The fibroblast growth factor receptor is at the site of convergence between μ-opioid receptor and growth factor signaling pathways in rat C6 glioma cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 303, Issue 3, 2002, Pages 909-918

  Belcheva, Mariana M ^a   Haas, Paul D ^a   Tan, Yun ^a   Heaton, Virginia M ^a   Coscia, Carmine J ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DIMETHYL 5 (2 OXO 1H INDOL 3 YLMETHYLENE) 3 PYRROLEPROPIONIC ACID; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; CALCIUM ION; DANTROLENE; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLARGINYLTHREONYLPENICILLAMINYLTHREONINAMIDE; ENDOMORPHIN 1; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; FIBROBLAST GROWTH FACTOR RECEPTOR; GROWTH FACTOR; MATRIX METALLOPROTEINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; MU OPIATE RECEPTOR ANTAGONIST; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; NIFEDIPINE; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; SEMAXANIB; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENCY; FIBROBLAST; GLIOMA CELL; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSACTIVATION;

ANIMALS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; GLIOMA; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RECEPTORS, FIBROBLAST GROWTH FACTOR; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TUMOR CELLS, CULTURED;

EID: 0036895875     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: 10.1124/jpet.102.038554     Document Type: Article

References (45)

1. Ai WD, Gong JH, and Yu L (1999) MAP kinase activation by μ-opioid receptor involves phosphatidylinositol 3-kinase but not the cAMP/PKA pathway. FEBS Lett 456:196-200.
2. Amberger VR, Paganetti PA, Seulberger H, Eldering JA, and Schwab ME (1994) Characterization of a membrane-bound metalloendoprotease of rat C6 glioblastoma cells. Cancer Res 54:4017-4025.
3. 3H]thymidine incorporation into DNA: Evidence for the involvement of pertussis toxin-sensitive G protein-coupled phosphoinositide turnover. J Neurochem 60:1505-1511.
4. 2+ mobilization in rat C6 glioma cells. J Neurosci 14:5858-5864.
5. Bashkin P, Doctrow S, Klagsbrun M, Svahn CM, Folkman J, and Vlodavsky I (1989) Basic fibroblast growth factor binds to subendothelial extracellular matrix and is released by heparanase and heparin-like molecules. Biochemistry 28:1737-1743.
6. Belcheva M, Barg J, Rowinski J, Clark WG, Gloeckner CA, Ho A, Gao XM, Chuang DM, and Coscia C (1993) Novel opioid binding sites associated with nuclei of NG108-15 neurohybrid cells. J Neurosci 13:104-114.
7. Belcheva MM and Coscia CJ (2002) Diversity of G protein-coupled receptor signaling pathways to ERK/MAP kinase. Neurosignals 11:34-44.
8. Belcheva MM, Szucs M, Wang DX, Sadee W, and Coscia CJ (2001) μ-opioid receptor-mediated ERK activation involves calmodulin-dependent epidermal growth factor receptor transactivation. J Biol Chem 276:33847-33853.
9. Belcheva MM, Vogel Z, Ignatova E, Avidor-Reiss T, Zippel R, Levy R, Young EC, Barg J, and Coscia CJ (1998) Opioid modulation of extracellular signal-regulated protein kinase activity is Ras-dependent and involves G(β-γ) subunits. J Neurochem 70:635-645.
10. Bohn LM, Belcheva MM, and Coscia CJ (2000a) Mitogenic signaling via endogenous κ-opioid receptors in C6 glioma cells: Evidence for the involvement of protein kinase C and the mitogen-activated protein kinase signaling cascade. J Neurochem 74:564-573.
11. Bohn LM, Belcheva MM, and Coscia CJ (2000b) μ-opioid agonist inhibition of κ-opioid receptor-stimulated extracellular signal-regulated kinase phosphorylation is dynamin-dependent in C6 glioma cells. J Neurochem 74:574-581.
12. Chernausek SD (1993) Insulin-like growth factor-1 (IGF-1) production by astroglial cells: Regulation and importance for epidermal growth factor-induced cell replication. J Neurosci Res 34:189-197.
13. Della Rocca GJ, Maudsley S, Daaka Y, Lefkowitz RJ, and Luttrell LM (1999) Pleiotropic coupling of G protein-coupled receptors to the mitogen-activated protein kinase cascade: Role of focal adhesions and receptor tyrosine kinases. J Biol Chem 274:13978-13984.
14. q-mediated pathways on calcium/ calmodulin, PYK2 and Src kinase. J Biol Chem 272:19125-19132.
15. Daub H, Wallasch C, Lankenau A, Herrlich A, and Ullrich A (1997) Signal characteristics of G protein-transactivated EGF receptor. EMBO (Eur Mol Biol Organ) J 16:7032-7044.
16. Daub H, Weiss FU, Wallasch C, and Ullrich A (1996) Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature (Lond) 379:557-560.
17. Duckworth BC and Cantley LC (1997) Conditional inhibition of the mitogen-activated protein kinase cascade by wortmannin: Dependence of signal strength. J Biol Chem 272:27665-27670.
18. Dugan LL, Kim JS, Zhang YJ, Bart RD, Sun YL, Holtzman DM, and Gutmann DH (1999) Differential effects of cAMP in neurons and astrocytes. Role of B-Raf J Biol Chem 274:25842-25848.
