Nerve Growth Factor Stimulates the Concentration of TrkA within Lipid Rafts and Extracellular Signal-Regulated Kinase Activation through c-Cbl-Associated Protein

REFERENCES

• Ahn, M. Y., K. D. Katsanakis, F. Bheda, and T. S. Pillay. 2004. Primary and essential role of the adaptor protein APS for recruitment of both c-Cbl and its associated protein CAP in insulin signaling. J. Biol. Chem. 279:21526–21532.
   PubMedGoogle Scholar
• Anderson, R. G. 1998. The caveolae membrane system. Annu. Rev. Biochem. 67:199–225.
   PubMed Web of Science ®Google Scholar
• Arispe, N., and M. Doh. 2002. Plasma membrane cholesterol controls the cytotoxicity of Alzheimer's disease AbetaP (1-40) and (1-42) peptides. FASEB J. 16:1526–1536.
   PubMed Web of Science ®Google Scholar
• Baumann, C. A., V. Ribon, M. Kanzaki, D. C. Thurmond, S. Mora, S. Shigematsu, P. E. Bickel, J. E. Pessin, and A. R. Saltiel. 2000. CAP defines a second signalling pathway required for insulin-stimulated glucose transport. Nature 407:202–207.
   PubMed Web of Science ®Google Scholar
• Bickel, P. E., P. E. Scherer, J. E. Schnitzer, P. Oh, M. P. Lisanti, and H. F. Lodish. 1997. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272:13793–13802.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.
   PubMed Web of Science ®Google Scholar
• Chamberlain, L. H., and G. W. Gould. 2002. The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes. J. Biol. Chem. 277:49750–49754.
   PubMedGoogle Scholar
• Chiang, S. H., C. A. Baumann, M. Kanzaki, D. C. Thurmond, R. T. Watson, C. L. Neudauer, I. G. Macara, J. E. Pessin, and A. R. Saltiel. 2001. Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410:944–948.
   PubMed Web of Science ®Google Scholar
• Douglass, A. D., and R. D. Vale. 2005. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121:937–950.
   PubMed Web of Science ®Google Scholar
• Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:257–283.
   PubMedGoogle Scholar
• Frade, J. M., and Y. A. Barde. 1998. Nerve growth factor: two receptors, multiple functions. Bioessays 20:137–145.
   PubMed Web of Science ®Google Scholar
• Friedman, W. J., and L. A. Greene. 1999. Neurotrophin signaling via Trks and p75. Exp. Cell Res. 253:131–142.
   PubMed Web of Science ®Google Scholar
• Galisteo, M. L., I. Dikic, A. G. Batzer, W. Y. Langdon, and J. Schlessinger. 1995. Tyrosine phosphorylation of the c-cbl proto-oncogene protein product and association with epidermal growth factor (EGF) receptor upon EGF stimulation. J. Biol. Chem. 270:20242–20245.
   PubMed Web of Science ®Google Scholar
• Howe, C. L., and W. C. Mobley. 2004. Signaling endosome hypothesis: a cellular mechanism for long distance communication. J. Neurobiol. 58:207–216.
   PubMedGoogle Scholar
• Howe, C. L., J. S. Valletta, A. S. Rusnak, and W. C. Mobley. 2001. NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 32:801–814.
   PubMed Web of Science ®Google Scholar
• Huang, C. S., J. Zhou, A. K. Feng, C. C. Lynch, J. Klumperman, S. J. DeArmond, and W. C. Mobley. 1999. Nerve growth factor signaling in caveolae-like domains at the plasma membrane. J. Biol. Chem. 274:36707–36714.
   PubMed Web of Science ®Google Scholar
• Huang, E. J., and L. F. Reichardt. 2003. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72:609–642.
   PubMed Web of Science ®Google Scholar
• Huang, E. J., G. A. Wilkinson, I. Farinas, C. Backus, K. Zang, S. L. Wong, and L. F. Reichardt. 1999. Expression of Trk receptors in the developing mouse trigeminal ganglion: in vivo evidence for NT-3 activation of TrkA and TrkB in addition to TrkC. Development 126:2191–2203.
   PubMedGoogle Scholar
• Jaiswal, R. K., S. A. Moodie, A. Wolfman, and G. E. Landreth. 1994. The mitogen-activated protein kinase cascade is activated by B-Raf in response to nerve growth factor through interaction with p21ras. Mol. Cell. Biol. 14:6944–6953.
