17
Views
156
CrossRef citations to date
0
Altmetric
Research Article

Requirement of Phosphatidylinositol 3-Kinase-Dependent Pathway and Src for Gas6-Axl Mitogenic and Survival Activities in NIH 3T3 Fibroblasts

, , &
Pages 4442-4453 | Received 28 Jan 1997, Accepted 29 Apr 1997, Published online: 29 Mar 2023

REFERENCES

  • Barone, M. V., and S. A. Courtneidge. 1995. Myc but not Fos rescue of PDGF signalling block caused by kinase inactive Src. Nature (London) 378:509–512.
  • Barres, B. A., I. K. Hart, D. Hockenbery, M. Alexander, J. P. McKearn, and M. C. Raff. 1992. Cell death in the oligodendrocyte lineage. J. Neurobiol. 23:1221–1230.
  • Bellacosa, A., J. R. Testa, S. P. Staal, and P. N. Tschilis. 1991. A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 254:274–277.
  • Brancolini, C., M. Benedetti, and C. Schneider. 1995. Microfilament reorganization during apoptosis: the role of Gas2, a possible substrate for ICElike proteases. EMBO J. 14:5179–5190.
  • Brunn, G. J., J. Williams, C. Sabers, G. Wiederrecht, J. C. Lawrence, and R. T. Abraham. 1996. Direct inhibition of the signalling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15:5256–5267.
  • Burgering, B. M. T., and P. J. Coffer. 1995. Protein kinase B (Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature (London) 376:599–602.
  • Cantley, L. C., K. R. Auger, C. Carpenter, B. Duckworth, A. Graziani, R. Kapeller, and S. Soltoff. 1991. Oncogenes and signal transduction. Cell 64:281–302.
  • Carpenter, L. C., and L. C. Cantley. 1996. Phosphoinositide kinases. Curr. Biol. 8:153–158.
  • Carraway, K. L., and L. C. Cantley. 1994. A Neu acquaintance for ErB3 and Erb4: a role for receptor heterodimerization in growth signalling. Cell 78:5–8.
  • Cheatham, B., C. J. Vlahos, L. Cheatham, L. Wang, J. Blenis, and C. R. Kahn. 1994. Phosphatidylinositol 3 kinase activation is required for insulin stimulation of pp70S6K, DNA synthesis, and glucose transporter translocation. Mol. Cell. Biol. 14:4902–4911.
  • Chou, M. M., and J. Blenis. 1995. The 70 kDa S6 kinase: regulation of a kinase with multiple roles in mitogenic signaling. Curr. Opin. Cell Biol. 7:806–814.
  • Chung, J., C. J. Kuo, G. R. Crabtree, and J. Blenis. 1992. Rapamycin-FKBP specifically blocks growth dependent activation of and signalling by the 70 kD S6 protein kinase. Cell 69:1227–1236.
  • Chung, J., T. C. Grammer, K. P. Lemon, A. Kazlauskas, and J. Blenis. 1994. PDGF- and insulin dependent pp70S6k activation mediated by phosphatidyl-inositol-3-OH kinase. Nature (London) 370:71–75.
  • Del Sal, G., M. E. Ruaro, L. Philipson, and C. Schneider. 1992. The growth arrest specific gene gas 1 is involved in growth suppression. Cell 70:595–607.
  • Dhand, R., K. Hara, I. Hiles, B. Bax, I. Gout, G. Panayotou, M. J. Fry, K. Yonezawa, M. Kasuga, and M. D. Waterfield. 1994. PI3-kinase: structural and functional analysis of intersubunit interactions. EMBO J. 13:511–521.
  • Downward, J. 1996. Regulating S6 kinase. Nature (London) 371:378–379.
  • End, P., I. Gout, M. J. Fry, G. Panayotou, R. Dhand, K. Yonezawa, M. Kasuga, and M. D. Waterfield. 1993. A biosensor approach to the structure and function of the p85a subunit of phosphatidylinositol 3-kinase complex. J. Biol. Chem. 268:10066–10075.
