PDGF induces an early and a late wave of PI 3-kinase activity, and only the late wave is required for progression through G1

Current Biology

Volumn 9, Issue 10, 1999, Pages 512-521

  Jones, Steven M ^a,b   Klinghoffer, Richard ^c   Prestwich, Glenn D ^d   Toker, Alex ^e   Kazlauskas, Andrius ^a,b  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c USA   (United States)

^d UNIVERSITY OF UTAH   (United States)

^e BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0033587047     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-9822(99)80235-8     Document Type: Article

References (66)

1. Westermark B, Siegbahn A, Heldin CH, Claesson-Welsh L: B-type receptor for platelet-derived growth factor mediates a chemotactic response by means of ligand-induced activation of the receptor protein-tyrosine kinase. Proc Natl Acad Sci USA 1990, 87:128-132.
2. Mellstrom K, Heldin CH, Westermark B: Induction of circular membrane ruffling on human fibroblasts by platelet-derived growth factor. Exp Cell Res 1988, 177:347-359.
3. Arvidsson AK, Heldin CH, Claesson-Welsh L: Transduction of circular membrane ruffling by the platelet-derived growth factor beta-receptor is dependent on its kinase insert. Cell Growth Differ 1992, 3:881-887.
4. Hammacher A, Mellstrom K, Heldin CH, Westermark B: Isoform-specific induction of actin reorganization by platelet-derived growth factor suggests that the functionally active receptor is a dimer. EMBO J 1989, 8:2489-2495.
5. Eriksson A, Siegbahn A, Westermark B, Heldin CH, Claesson-Welch L: PDGF alpha- and beta-receptors activate unique and common signal transduction pathways. EMBO J 1992, 11:543-550.
6. Heldin CH, Hammacher A, Nister M, Westermark B: Structural and functional aspects of platelet-derived growth factor. Br J Cancer 1988, 57:591-593.
7. Kundra V, Escobedo JA, Kazlauskas A, Kim HK, Rhee SG, Williams LT, Zetter BR: Regulation of chemotaxis by the platelet-derived growth factor receptor-beta. Nature 1994, 367:474-476.
8. Hooshmand-Rad R, Claesson-Welsh L, Wennström S, Yokote K, Siegbahn A, Heldin CH: Involvement of phosphatidylinositide 3′-kinase and Rac in platelet-derived growth factor-induced actin reorganization and chemotaxis. Exp Cell Res 1997, 234:434-441.
9. Yokote K, Mori S, Siegbahn A, Rönnstrand L, Wernstedt C, Heldin CH, Claesson-Welsh L: Structural determinants in the platelet-derived growth factor alpha-receptor implicated in modulation of chemotaxis. J Biol Chem 1996, 271:5101 -5111.
10. Wennström S, Siegbahn A, Yokote K, Arvidsson AK, Heldin CH, Mori S, Claesson-Welsh L: Membrane ruffling and chemotaxis transduced by the PDGF beta-receptor require the binding site for phosphatidylinositol 3′ kinase. Oncogene 1994, 9:651-660.
11. Wymann M, Arcaro A: Platelet-derived growth factor-induced phosphatidylinositol 3-kinase activation mediates actin rearrangements in fibroblasts. Biochem J 1994, 298:517-520.
12. Dhand R, Hara K, Hiles I, Bax B, Gout I, Panayotou G: PI 3-kinase: Structural and functional analysis of intersubunit interactions. EMBO J 1994, 13:511-521.
13. Carpenter CL, Auger KR, Duckworth BC, Hou WM, Schaffhausen B, Cantley LC: A tightly associated serine/threonine protein kinase regulates phosphoinositide 3-kinase activity. Mol Cell Biol 1993, 13:1657-1665.
14. Kapeller R, Cantley LC: Phosphatidylinositol 3-kinase. Bioessays 1994, 16:565-576.
15. Fruman DA, Meyers RE, Cantley LC: Phosphoinositide kinases. Annu Rev Biochem 1998, 67:481-507.
16. Klinghoffer RA, Duckworth B, Valius M, Cantley L, Kazlauskas A: Platelet-derived growth factor-dependent activation of phosphatidylinositol 3-kinase is regulated by receptor binding of SH2-domain-containing proteins which influence Ras activity. Mol Cell Biol 1996, 16:5905-5914.
17. Kodaki T, Woscholski R, Hallberg B, Rodriguez-Viciana P, Downward J, Parker PJ: The activation of phosphatidylinositol 3-kinase by Ras. Curr Biol 1994, 4:798-806.
18. Rodriguez-Viciana P, Warne PH, Dhand R, Vanhaesebroeck B, Gout I, Fry MJ, et al.: Phosphatidylinositol-3-Oh kinase as a direct target of Ras. Nature 1994, 370:527-532.
19. Derman MP, Toker A, Hartwig JH, Spokes K, Falck JR, Chen CS, et al.: The lipid products of phosphoinositide 3-kinase increase cell motility through protein kinase C. J Biol Chem 1997, 272:6465-6470.
