Nerve Growth Factor Stimulates Multisite Tyrosine Phosphorylation and Activation of the Atypical Protein Kinase C's via a src Kinase Pathway

REFERENCES

• Abu-Amer, Y., F. P. Ross, K. P. McHugh, A. Livolsi, J. F. Peyron, and S. L. Teitelbaum. 1998. Tumor necrosis factor alpha activation of nuclear transcription factor kappaB in marrow macrophages is mediated by c-Src tyrosine phosphorylation of IkBalpha. J. Biol. Chem. 273:29417–29423.
   PubMed Web of Science ®Google Scholar
• Ahn, S., S. Maudsley, L. M. Luttrell, R. J. Lefkowitz, and Y. Daaka. 1999. Src-medicated tyrosine phosphorylation of dynamin is required for β-adrenergic receptor internalization and mitogen-activated protein kinase signaling. J. Biol. Chem. 274:1185–1188.
   PubMedGoogle Scholar
• Akiyama, T., and H. Ogawara. 1991. Use and specificity of genistein as an inhibitor of protein-tyrosine kinases. Methods Enzymol. 201:362–370.
   PubMed Web of Science ®Google Scholar
• Berra, E., M. T. Diaz-Meco, J. Lozano, S. Frutos, M. M. Munico, P. Sanchez, L. Sanz, and J. Moscat. 1995. Evidence for a role of MEK and MAPK during signal transduction by protein kinase C zeta. EMBO J. 14:6157–6163.
   PubMedGoogle Scholar
• Blake, R. A., P. Garcia-Paramio, P. J. Parker, and S. A. Courtneidge. 1999. Src promotes PKC-δ degradation. Cell Growth Differ. 10:231–241.
   PubMedGoogle Scholar
• Brodie, C., K. Bogi, P. Acs, P. Lazarovici, G. Petrovics, W. B. Anderson, and P. M. Blumberg. 1999. Protein kinase epsilon plays a role in neurite outgrowth in response to epidermal growth factor and nerve growth factor in PC12 cells. Cell Growth Differ. 10:183–191.
   PubMedGoogle Scholar
• Brodie, C., K. Bogi, P. Acs, P. S. Lorenzo, L. Baskin, and P. M. Blumberg. 1998. Protein kinase C delta inhibits the expression of glutamine synthetase in glial cells via the PKC delta regulatory domain and its tyrosine phosphorylation. J. Biol. Chem. 273:30713–30718.
   PubMedGoogle Scholar
• Coleman, E. S., and M. W. Wooten. 1994. Nerve growth factor-induced differentiation of PC12 cells employs the PMA-insensitive protein kinase C zeta isoform. J. Mol. Neurosci. 5:39–57.
   PubMedGoogle Scholar
• Cooper, J. A., F. S. Esch, S. S. Taylor, and T. Hunter. 1984. Phosphorylation sites in enolase and lactate dehydrogenase utilized by tyrosine kinases in vivo and in vitro. J. Biol. Chem. 259:7835–7841.
   PubMed Web of Science ®Google Scholar
• Denning, M. F., A. A. Dlugosz, M. K. Howett, and S. H. Yuspa. 1993. Expression of an oncogenic rasHa gene in murine keratinocytes induces tyrosine phosphorylation and reduced activity of protein kinase C delta. J. Biol. Chem. 268:26079–26081.
   PubMed Web of Science ®Google Scholar
• Denning, M. F., A. A. Dlugosz, D. W. Threadgill, T. Magnuson, and S. H. Yuspa. 1996. Activation of the epidermal growth factor receptor signal transduction pathway stimulates tyrosine phosphorylation of protein kinase C delta. J. Biol. Chem. 271:5325–5331.
   PubMedGoogle Scholar
• Diaz-Meco, M. T., J. Lozano, M. M. Municio, E. Berra, S. Frutos, L. Sanz, and J. Moscat. 1994. Evidence for the in vitro and in vivo interaction of Ras with protein kinase C zeta. J. Biol. Chem. 269:31706–31710.
   PubMedGoogle Scholar
• Diaz-Meco, M. T., I. Dominguez, L. Sanz, P. Dent, J. Lozano, M. M. Municio, E. Berra, R. T. Hay, T. W. Sturgill, and J. Moscat. 1994. ZetaPKC induces phosphorylation and inactivation of IkBalpha in vitro. EMBO J. 13:2842–2848.
