26
Views
158
CrossRef citations to date
0
Altmetric
Cell Growth and Development

The Gab1 PH Domain Is Required for Localization of Gab1 at Sites of Cell-Cell Contact and Epithelial Morphogenesis Downstream from the Met Receptor Tyrosine Kinase

, , , , , & show all
Pages 1784-1799 | Received 10 Aug 1998, Accepted 30 Nov 1998, Published online: 27 Mar 2023

REFERENCES

  • Auger, K. R., L. A. Serunian, S. P. Soltoff, P. Libby, and J. Cantley 1989. PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells. Cell 57:167–175.
  • Backer, J. M., M. J. Myers Jr., S. E. Shoelson, D. J. Chin, X. J. Sun, M. Miralpeix, P. Hu, B. Margolis, E. Y. Skolnik, and J. Schlessinger 1992. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11:3469–3479.
  • Bardelli, A., P. Longati, D. Gramaglia, M. C. Stella, and J. Comoglio 1997. Gab1 coupling to the HGF/Met receptor multifunctional docking site requires binding of Grb2 and correlates with the transforming potential. Oncogene 15:3103–3111.
  • Bellusci, S., G. Moens, G. Gaudino, P. Comoglio, T. Nakamura, J. P. Thiery, and J. Jouanneau 1994. Creation of an hepatocyte growth factor/scatter factor autocrine loop in carcinoma cells induces invasive properties associated with increased tumorigenicity. Oncogene 9:1091–1099.
  • Burks, D. J., S. Pons, H. Towery, J. Smith-Hall, M. G. Myers Jr., L. Yenush, and J. White 1997. Heterologous pleckstrin homology domains do not couple IRS-1 to the insulin receptor. J. Biol. Chem. 272:27716–27721.
  • Carpino, N., D. Wisniewski, A. Strife, D. Marshak, R. Kobayashi, B. Stillman, and J. Clarkson 1997. p62dok: A constitutively tyrosine-phosphorylated, GAP-associated protein in chronic myelogenous leukemia progenitor cells. Cell 88:197–204.
  • Chen, R. H., S. Corbalan-Garcia, and J. Bar-Sagi 1997. The role of the PH domain in the signal-dependent membrane targeting of Sos. EMBO J. 16:1351–1359.
  • Derman, M. P., M. J. Cunha, E. J. Barros, S. K. Nigam, and J. Cantley 1995. HGF-mediated chemotaxis and tubulogenesis require activation of the phosphatidylinositol 3-kinase. Am. J. Physiol. 268:1211–1217.
  • Ebens, A., K. Brose, E. D. Leonardo, M. G. Jr. Hanson, F. Bladt, C. Birchmeier, B. A. Barres, and J. Tessier-Lavigne 1996. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17:1157–1172.
  • Falasca, M., S. K. Logan, V. P. Lehto, G. Baccante, M. A. Lemmon, and J. Schlessinger 1988. Activation of phospholipase Cγ by PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO J. 17:414–422.
  • Faletto, D. L., D. R. Kaplan, D. O. Halverson, E. M. Rosen, and J. Vande Woude 1993. Signal transduction in c-met mediated motogenesis. Hepatocyte growth factor: scatter factor. EXS 65:107–130.
  • Ferguson, K. M., M. A. Lemmon, J. Schlessinger, and J. Sigler 1995. Structure of the high affinity complex of inositol triphosphate with a phospholipase C pleckstrin homology domain. Cell 83:1037–1046.
  • Fixman, E. D., T. M. Fournier, D. M. Kamikura, M. A. Naujokas, and J. Park 1996. Pathways downstream of Shc and Grb2 are required for cell transformation by the Tpr-Met oncoprotein. J. Biol. Chem. 271:13116–13122.
  • Fixman, E. D., M. Holgado-Madruga, L. Nguyen, D. M. Kamikura, T. M. Fournier, A. J. Wong, and J. Park 1997. Efficient cellular transformation by the Met oncoprotein requires a functional Grb2 binding site and correlates with phosphorylation of the Grb2-associated proteins Cbl and Gab1. J. Biol. Chem. 272:20167–20172.
