μ-opioid receptor activation prevents apoptosis following serum withdrawal in differentiated SH-SY5Y cells and cortical neurons via phosphatidylinositol 3-kinase

Neuropharmacology

Volumn 44, Issue 4, 2003, Pages 482-492

  Iglesias, M ^a   Segura, M F ^a   Comella, J X ^a   Olmos, G ^b  

^a UNIVERSITY OF LLEIDA   (Spain)

^b UNIVERSITAT DE LES ILLES BALEARS   (Spain)

Author keywords

Akt; Apoptosis; Cortical neurons; Opioid; Phosphatidylinositol 3 kinase; SH SY5Y cells

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ALKALOID; BETA FUNALTREXAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; ENKEPHALIN DERIVATIVE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; MU OPIATE RECEPTOR ANTAGONIST; NALOXONE; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RETINOIC ACID; TRYPAN BLUE;

APOPTOSIS; ARTICLE; BRAIN CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STAINING;

EID: 0037333912     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3908(03)00024-8     Document Type: Article

References (63)

1. Alessi D.R., Cohen P. Mechanism of activation and function of protein kinase B. Current Opinion in Genetics and Development. 8:1998;55-62.
2. Alessi D.R., Cuenda A., Cohen P., Dudley D.T., Saltiel A.R. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. Journal of Biological Chemistry. 270:1995;27489-27494.
3. Andjelkovic M., Alessi D.R., Meier R., Fernandez A., Lamb N.J.C., Frech M., et al. Role of translocation in the activation and function of protein kinase B. Journal of Biological Chemistry. 272:1997;31515-31524.
4. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., et al. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 15:1995;961-973.
5. Behrens M.M., Strasser U., Koh J.Y., Gwag B.J., Choi D.W. Prevention of neuronal apoptosis by phorbol ester-induced activation of protein kinase C: blockade of p38 mitogen-activated protein kinase. Neuroscience. 94:1999;917-927.
6. Bommakanti R.J., Vinayak S., Simonds W.F. Dual regulation of Akt/protein kinase B by heterotrimeric G protein subunits. Journal of Biological Chemistry. 275:2000;38870-38876.
7. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 96:1999;857-868.
8. Connor M., Christie M.D. Opioid receptor signalling mechanisms. Clinical and Experimental Pharmacology and Physiology. 26:1999;493-499.
9. Dawson G., Dawson S.A., Goswami R. Chronic exposure to κ-opioids enhances the susceptibility of inmortalized neurons (F-11κ7). to apoptosis-inducing drugs by a mechanism that may involve ceramide. Journal of Neurochemistry. 68:1997;2363-2370.
10. Dermitzaki E., Chatzaki E., Margioris A.N. Opioids transiently prevent activation of apoptotic mechanisms following short periods of serum withdrawal. Journal of Neurochemistry. 74:2000;960-969.
11. Dhawan B.N., Cesselin F., Raghubir R., Reisine T., Bradley P.B., Portoghese P.S., et al. International Union of Pharmacology. XII. Classification of opioid receptors. Pharmacological Reviews. 48:1996;567-592.
12. Downward J. How BAD phosphorylation is good for survival. Nature Cell Biology. 1:1999;E33-E35.
13. Dudek H., Datta S.R., Franke T.F., Bimbaum M.J., Yao R., Cooper G.M., et al. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science. 275:1997;661-665.
14. 35S]-thio)triphosphate binding. British Journal of Pharmacology. 121:1997;1422-1428.
15. Encinas M., Iglesias M., Llecha N., Comella J.X. Extracellular-regulated kinases and phosphatidylinositol 3-kinase are involved in brain-derived neurotrophic factor-mediated survival and neuritogenesis of the neuroblastoma cell line SH-SY5Y. Journal of Neurochemistry. 73:1999;1409-1421.
16. Encinas M., Iglesias M., Liu Y., Wang H., Muhaisen A., Ceña V., et al. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. Journal of Neurochemistry. 75:2000;991-1003.
17. Fecho K., Lysle D.T. Heroin-induced alterations in leukocyte numbers and apoptosis in the rat spleen. Cellular Immunology. 202:2000;113-123.
18. Fukuda K., Kato S., Morikawa H., Shoda T., Mori K. Functional coupling of the δ-, μ-, and κ-opioid receptors to mitogen-activated protein kinase and arachidonate release in chinese hamster ovary cells. Journal of Neurochemistry. 67:1996;1309-1316.
19. Gilman A.G. G proteins: transducers of receptor-generated signals. Annual Review of Biochemistry. 56:1987;615-649.
