δ-Opioid receptor-stimulated Akt signaling in neuroblastoma × glioma (NG108-15) hybrid cells involves receptor tyrosine kinase-mediated PI3K activation

Experimental Cell Research

Volumn 315, Issue 12, 2009, Pages 2115-2125

  Heiss, Anika ^a   Ammer, Hermann ^a   Eisinger, Daniela A ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Akt; Apoptosis; Caspase 3; PI3K; Receptor tyrosine kinases; Opioid receptor

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; ANTIBODY; CASPASE 3; DELTA OPIATE RECEPTOR; ENKEPHALIN[2 DEXTRO PENICILLAMINE 5 PENICILLAMINE]; ETORPHINE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; LIPOCORTIN 5; NALOXONE; OPIATE; PERTUSSIS TOXIN; PHOSDUCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOSERINE; PROPIDIUM IODIDE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; WORTMANNIN;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; CELL NUCLEUS MEMBRANE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GLIOMA CELL; HYBRID CELL; IMMUNOCYTOCHEMISTRY; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 67349089537     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.04.002     Document Type: Article

References (56)

1. Chen Y.L., Law P.Y., and Loh H.H. The other side of the opioid story: modulation of cell growth and survival signaling. Curr. Med. Chem. 15 (2008) 772-778
2. Sharp B.M. Multiple opioid receptors on immune cells modulate intracellular signalling. Brain. Behav. Immun. 1 (2006) 9-14
3. 5] enkephalin in neuronal death and retarded behavior induced by forebrain ischemia in rats. Neurosci. Lett. 423 (2007) 113-117
4. Förster K., Kuno A., Solenkova N., Felix S.B., and Krieg T. The delta-opioid receptor agonist DADLE at reperfusion protects the heart through activation of pro-survival kinases via EGF receptor transactivation. Am. J. Physiol. Heart Circ. Physiol. 293 (2007) H1604-H1608
5. Thomas C.C., Deak M., Alessi D.R., and van Aalten D.M. High-resolution structure of the pleckstrin homology domain of protein kinase B/Akt bound to phosphatidylinositol (3,4,5)-trisphosphate. Curr. Biol. 12 (2002) 1256-1262
6. Alessi D.R., James S.R., Downes C.P., Holmes A.B., Gaffney P.R., Reese C.B., and Cohen P. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol. 7 (1997) 261-269
7. Toker A., and Newton A.C. Akt/protein kinase B is regulated by autophosphorylation at the hypothetical PDK-2 site. J. Biol. Chem. 275 (2000) 8271-8274
8. Sale E.M., and Sale G.J. Protein kinase B: signalling roles and therapeutic targeting. Cell. Mol. Life Sci. 65 (2008) 113-127
9. Stephens L., Smrcka A., Cooke F.T., Jackson T.R., Sternweis P.C., and Hawkins P.T. A novel phosphoinositide 3 kinase activity in myeloid-derived cells is activated by G protein beta gamma subunits. Cell 77 (1994) 83-93
10. Seely B.L., Reichart D.R., Staubs P.A., Jhun B.H., Hsu D., Maegawa H., Milarski K.L., Saltiel A.R., and Olefsky J.M. Localization of the insulin-like growth factor I receptor binding sites for the SH2 domain proteins p85, Syp, and GTPase activating protein. J. Biol. Chem. 270 (1995) 19151-19157
11. Giorgetti S., Ballotti R., Kowalski-Chauvel A., Tartare S., and Van Obberghen E. The insulin and insulin-like growth factor-I receptor substrate IRS-1 associates with and activates phosphatidylinositol 3-kinase in vitro. J. Biol. Chem. 268 (1993) 7358-7364
12. Yamada M., Ohnishi H., Sano S., Nakatani A., Ikeuchi T., and Hatanaka H. Insulin receptor substrate (IRS)-1 and IRS-2 are tyrosine-phosphorylated and associated with phosphatidylinositol 3-kinase in response to brain-derived neurotrophic factor in cultured cerebral cortical neurons. J. Biol. Chem. 272 (1997) 30334-30339
13. Murga C., Laguinge L., Wetzker R., Cuadrado A., and Gutkind J.S. Activation of Akt/protein kinase B by G protein-coupled receptors. A role for alpha and beta gamma subunits of heterotrimeric G proteins acting through phosphatidylinositol-3-OH kinasegamma. J. Biol. Chem. 273 (1998) 19080-19085
14. El Zein N., Badran B.M., and Sariban E. The neuropeptide pituitary adenylate cyclase activating protein stimulates human monocytes by transactivation of the Trk/NGF pathway. Cell. Signal 19 (2007) 152-162
15. Rodriguez-Viciana P., Warne P.H., Dhand R., Vanhaesebroeck B., Gout I., Fry M.J., Waterfield M.D., and Downward J. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 370 (1994) 527-532
16. Joyal J.L., Burks D.J., Pons S., Matter W.F., Vlahos C.J., White M.F., and Sacks D.B. Calmodulin activates phosphatidylinositol 3-kinase. J. Biol. Chem. 272 (1997) 28183-28186