  • Fixman, E. D., M. A. Naujokas, G. A. Rodrigues, M. F. Moran, and J. Park 1995. Efficient cell transformation by the Tpr-Met oncoprotein is dependent upon tyrosine 489 in the carboxy-terminus. Oncogene 10:237–249.
  • Fixman, E. D., I. Royal, and M. Park. Unpublished observations.
  • Fournier, T., D. Kamikura, K. Teng, and J. Park 1996. Branching tubulogenesis, but not scatter of Madin-Darby canine kidney cells requires a functional Grb2 binding site in the Met receptor tyrosine kinase. J. Biol. Chem. 271:22211–22217.
  • Franke, T. F., D. R. Kaplan, L. C. Cantley, and J. Toker 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275:665–668.
  • Frech, M., M. Andjelkovic, E. Ingley, K. K. Reddy, J. R. Falck, and J. Hemmings 1997. High affinity binding of inositol phosphates and phosphoinositides to the pleckstrin homology domain of RAC/protein kinase B and their influence on kinase activity. J. Biol. Chem. 272:84474–84481.
  • Garcia, P., R. Gupta, S. Shah, A. J. Morris, S. A. Rudge, S. Scarlata, V. Petrova, S. McLaughlin, and J. Rebecchi 1995. The pleckstrin homology domain of phospholipase C-δ1 binds with high affinity to phosphatidylinositol 4,5-biphosphate in bilayer membranes. Biochemistry 34:16228–16234.
  • Gibson, T. J., M. Hyvönen, A. Musacchio, M. Saraste, and J. Birney 1994. PH domain: the first anniversary. Trends Biochem. Sci. 19:349–353.
  • Grant, D. S., H. K. Kleinman, I. D. Goldberg, M. M. Bhargava, B. J. Nickoloff, J. L. Kinsella, P. Polverini, and J. Rosen 1993. Scatter factor induces blood vessel formation in vivo. Proc. Natl. Acad. Sci. USA 90:1937–1941.
  • Harlan, J. E., P. J. Hajduk, H. S. Yoon, and J. Fesik 1994. Pleckstrin homology domains bind to phosphatidylinositol 4,5-bisphosphate. Nature 371:168–170.
  • Herbst, R., P. M. Caroll, J. D. Allard, J. Schilling, T. Raabe, and J. Simon 1996. Daughter of sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during sevenless signaling. Cell 85:899–909.
  • Holgado-Madruga, M., D. R. Emlet, D. K. Moscatello, A. K. Godwin, and J. Wong 1996. A Grb2-associated docking protein in EGF- and insulin-receptor signaling. Nature 379:560–564.
  • Holgado-Madruga, M., D. K. Moscatello, D. R. Emlet, R. Dieterich, and J. Wong 1997. Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc. Natl. Acad. Sci. USA 94:12419–12424.
  • Holgado-Madruga, M., and A. J. Wong. Submitted for publication.
  • Hordijk, P. L., J. P. ten Klooster, R. A. van der Kammen, F. Michiels, L. C. Oomen, and J. Collard 1997. Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 278:1464–1466.
  • Hu, Q., A. Klippel, A. J. Muslin, W. J. Fantl, and J. Williams 1995. Ras-dependent induction of cellular responses by constitutively active phosphatidylinositol-3 kinase. Science 268:100–102.
  • Hyvönen, M., M. J. Macias, M. Nilges, H. Oschkinat, M. Saraste, and J. Wilmanns 1995. Structure of the binding site for inositol phosphates in a PH domain. EMBO J. 14:4676–4685.
  • Kan, M., G. Zhang, R. Zarnegar, G. Michalopoulos, Y. Myoken, W. L. McKeehan, and J. Stevens 1991. Hepatocyte growth factor/hepatopoietin A stimulates the growth of rat kidney proximal tubule epithelial cells (RPTE), rat nonparenchymal liver cells, human melanoma cells, mouse keratinocytes and stimulates anchorage-independent growth of SV-40 transformed RPTE. Biochem. Biophys. Res. Commun. 174:331–337.