   PubMed Web of Science ®Google Scholar
• Diaz-Meco, M. T., M. M. Municio, P. Sanchez, J. Lozano, and J. Moscat. 1996. Lambda-interacting protein, a novel protein that specifically interacts with the zinc finger domain of the atypical protein kinase C isotype λ/ι and stimulates its kinase activity in vitro and in vivo. Mol. Cell. Biol. 16:105–114.
   PubMed Web of Science ®Google Scholar
• Diaz-Meco, M. T., M. M. Munico, S. Frutos, P. Sanchez, J. Lozano, L. Sanz, and J. Moscat. 1996. The product of Par-4, a gene induced during apoptosis, interacts selectively with the atypical isoforms of protein kinase C. Cell 86:777–786.
   PubMed Web of Science ®Google Scholar
• Garcia-Rocha, M., J. Avila, and J. Lozano. 1997. The zeta-isozyme of protein kinase C binds to tubulin through the pseduosubstrate domain. Exp. Cell Res. 230:1–8.
   PubMedGoogle Scholar
• Gschwendt, M., K. Kielbassa, W. Kittstein, and M. Marks. 1994. Tyrosine phosphorylation and stimulation of protein kinase C delta from porcine spleen by src in vitro. Dependence of the activated state of protein kinase C delta. FEBS Lett. 347:85–89.
   PubMed Web of Science ®Google Scholar
• Haleem-Smith, H., E. Y. Chang, Z. Szallasi, P. Blumberg, and J. Rivera. 1995. Tyrosine phosphorylation of protein kinase C delta in response to the activation of the high-affinity receptor for immunoglobulin E modifies its substrate recognition. Proc. Natl. Acad. Sci. USA 92:9112–9116.
   PubMedGoogle Scholar
• Hama, T., K. P. Huang, and G. Guroff. 1986. Protein kinase C as a component of a nerve growth factor-sensitive phosphorylation system in PC12 cells. Proc. Natl. Acad. Sci. USA 83:2353–2357.
   PubMed Web of Science ®Google Scholar
• Hubner, S., C. Xiao, and D. A. Jans. 1997. The protein kinase CK2 site enhances recognition of the simian virus 40 large T-antigen nuclear localization sequence by importin. J. Biol. Chem. 272:17191–17195.
   PubMedGoogle Scholar
• Izumi, Y., T. Hirose, Y. Tamai, S. Hirai, Y. Nagashima, T. Fujimoto, Y. Tabuse, K. J. Kemphues, and S. Ohno. 1998. An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J. Cell Biol. 143:95–106.
   PubMed Web of Science ®Google Scholar
• Jamieson, L., L. Carpenter, T. J. Biden, and A. P. Fields. 1999. Protein kinase C iota activity is necessary for Bcr-Abl mediated resistance to drug-induced apoptosis. J. Biol. Chem. 274:3927–3930.
   PubMedGoogle Scholar
• Joberty, G., C. Petersen, L. Gao, and I. G. Macara. 2000. The cell-polarity protein Par5 links Par3 and atypical protein kinase C to cdc42. Nat. Cell Biol. 2:531–539.
   PubMed Web of Science ®Google Scholar
• Kadotani, M., T. Nishiuma, M. Nanahoshi, Y. Tsujishita, K. Ogita, S. I. Nakamura, U. Kikkawa, and Y. Asaoka. 1997. Characterization of tyrosine-phosphorylated delta isoform of protein kinase C isolated from Chinese hamster ovary cells. J. Biochem. 121:1047–1053.
   PubMedGoogle Scholar
• Kaplan, D. R., and F. A. Miller. 1997. Signal transduction by the neurotrophin receptors. Curr. Opin. Cell Biol. 9:213–221.
   PubMed Web of Science ®Google Scholar
• Kazanietz, M. G., L. B. Areces, A. Bahador, H. Mischak, J. Goodnight, J. F. Mushinski, and P. M. Blumberg. 1993. Characterization of ligand and substrate specificity for the calcium-dependent and calcium-independent protein kinase C isozymes. Mol. Pharmacol. 44:298–307.
   PubMed Web of Science ®Google Scholar
• Konishi, H., M. Tanaka, Y. Takemura, H. Matsuzaki, Y. Ono, U. Kikkawa, and Y. Nishizuka. 1997. Activation of protein kinase C by tyrosine phosphorylation in response to H202. Proc. Natl. Acad. Sci. USA 94:11233–11237.
   PubMed Web of Science ®Google Scholar
• Kuroda, S., N. Nakagawa, C. Tokunaga, K. Tatematsu, and K. Tanizawa. 1999. Mammalian homologue of the Caenorhabditis elegans UNC-76 protein involved in axonal outgrowth is a protein kinase C zeta interacting protein. J. Cell Biol. 144:403–411.