  • Erpel, T., and S. Courtneidge. 1995. Src family protein kinases and cellular signal transduction pathways. Curr. Opin. Cell Biol. 7:176–182.
  • Evan, G. I., A. Wyllie, C. Gilbert, T. Littlewood, H. Land, M. Brooks, C. Waters, L. Penn, and D. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 63:119–125.
  • Franke, T. F., D. R. Kaplan, and L. W. Cantley. 1997. PI3K, downstream action blocks apoptosis. Cell 88:435–437.
  • Franke, T. F., S. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tschilis. 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727–738.
  • Fridell, Y.-W. C., Y. Jin, L. A. Quilliam, A. Burchert, P. McCloskey, G. Spizz, B. Varnum, C. Der, and E. T. Liu. 1996. Differential activation of the Ras/extracellular signal-regulated protein kinase pathway is responsible for the biological consequences induced by the Axl receptor tyrosine kinase. Mol. Cell. Biol. 16:135–145.
  • Fujimoto, J., and T. Yamamoto. 1994. Brt, a mouse gene encoding a novel receptor type protein tyrosine kinase, is preferentially expressed in the brain. Oncogene 9:693–698.
  • Godowsky, P. J., R. M. Mark, J. Chen, M. D. Sadick, H. Raab, and R. G. Hammonds. 1995. Reevaluation of the roles of protein S and Gas6 as ligands for the receptor tyrosine kinase Rse/Tyro3. Cell 62:355–358.
  • Goruppi, S. Unpublished results.
  • Goruppi, S., S. Gustincich, C. Brancolini, W. M. F. Lee, and C. Schneider. 1994. Dissection of c-myc domains involved in S phase induction of serum starved NIH 3T3 fibroblasts. Oncogene 9:1537–1544.
  • Goruppi, S., E. Ruaro, and C. Schneider. 1996. Gas6, the ligand of Axl tyrosine kinase receptor has mitogenic and survival activities for serum starved NIH3T3 fibroblasts. Oncogene 12:471–480.
  • Gould, K., and T. Hunter. 1988. Platelet-derived growth factor induces multisite phosphorylation of pp60src and increases its protein-tyrosine kinase activity. Mol. Cell. Biol. 8:3345–3356.
  • Graham, D. K., T. L. Dawson, D. L. Mullaney, H. R. Snodgass, and H. S. Earp. 1994. Cloning and mRNA expression analysis of a novel human protooncogene, c-mer. Cell Growth Differ. 5:647–657.
  • Hara, K., K. Yonezawa, H. Sakaue, A. Ando, K. Kotani, T. Kitamura, Y. Kitamura, H. Ueda, L. Stephens, T. R. Jackson, P. T. Hawkins, R. Dhand, A. E. Clark, G. D. Holman, M. D. Waterfield, and M. Kasuga. 1994. 1-Phos-phatidylinositol 3-kinase activity is required for insulin-stimulated glucose transport but not RAS activation in CHO cells. Proc. Natl. Acad. Sci. USA 91:7415–7419.
  • Harrington, E. A., M. A. Bennett, A. Fanidi, and G. I. Evan. 1994. C-Myc induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 12:3286–3295.
  • Harrington, E. A., A. Fanidi, and G. I. Evan. 1994. Oncogenes and cell death. Curr. Opin. Cell Biol. 4:120–129.
  • Janssen, J. W. G., A. S. Schultz, A. C. N. Steendoorden, M. Schmidberger, S. Strehl, P. F. Ambros, and C. R. Bartram. 1991. A novel putative tyrosine kinase receptor with oncogenic potential. Oncogene 6:2113–2120.
  • Jia, R., and H. Hanafusa. 1994. The proto-oncogene of v-eyk (v-ryk) is a novel receptor type protein tyrosine kinase with extracellular Ig/FNIII domains. J. Biol. Chem. 269:1839–1844.
  • Kaufmann-Zeh, A., P. Rodriguez-Viciana, E. Ulrich, C. Gilbert, P. Coffer, J. Downward, and G. Evan. 1997. Suppression of Myc induced apoptosis by Ras signalling through PI(3)K and Pkb. Nature (London) 385:544–548.