  • Khwaja, A., K. Lehmann, B. M. Marte, and J. Downward 1998. Phosphoinositide 3-kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J. Biol. Chem. 273:18793–18801.
  • Klippel, A., J. A. Escobedo, M. Hirano, and J. Williams 1994. The interaction of small domains between the subunits of phosphatidylinositol 3-kinase determines enzyme activity. Mol. Cell. Biol. 14:2675–2685.
  • Komada, M., and J. Kitamura 1993. The cell dissociation and motility triggered by scatter factor/hepatocyte growth factor are mediated through the cytoplasmic domain of the c-Met receptor. Oncogene 8:2381–2390.
  • Konishi, H., S. Kuroda, and J. Kikkawa 1994. The pleckstrin homology domain of RAC protein kinase associates with the regulatory domain of protein kinase Cζ. Biochem. Biophys. Res. Commun. 205:1770–1775.
  • Lemmon, M. A., M. Falasca, K. M. Ferguson, and J. Schlessinger 1997. Regulatory recruitment of signaling molecules to the cell membrane by pleckstrin homology domains. Trends Cell Biol. 7:237–242.
  • Lemmon, M. A., K. M. Ferguson, R. O’Brien, P. B. Sigler, and J. Schlessinger 1995. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl. Acad. Sci. USA 92:10472–10476.
  • Lemmon, M. A., K. M. Ferguson, and J. Schlessinger 1996. PH domains: diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell 85:621–624.
  • Maina, F., M. C. Hilton, C. Ponzetto, A. M. Davies, and J. Klein 1997. Met receptor signaling is required for sensory nerve development and HGF promotes axonal growth and survival of sensory neurones. Genes Dev. 11:3341–3350.
  • Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179–185.
  • Matsumoto, K., and J. Nakamura 1993. Roles of HGF as a pleiotropic factor in organ regeneration. EXS 65:225–249.
  • Michiels, F., J. C. Stam, P. L. Hordijk, R. A. van der Kammen, L. Ruuls-vanStalle, C. A. Feltkamp, and J. Collard 1997. Regulated membrane localization of Tiam1, mediated by the NH2-terminal pleckstrin homology domain, is required for Rac-dependent membrane ruffling and C-Jun NH2-terminal kinase activation. J. Cell Biol. 137:387–398.
  • Montesano, R., G. Schaller, and J. Orci 1991. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66:697–711.
  • Myers, M. G. Jr., J. M. Backer, X. J. Sun, S. Shoelson, P. Hu, J. Schlessinger, M. Yoakim, B. Schaffhausen, and J. White 1992. IRS-1 activates phosphatidylinositol 3′-kinase by associating with src homology domains of p85. Proc. Natl. Acad. Sci. USA 89:10350–10354.
  • Nakamura, T. 1991. Structure and function of hepatocyte growth factor. Prog. Growth Factor Res. 3:67–85.
  • Nguyen, L., M. Holgado-Madruga, C. Maroun, E. D. Fixman, D. Kamikura, T. Fournier, A. Charest, M. L. Tremblay, A. J. Wong, and J. Park 1997. Association of the multisubstrate docking protein Gab1 with the hepatocyte growth factor receptor requires a functional Grb2 binding site involving tyrosine 1356. J. Biol. Chem. 272:20811–20819.
  • Pasdar, M., and J. Nelson 1989. Regulation of desmosome assembly in epithelial cells: kinetics of synthesis, transport, and stabilization of desmoglein I, a major protein of the membrane core domain. J. Cell Biol. 109:163–177.
  • Paterson, H. F., J. W. Savopoulos, O. Perisic, R. Cheung, M. V. Ellis, R. L. Williams, and J. Katan 1995. Phospholipase C δ1 requires a pleckstrin homology domain for interaction with the plasma membrane. Biochem. J. 312:661–666.
  • Pawson, T. 1995. Protein modules and signaling networks. Nature 373:573–580.
  • Ponzetto, C., A. Bardelli, Z. Zhen, F. Maina, P. dalla Zonca, S. Giordano, A. Graziani, G. Panayotou, and J. Comoglio 1994. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 77:261–271.