17. Eisinger D.A., and Ammer H. delta-Opioid receptors stimulate ERK1/2 activity in NG108-15 hybrid cells by integrin-mediated transactivation of TrkA receptors. FEBS Lett. 582 (2008) 3325-3329
18. Selley D.E., Breivogel C.S., and Childers S.R. Opioid inhibition of adenylyl cyclase in membranes from pertussis toxin-treated NG108-15 cells. J. Recept. Signal Transduct. Res. 18 (1998) 25-49
19. Wu E.H., and Wong Y.H. Activation of delta-, kappa-, and mu-opioid receptors induces phosphorylation of tuberin in transfected HEK 293 cells and native cells. Biochem. Biophys. Res. Commun. 334 (2005) 838-844
20. Schulz K., Danner S., Bauer P., Schröder S., and Lohse M.J. Expression of phosducin in a phosducin-negative cell line reveals functions of a Gbetagamma-binding protein. J. Biol. Chem. 271 (1996) 22546-22551
21. Rochdi M.D., and Parent J.L. Galphaq-coupled receptor internalization specifically induced by Galphaq signaling. Regulation by EBP50. J. Biol. Chem. 278 (2003) 17827-17837
22. Sallese M., Mariggiò S., D'Urbano E., Iacovelli L., and De Blasi A. Selective regulation of Gq signaling by G protein-coupled receptor kinase 2: direct interaction of kinase N terminus with activated galphaq. Mol. Pharmacol. 57 (2000) 826-831
23. Polakiewicz R.D., Schieferl S.M., Gingras A.C., Sonenberg N., and Comb M.J. mu-Opioid receptor activates signaling pathways implicated in cell survival and translational control. J. Biol. Chem. 273 (1998) 23534-23541
24. Clark M.J., Emmerson P.J., Mansour A., Akil H., Woods J.H., Portoghese P.S., Remmers A.E., and Medzihradsky F. Opioid efficacy in a C6 glioma cell line stably expressing the delta opioid receptor. J. Pharmacol. Exp. Ther. 283 (1997) 501-510
25. Ikeda K., Kobayashi T., Ichikawa T., Usui H., and Kumanishi T. Functional couplings of the delta- and the kappa-opioid receptors with the G-protein-activated K+ channel. Biochem. Biophys. Res. Commun. 208 (1995) 302-308
26. Andjelković M., Jakubowicz T., Cron P., Ming X.F., Han J.W., and Hemmings B.A. Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 5699-5704
27. Strassheim D., Law P.Y., and Loh H.H. Contribution of phospholipase C-beta3 phosphorylation to the rapid attenuation of opioid-activated phosphoinositide response. Mol. Pharmacol. 53 (1998) 1047-1053
28. Wollemann M., and Benyhe S. Non-opioid actions of opioid peptides. Life Sci. 75 (2004) 257-270
29. Lee J.W., Joshi S., Chan J.S., and Wong Y.H. Differential coupling of mu-, delta-, and kappa-opioid receptors to G alpha16-mediated stimulation of phospholipase C. J. Neurochem. 70 (1998) 2203-2211
30. Ciccarelli M., Cipolletta E., Santulli G., Campanile A., Pumiglia K., Cervero P., Pastore L., Astone D., Trimarco B., and Iaccarino G. Endothelial beta2 adrenergic signaling to AKT: role of Gi and SRC. Cell. Signal. 19 (2007) 1949-1955
31. Dickenson J.M. Stimulation of protein kinase B and p70 S6 kinase by the histamine H1 receptor in DDT1MF-2 smooth muscle cells. Br. J. Pharmacol. 135 (2002) 1967-1976
32. Moule S.K., Welsh G.I., Edgell N.J., Foulstone E.J., Proud C.G., and Denton R.M. Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and beta-adrenergic agonists in rat epididymal fat cells. Activation of protein kinase B by wortmannin-sensitive and -insensitive mechanisms. J. Biol. Chem. 272 (1997) 7713-7719
33. Thelen M., Wymann M.P., and Langen H. Wortmannin binds specifically to 1-phosphatidylinositol 3-kinase while inhibiting guanine nucleotide-binding protein-coupled receptor signaling in neutrophil leukocytes. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 4960-4964
34. Vlahos C.J., Matter W.F., Hui K.Y., and Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269 (1994) 5241-5248
35. Pello O.M., Duthey B., García-Bernal D., Rodríguez-Frade J.M., Stein J.V., Teixido J., Martínez C., and Mellado M. Opioids trigger alpha 5 beta 1 integrin-mediated monocyte adhesion. J. Immunol. 176 (2006) 1675-1685
36. Scheid M.P., Huber M., Damen J.E., Hughes M., Kang V., Neilsen P., Prestwich G.D., Krystal G., and Duronio V. Phosphatidylinositol (3,4,5)P3 is essential but not sufficient for protein kinase B (PKB) activation; phosphatidylinositol (3,4)P2 is required for PKB phosphorylation at Ser-473: studies using cells from SH2-containing inositol-5-phosphatase knockout mice. J. Biol. Chem. 277 (2002) 9027-9035
37. Xu J., Wu D., Slepak V.Z., and Simon M.I. The N terminus of phosducin is involved in binding of beta gamma subunits of G protein. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 2086-2090