20. Gioannini T.L., Yao Y.H., Hiller J.M., Taylor L.P., Simon E.J. Antisera against peptides derived from a purified μ-opioid binding protein recognize the protein as well as μ-opioid receptors in brain regions and a cell line. Molecular Pharmacology. 44:1993;796-801.
21. 1 cannabinoid receptor is coupled to the activation of protein kinase B/Akt. Biochemical Journal. 347:2000;369-373.
22. Gómez del Pulgar T., de Ceballos M.L., Guzmán M., Velasco G. Cannabinoids protect astrocytes from ceramide-induced apoptosis through the phosphatidylinositol 3-kinase/protein kinase B. Journal of Biological Chemistry. 277:2002;36527-36533.
23. Goswami R., Dawson S.A., Dawson G. Cyclic AMP protects against staurosporine and wortmannin-induced apoptosis in both embryonic and immortalized (F-11κ7) neurons. Journal of Neurochemistry. 70:1998;1376-1382.
24. Harrison L.M., Kastin A.J., Zadina J.E. Tyr-W-MIF-1 attenuates down regulation of opiate receptors in SH-SY5Y human neuroblastoma cells. Journal of Pharmacology and Experimental Therapeutics. 284:1998;611-617.
25. Hetman M., Kanning K., Cavanaugh J.E., Xia Z. Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. Journal of Biological Chemistry. 274:1999;22569-22580.
26. Hou Y.N., Vlaskovska M., Cebers G., Kasakov L., Liljequist S., Terenius L. A μ-receptor opioid agonist induces AP-1 and NF-κB transcription factor activity in primary cultures of rat cortical neurons. Neuroscience Letters. 212:1996;159-162.
27. Katada T., Kurosu H., Okada T., Suzuki T., Tsujimoto N., Takasuga S., et al. Synergistic activation of a family of phosphoinositide 3-kinase via G-protein coupled and tyrosine kinase-related receptors. Chemistry and Physics of Lipids. 98:1999;79-86.
28. Kim M.S., Cheong Y.P., So H.S., Lee K.M., Kim T.Y., Oh J., et al. Protective effects of morphine in peroxynitrite-induced apoptosis of primary rat neonatal astrocytes: potential involvement of G protein and phosphatidylinositol 3-kinase (PI3 kinase). Biochemical Pharmacology. 61:2001a;779-786.
29. Kim A.H., Khursigara G., Sun X., Franke T., Chao M.V. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Molecular and Cellular Biology. 21:2001b;893-901.
30. Kops G.J., Burgering B.M. Forkhead transcription factors: new insights into protein kinase B (c-Akt) signaling. Journal of Molecular Medicine. 77:1999;656-665.
31. Kugawa F., Arae K., Ueno A., Aoki M. Buprenorphine hydrochloride induces apoptosis in NG108-15 nerve cells. European Journal of Pharmacology. 347:1998;105-112.
32. Kurosu H., Maehama T., Okada T., Yamamoto T.S.H., Fukui Y., Ui M., et al. Heterodimeric phosphoinositide 3-kinase consisting of p85 and p110β is synergistically activated by the βγ subunits of G proteins and phosphotyrosyl peptide. Journal of Biological Chemistry. 272:1997;24252-24256.
33. Law P.Y., McGinn T.M., Campbell K.M., Erickson L.E., Loh H.H. Agonist activation of δ-opioid receptor but not μ-opioid receptor potentiates fetal calf serum of tyrosine kinase receptor-mediated cell proliferation in a cell-line-specific manner. Molecular Pharmacology. 51:1997;152-160.
34. Lawlor M.A., Alessi D.R. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? Journal of Cell Science. 114:2001;2903-2910.
35. Lee F.S., Chao M.V. Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proceedings of the National Academy of Sciences of the USA. 98:2001;3555-3560.
36. Leopoldt D., Hanck T., Exner T., Maier U., Wetzker R., Nürnberg B. Gβγ stimulates phosphoinositide 3-kinase by direct interaction with two domains of the catalytic p110 subunit. Journal of Biological Chemistry. 273:1998;7024-7029.
37. Lopez-Ilasaca M. Signaling from G-protein-coupled receptors to mitogen-activated protein (MAP)-kinase cascades. Biochemical Pharmacology. 56:1998;269-277.
38. Loughlin S.E., Leslie F.M. Opioid receptors and the developing nervous system. Zagon I.S., McLaughlin P.J. Receptors in the Developing Nervous System. Neurotransmitters. vol. 2:1993;185-214 Chapman & Hall, London.
39. Luttrell L.M., Daaka Y., Lefkowitz R.J. Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Current Opinion in Cell Biology. 11:1999;177-183.
40. Mansour A., Fox C.A., Akil H., Watson S.J. Opiod-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends in Neuroscience. 18:1995;22-29.
41. Mattson M.P., Camandola S. NF-κB in neuronal plasticity and neurodegenerative disorders. Journal of Clinical Investigation. 107:2001;247-254.