  • Raabe, T., J. Riesgo-Escovar, X. Liu, B. S. Bausenwein, P. Deak, P. Maroy, and J. Hafen 1996. DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between sevenless and RAS1 in Drosophila. Cell 85:911–920.
  • Rameh, L. E., A.-K. Arvidsson, K. L. Carraway III, A. D. Couvillon, G. Rathbun, A. Crompton, B. VanRenterghem, M. P. Czech, K. S. Ravichandran, S. J. Burakoff, D. S. Wang, C. S. Chen, and J. Cantley 1997. A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem. 272:22059–22066.
  • Rodrigues, G. A., M. A. Naujokas, and J. Park 1991. Alternative splicing generates isoforms of the met receptor tyrosine kinase which undergo differential processing. Mol. Cell. Biol. 11:2962–2970.
  • Rodrigues, G. A., and J. Park 1994. Autophosphorylation modulates the kinase activity and oncogenic potential of the Met receptor tyrosine kinase. Oncogene 9:2019–2027.
  • Rong, S., M. Bodescot, D. Blair, J. Dunn, T. Nakamura, K. Mizuno, M. Park, A. Chan, S. Aaronson, and J. Vande Woude 1992. Tumorigenicity of the met proto-oncogene and the gene for hepatocyte growth factor. Mol. Cell. Biol. 12:5152–5158.
  • Ronsin, C., F. Muscatelli, M. G. Mattei, and J. Breathnach 1993. A novel putative receptor protein tyrosine kinase of the met family. Oncogene 8:1195–1202.
  • Royal, I., and J. Park 1995. Hepatocyte growth factor induced scatter of Madin-Darby canine kidney cells requires phosphatidylinositol 3-kinase. J. Biol. Chem. 270:27780–27787.
  • Salim, K., M. J. Bottomly, E. Querfurth, M. J. Zvelebil, I. Gout, R. Scaife, R. L. Margolis, R. Gigg, C. I. Smith, P. C. Driscoll, M. D. Waterfield, and J. Panayotou 1996. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton’s tyrosine kinase. EMBO J. 15:6241–6250.
  • Schmidt, C., F. Bladt, S. Goedecke, V. Brinkmann, W. Zschiesche, M. Sharpe, E. Gherardi, and J. Birchmeier 1995. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373:699–702.
  • Schmidt, L., F. M. Duh, F. Chen, T. Kishida, G. Glenn, P. Choyke, S. W. Scherer, Z. Zhuang, I. Lubensky, M. Dean, R. Allikmets, A. Chidambaram, U. R. Bergerheim, J. T. Feltis, C. Casadevall, A. Zamarron, M. Bernues, S. Richard, C. J. Lips, M. M. Walther, L. C. Tsui, L. Geil, M. L. Orcutt, T. Stackhouse, J. Lipan, L. Slife, H. Brauch, J. Decker, G. Niehans, M. D. Hughson, H. Moch, S. Storkel, M. I. Lerman, W. M. Linehan, and J. Zbar 1997. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nat. Genet. 16:68–73.
  • Soriano, J. V., M. S. Pepper, T. Nakamura, L. Orci, and J. Montesano 1995. Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells. J. Cell Sci. 108:413–430.
  • Stam, J. C., E. E. Sander, F. Michiels, F. N. van Leeuwen, H. E. Kain, R. A. van der Kammen, and J. Collard 1997. Targeting Tiam1 to the plasma membrane requires the cooperative function of the N-terminal pleckstrin homology domain and an adjacent protein interaction domain. J. Biol. Chem. 272:28447–28454.
  • Stephens, L. R., K. T. Hughes, and J. Irvine 1991. Pathway of phophatidylinositol (3,4,5)-trisphosphate synthesis in activated neutrophils. Nature 351:33–39.
  • Takahashi-Tezuka, M., Y. Yoshida, T. Fukada, T. Ohtany, Y. Yamanaka, K. Nishida, M. Hibi, and J. Hirano 1998. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol. Cell. Biol. 18:4109–4117.