   PubMed Web of Science ®Google Scholar
• Lallena, M. J., M. T. Diaz-Meco, G. Bren, C. V. Paya, and J. Moscat. 1999. Activation of IkB kinase B by protein kinase C isoforms. Mol. Cell. Biol. 19:2180–2188.
   PubMedGoogle Scholar
• Lee, R. J., C. Albanese, R. J. Stenger, G. Watanabe, G. Inghirami, G. K. Haines, M. Webster, W. J. Muller, J. S. Brugge, R. J. Davis, and R. G. Pestell. 1999. pp60v-src induction of cyclin D1 requires collaborative interactions between the extracellular signal-regulated kinase, p38, and jun kinase pathways. J. Biol. Chem. 274:7341–7350.
   PubMed Web of Science ®Google Scholar
• Li, S., R. Seitz, and M. P. Lisanti. 1996. Phosphorylation of caveolin by src tyrosine kinases. J. Biol. Chem. 271:3863–3868.
   PubMedGoogle Scholar
• Li, W., H. Mischak, J. C. Yu, L. M. Wang, J. F. Mushinski, M. A. Heidaran, and J. H. Pierce. 1994. Tyrosine phosphorylation of protein kinase C delta in response to its activation. J. Biol. Chem. 269:2349–2352.
   PubMed Web of Science ®Google Scholar
• Li, W., X. H. Chen, C. A. Kelley, M. Alimandi, J. Zhang, Q. Chen, D. P. Bottaro, and J. H. Pierce. 1996. Identification of tyrosine 187 as a protein kinase C delta phosphorylation site. J. Biol. Chem. 271:26404–26409.
   PubMedGoogle Scholar
• Liu, Y., S. Witte, Y. C. Liu, M. Doyle, C. Elly, and A. Altman. 2000. Regulation of protein kinase C theta function during T cell activation by Lck-mediated tyrosine phosphorylation. J. Biol. Chem. 275:3603–3609.
   PubMed Web of Science ®Google Scholar
• Lloyd, E. D., and M. W. Wooten. 1992. MAP kinase is a component of the neurogenic pathway utilized by nerve growth factor in PC12 cells. J. Neurochem. 59:1099–1109.
   PubMedGoogle Scholar
• Meakin, S. O., J. I. S. 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 TrkA. A model for discriminating proliferation and differentiation. J. Biol. Chem. 274:9861–9870.
   PubMed Web of Science ®Google Scholar
• Mellor, H., and P. J. Parker. 1998. The extended protein kinase C superfamily. Biochem. J. 332:281–292.
   PubMed Web of Science ®Google Scholar
• Moscat, J., and M. T. Diaz-Meco. 2000. The atypical protein kinase Cs. Functional specificity mediated by specific protein adapters. EMBO Rep. 1:399–403.
   PubMed Web of Science ®Google Scholar
• Müller, G., M. Ayoub, P. Storz, J. Rennecke, D. Fabbro, and K. Pfizenmaier. 1995. PKCζ is a molecular switch in signal transduction of the TNF-a bifunctionally regulated by ceramide and arachidonic acid. EMBO J. 14:1961–1969.
   PubMedGoogle Scholar
• Newton, A. C.. 1997. Regulation of protein kinase C. Curr. Opin. Cell Biol. 9:161–167.
   PubMed Web of Science ®Google Scholar
• Nye, S. H., S. P. Squinto, D. Glass, T. N. Stitt, P. Hantzopoulos, M. J. Macchi, N. S. Lindsay, N. Y. Ip, and G. D. Yancopoulos. 1992. K252a and staurosporine selectively block autophosphorylation of neurotrophin-mediated responses. Mol. Biol. Cell 3:677–686.
   PubMed Web of Science ®Google Scholar
• O'Driscoll, K. R., K. K. Teng, D. Fabbro, L. A. Greene, and I. B. Weinstein. 1995. Selective translocation of protein kinase C delta in PC12 cells during nerve growth factor-induced neuritogenesis. Mol. Biol. Cell 6:449–458.
   PubMedGoogle Scholar
• Olivier, A. R., and P. J. Parker. 1994. Bombesin, platelet-derived growth factor, and diacylglycerol induce selective membrane association and down-regulation of protein kinase C isotypes in Swiss 3T3 cells. J. Biol. Chem. 269:2758–2763.