42. Meriney S.D., Gray D.B., Pilar G. Morphine-induced delay of normal cell death in the avian ciliary ganglion. Science. 228:1985;1451-1453.
43. Meriney S.D., Ford M.J., Oliva D., Pilar G. Endogenous opioids modulate neuronal survival in the developing avian ciliary ganglion. Journal of Neuroscience. 11:1991;3705-3717.
44. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods. 65:1983;55-63.
45. Moule S.K., Welsh G.I., Edgell N.J., Foulstone E.J., Proud C.G., Denton R.M. Regulation of protein kinase B and glycogen synthase kinase-3 by insulin and β-adrenergic agonists in rat epididymal fat cells. Activation of protein kinase B by wortmannin-sensitive and -insensitive mechanisms. Journal of Biological Chemistry. 272:1997;7713-7719.
46. Murga C., Laguinge L., Wetzker R., Cuadrado A., Gutkind J.S. Activation of Akt/protein kinase B by G protein-coupled receptors. Journal of Biological Chemistry. 273:1998;19080-19085.
47. Murga C., Fukuhara S., Gutkind J.S. A novel role for phosphatidylinositol 3-kinase β in signaling from G protein-coupled receptors to Akt. Journal of Biological Chemistry. 275:2000;12069-12073.
48. Nestler E.J., Berhow M.T., Brodkin E.S. Molecular mechanism of drug addiction: adaptations in signal transduction pathways. Molecular Psychiatry. 1:1996;190-199.
49. Opanashuk L.A., Hauser K.F. Opposing actions of the EGF family and opioids: heparin binding-epidermal growth factor (HB-EGF) protects mouse cerebellar neuroblasts against the antiproliferative effect of morphine. Brain Research. 804:1998;87-94.
50. Pérez-Navarro E., Alberch J., Arenas E., Marsal J. Nerve growth factor and its receptor are differentially modified by chronic naltrexone treatment during rat brain development. Neuroscience Letters. 149:1993;47-50.
51. Polakiewicz R.D., Schieferl S.M., Gingras A.-C., Sonenberg N., Comb M.J. μ-Opioid receptor activates signaling pathways implicated in cell survival and translational control. Journal of Biological Chemistry. 273:1998;23534-23541.
52. Raynor K., Kong H., Chen Y., Yasuda K., Yu L., Bell G.I., et al. Pharmacological characterization of the cloned κ-, δ- and μ-opioid receptors. Molecular Pharmacology. 45:1994;330-334.
53. Sakaguchi M., Fujimori T., Satoh T., Satoh M., Takeuchi M., Matsumura E. Effects of opioids on neuronal survival in culture of embryonic chick dorsal root ganglion neurons. Neuroscience Letters. 262:1999;17-20.
54. Schmahl W., Funk R., Miaskowski U., Plendl J. Long-lasting effects of naltrexone, an opioid antagonist, on cell proliferation in developing rat forebrain. Brain Research. 486:1989;297-300.
55. Singhal P.C., Kapasi A.A., Reddy K., Franki N., Gibbons N., Ding G. Morphine promotes apoptosis in Jurkat cells. Journal of Leukocyte Biology. 66:1999;650-658.
56. Takemori A.E., Larson D.L., Portoghese P.S. The irreversible narcotic antagonistic and reversible agonistic properties of the fumaramate methyl ester derivative of naltrexone. European Journal of Pharmacology. 70:1981;445-451.
57. Vlahos C.J., Matter W.F., Hui K.Y., Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). Journal of Biological Chemistry. 269:1994;5241-5248.
58. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science. 284:1999;339-343.
59. Weiner J.A., Chun J. Schwann cell survival mediated by the signaling phospholipid lysophosphatidic acid. Proceedings of the National Academy of Sciences of the USA. 96:1999;5233-5238.
60. q- and Gβγ-dependent pathway that involves phosphoinositide 3-kinase and Akt. Journal of Biological Chemistry. 275:2000;24907-24914.
61. Yin D.L., Ren X.H., Zheng Z.L., Pu L., Jiang L.Z., Ma L., et al. Etorphine inhibits cell growth and induces apoptosis in SK-N-SH cells: involvement of pertussis toxin-sensitive G proteins. Neuroscience Research. 29:1997;121-127.
62. Yu V.C., Sadée W. Efficacy and tolerance of narcotic analgesics at the Mu opioid receptor in differentiated human neuroblastoma cells. Journal of Pharmacology and Experimental Therapeutics. 245:1988;350-355.
63. Zadina J.E., Harrison L.M., Ge L.J., Kastin A.J., Chang S.L. Differential regulation of Mu and Delta opiate receptors by morphine, selective agonists and antagonists and differentiating agents in SH-SY5Y human neuroblastoma cells. Journal of Pharmacology and Experimental Therapeutics. 270:1994;1086-1096.