   PubMedGoogle Scholar
• Jullien, J., V. Guili, E. A. Derrington, J. L. Darlix, L. F. Reichardt, and B. B. Rudkin. 2003. Trafficking of TrkA-green fluorescent protein chimerae during nerve growth factor-induced differentiation. J. Biol. Chem. 278:8706–8716.
   PubMedGoogle Scholar
• Kao, S., R. K. Jaiswal, W. Kolch, and G. E. Landreth. 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.
   PubMed Web of Science ®Google Scholar
• Kaplan, D. R., and F. D. Miller. 1997. Signal transduction by the neurotrophin receptors. Curr. Opin. Cell Biol. 9:213–221.
   PubMed Web of Science ®Google Scholar
• Kimura, A., C. A. Baumann, S. H. Chiang, and A. R. Saltiel. 2001. The sorbin homology domain: a motif for the targeting of proteins to lipid rafts. Proc. Natl. Acad. Sci. USA 98:9098–9103.
   PubMedGoogle Scholar
• Kurakin, A., N. G. Hoffman, and B. K. Kay. 1998. Molecular recognition properties of the C-terminal Sh3 domain of the Cbl associated protein, Cap. J. Pept. Res. 52:331–337.
   PubMedGoogle Scholar
• Lachyankar, M. B., P. J. Condon, M. C. Daou, A. K. De, J. B. Levine, A. Obermeier, and A. H. Ross. 2003. Novel functional interactions between Trk kinase and p75 neurotrophin receptor in neuroblastoma cells. J. Neurosci. Res. 71:157–172.
   PubMedGoogle Scholar
• Lang, D. M., S. Lommel, M. Jung, R. Ankerhold, B. Petrausch, U. Laessing, M. F. Wiechers, H. Plattner, and C. A. Stuermer. 1998. Identification of reggie-1 and reggie-2 as plasma membrane-associated proteins which cocluster with activated GPI-anchored cell adhesion molecules in non-caveolar micropatches in neurons. J. Neurobiol. 37:502–523.
   PubMedGoogle Scholar
• Le Roy, C., and J. L. Wrana. 2005. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell. Biol. 6:112–126.
   PubMed Web of Science ®Google Scholar
• Liu, H. Y., and S. O. Meakin. 2002. ShcB and ShcC activation by the Trk family of receptor tyrosine kinases. J. Biol. Chem. 277:26046–26056.
   PubMedGoogle Scholar
• Liu, J., S. M. DeYoung, J. B. Hwang, E. E. O'Leary, and A. R. Saltiel. 2003. The roles of Cbl-b and c-Cbl in insulin-stimulated glucose transport. J. Biol. Chem. 278:36754–36762.
   PubMed Web of Science ®Google Scholar
• Liu, J., A. Kimura, C. A. Baumann, and A. R. Saltiel. 2002. APS facilitates c-Cbl tyrosine phosphorylation and GLUT4 translocation in response to insulin in 3T3-L1 adipocytes. Mol. Cell. Biol. 22:3599–3609.
   PubMed Web of Science ®Google Scholar
• Lucero, H. A., and P. W. Robbins. 2004. Lipid rafts-protein association and the regulation of protein activity. Arch. Biochem. Biophys. 426:208–224.
   PubMed Web of Science ®Google Scholar
• MacPhee, I., and P. A. Barker. 1999. Extended ceramide exposure activates the trkA receptor by increasing receptor homodimer formation. J. Neurochem. 72:1423–1430.
   PubMedGoogle Scholar
• Marshall, C. J. 1998. Signal transduction. Taking the Rap. Nature 392:553–554.
   PubMedGoogle Scholar
• Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179–185.
   PubMed Web of Science ®Google Scholar
• McCarty, J. H., and S. C. Feinstein. 1999. The TrkB receptor tyrosine kinase regulates cellular proliferation via signal transduction pathways involving SHC, PLCγ, and CBL. J. Recept. Signal Transduct. Res. 19:953–974.
   PubMed Web of Science ®Google Scholar
• Meakin, S. O., J. I. MacDonald, E. A. Gryz, C. J. Kubu, and J. M. Verdi. 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.