   PubMedGoogle Scholar
• Puls, A., S. Schimdt, F. Grawe, and S. Stabel. 1997. Interaction of protein kinase C zeta with ZIP, a novel protein kinase C binding protein. Proc. Natl. Acad. Sci. USA 94:6191–6196.
   PubMed Web of Science ®Google Scholar
• Rausch, D. M., G. Dickens, S. Doll, K. Fujita, S. Koizumi, B. B. Rudkin, M. Tocco, L. E. Eiden, and G. Guroff. 1989. Differentiation of PC12 cells with v-src: comparison with nerve growth factor. J. Neurosci. Res. 24:49–58.
   PubMedGoogle Scholar
• Rusanescu, G., H. Qi, S. M. Thomas, J. S. Brugge, and S. Halegoua. 1995. Calcium influx induces neurite outgrowth through a Src-Ras signaling cassette. Neuron 15:1415–1425.
   PubMed Web of Science ®Google Scholar
• Samuels, I. S., M. L. Seibenhener, K. B. W. Neidigh, and M. W. Wooten. 2001. Nerve growth factor stimulates the interaction of ZIP/p62 with atypical protein kinase C and targets endosomal localization: evidence for regulation of nerve growth factor-induced differentiation. J. Cell. Biochem. 82:452–466.
   PubMedGoogle Scholar
• Sanchez, P., G. De Carcer, I. V. Sandoval, J. Moscat, and M. T. Diaz-Meco. 1998. Localization of atypical protein kinase C isoforms into lysosome-targeted endosomes through interaction with p62. Mol. Cell. Biol. 18:3069–3080.
   PubMed Web of Science ®Google Scholar
• Sanz, L., P. Sanchez, M. J. Lallena, M. T. Diaz-Meco, and J. Moscat. 1999. The interaction of p62 with RIP links the atypical PKCs to NF-kappaB activation. EMBO J. 18:3044–3053.
   PubMed Web of Science ®Google Scholar
• Seibenhener, M. L., J. Roehm, W. O. White, K. B. W. Neidigh, M. L. Vandenplas, and M. W. Wooten. 1999. Identification of src as a novel atypical protein kinase C interacting protein. Mol. Cell Biol. Res. Commun. 2:28–31.
   PubMedGoogle Scholar
• Song, J. S., P. G. Swann, Z. Szallasi, U. Blank, P. M. Blumberg, and J. Rivera. 1998. Tyrosine phosphorylation-dependent and independent association of protein kinase C delta with Src family kinases in RBL-2H3 mast cell line: regulation of src family kinase activity by protein kinase C delta. Oncogene 16:3357–3368.
   PubMedGoogle Scholar
• Sun, X., F. Wu, R. Datta, S. Kharbanda, and D. Kufe. 2000. Interaction between protein kinase C delta and the c-Abl tyrosine kinase in the cellular response to oxidative stress. J. Biol. Chem. 275:7470–7473.
   PubMedGoogle Scholar
• Szallasi, Z., M. F. Denning, E. Chang, J. Rivera, S. H. Yuspa, C. Lehel, Z. Olah, W. B. Anderson, and P. M. Blumberg. 1995. Development of rapid approach to identification of tyrosine phosphorylation sites: application to PKCdelta phosphorylated upon activation of the high affinity receptor for IgE in rat basophilic leukemia cells. Biochem. Biophys. Res. Commun. 214:888–894.
   PubMedGoogle Scholar
• Szeberenyi, J., and P. Erhardt. 1994. Cellular components of nerve growth factor signaling. Biochim. Biophys. Acta 1222:87–202.
   Google Scholar
• Tanaka, C., and Y. Nishizuka. 1994. The protein kinase C family for neuronal signaling. Annu. Rev. Neurosci. 17:551–567.
   PubMed Web of Science ®Google Scholar
• Tapley, P., F. Lamballe, and M. Barbacid. 1992. K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7:371–381.
   PubMed Web of Science ®Google Scholar
• Uehara, Y., and H. Fukazawa. 1991. Use and selectivity of herbimycin A as an inhibitor of protein-tyrosine kinases. Methods Enzymol. 201:370–379.
   PubMed Web of Science ®Google Scholar
• VanRenterghem, B., M. D. Browning, and J. L. Maller. 1994. Regulation of mitogen-activated protein kinase activation by protein kinase A and C in a cell-free system. J. Biol. Chem. 269:24666–24672.
