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Cell Growth and Development

A Unique Autophosphorylation Site on Tie2/Tek Mediates Dok-R Phosphotyrosine Binding Domain Binding and Function

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Pages 2658-2668 | Received 11 Sep 2002, Accepted 22 Jan 2003, Published online: 27 Mar 2023

REFERENCES

  • Asahara, T., D. Chen, T. Takahashi, K. Fujikawa, M. Kearney, M. Magner, G. D. Yancopoulos, and J. M. Isner. 1998. Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circ. Res. 83: 233–240.
  • Blaikie, P., D. Immanuel, J. Wu, N. Li, V. Yajnik, and B. Margolis. 1994. A region in Shc distinct from the SH2 domain can bind tyrosine-phosphorylated growth factor receptors. J. Biol. Chem. 269: 32031–32034.
  • Borg, J. P., J. Ooi, E. Levy, and B. Margolis. 1996. The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol. Cell. Biol. 16: 6229–6241.
  • Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655–1657.
  • Carpino, N., D. Wisniewski, A. Strife, D. Marshak, R. Kobayashi, B. Stillman, and B. Clarkson. 1997. p62(dok): a constitutively tyrosine-phosphorylated, GAP-associated protein in chronic myelogenous leukemia progenitor cells. Cell 88: 197–204.
  • Charest, A., J. Wagner, S. Jacob, C. J. McGlade, and M. L. Tremblay. 1996. Phosphotyrosine-independent binding of SHC to the NPLH sequence of murine protein-tyrosine phosphatase-PEST. Evidence for extended phosphotyrosine binding/phosphotyrosine interaction domain recognition specificity. J. Biol. Chem. 271: 8424–8429.
  • Chien, C. T., S. Wang, M. Rothenberg, L. Y. Jan, and Y. N. Jan. 1998. Numb-associated kinase interacts with the phosphotyrosine binding domain of Numb and antagonizes the function of Numb in vivo. Mol. Cell. Biol. 18: 598–607.
  • Cong, F., B. Yuan, and S. P. Goff. 1999. Characterization of a novel member of the DOK family that binds and modulates Abl signaling. Mol. Cell. Biol. 19: 8314–8325.
  • D'Amore, P. A. 1992. Capillary growth: a two-cell system. Semin. Cancer Biol. 3: 49–56.
  • Davis, S., T. H. Aldrich, P. F. Jones, A. Acheson, D. L. Compton, V. Jain, T. E. Ryan, J. Bruno, C. Radziejewski, P. C. Maisonpierre, and G. D. Yancopoulos. 1996. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87: 1161–1169.
  • Dho, S. E., S. Jacob, C. D. Wolting, M. B. French, L. R. Rohrschneider, and C. J. McGlade. 1998. The mammalian numb phosphotyrosine-binding domain. Characterization of binding specificity and identification of a novel PDZ domain-containing numb binding protein, LNX. J. Biol. Chem. 273: 9179–9187.
  • Di Cristofano, A., N. Carpino, N. Dunant, G. Friedland, R. Kobayashi, A. Strife, D. Wisniewski, B. Clarkson, P. P. Pandolfi, and M. D. Resh. 1998. Molecular cloning and characterization of p56dok-2 defines a new family of RasGAP-binding proteins. J. Biol. Chem. 273: 4827–4830.
  • Dumont, D. J., G. Gradwohl, G. H. Fong, M. C. Puri, M. Gertsenstein, A. Auerbach, and M. L. Breitman. 1994. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes. Dev. 8: 1897–1909.
  • Ferguson, K. M., J. M. Kavran, V. G. Sankaran, E. Fournier, S. J. Isakoff, E. Y. Skolnik, and M. A. Lemmon. 2000. Structural basis for discrimination of 3-phosphoinositides by pleckstrin homology domains. Mol. Cell 6: 373–384.
  • Fujikawa, K., I. de Aos Scherpenseel, S. K. Jain, E. Presman, and L. Varticovski. 1999. Role of PI 3-kinase in angiopoietin-1-mediated migration and attachment-dependent survival of endothelial cells. Exp. Cell Res. 253: 663–672.
  • Garrity, P. A., Y. Rao, I. Salecker, J. McGlade, T. Pawson, and S. L. Zipursky. 1996. Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 85: 639–650.
  • Grimm, J., M. Sachs, S. Britsch, S. Di Cesare, T. Schwarz-Romond, K. Alitalo, and W. Birchmeier. 2002. Novel p62dok family members, dok-4 and dok-5, are substrates of the c-Ret receptor tyrosine kinase and mediate neuronal differentiation. J. Cell Biol. 154: 345–354.