20. Valius M, Kazlauskas A: Phospholipase C-gamma 1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 1993, 73:321-334.
21. Montmayeur JP, Valius M, Vandenheede J, Kazlauskas A: The platelet-derived growth factor beta receptor triggers multiple cytoplasmic signaling cascades which arrive at the nucleus as distinguishable inputs. J Biol Chem 1997, 272:32670-32678.
22. K. Yokote, Mori S, Hansen K, McGlade J, Pawson T, Heldin CH, Claesson-Welsh L: Direct interaction between Shc and the platelet-derived growth factor beta-receptor. J Biol Chem 1994, 269:15337-15343.
23. Escobedo JA, Williams LT: A PDGF receptor domain essential for mitogenesis but not for many other responses to PDGF. Nature 1988, 335:85-87.
24. Yu JC, Heidaran MA, Pierce JH, Gutkind JS, Lombardi D, Ruggiero M, Aaronson SA: Tyrosine mutations within the alpha platelet-derived growth factor receptor kinase insert domain abrogate receptor-associated phosphatidylinositol-3 kinase activity without affecting mitogenic or chemotactic signal transduction. Mol Cell Biol 1991, 11:3780-3785.
25. Stiles CD, Isberg RR, Pledger WJ, Antoniades HN, Scher CD: Control of the Balb/c-3T3 cell cycle by nutrients and serum factors: Analysis using platelet-derived growth factor and platelet-poor plasma. J Cell Physiol 1979, 99:395-405.
26. Stiles CD, Capone GT, Scher CD, Antoniades HN, Van Wyk JJ, Pledger WJ: Dual control of cell growth by somatomedins and platelet-derived growth factor. Proc Natl Acad Sci USA 1979, 76:1279-1283.
27. Bennett AM, Hausdorff SF, O'Reilly AM, Freeman RM, Neel BG: Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol Cell Biol 1996, 16:1189-1202.
28. Shapiro PS, Ahn NG: Feedback regulation of Raf-1 and mitogen-activated protein kinase (MAP) kinase kinases 1 and 2 by MAP kinase phosphatase-1 (MKP-1). J Biol Chem 1998, 273:1788-1793.
29. Sun H, Charles CH, Lau LF, Tonks NK: MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 1993, 75:487-493.
30. Taylor SJ, Shalloway D: Cell cycle-dependent activation of Ras. Curr Biol 1996, 6:1621-1627.
31. Mulcahy LS, Smith MR, Stacey DW: Requirement for ras proto-oncogene function during serum-stimulated growth of NIH 3T3 cells. Nature 1985, 313:241-243.
32. Dobrowolski S, Harter M, Stacey DW: Cellular ras activity is required for passage through multiple points of the G0/G1 phase in BALB/c 3T3 cells. Mol Cell Biol 1994, 14:5441-5449.
33. Roche S, Koegl M, Courtneidge SA: The phosphatidylinositol 3-kinase alpha is required for DNA synthesis induced by some, but not all, growth factors. Proc Natl Acad Sci USA 1994, 91:9185-9189.
34. Roche S, Downward J, Raynal P, Courtneidge SA: A function for phosphatidylinositol 3-kinase beta (p85alpha-p110beta) in fibroblasts during mitogenesis: Requirement for insulin- And lysophosphatidic acid-mediated signal transduction. Mol Cell Biol 1998, 18:7119-7129.
35. Siddhanta U, McLlroy J, Shah A, Zhang Y, Backer JM: Distinct roles for the p110alpha and hVps34 phosphatidylinositol 3′- Kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J Cell Biol 1998, 143:1647-1659.
36. Bacqueville D, Casagrande F, Perret B, Chap H, Darbon JM, Breton-Douillon M: Phosphatidylinositol 3-kinase inhibitors block aortic smooth muscle cell proliferation in mid-late G1 phase: Effect on cyclin-dependent kinase 2 and the inhibitory protein p27KIP1. Biochem Biophys Res Commun 1998, 244:630-636.
37. Casagrande F, Bacqueville D, Pillaire MJ, Malecaze F, Manenti S, Breton-Douillon M, Darbon JM: G1 phase arrest by the phosphatidylinositol 3-kinase inhibitor LY 294002 is correlated to up-regulation of p27Kip1 and inhibition of G1 CDKs in choroidal melanoma cells. FEBS Lett 1998, 422:385-390.
38. Takuwa N, Takuwa Y: Ras activity late in G1 phase required for p27kip1 downregulation, passage through the restriction point, and entry into S phase in growth factor-stimulated NIH 3T3 fibroblasts. Mol Cell Biol 1997, 17:5348-5358.
39. Whiteford C, Best C, Kazlauskas A, Ulug E: D-3 phosphoinositide metabolism in cells treated with platelet-derived growth factor. Biochem J 1996, 319:851-860.
40. Auger KR, Serunian LA, Soltoff SP, Libby P, Cantley LC: PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells. Cell 1989, 57:167-175.
41. Bondeva T, Pirola L, Bulgarelli-Leva G, Rubio I, Wetzker R, Wymann MP: Bifurcation of lipid and protein kinase signals of PI 3-kinase gamma to the protein kinases PKB and MAPK. Science 1998, 282:293-296.