   PubMed Web of Science ®Google Scholar
• Mineo, C., G. L. James, E. J. Smart, and R. G. Anderson. 1996. Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J. Biol. Chem. 271:11930–11935.
   PubMed Web of Science ®Google Scholar
• Munro, S. 2003. Lipid rafts: elusive or illusive? Cell 115:377–388.
   PubMed Web of Science ®Google Scholar
• Nishio, M., S. Fukumoto, K. Furukawa, A. Ichimura, H. Miyazaki, S. Kusunoki, and T. Urano. 2004. Overexpressed GM1 suppresses nerve growth factor (NGF) signals by modulating the intracellular localization of NGF receptors and membrane fluidity in PC12 cells. J. Biol. Chem. 279:33368–33378.
   PubMed Web of Science ®Google Scholar
• Ohrt, T., A. Mancini, T. Tamura, and R. Niedenthal. 2004. c-Cbl binds to tyrosine-phosphorylated neurotrophin receptor p75 and induces its ubiquitination. Cell. Signal. 16:1291–1298.
   PubMedGoogle Scholar
• Paratcha, G., and C. F. Ibanez. 2002. Lipid rafts and the control of neurotrophic factor signaling in the nervous system: variations on a theme. Curr. Opin. Neurobiol. 12:542–549.
   PubMedGoogle Scholar
• Patapoutian, A., and L. F. Reichardt. 2001. Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11:272–280.
   PubMed Web of Science ®Google Scholar
• Peiro, S., J. X. Comella, C. Enrich, D. Martin-Zanca, and N. Rocamora. 2000. PC12 cells have caveolae that contain TrkA. Caveolae-disrupting drugs inhibit nerve growth factor-induced, but not epidermal growth factor-induced, MAPK phosphorylation. J. Biol. Chem. 275:37846–37852.
   PubMedGoogle Scholar
• Pike, L. J. 2003. Lipid rafts: bringing order to chaos. J. Lipid Res. 44:655–667.
   PubMed Web of Science ®Google Scholar
• Prior, I. A., and J. F. Hancock. 2001. Compartmentalization of Ras proteins. J. Cell Sci. 114:1603–1608.
   PubMed Web of Science ®Google Scholar
• Prior, I. A., A. Harding, J. Yan, J. Sluimer, R. G. Parton, and J. F. Hancock. 2001. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3:368–375.
   PubMed Web of Science ®Google Scholar
• Puri, C., D. Tosoni, R. Comai, A. Rabellino, D. Segat, F. Caneva, P. Luzzi, P. P. Di Fiore, and C. Tacchetti. 2005. Relationships between EGFR signaling-competent and endocytosis-competent membrane microdomains. Mol. Biol. Cell 16:2704–2718.
   PubMed Web of Science ®Google Scholar
• Qian, X., and D. D. Ginty. 2001. SH2-B and APS are multimeric adapters that augment TrkA signaling. Mol. Cell. Biol. 21:1613–1620.
   PubMed Web of Science ®Google Scholar
• Qian, X., A. Riccio, Y. Zhang, and D. D. Ginty. 1998. Identification and characterization of novel substrates of Trk receptors in developing neurons. Neuron 21:1017–1029.
   PubMed Web of Science ®Google Scholar
• Ribon, V., R. Herrera, B. K. Kay, and A. R. Saltiel. 1998. A role for CAP, a novel, multifunctional Src homology 3 domain-containing protein in formation of actin stress fibers and focal adhesions. J. Biol. Chem. 273:4073–4080.
   PubMed Web of Science ®Google Scholar
• Ribon, V., J. A. Printen, N. G. Hoffman, B. K. Kay, and A. R. Saltiel. 1998. A novel, multifuntional c-Cbl binding protein in insulin receptor signaling in 3T3-L1 adipocytes. Mol. Cell. Biol. 18:872–879.
   PubMed Web of Science ®Google Scholar
• Ridyard, M. S., and S. M. Robbins. 2003. Fibroblast growth factor-2-induced signaling through lipid raft-associated fibroblast growth factor receptor substrate 2 (FRS2). J. Biol. Chem. 278:13803–13809.
   PubMed Web of Science ®Google Scholar
• Rubin, D., and F. Ismail-Beigi. 2003. Distribution of Glut1 in detergent-resistant membranes (DRMs) and non-DRM domains: effect of treatment with azide. Am. J. Physiol. Cell Physiol. 285:C377-C383.