  • Gustafson, T. A., W. He, A. Craparo, C. D. Schaub, and T. J. O'Neill. 1995. Phosphotyrosine-dependent interaction of SHC and insulin receptor substrate 1 with the NPEY motif of the insulin receptor via a novel non-SH2 domain. Mol. Cell. Biol. 15: 2500–2508.
  • Hayes, A. J., W. Q. Huang, J. Mallah, D. Yang, M. E. Lippman, and L. Y. Li. 1999. Angiopoietin-1 and its receptor tie-2 participate in the regulation of capillary-like tubule formation and survival of endothelial cells. Microvasc. Res. 58: 224–237.
  • Hing, H., J. Xiao, N. Harden, L. Lim, and S. L. Zipursky. 1999. Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97: 853–863.
  • Hosooka, T., T. Noguchi, H. Nagai, T. Horikawa, T. Matozaki, M. Ichihashi, and M. Kasuga. 2002. Inhibition of the motility and growth of B16F10 mouse melanoma cells by dominant negative mutants of Dok-1. Mol. Cell. Biol. 21: 5437–5546.
  • Jones, N., and D. J. Dumont. 1998. The Tek/Tie2 receptor signals through a novel Dok-related docking protein, Dok-R. Oncogene 17: 1097–1108.
  • Jones, N., and D. J. Dumont. 1999. Recruitment of Dok-R to the EGF receptor through its PTB domain is required for attenuation of erk MAP kinase activation. Curr. Biol. 9: 1057–1060.
  • Jones, N., Z. Master, J. Jones, D. Bouchard, Y. Gunji, H. Sasaki, R. Daly, K. Alitalo, and D. J. Dumont. 1999. Identification of Tek/Tie2 binding partners. Binding to a multifunctional docking site mediates cell survival and migration. J. Biol. Chem. 274: 30896–30905.
  • Jones, N., D. Voskas, Z. Master, R. Sarao, J. Jones, and D. J. Dumont. 2001. Rescue of the early vascular defects in Tek/Tie2 null mice reveals an essential survival function. EMBO Rep. 2: 438–445.
  • Kavanaugh, W. M., C. W. Turck, and L. T. Williams. 1995. PTB domain binding to signaling proteins through a sequence motif containing phosphotyrosine. Science 268: 1177–1179.
  • Kavanaugh, W. M., and L. T. Williams. 1994. An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science 266: 1862–1865.
  • Koblizek, T. I., C. Weiss, G. D. Yancopoulos, U. Deutsch, and W. Risau. 1998. Angiopoietin-1 induces sprouting angiogenesis in vitro. Curr. Biol. 8: 529–532.
  • Kontos, C. D., T. P. Stauffer, W. P. Yang, J. D. York, L. Huang, M. A. Blanar, T. Meyer, and K. G. Peters. 1998. Tyrosine 1101 of Tie2 is the major site of association of p85 and is required for activation of phosphatidylinositol 3-kinase and Akt. Mol. Cell. Biol. 18: 4131–4140.
  • Kulkarni, S. V., G. Gish, P. van der Geer, M. Henkemeyer, and T. Pawson. 2000. Role of p120 Ras-GAP in directed cell movement. J. Cell Biol. 149: 457–470.
  • Kwak, H. J., J. N. So, S. J. Lee, I. Kim, and G. Y. Koh. 1999. Angiopoietin-1 is an apoptosis survival factor for endothelial cells. FEBS Lett. 448: 249–253.
  • Lemay, S., D. Davidson, S. Latour, and A. Veillette. 2000. Dok-3, a novel adapter molecule involved in the negative regulation of immunoreceptor signaling. Mol. Cell. Biol. 20: 2743–2754.
  • Li, S. C., Z. Songyang, S. J. Vincent, C. Zwahlen, S. Wiley, L. Cantley, L. E. Kay, J. Forman-Kay, and T. Pawson. 1997. High-affinity binding of the Drosophila Numb phosphotyrosine-binding domain to peptides containing a Gly-Pro-(p)Tyr motif. Proc. Natl. Acad. Sci. USA 94: 7204–7209.
  • Liang, X., D. Wisniewski, A. Strife, Shivakrupa, B. Clarkson, and M. D. Resh. 2002. Phosphatidylinositol 3-kinase and Src family kinases are required for phosphorylation and membrane recruitment of Dok-1 in c-Kit signaling. J. Biol. Chem. 277: 13732–13738.