  • Kozma, S. C., and G. Thomas. 1994. p70S6K/p85S6K: mechanism of activation and role in mitogenesis. Semin. Cancer Biol. 5:255–260.
  • Kuo, C. J., J. Chung, D. F. Fiorentino, W. M. Flanagan, J. Blenis, and G. R. Crabtree. 1992. Rapamycin selectively inhibits interleukin-2 activation of p70 S6 kinase. Nature (London) 358:70–73.
  • Kypta, R. M., Y. Goldberg, E. T. Ulug, and S. A. Courtneidge. 1990. Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell 62:481–492.
  • Lai, C., and G. Lemke. 1991. An extended family of protein tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 6:691–704.
  • Li, R., J. Chen, G. Hammonds, H. Philips, M. Armanini, P. Wood, R. Bunge, P. J. Godowsky, M. X. Slikowsky, and J. P. Mather. 1996. Identification of Gas6 as a growth factor for human Schwann cells. J. Neurosci. 16:2012–2019.
  • Ling, L., and H. Kung. 1995. Mitogenic signals and transforming potential of Nyk, a newly identified neural cell adhesion molecule related receptor tyrosine kinase. Mol. Cell. Biol. 15:6582–6592.
  • Lipsich, L. A., A. J. Lewis, and J. S. Brugge. 1983. Isolation of monoclonal antibodies that recognize the transforming protein of avian sarcoma viruses. J. Virol. 48:352–60.
  • Manfioletti, G., C. Brancolini, G. Avanzi, and C. Schneider. 1993. The protein encoded by a growth arrest specific gene (gas6) is a new member of the vitamin K-dependent proteins related to protein S, the negative coregulator in the blood coagulation cascade. Mol. Cell. Biol. 13:4976–4985.
  • Marcandalli, P. et al. Unpublished data.
  • Mark, M. R., J. Chen, R. G. Hammonds, M. Sadick, and P. J. Godowsky. 1996. Characterisation of Gas6, a member of the superfamily of G domaincontaining proteins, as a ligand for Rse and Axl. J. Biol. Chem. 271:9785–9789.
  • Mark, M. R., D. T. Scadden, Z. Wang, Q. Gu, A. Goddard, and P. J. Godowsky. 1994. Rse, a novel receptor type tyrosine kinase with homology to Axl/Ufo, is expressed at high levels in the brain. J. Biol. Chem. 269:10720–10728.
  • Nakano, T., K. Higashino, N. Kikuci, J. Kishino, K. Nomura, H. Fujita, O. Ohara, and H. Arita. 1995. Vascular smooth muscle cell derived, Gla containing growth potentiating factor for Ca-mobilizing growth factors. J. Biol. Chem. 270:5702–5705.
  • Nakano, T., K. Kawamoto, K. Higashino, and H. Arita. 1996. Prevention of growth arrest-induced cell death of vascular smooth muscle cells by a product of growth arrest-specific gene, gas6. FEBS Lett. 387:78–80.
  • O’Bryan, J. P., R. A. Frye, P. C. Cogswell, A. Neubauer, B. Kitch, C. Prokop, R. Espinosa III, M. M. Le Beau, H. S. Earp, and E. T. Liu. 1991. Axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol. Cell. Biol. 11:5016–5031.
  • Ohashi, K., K. Mizuno, K. Kuma, T. Miyata, and T. Nakamura. 1994. Cloning of the cDNA for a novel receptor tyrosine kinase. Oncogene 9:699–705.
  • Ohashi, K., K. Nagata, J. Toshima, T. Nakano, H. Arita, H. Tsuda, K. Suzuki, and K. Mizuno. 1995. Stimulation of Sky receptor tyrosine kinase by the product of growth arrest specific gene 6. J. Biol. Chem. 270:22681–22684.
  • Pleiman, C. M., W. M. Hertz, and J. C. Cambier. 1994. Activation of phosphatidylinositol 3′ kinase by src-kinase SH3 binding to the p85 subunit. Science 263:1609–1612.
