Deciphering the Cross Talk between hnRNP K and c-Src: the c-Src Activation Domain in hnRNP K Is Distinct from a Second Interaction Site

REFERENCES

• Alexandropoulos, K., and D. Baltimore. 1996. Coordinate activation of c-Src by SH3- and SH2-binding sites on a novel, p130 Cas-related protein, Sin. Genes Dev. 10:1341–1355.
   PubMed Web of Science ®Google Scholar
• Alonso, G., M. Koegl, N. Mazurenko, and S. A. Courtneidge. 1995. Sequence requirements for binding of Src family tyrosine kinases to activated growth factor receptors. J. Biol. Chem. 270:9840–9848.
   PubMed Web of Science ®Google Scholar
• Ball, L. J., R. Kuhne, J. Schneider-Mergener, and H. Oschkinat. 2005. Recognition of proline-rich motifs by protein-protein-interaction domains. Angew. Chem. Int. Ed. Engl. 44:2852–2869.
   PubMed Web of Science ®Google Scholar
• Brown, M. T., and J. A. Cooper. 1996. Regulation, substrates and functions of Src. Biochim. Biophys. Acta 1287:121–149.
   PubMed Web of Science ®Google Scholar
• Burnham, M. R., P. J. Bruce-Staskal, M. T. Harte, C. L. Weidow, A. Ma, S. A. Weed, and A. H. Bouton. 2000. Regulation of c-SRC activity and function by the adapter protein CAS. Mol. Cell. Biol. 20:5865–5878.
   PubMed Web of Science ®Google Scholar
• Collier, B., L. Goobar-Larsson, M. Sokolowski, and S. Schwartz. 1998. Translational inhibition in vitro of human papillomavirus type 16 L2 mRNA mediated through interaction with heterogenous ribonucleoprotein K and poly(rC)-binding proteins 1 and 2. J. Biol. Chem. 273:22648–22656.
   PubMed Web of Science ®Google Scholar
• Craig, D., M. T. Howell, C. L. Gibbs, T. Hunt, and R. J. Jackson. 1992. Plasmid cDNA-directed protein synthesis in a coupled eukaryotic in vitro transcription-translation system. Nucleic Acids Res. 20:4987–4995.
   PubMedGoogle Scholar
• Dejgaard, K., and H. Leffers. 1996. Characterization of the nucleic-acid binding activity of KH domains. Different properties of different domains. Eur. J. Biochem. 241:425–431.
   PubMedGoogle Scholar
• Dreyfuss, G., V. N. Kim, and N. Kataoka. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3:195–205.
   PubMed Web of Science ®Google Scholar
• Dreyfuss, G., M. J. Matunis, S. Pinol-Roma, and C. G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289–321.
   PubMed Web of Science ®Google Scholar
• Erpel, T., G. Superti-Furga, and S. A. Courtneidge. 1995. Mutational analysis of the Src SH3 domain: the same residues of the ligand binding surface are important for intra- and intermolecular interactions. EMBO J. 14:963–975.
   PubMed Web of Science ®Google Scholar
• Evans, J. R., S. A. Mitchell, K. A. Spriggs, J. Ostrowski, K. Bomsztyk, D. H. Ostareck, and A. E. Willis. 2003. Members of the poly (rC) binding protein family stimulate the activity of the c-myc internal ribosome entry segment in vitro and in vivo. Oncogene 22:8012–8020.
   PubMed Web of Science ®Google Scholar
• Expert-Bezancon, A., L. P. Le Caer, and J. Marie. 2002. hnRNP K is a component of an intronic splicing enhancer complex that activates the splicing of the alternative exon 6A from chicken-beta-tropomyosin pre-mRNA. J. Biol. Chem. 277:16614–16623.
   PubMed Web of Science ®Google Scholar
• Feng, S., J. K. Chen, H. Yu, J. A. Simon, and S. L. Schreiber. 1994. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266:1241–1247.
   PubMed Web of Science ®Google Scholar
• Feng, S., C. Kasahara, R. J. Rickles, and S. L. Schreiber. 1995. Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc. Natl. Acad. Sci. USA 92:12408–12415.