  • Maisonpierre, P. C., C. Suri, P. F. Jones, S. Bartunkova, S. J. Wiegand, C. Radziejewski, D. Compton, J. McClain, T. H. Aldrich, N. Papadopoulos, T. J. Daly, S. Davis, T. N. Sato, and G. D. Yancopoulos. 1997. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55–60.
  • Master, Z., N. Jones, J. Tran, J. Jones, R. S. Kerbel, and D. J. Dumont. 2001. Dok-R plays a pivotal role in angiopoietin-1-dependent cell migration through recruitment and activation of Pak. EMBO J. 20: 5919–5928.
  • McGlade, J., B. Brunkhorst, D. Anderson, G. Mbamalu, J. Settleman, S. Dedhar, M. Rozakis-Adcock, L. B. Chen, and T. Pawson. 1993. The N-terminal region of GAP regulates cytoskeletal structure and cell adhesion. EMBO J. 12: 3073–3081.
  • Mochizuki, Y., T. Nakamura, H. Kanetake, and S. Kanda. 2002. Angiopoietin 2 stimulates migration and tube-like structure formation of murine brain capillary endothelial cells through c-Fes and c-Fyn. J. Cell Sci. 115: 175–183.
  • Murray, B. W., E. S. Padrique, C. Pinko, and M. A. McTigue. 2002. Mechanistic effects of autophosphorylation on receptor tyrosine kinase catalysis: enzymatic characterization of Tie2 and phospho-Tie2. Biochemistry 40: 10243–10253.
  • Nelms, K., A. L. Snow, J. Hu-Li, and W. E. Paul. 1998. FRIP, a hematopoietic cell-specific rasGAP-interacting protein phosphorylated in response to cytokine stimulation. Immunity 9: 13–24.
  • Noguchi, T., T. Matozaki, K. Inagaki, M. Tsuda, K. Fukunaga, Y. Kitamura, T. Kitamura, K. Shii, Y. Yamanashi, and M. Kasuga. 1999. Tyrosine phosphorylation of p62(Dok) induced by cell adhesion and insulin: possible role in cell migration. EMBO J. 18: 1748–1760.
  • Ong, S. H., G. R. Guy, Y. R. Hadari, S. Laks, N. Gotoh, J. Schlessinger, and I. Lax. 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.
  • Papapetropoulos, A., G. Garcia-Cardena, T. J. Dengler, P. C. Maisonpierre, G. D. Yancopoulos, and W. C. Sessa. 1999. Direct actions of angiopoietin-1 on human endothelium: evidence for network stabilization, cell survival, and interaction with other angiogenic growth factors. Lab. Investig. 79: 213–223.
  • Patan, S. 1998. TIE1 and TIE2 receptor tyrosine kinases inversely regulate embryonic angiogenesis by the mechanism of intussusceptive microvascular growth. Microvasc. Res. 56: 1–21.
  • Pawson, T., and J. D. Scott. 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science 278: 2075–2080.
  • Puri, M. C., J. Partanen, J. Rossant, and A. Bernstein. 1999. Interaction of the TEK and TIE receptor tyrosine kinases during cardiovascular development. Development 126: 4569–4580.
  • Risau, W., H. Sariola, H. G. Zerwes, J. Sasse, P. Ekblom, R. Kemler, and T. Doetschman. 1988. Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development 102: 471–478.
  • Sato, A., A. Iwama, N. Takakura, H. Nishio, G. D. Yancopoulos, and T. Suda. 1998. Characterization of TEK receptor tyrosine kinase and its ligands, angiopoietins, in human hematopoietic progenitor cells. Int. Immunol. 10: 1217–1227.
  • Sato, T. N., Y. Tozawa, U. Deutsch, K. Wolburg-Buchholz, Y. Fujiwara, M. Gendron-Maguire, T. Gridley, H. Wolburg, W. Risau, and Y. Qin. 1995. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376: 70–74.
  • Sattler, M., S. Verma, Y. B. Pride, R. Salgia, L. R. Rohrschneider, and J. D. Griffin. 2001. SHIP1, an SH2 domain containing polyinositol-5-phosphatase, regulates migration through two critical tyrosine residues and forms a novel signaling complex with DOK1 and CRKL. J. Biol. Chem. 276: 2451–2458.