  • Proud, C. G. 1996. p70 S6 kinase: an enigma with variations. Trends Biochem. Sci. 21:181–185.
  • Raff, M. C., B. Barres, H. Coles, Y. Ishizaky, and M. Jacobson. 1993. Programmed cell death and the control of survival: lessons from the immune system. Science 262:695–700.
  • Rescigno, J., A. Mansukhani, and C. Basilico. 1991. A putative receptor tyrosine kinase with unique structural topology. Oncogene 6:1909–1913.
  • Roche, S., M. Koegl, and S. A. Courtneidge. 1994. The phosphatidylinositol 3-kinase alpha is required for DNA synthesis induced by some, but not all, growth factors. Proc. Natl. Acad. Sci. USA 91:9185–9189.
  • Roche, S., M. Koegl, M. V. Barone, M. Roussel, and S. A. Courtneidge. 1995. DNA synthesis induced by some, but not all, growth factors requires Src family protein tyrosine kinases. Mol. Cell. Biol. 15:1102–1109.
  • Royal, I., and M. Park. 1996. Hepatocyte growth factor-induced scatter of Madin-Darby canine kidney cells requires phosphatidylinositol 3-kinase. J. Biol. Chem. 270:27780–27787.
  • Sakaue, H., K. Hara, T. Noguchi, T. Matozak, K. Kotani, W. Ogawa, K. Yonezawa, M. D. Waterfield, and M. Kasuga. 1995. Ras-independent and wortmannin sensitive activation of glycogen synthase by insulin in Chinese hamster ovary cells. J. Biol. Chem. 270:11304–11309.
  • Schneider, C., R. M. King, and L. Philipson. 1988. Genes specifically expressed at growth arrest of mammalian cells. Cell 54:787–793.
  • Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Fajardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, and L. C. Cantley. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767–778.
  • Stitt, T. N., G. Conn, M. Gore, C. Lai, J. Bruno, C. Radziejewsky, K. Mattsson, J. Fisher, D. R. Gies, P. F. Jones, P. Masiakowsky, T. E. Ryan, N. J. Tobkes, D. H. Chen, P. S. DiStefano, G. L. Long, C. Basilico, M. P. Goldfarb, G. Lemke, D. J. Glass, and G. D. Yancopoulos. 1995. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro3/Axl family of receptor tyrosine kinase. Cell 80:661–670.
  • Superti-Furga, G., and S. A. Courtneidge. 1995. Structure-function relationships in Src family and related protein tyrosine kinases. BioEssays 17:321–330.
  • Twamley-Stein, G. M., R. Pepperkok, W. Ansorge, and S. A. Courtneidge. 1993. The Src family tyrosine kinases are required for platelet-derived growth factor-mediated signal transduction in NIH3T3 cells. Proc. Natl. Acad. Sci. USA 90:7696–7700.
  • Ui, M., T. Okada, K. Hazeki, and O. Hazeki. 1995. Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem. Sci. 20:303–307.
  • Van der Geer, P., R. Lindberg, and T. Hunter. 1994. Receptor protein tyrosine kinases and their signal transduction. Annu. Rev. Cell Biol. 10:251–337.
  • Varnum, B. C., C. Young, G. Elliott, A. Garcia, T. D. Bartley, Y. W. Fridell, R. W. Hunt, G. Trail, C. Clogson, R. J. Toso, D. Yanagihara, L. Bennett, M. Sylber, L. A. Merewether, A. Tseng, E. Escobar, E. T. Liu, and H. K. Yamane. 1995. Axl receptor tyrosine kinase is stimulated by the vitamin K dependent protein encoded by the growth arrest specific gene gas6. Nature (London) 373:623–626.
  • Yao, R., and G. M. Cooper. 1995. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 264:2003–2006.
  • Ziemiecki, A., R. R. Friis, and H. Bauer. 1982. Half-life of the Rous sarcoma virus transforming protein pp60src and its associated kinase activity. Mol. Cell. Biol. 2:355–360.

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.