   PubMed Web of Science ®Google Scholar
• Gonfloni, S., A. Weijland, J. Kretzschmar, and G. Superti-Furga. 2000. Crosstalk between the catalytic and the regulatory domains allows bidirectional regulation of Src. Nat. Struct. Biol. 7:281–286.
   PubMedGoogle Scholar
• Gonfloni, S., J. C. Williams, K. Hattula, A. Weijland, R. K. Wierenga, and G. Superti-Furga. 1997. The role of the linker between the SH2 domain and the catalytic domain in the regulation and function of Src. EMBO J. 16:7261–7271.
   PubMedGoogle Scholar
• Graham, F. L., and A. J. Van der Eb. 1973. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52:456–464.
   PubMed Web of Science ®Google Scholar
• Habelhah, H., K. Shah, L. Huang, A. Ostareck-Lederer, A. L. Burlingame, K. M. Shokat, M. W. Hentze, and Z. Ronai. 2001. Erk phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nat. Cell Biol. 3:325–330.
   PubMed Web of Science ®Google Scholar
• Hu, C. D., Y. Chinenov, and T. K. Kerppola. 2002. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9:789–798.
   PubMed Web of Science ®Google Scholar
• Hüttelmaier, S., S. Illenberger, I. Grosheva, M. Rüdiger, R. H. Singer, and B. M. Jockusch. 2001. Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins. J. Cell Biol. 155:775–786.
   PubMedGoogle Scholar
• Hüttelmaier, S., D. Zenklusen, M. Lederer, J. Dictenberg, M. Lorenz, X. Meng, G. J. Bassell, J. Condeelis, and R. H. Singer. 2005. Spatial regulation of β-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438:512–515.
   PubMed Web of Science ®Google Scholar
• Jackson., R. J., and T. Hunt. 1983. Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA. Methods Enzymol. 96:50–74.
   PubMed Web of Science ®Google Scholar
• Kato, J. Y., T. Takeya, C. Grandori, H. Iba, J. B. Levy, and H. Hanafusa. 1986. Amino acid substitutions sufficient to convert the nontransforming p60c-src protein to a transforming protein. Mol. Cell. Biol. 6:4155–4160.
   PubMed Web of Science ®Google Scholar
• Lee, C. H., B. Leung, M. A. Lemmon, J. Zheng, D. Cowburn, J. Kuriyan, and K. Saksela. 1995. A single amino acid in the SH3 domain of Hck determines its high affinity and specificity in binding to HIV-1 Nef protein. EMBO J. 14:5006–5015.
   PubMed Web of Science ®Google Scholar
• Levin, V. A. 2004. Basis and importance of Src as a target in cancer. Cancer Treat. Res. 119:89–119.
   PubMedGoogle Scholar
• Lim, W. A., F. M. Richards, and R. O. Fox. 1994. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature 372:375–379.
   PubMed Web of Science ®Google Scholar
• Lynch, M., L. Chen, M. J. Ravitz, S. Mehtani, K. Korenblat, M. J. Pazin, and E. V. Schmidt. 2005. hnRNP K binds a core polypyrimidine element in the eukaryotic translation initiation factor 4E (eIF4E) promoter, and its regulation of eIF4E contributes to neoplastic transformation. Mol. Cell. Biol. 25:6436–6453.
   PubMed Web of Science ®Google Scholar
• Messias, A. C., C. Harnisch, A. Ostareck-Lederer, M. Sattler, and D. H. Ostareck. 2006. The DICE-binding activity of KH domain 3 of hnRNP K is affected by c-Src mediated tyrosine phosphorylation. J. Mol. Biol. 361:470–481.
   PubMedGoogle Scholar
• Michael, W. M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell 83:415–422.
   PubMed Web of Science ®Google Scholar
• Michael, W. M., P. S. Eder, and G. Dreyfuss. 1997. The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO J. 16:3587–3598.
   PubMed Web of Science ®Google Scholar
• Michelotti, E. F., G. A. Michelotti, A. I. Aronsohn, and D. Levens. 1996. Heterogeneous ribonucleoprotein K is a transcription factor. Mol. Cell. Biol. 6:2350–2360.