19. Fitzgerald M, Hayward IP, Thomas AC, Campbell GR, and Campbell JH (1999) Matrix metalloproteinase can facilitate the heparanase-induced promotion of phenotype change in vascular smooth muscle cells. Atherosclerosis 145:97-106.
20. Fukuda K, Kato S, Morikawa H, Shoda T, and Mori K (1996) Functional coupling of the δ-, μ-, and κ-opioid receptors to mitogen-activated protein kinase and arachidonate release in Chinese hamster ovary cells. J Neurochem 67:1309-1316.
21. Hamel W and Westphal M (2000) Growth factors in gliomas revisited. Acta Neurochir (Wien) 142:113-137.
22. Hawes BE, Fried S, Yao XR, Weig B, and Graziano MP (1998) Nociceptin (ORL-1) and μ-opioid receptors mediate mitogen-activated protein kinase activation in CHO cells through a G(i)-coupled signaling pathway. Evidence for distinct mechanisms of agonist-mediated desensitization. J Neurochem 71:1024-1033.
23. i proteins use a novel βγ- and Ras-independent pathway to activate extracellular signal-regulated kinase and mobilize AP-1 transcription factors in Jurkat T lymphocytes. J Biol Chem 274:19992-20001.
24. Herrlich A, Daub H, Knebel A, Herrlich P, Ullrich A, Schultz G, and Gudermann T (1998) Ligand-independent activation of platelet-derived growth factor receptor is a necessary intermediate in lysophosphatidic acid-stimulated mitogenic activity in L cells. Proc Natl Acad Sci USA 95:8985-8990.
25. Kinkl N, Sahel J, and Hicks D (2001) Alternate FGF2-Erk1/2 signaling pathways in retinal photoreceptor and glial cells in vitro. J Biol Chem 276:43871-43878.
26. Kramer HK, Andria ML, Kushner SA, Esposito DH, Hiller JM, and Simon EJ (2000) Mutation of tyrosine 318 (Y318F) in the μ-opioid receptor attenuates tyrosine phosphorylation, agonist-dependent receptor internalization and mitogen-activated protein kinase activation. Mol Brain Res 79:55-66.
27. Laird AD, Vajkoczy P, Shawver LK, Thurnher A, Liang C, Mohammadi M, Schlessinger J, Ullrich A, Hubbard SR, Blake RA, et al. (2000) Su6668 is a potent antiangiogenic and antitumor agent that induces regression of established tumors. Cancer Res 60:4152-4160.
28. 2+ rise in rat C6 glioma cells. J Neurosci 12:1077-1085.
29. Linseman DA, Benjamin CW, and Jones DA (1995) Convergence of angiotensin II and platelet-derived growth factor receptor signaling cascades in vascular smooth muscle cells. J Biol Chem 270:12563-12568.
30. Mendel DB, Laird AD, Smolich BD, Blake RA, Liang CX, Hannah AL, Shaheen RM, Ellis LM, Weitman S, Shawver LK, et al. (2000) Development of Su5416, a selective small molecule inhibitor of VEGF receptor tyrosine kinase activity, as an anti-angiogenesis agent. Anticancer Drug Des 15:29-41.
31. Oak JN, Lavine N, and Van Tol HHM (2001) Dopamine D-4 and D-2L receptor stimulation of the mitogen-activated protein kinase pathway is dependent on transactivation of the platelet-derived growth factor receptor. Mol Pharmacol 60:92-103.
32. Oh LYS, Larsen PH, Krekoski CA, Edwards DR, Donovan F, Werb Z, and Yong VW (1999) Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci 19:8464-8475.
33. Okumura N, Takimoto K, Okada M, and Nakagawa H (1989) C6 glioma cells produce basic fibroblast growth factor that can stimulate their own proliferation. J Biochem 106:904-909.
34. Oliet SHR, Piet R, and Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science (Wash DC) 292:923-926.
35. Ornitz DM (2000) FGFs, heparan sulfate and FGFRs: Complex interactions essential for development. Bioessays 22:108-112.
36. Pierce KL, Luttrell LM, and Lefkowitz RJ (2001) New mechanisms in heptahelical receptor signaling to mitogen activated protein kinase cascades. Oncogene 20:1532-1539.
37. Powers CJ, McLeskey SW, and Wellstein A (2000) Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer 7:165-197.
38. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, and Ullrich A (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature (Lond) 402:884-888.
39. Roudabush FL, Pierce KL, Maudsley S, Khan KD, and Luttrell LM (2000) Transactivation of the EGF receptor mediates IGF-1-stimulated Shc phosphorylation and ERK1/2 activation in COS-7 cells. J Biol Chem 275:22583-22589.
40. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, and Mohammadi M (2000) Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6:743-750.
41. Schmidt H, Schulz S, Klutzny M, Koch T, Handel M, and Hollt V (2000) Involvement of mitogen-activated protein kinase in agonist-induced phosphorylation of the μ-opioid receptor in HEK 293 cells. J Neurochem 74:414-422.
42. Stiene-Martin A and Hauser KF (1990) Opioid-dependent growth of glial cultures: Suppression of astrocyte DNA synthesis by met-enkephalin. Life Sci 46:91-98.
43. Ullian EM, Sapperstein SK, Christopherson KS, and Barres BA (2001) Control of synapse number by glia. Science (Wash DC) 291:657-661.
44. Vlodavsky I and Friedmann Y (2001) Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J Clin Invest 108:341-347.
45. Vossler MR, Yao H, York RD, Pan MG, Rim CS, and Stork PJS (1997) cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89:73-82.