosine phosphorylation of reggie-1/flotillin-2 in cell spreading and signaling to the actin cytoskeleton. J Cell Sci 120: 395-406.
28. Chiang SH, Baumann CA, Kanzaki M, Thurmond DC, Watson RT, et al. (2001) Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410: 944-948.
29. Glebov OO, Bright NA, Nichols BJ, (2006) Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 8: 46-54.
30. Dermine JF, Duclos S, Garin J, St-Louis F, Rea S, et al. (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 276: 18507-18512.
31. Munderloh C, Solis GP, Bodrikov V, Jaeger FA, Wiechers M, et al. (2009) Reggies/flotillins regulate retinal axon regeneration in the zebrafish optic nerve and differentiation of hippocampal and N2a neurons. J Neurosci 29: 6607-6615.
32. Schulte T, Paschke KA, Laessing U, Lottspeich F, Stuermer CA, (1997) Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 124: 577-587.
33. Kimura A, Baumann CA, Chiang SH, Saltiel AR, (2001) The sorbin homology domain: a motif for the targeting of proteins to lipid rafts. Proc Natl Acad Sci U S A 98: 9098-9103.
34. Zhang M, Liu J, Cheng A, Deyoung SM, Chen X, et al. (2006) CAP interacts with cytoskeletal proteins and regulates adhesion-mediated ERK activation and motility. EMBO J 25: 5284-5293.
35. Fernow I, Tomasovic A, Siehoff-Icking A, Tikkanen R, (2009) Cbl-associated protein is tyrosine phosphorylated by c-Abl and c-Src kinases. BMC Cell Biol 10: 80.
36. Solis GP, Hoegg M, Munderloh C, Schrock Y, Malaga-Trillo E, et al. (2007) Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains. Biochem J 403: 313-322.
37. Resh MD, (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451: 1-16.
38. Limpert AS, Karlo JC, Landreth GE, (2007) Nerve growth factor stimulates the concentration of TrkA within lipid rafts and extracellular signal-regulated kinase activation through c-Cbl-associated protein. Mol Cell Biol 27: 5686-5698.
39. Ridyard MS, Robbins SM, (2003) Fibroblast growth factor-2-induced signaling through lipid raft-associated fibroblast growth factor receptor substrate 2 (FRS2). J Biol Chem 278: 13803-13809.
40. Harder T, Scheiffele P, Verkade P, Simons K, (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-942.
41. Burgar HR, Burns HD, Elsden JL, Lalioti MD, Heath JK, (2002) Association of the signaling adaptor FRS2 with fibroblast growth factor receptor 1 (Fgfr1) is mediated by alternative splicing of the juxtamembrane domain. J Biol Chem 277: 4018-4023.
42. Zhang Y, McKeehan K, Lin Y, Zhang J, Wang F, (2008) Fibroblast growth factor receptor 1 (FGFR1) tyrosine phosphorylation regulates binding of FGFR substrate 2alpha (FRS2alpha) but not FRS2 to the receptor. Mol Endocrinol 22: 167-175.
43. Liu J, Kimura A, Baumann CA, Saltiel AR, (2002) APS facilitates c-Cbl tyrosine phosphorylation and GLUT4 translocation in response to insulin in 3T3-L1 adipocytes. Mol Cell Biol 22: 3599-3609.
44. Qian X, Riccio A, Zhang Y, Ginty DD, (1998) Identification and characterization of novel substrates of Trk receptors in developing neurons. Neuron 21: 1017-1029.
45. Huang L, Watanabe M, Chikamori M, Kido Y, Yamamoto T, et al. (2006) Unique role of SNT-2/FRS2beta/FRS3 docking/adaptor protein for negative regulation in EGF receptor tyrosine kinase signaling pathways. Oncogene 25: 6457-6466.
46. Wong A, Lamothe B, Lee A, Schlessinger J, Lax I, (2002) FRS2 alpha attenuates FGF receptor signaling by Grb2-mediated recruitment of the ubiquitin ligase Cbl. Proc Natl Acad Sci U S A 99: 6684-6689.
47. Kato N, Nakanishi M, Hirashima N, (2006) Flotillin-1 regulates IgE receptor-mediated signaling in rat basophilic leukemia (RBL-2H3) cells. J Immunol 177: 147-154.
48. Langhorst MF, Jaeger FA, Mueller S, Sven Hartmann L, Luxenhofer G, et al. (2008) Reggies/flotillins regulate cytoskeletal remodeling during neuronal differentiation via CAP/ponsin and Rho GTPases. Eur J Cell Biol 87: 921-931.
49. Sugawara Y, Nishii H, Takahashi T, Yamauchi J, Mizuno N, et al. (2007) The lipid raft proteins flotillins/reggies interact with Galphaq and are involved in Gq-mediated p38 mitogen-activated protein kinase activation through tyrosine kinase. Cell Signal 19: 1301-1308.
50. Vomastek T, Schaeffer HJ, Tarcsafalvi A, Smolkin ME, Bissonette EA, et al. (2004) Modular construction of a signaling scaffold: MORG1 interacts with components of the ERK cascade and links ERK signaling to specific agonists. Proc Natl Acad Sci U S A 101: 6981-6986.
51. Hopfer U, Hopfer H, Jablonski K, Stahl RA, Wolf G, (2006) The novel WD-repeat protein Morg1 acts as a molecular scaffold for hypoxia-inducible factor prolyl hydroxylase 3 (PHD3). J Biol Chem 281: 8645-8655.
52. Fernow I, Icking A, Tikkanen R, (2007) Reggie-1 and reggie-2 localize in non-caveolar rafts in epithelial cells: cellular localization is not dependent on the expression of caveolin proteins. Eur J Cell Biol 86: 345-352.