   Google Scholar
• Moarefi, I., F. Lafevre-Bernt, F. Sicheri, M. Huse, C.-H. Lee, J. Kuriyan, and W. T. Miller. 1997. Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385:650–653.
   PubMed Web of Science ®Google Scholar
• Mori, S., L. Rönnstrand, K. Yokote, A. Engström, S. A. Courtneidge, L. Claesson-Welsh, and C. H. Heldin. 1993. Identification of two juxtamembrane autophosphorylation sites in the PDGF beta-receptor; involvement in the interaction with Src family tyrosine kinases. EMBO J. 12:2257–2264.
   PubMed Web of Science ®Google Scholar
• Nagai, T., K. Ibata, E. S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20:87–90.
   PubMed Web of Science ®Google Scholar
• Ostareck, D. H., A. Ostareck-Lederer, I. N. Shatsky, and M. W. Hentze. 2001. Lipoxygenase mRNA silencing in erythroid differentiation: the 3′UTR regulatory complex controls 60S ribosomal subunit joining. Cell 104:281–290.
   PubMed Web of Science ®Google Scholar
• Ostareck, D. H., A. Ostareck-Lederer, M. Wilm, B. J. Thiele, M. Mann, and M. W. Hentze. 1997. mRNA silencing in erythroid maturation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89:597–606.
   PubMed Web of Science ®Google Scholar
• Ostareck-Lederer, A., and D. H. Ostareck. 2004. Control of mRNA translation and stability in haematopoietic cells: the function of hnRNPs K and E1/E2. Biol. Cell 96:407–411.
   PubMed Web of Science ®Google Scholar
• Ostareck-Lederer, A., D. H. Ostareck, C. Cans, G. Neubauer, K. Bomsztyk, G. Superti-Furga, and M. W. Hentze. 2002. c-Src mediated phosphorylation of hnRNP K drives translation activation of specifically silenced mRNAs. Mol. Cell. Biol. 22:4535–4543.
   PubMed Web of Science ®Google Scholar
• Ostareck-Lederer, A., D. H. Ostareck, K. P. Rücknagel, A. Schierhorn, B. Moritz, S. Hüttelmaier, N. Flach, L. Handoko, and E. Wahle. 2006. Asymmetric arginine dimethylation of hnRNP K by PRMT1 inhibits its interaction with c-Src. J. Biol. Chem. 281:11115–11125.
   PubMed Web of Science ®Google Scholar
• Ostrowski, J., D. S. Schullery, O. N. Denisenko, Y. Higaki, J. Watts, R. Aebersold, M. Stempka, M. Geschwendt, and K. Bomsztyk. 2000. Role of tyrosine phosphorylation in the regulation of the interaction of heterogenous nuclear ribonucleoprotein K protein with its protein and RNA partners. J. Biol. Chem. 275:3619–3628.
   PubMed Web of Science ®Google Scholar
• Ostrowski, J., Y. Kawata, D. S. Schullery, O. N. Denisenko, and K. Bomsztyk. 2003. Transient recruitment of the hnRNP K protein to inducibly transcribed gene loci. Nucleic Acids Res. 14:3954–3962.
   Google Scholar
• Parang, K., and G. Sun. 2004. Design strategies for protein kinase inhibitors. Curr. Opin. Drug Discov. Dev. 7:617–629.
   PubMed Web of Science ®Google Scholar
• Persson, P. B., A. Skalweit, R. Mrowka, and B. J. Thiele. 2003. Control of renin synthesis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285:R491–R497.
   PubMedGoogle Scholar
• Skalweit, A., A. Doller, A. Huth, T. Kahne, P. B. Persson, and B. J. Thiele. 2003. Posttranscriptional control of renin synthesis: identification of proteins interacting with renin mRNA 3′-untranslated region. Circ. Res. 92:419–427.
   PubMedGoogle Scholar
• Smart, J. E., H. Oppermann, A. P. Czernilofsky, A. F. Purchio, R. L. Erikson, and J. M. Bishop. 1981. Characterization of sites for tyrosine phosphorylation in the transforming protein of Rous sarcoma virus (pp60v-src) and its normal cellular homologue (pp60c-src). Proc. Natl. Acad. Sci. USA 78:6013–6017.