38. Zhang W.B., Zhang Z., Ni Y.X., Wu Y.L., and Pei G. A novel function of Goalpha: mediation of extracellular signal-regulated kinase activation by opioid receptors in neural cells. J. Neurochem. 86 (2003) 1213-1222
39. Kroll S.D., Omri G., Landau E.M., and Iyengar R. Activated alpha subunit of Go protein induces oocyte maturation. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 5182-5186
40. Gliki G., Wheeler-Jones C., and Zachary I. Vascular endothelial growth factor induces protein kinase C (PKC)-dependent Akt/PKB activation and phosphatidylinositol 3′-kinase-mediates PKC delta phosphorylation: role of PKC in angiogenesis. Cell. Biol. Int. 26 (2002) 751-759
41. Ohmichi M., Pang L., Ribon V., Gazit A., Levitzki A., and Saltiel A.R. The tyrosine kinase inhibitor tyrphostin blocks the cellular actions of nerve growth factor. Biochemistry 32 (1993) 4650-4658
42. Burgaud J.L., and Baserga R. Intracellular transactivation of the insulin-like growth factor I receptor by an epidermal growth factor receptor. Exp. Cell Res. 223 (1996) 412-419
43. Párrizas M., Gazit A., Levitzki A., Wertheimer E., and LeRoith D. Specific inhibition of insulin-like growth factor-1 and insulin receptor tyrosine kinase activity and biological function by tyrphostins. Endocrinology 138 (1997) 1427-1433
44. Kremer N.E., D'Arcangelo G., Thomas S.M., DeMarco M., Brugge J.S., and Halegoua S. Signal transduction by nerve growth factor and fibroblast growth factor in PC12 cells requires a sequence of src and ras actions. J. Cell. Biol. 115 (1991) 809-819
45. Peterson J.E., Kulik G., Jelinek T., Reuter C.W., Shannon J.A., and Weber M.J. Src phosphorylates the insulin-like growth factor type I receptor on the autophosphorylation sites. Requirement for transformation by src. J. Biol. Chem. 271 (1996) 31562-31571
46. Belcheva M.M., Gucker S., Chuang D.M., Clark W.G., Jefcoat L.B., McHale R.J., Toth G., Borsodi A., and Coscia C.J. Modulation of opioid binding associated with nuclear matrix and nuclear membranes of NG108-15 cells. J. Pharmacol. Exp. Ther. 274 (1995) 1513-1523
47. Martelli A.M., Borgatti P., Bortul R., Manfredini M., Massari L., Capitani S., and Neri L.M. Phosphatidylinositol 3-kinase translocates to the nucleus of osteoblast-like MC3T3-E1 cells in response to insulin-like growth factor I and platelet-derived growth factor but not to the proapoptotic cytokine tumor necrosis factor alpha. J. Bone Miner. Res. 15 (2000) 1716-1730
48. Lim M.A., Kikani C.K., Wick M.J., and Dong L.Q. Nuclear translocation of 3′-phosphoinositide-dependent protein kinase 1 (PDK-1): a potential regulatory mechanism for PDK-1 function. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 14006-14011
49. Pap M., and Cooper G.M. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J. Biol. Chem. 273 (1998) 19929-19932
50. Kugawa F., Nakamura M., Ueno A., and Aoki M. Over-expressed Bcl-2 cannot suppress apoptosis via the mitochondria in buprenorphine hydrochloride-treated NG108-15 cells. Biol. Pharm. Bull. 27 (2004) 1340-1347
51. Zhang J., Haddad G.G., and Xia Y. delta-, but not mu- and kappa-, opioid receptor activation protects neocortical neurons from glutamate-induced excitotoxic injury. Brain Res. 885 (2000) 143-153
52. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., Frisch S., and Reed J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science. 282 (1998) 1318-1321
53. Huigsloot M., Tijdens I.B., Mulder G.J., and van de Water B. Differential regulation of phosphatidylserine externalization and DNA fragmentation by caspases in anticancer drug-induced apoptosis of rat mammary adenocarcinoma MTLn3 cells. Biochem. Pharmacol. 62 (2001) 1087-1097
54. Yao L.L., Wang Y.G., Cai W.J., Yao T., and Zhu Y.C. Survivin mediates the anti-apoptotic effect of delta-opioid receptor stimulation in cardiomyocytes. J. Cell Sci. 120 (2007) 895-907
55. Mitsiades C.S., Mitsiades N., Poulaki V., Schlossman R., Akiyama M., Chauhan D., Hideshima T., Treon S.P., Munshi N.C., Richardson P.G., and Anderson K.C. Activation of NF-kappaB and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene 21 (2002) 5673-5683
56. Russo S.J., Bolanos C.A., Theobald D.E., DeCarolis N.A., Renthal W., Kumar A., Winstanley C.A., Renthal N.E., Wiley M.D., Self D.W., Russell D.S., Neve R.L., Eisch A.J., and Nestler E.J. IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat. Neurosci. 10 (2007) 93-99