   PubMed Web of Science ®Google Scholar
• Vertommen, D., M. Rider, Y. Ni, E. Waelkens, W. Merlevede, J. R. Vanderheede, and J. Van Lin. 2000. Regulation of protein kinase D by multisite phosphorylation. J. Biol. Chem. 275:19567–19576.
   PubMed Web of Science ®Google Scholar
• Wang, Y., M. L. Seibenhener, M. L. Vandenplas, and M. W. Wooten. 1999. Atypical PKC zeta is activated by ceramide, resulting in co-activation of NF-kappaB/JNK kinase and cell survival. J. Neurosci. Res. 55:293–302.
   PubMed Web of Science ®Google Scholar
• Wong, B. R., D. Besser, N. Kim, J. R. Arron, M. Vologodskai, H. Hanafusa, and V. Choi. 1999. TRANCE, a TNF family member, activates Akt/PKB through a signaling complex involving TRAF6 and c-Src. Mol. Cell 4:1041–1049.
   PubMed Web of Science ®Google Scholar
• Wooten, M. W., M. L. Seibenhener, Y. Soh, S. Ewald, K. R. White, E. D. Lloyd, A. Olivier, and P. J. Parker. 1992. Characterization and differential expression of protein kinase C isoforms in PC12 cells. FEBS Lett. 298:74–78.
   PubMedGoogle Scholar
• Wooten, M. W., G. Zhou, M. L. Seibenhener, and E. S. Coleman. 1994. A role for zeta protein kinase C in nerve growth factor-induced differentiation of PC12 cells. Cell Growth Differ. 5:395–403.
   PubMedGoogle Scholar
• Wooten, M. W., G. Zhou, M. C. Wooten, and M. L. Siebenhener. 1997. Transport of protein kinase C isoforms to the nucleus of PC12 cells by nerve growth factor: association of atypical PKC-zeta with the nuclear matrix. J. Neurosci. Res. 49:393–403.
   PubMedGoogle Scholar
• Wooten, M. W., M. L. Seibenhener, G. Zhou, M. L. Vandenplas, and T. H. Tan. 1999. Overexpression of atypical PKC in PC12 cells enhances NGF responsiveness and survival through an NF-kappaB dependent pathway. Cell Death Differ. 6:753–764.
   PubMed Web of Science ®Google Scholar
• Wooten, M. W., M. L. Seibenhener, K. B. W. Neidigh, and M. L. Vandenplas. 2000. Mapping of atypical protein kinase C within the nerve growth factor signaling cascade: relationship to differentiation and survival of PC12 cells. Mol. Cell. Biol. 20:4494–4504.
   PubMed Web of Science ®Google Scholar
• Wooten, M. W., M. L. Seibenhener, V. Mamidipudi, M. T. Diaz-Meco, P. Barker, and J. Moscat. 2001. The atypical protein kinase C interacting protein p62 is a scaffold for NF-kappaB activation by nerve growth factor. J. Biol. Chem. 276:7709–7712.
   PubMed Web of Science ®Google Scholar
• Yen, A., S. Soong, H. J. Kwon, M. Yoshida, T. Beppu, and S. Varvayanis. 1994. Enhanced cell differentiation when RB is hypophosphorylated and down-regulated by radicicol, a src-kinase inhibitor. Exp. Cell Res. 214:163–171.
   PubMedGoogle Scholar
• Yu, H., J. K. Chen, S. Feng, D. C. Dalgarno, A. Brauer, and S. L. Schreiber. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76:933–945.
   PubMed Web of Science ®Google Scholar
• Yuan, Z.-M., T. Utsugisawa, T. Ishiko, S. Nakada, Y. Huang, S. Kharbanda, R. Weichselbaum, and D. Kufe. 1998. Activation of protein kinase C delta by the c-abl tyrosine kinase in response to ionizing radiation. Oncogene 16:1643–1648.
   PubMed Web of Science ®Google Scholar
• Zang, Q., Z. Lu, M. Curto, N. Barile, D. Shalloway, and D. A. Foster. 1997. Association between v-src and protein kinase C delta in v-src transformed fibroblasts. J. Biol. Chem. 272:13275–13280.
   PubMedGoogle Scholar
• Zhang, Y., D. B. Moheban, B. R. Conway, A. Bhattacharyya, and R. A. Segal. 2000. Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation. J. Neurosci. 20:5671–5678.
   PubMed Web of Science ®Google Scholar
• Zhou, G., M. L. Seibenhener, and M. W. Wooten. 1997. Nucleolin is a protein kinase C zeta substrate. J. Biol. Chem. 272:31130–31137.
   PubMedGoogle Scholar