  • Shewchuk, L. M., A. M. Hassell, B. Ellis, W. D. Holmes, R. Davis, E. L. Horne, S. H. Kadwell, D. D. McKee, and J. T. Moore. 2000. Structure of the Tie2 RTK domain: self-inhibition by the nucleotide binding loop, activation loop, and C-terminal tail. Struct. Fold. Design 8: 1105–1113.
  • Songyang, Z., Y. Yamanashi, D. Liu, and D. Baltimore. 2001. Domain-dependent function of the rasGAP-binding protein p62Dok in cell signaling. J. Biol. Chem. 276: 2459–2465.
  • Stoletov, K. V., K. E. Ratcliffe, S. C. Spring, and B. I. Terman. 2001. NCK and PAK participate in the signaling pathway by which vascular endothelial growth factor stimulates the assembly of focal adhesions. J. Biol. Chem. 276: 22748–22755.
  • Suri, C., P. F. Jones, S. Patan, S. Bartunkova, P. C. Maisonpierre, S. Davis, T. N. Sato, and G. D. Yancopoulos. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87: 1171–1180.
  • Tallquist, M. D., P. Soriano, and R. A. Klinghoffer. 1999. Growth factor signaling pathways in vascular development. Oncogene 18: 7917–7932.
  • Tamir, I., J. C. Stolpa, C. D. Helgason, K. Nakamura, P. Bruhns, M. Daeron, and J. C. Cambier. 2000. The RasGAP-binding protein p62dok is a mediator of inhibitory FcgammaRIIB signals in B cells. Immunity 12: 347–358.
  • Teichert-Kuliszewska, K., P. C. Maisonpierre, N. Jones, A. I. Campbell, Z. Master, M. P. Bendeck, K. Alitalo, D. J. Dumont, G. D. Yancopoulos, and D. J. Stewart. 2001. Biological action of angiopoietin-2 in a fibrin matrix model of angiogenesis is associated with activation of Tie2. Cardiovasc. Res. 49: 659–670.
  • Valenzuela, D. M., J. A. Griffiths, J. Rojas, T. H. Aldrich, P. F. Jones, H. Zhou, J. McClain, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, T. Huang, N. Papadopoulos, P. C. Maisonpierre, S. Davis, and G. D. Yancopoulos. 1999. Angiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proc. Natl. Acad. Sci. USA 96: 1904–1909.
  • van der Geer, P., S. Wiley, G. D. Gish, V. K. Lai, R. Stephens, M. F. White, D. Kaplan, and T. Pawson. 1996. Identification of residues that control specific binding of the Shc phosphotyrosine-binding domain to phosphotyrosine sites. Proc. Natl. Acad. Sci. USA 93: 963–968.
  • Williams, R. L., S. A. Courtneidge, and E. F. Wagner. 1988. Embryonic lethalities and endothelial tumors in chimeric mice expressing polyoma virus middle T oncogene. Cell 52: 121–131.
  • Witzenbichler, B., P. C. Maisonpierre, P. Jones, G. D. Yancopoulos, and J. M. Isner. 1998. Chemotactic properties of angiopoietin-1 and -2, ligands for the endothelial-specific receptor tyrosine kinase Tie2. J. Biol. Chem. 273: 18514–18521.
  • Xu, H., K. W. Lee, and M. Goldfarb. 1998. Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J. Biol. Chem. 273: 17987–17990.
  • Yaffe, M. B. 2002. Phosphotyrosine-binding domains in signal transduction. Nat. Rev. Mol. Cell Biol. 3: 177–186.
  • Yamanashi, Y., and D. Baltimore. 1997. Identification of the Abl- and rasGAP-associated 62 kDa protein as a docking protein, Dok. Cell 88: 205–211.
  • Yancopoulos, G. D., S. Davis, N. W. Gale, J. S. Rudge, S. J. Wiegand, and J. Holash. 2000. Vascular-specific growth factors and blood vessel formation. Nature 407: 242–248.
  • Zhao, M., A. A. Schmitz, Y. Qin, A. Di Cristofano, P. P. Pandolfi, and L. Van Aelst. 2001. Phosphoinositide 3-kinase-dependent membrane recruitment of p62(dok) is essential for its negative effect on mitogen-activated protein (MAP) kinase activation. J. Exp. Med. 194: 265–274.
  • Zhou, M. M., B. Huang, E. T. Olejniczak, R. P. Meadows, S. B. Shuker, M. Miyazaki, T. Trub, S. E. Shoelson, and S. W. Fesik. 1996. Structural basis for IL-4 receptor phosphopeptide recognition by the IRS-1 PTB domain. Nat. Struct. Biol. 3: 388–393.

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