42. Valius M, Kazlauskas A: Phospholipase C-gamma1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 1993, 73:321 -334.
43. Akimoto K, Takahashi R, Moriya S, Nishioka N, Takayanagi J, Kimura K, et al.: EGF or PDGF receptors activate atypical PKClambda through phosphatidylinositol 3-kinase. EMBO J 1996, 15:788-798.
44. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, et al.: The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 1995, 81:727-736.
45. Moriya S, Kazlauskas A, Akimoto K, Hirai S, Mizuno K, Takenawa T, et al.: Platelet-derived growth factor activates protein kinase C epsilon through redundant and independent signaling pathways involving phospholipase C gamma or phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 1996, 93:151-155.
46. Vlahos CJ, Matter WF, Hui KY, Brown RF: A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4- morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994, 269:5241-5248.
47. Powis G, Bonjouklian R, Berggren MM, Gallegos A, Abraham R, Ashendel C, et al.: Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3- kinase. Cancer Res 1994, 54:2419-2423.
48. Brown WJ, DeWald DB, Emr SD, Plutner H, Balch WE: Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J Cell Biol 1995, 130:781-796.
49. Wymann MP, Bulgarelli-Leva G, Zvelebil MJ, Pirola L, Vanhaesebroeck B, Waterfield MD, Panayotou G: Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys-802, a residue involved in the phosphate transfer reaction. Mol Cell Biol 1996, 16:1722-1733.
50. Yao R, Cooper GM: Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 1995, 267:2003-2006.
51. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME: Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997, 91:231-241.
52. Kulik G, Klippel A, Weber MJ: Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol Cell Biol 1997, 17:1595-1606.
53. Eves EM, Xiong W, Bellacosa A, Kennedy SG, Tsichlis PN, Rosner MR, Hay N: Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol Cell Biol 1998, 18:2143-2152.
54. Downward J: Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol 1998, 10:262-267.
55. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD: The Molecular Biology of The Cell, 3rd Edn. New York: Garland Publishing; 1994.
56. Kazlauskas A, Kashishian A, Cooper JA, Valius M: Gtpase-activating protein and phosphatidylinositol 3-kinase bind to distinct regions of the platelet-derived growth factor receptor beta subunit. Mol Cell Biol 1992, 12:2534-2544.
57. Agrawal D, Hauser P, McPherson F, Dong F, Garcia A, Pledger WJ: Repression of p27kip1 synthesis by platelet-derived growth factor in BALB/c 3T3 cells. Mol Cell Biol 1996, 16:4327-4336.
58. Weber JD, Hu W, Jefcoat SC Jr, Raben DM, Baldassare JJ: Ras-stimulated extracellular signal-related kinase 1 and RhoA activities coordinate platelet-derived growth factor-induced G1 progression through the independent regulation of cyclin D1 and p27. J Biol Chem 1997, 272:32966-32971.
59. DeMali K, Kazlauskas A: Activation of Src family members is not required for role for PDGF beta receptor to initiate mitogenesis. Mol Cell Biol 1998, 18:2014-2022.
60. Gelderloos JA, Rosenkranz S, Bazenet C, Kazlauskas A: A role for Src in signal relay by the platelet-derived growth factor alpha receptor. J Biol Chem 1998, 273:5908-5915.
61. Hooshmand-Rad R, Yokote K, Heldin CH, Claesson-Welsh L: PDGF alpha-receptor mediated cellular responses are not dependent on Src family kinases in endothelial cells. J Cell Sci 1998, 111:607-614.
62. Pardee AB: G1 events and regulation of cell proliferation. Science 1989, 246:603-608.
63. Klippel A, Escobedo MA, Wachowicz MS, Apell G, Brown TW, Giedlin MA, et al.: Activation of phosphatidylinositol 3-kinase is sufficient for cell cycle entry and promotes cellular changes characteristic of oncogenic transformation. Mol Cell Biol 1998, 18:5699-5711.
64. Dolmetsch RE, Xu K, Lewis RS: Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998, 392:933-936.
65. 2+ spike frequency can optimize gene expression. Nature 1998, 392:936-941.
66. Kazlauskas A, Cooper JA: Phosphorylation of the PDGF receptor beta subunit creates a tight binding site for phosphatidylinositol 3 kinase. EMBO J 1990, 9:3279-3286.