   Google Scholar
• Sargiacomo, M., M. Sudol, Z. Tang, and M. P. Lisanti. 1993. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122:789–807.
   PubMed Web of Science ®Google Scholar
• Schlessinger, J., and M. A. Lemmon. 2003. SH2 and PTB domains in tyrosine kinase signaling. Sci. STKE 2003:RE12.
   PubMedGoogle Scholar
• Segal, R. A., and M. E. Greenberg. 1996. Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19:463–489.
   PubMed Web of Science ®Google Scholar
• Shaul, P. W., and R. G. Anderson. 1998. Role of plasmalemmal caveolae in signal transduction. Am. J. Physiol. 275:L843-L851.
   Google Scholar
• Shogomori, H., and D. A. Brown. 2003. Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol. Chem. 384:1259–1263.
   PubMed Web of Science ®Google Scholar
• Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol. 1:31–39.
   PubMed Web of Science ®Google Scholar
• Smart, E. J., and R. G. Anderson. 2002. Alterations in membrane cholesterol that affect structure and function of caveolae. Methods Enzymol. 353:131–139.
   PubMed Web of Science ®Google Scholar
• Sofroniew, M. V., C. L. Howe, and W. C. Mobley. 2001. Nerve growth factor signaling, neuroprotection, and neural repair. Annu. Rev. Neurosci. 24:1217–1281.
   PubMed Web of Science ®Google Scholar
• Sternberg, P. W., and S. L. Schmid. 1999. Caveolin, cholesterol and Ras signalling. Nat. Cell Biol. 1:E35-E37.
   Google Scholar
• Suzuki, S., T. Numakawa, K. Shimazu, H. Koshimizu, T. Hara, H. Hatanaka, L. Mei, B. Lu, and M. Kojima. 2004. BDNF-induced recruitment of TrkB receptor into neuronal lipid rafts: roles in synaptic modulation. J. Cell Biol.
   Google Scholar
• Tansey, M. G., R. H. Baloh, J. Milbrandt, and E. M. Johnson, Jr. 2000. GFRalpha-mediated localization of RET to lipid rafts is required for effective downstream signaling, differentiation, and neuronal survival. Neuron 25:611–623.
   PubMed Web of Science ®Google Scholar
• Urdiales, J. L., E. Becker, M. Andrieu, A. Thomas, J. Jullien, L. A. van Grunsven, S. Menut, G. I. Evan, D. Martin-Zanca, and B. B. Rudkin. 1998. Cell cycle phase-specific surface expression of nerve growth factor receptors TrkA and p75(NTR). J. Neurosci. 18:6767–6775.
   PubMedGoogle Scholar
• Waugh, M. G., S. Minogue, J. S. Anderson, M. dos Santos, and J. J. Hsuan. 2001. Signalling and non-caveolar rafts. Biochem. Soc. Trans. 29:509–511.
   PubMedGoogle Scholar
• Wu, C., S. Butz, Y. Ying, and R. G. Anderson. 1997. Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane. J. Biol. Chem. 272:3554–3559.
   PubMed Web of Science ®Google Scholar
• Wu, C., C. F. Lai, and W. C. Mobley. 2001. Nerve growth factor activates persistent Rap1 signaling in endosomes. J. Neurosci. 21:5406–5416.
   PubMed Web of Science ®Google Scholar
• Yan, K. S., M. Kuti, S. Yan, S. Mujtaba, A. Farooq, M. P. Goldfarb, and M. M. Zhou. 2002. FRS2 PTB domain conformation regulates interactions with divergent neurotrophic receptors. J. Biol. Chem. 277:17088–17094.
   PubMedGoogle Scholar
• York, R. D., H. Yao, T. Dillon, C. L. Ellig, S. P. Eckert, E. W. McCleskey, and P. J. Stork. 1998. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392:622–626.
   PubMed Web of Science ®Google Scholar
• Zhang, M., J. Liu, A. Cheng, S. M. Deyoung, X. Chen, L. H. Dold, and A. R. Saltiel. 2006. CAP interacts with cytoskeletal proteins and regulates adhesion-mediated ERK activation and motility. EMBO J. 25:5284–5293.
   PubMed Web of Science ®Google Scholar