  • Takaishi, K., T. Sasaki, H. Kotani, H. Nishioka, and J. Takai 1997. Regulation of cell-cell adhesion by Rac and Rho small G proteins in MDCK cells. J. Biol. Chem. 139:1047–1059.
  • Takayama, H., W. J. LaRochelle, R. Sharp, T. Otsuka, P. Kriebel, M. Anver, S. A. Aaronson, and J. Merlino 1997. Diverse tumorigenesis associated with aberrant development in mice overexpressing hepatocyte growth factor/scatter factor. Proc. Natl. Acad. Sci. USA 94:701–706.
  • Uehara, Y., O. Minowa, C. Mori, K. Shiota, J. Kuno, T. Noda, and J. Kitamura 1995. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373:702–705.
  • Venkateswarlu, K., P. B. Oaty, J. M. Tavaré, and J. Cullen 1998. Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase. Curr. Biol. 8:463–466.
  • Vlahos, C. J., W. F. Matter, K. Y. Hui, and J. Brown 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269:5241–5248.
  • Wang, D.-S., R. Miller, R. Shaw, and J. Shaw 1996. The pleckstrin homology domain of human ßIΣII spectrin is targeted to the plasma membrane in vivo. Biochem. Biophys. Res. Commun. 225:420–426.
  • Weidner, K. M., S. Di Cesare, M. Sachs, V. Brinkmann, J. Behrens, and J. Birchmeier 1996. Interaction between Gab1 and c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature 384:173–176.
  • Weidner, K. M., M. Sachs, and J. Birchmeier 1993. The Met receptor tyrosine kinase transduces motility, proliferation, and morphogenic signals of scatter factor/hepatocyte growth factor in epithelial cells. J. Cell Biol. 121:145–154.
  • Weidner, K. M., M. Sachs, D. Riethmacher, and J. Birchmeier 1995. Mutation of juxtamembrane tyrosine residue 1001 suppresses loss-of-function mutations of the met receptor in epithelial cells. Proc. Natl. Acad. Sci. USA 92:2597–2601.
  • Wigler, M., A. Pellicer, S. Silverstein, R. Axel, G. Urlaub, and J. Chasin 1979. DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc. Natl. Acad. Sci. USA 76:1373–1376.
  • Yamanashi, Y., and J. Baltimore 1997. Identification of the Abl- and rasGAP-associated 62 kDa protein as a docking protein, Dok. Cell 88:205–211.
  • Yang, X. M., and J. Park 1995. Expression of the hepatocyte growth factor/scatter factor receptor tyrosine kinase is localized to epithelia in the adult mouse. Lab. Investig. 73:483–491.
  • Yenush, L., and J. White 1997. The IRS-signaling system during insulin and cytokine action. Bioessays 19:491–500.
  • Yenush, L., K. J. Makati, J. Smith-Hall, O. Ishibashi, M. G. Myers Jr., and J. White 1996. The pleckstrin homology domain is the principle link between the insulin receptor and IRS-1. J. Biol. Chem. 271:24300–24306.
  • Zarnegar, R., and J. Michalopoulos 1989. Purification and biological characterization of human hepatopoietin A, a polypeptide growth factor for hepatocytes. Cancer Res. 49:3314–3320.
  • Zheng, J., R.-H. Chen, S. Corblan-Garcia, S. M. Cahill, D. Bar-Sagi, and J. Cowburn 1997. The solution structure of the pleckstrin homology domain of human SOS1. J. Biol. Chem. 272:30340–30344.
  • Zhu, H., M. A. Naujokas, E. D. Fixman, K. Torossian, and J. Park 1994. Tyrosine 1356 in the carboxyl-terminal tail of the HGF/SF receptor is essential for the transduction of signals for cell motility and morphogenesis. J. Biol. Chem. 269:29943–29948.
  • Zhu, H., M. A. Naujokas, and J. Park 1994. Receptor chimeras indicate that the Met tyrosine kinase mediates the motility and morphogenic responses of hepatocyte growth/scatter factor. Cell Growth Differ. 5:359–366.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.