   PubMed Web of Science ®Google Scholar
• Superti-Furga, G., and S. Courtneidge. 1995. Structure-function relationships in Src family and related protein tyrosine kinases. Bioessays 17:321–330.
   PubMed Web of Science ®Google Scholar
• Takimoto, M., T. Tomonaga, M. Matunis, M. Avigan, and H. Krutzsch. 1993. Specific binding of heterogeneous ribonucleoprotein particle protein K to the human c-myc promoter, in vitro. J. Biol. Chem. 268:18249–18258.
   PubMed Web of Science ®Google Scholar
• Taylor, S. J., and D. Shalloway. 1994. An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature 368:867–871.
   PubMed Web of Science ®Google Scholar
• Thomas, S. M., and J. S. Brugge. 1997. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13:513–609.
   PubMed Web of Science ®Google Scholar
• Tilbrook, P. A., E. Ingley, J. H. Williams, M. L. Hibbs, and S. P. Klinken. 1997. Lyn tyrosine kinase is essential for erythropoietin-induced differentiation of J2E erythroid cells. EMBO J. 16:1610–1619.
   PubMed Web of Science ®Google Scholar
• Trible, R. P., L. Emert-Sedlak, and T. Smithgall. 2006. HIV-1 NEF selectively activates Src family kinases Hck, Lyn, and c-Src through direct SH3 domain interaction. J. Biol. Chem. 281:27029–27038.
   PubMed Web of Science ®Google Scholar
• Van Seuningen, I., J. Ostrowski, X. R. Bustelo, P. R. Sleath, and K. Bomsztyk. 1995. The K protein domain that recruits the interleukin 1-responsive K protein kinase lies at adjacent to a cluster of c-Src and Vav SH3-binding sites. Implications that K protein acts as a docking platform. J. Biol. Chem. 270:26976–26985.
   PubMed Web of Science ®Google Scholar
• Weng, Z., S. M. Thomas, J. J. Rickles, J. A. Taylor, A. W. Brauer, C. Seidel-Dugan, M. W. Michael, G. Dreyfuss, and J. S. Brugge. 1994. Identification of Src, Fyn, and Lyn SH3-binding proteins: implications for a function of SH3 domains. Mol. Cell. Biol. 14:4509–4521.
   PubMed Web of Science ®Google Scholar
• Williams, J. C., A. Weijland, S. Gonfloni, A. Thompson, S. A. Courtneidge, G. Superti-Furga, and R. K. Wierenga. 1997. The 2.35 Å crystal structure of the inactivated form of chicken Src: a dynamic molecule with multiple regulatory interactions. J. Mol. Biol. 274:757–775.
   PubMed Web of Science ®Google Scholar
• Wu, X., B. B. Knudsen, S. M. Feller, J. Zheng, A. Sali, D. Cowburn, H. Hanafusa, and J. Kuriyan. 1995. Structural basis for the specific interaction of lysine-containing proline-rich peptides with the N-terminal SH3 domain of c-Crk. Structure 3:215–226.
   PubMed Web of Science ®Google Scholar
• Xu, W., A. Doshi, M. Lei, M. J. Eck, and S. C. Harrison. 1999. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3:629–638.
   PubMed Web of Science ®Google Scholar
• Xu, W., S. C. Harrison, and M. J. Eck. 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385:595–602.
   PubMed Web of Science ®Google Scholar
• Yao, J., Y. Sasaki, Z. Wen, G. J. Bassell, and J. Q. Zheng. 2006. An essential role for β-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat. Neurosci. 10:1265–1273.
   Google Scholar
• Yurchak, L. K., and B. Sefton. 1995. Palmitoylation of either Cys-3 or Cys-5 is required for the biological activity of the Lck tyrosine protein kinase. Mol. Cell. Biol. 15:6914–6922.
   PubMed Web of Science ®Google Scholar
• Zheng, X. M., Y. Wang, and C. J. Pallen. 1992. Cell transformation and activation of pp60c-src by overexpression of a protein tyrosine phosphatase. Nature 359:336–339.
   PubMed Web of Science ®Google Scholar