Cannabinoids promote oligodendrocyte progenitor survival: Involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling

Journal of Neuroscience

Volumn 22, Issue 22, 2002, Pages 9742-9753

  Molina Holgado, Eduardo ^a   Vela, José M ^b   Arévalo Martín, Angel ^a   Almazán, Guillermina ^c   Molina Holgado, Francisco ^d   Borrell, José ^a   Guaza, Carmen ^a  

^a INSTITUTO CAJAL   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Akt; Apoptosis; CB1 receptors; CB2 receptors; Glycogen synthase kinase 3 ; Oligodendrocytes

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CASPASE 3; DEXANABINOL; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RIMONABANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNOCYTOCHEMISTRY; INFLAMMATION; NICK END LABELING; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; WESTERN BLOTTING; WHITE MATTER;

EID: 0037111841     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-22-09742.2002     Document Type: Article

References (65)

1. Achiron A, Miron S, Lavie V, Margalit R, Biegon A (2000) Dexanabinol (HU-211) effect on experimental autoimmune encephalomyelitis: Implications for the treatment of acute relapses of multiple sclerosis. J Neuroimmunol 102:26-31.
2. Almazan G, Afar DEH, Bell JC (1993) Phosphorylation and disruption of intermediate filament proteins in oligodendrocyte precursor cultures treated with calyculin A. J Neurosci Res 36:163-172.
3. Back SA, Gan X, Li Y, Rosenberg PA, Volpe JJ (1998) Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 18:6241-6253.
4. Back SA, Han BH, Lou NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22:455-463.
5. Baker D, Pryce G, Croxford JL, Brown P, Pertwee RG, Huffman JW, Layward L (2000) Cannabinoids control spasticity and tremor in a multiple sclerosis model. Nature 404:84-87.
6. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31-46.
7. Barres BA, Schmid R, Sendnter M, Raff MC (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118:283-295.
8. Berrendero F, García-Gil L, Hernández ML, Romero J, Cebeira M, de Miguel R, Ramos JA, Fernández-Ruiz JJ (1998) Localization of mRNA expression and activation of signal transduction mechanisms for cannabinoid receptor in rat brain during fetal development. Development 125:3179-3188.
9. Bouaboula M, Bourrie B, Rinaldi-Carmona M, Shire D, Le Fur G, Casellas P (1995a) Stimulation of cannabinoid receptor CB1 induces krox-24 expression in human astrocytoma cells. J Biol Chem 270:13973-13980.
10. Bouaboula M, Poinot-Chazel C, Bourrie B, Canat X, Calandra B, Rinaldi-Carmona M, Le Fur G, Casellas P (1995b) Activation of mitogen-activated protein kinases by stimulation of the central cannabinoid receptor CB1. Biochem J 312:637-641.
11. Breivogel CS, Griffin G, Di Marzo V, Martin BR (2001) Evidence for a new G-protein-coupled cannabinoid receptor in mouse brain. Mol Pharmacol 60:155-163.
12. Brunet A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11:297-305.
13. Cabral GA, Harmon KN, Carlisle SJ (2001) Cannabinoid-mediated inhibition of inducible nitric oxide production by rat microglial cells: Evidence for CB1 receptor participation. Adv Exp Med Biol 493:207-214.
14. Carlisle SJ, Marciano-Cabral F, Staab A, Ludwick C, Cabral GA (2002) Differential expression of the CB2 cannabinoid receptor by rodent macrophages and macrophage-like cells in relation to cell activation. Int Immunopharmacol 2:69-82.
15. Chan TO, Rittenhouse SE, Tsichlis PN (1999) AKT/PKB and other D3 phosphoinositide-regulated kinases: Kinase activation by phosphoinositide-dependent phosphorylation. Annu Rev Biochem 68:965-1014.
16. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD (2000) NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20:6404-6412.
17. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789.
18. Culbert AA, Brown MJ, Frame S, Hagen T, Cross DA, Bax B, Reith AD (2001) GSK-3 inhibition by adenoviral FRAT1 overexpression is neuroprotective and induces Tau dephosphorylation and β-catenin stabilization without elevation of glycogen synthase activity. FEBS Lett 507:288-294.
19. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946-1949.
20. Ebner S, Dunbar M, McKinnon RD (2000) Distinct roles for PI3K in proliferation and survival of oligodendrocyte progenitor cells. J Neurosci Res 62:336-345.
21. Elyaman W, Terro F, Wong NS, Hugon J (2002) In vivo activation and nuclear translocation of phosphorylated glycogen synthase kinase-3β in neuronal apoptosis: Links to tau phosphorylation. Eur J Neurosci 15:651-660.
22. Fernandez PA, Tang DG, Cheng L, Prochiantz A, Mudge AW, Raff MC (2000) Evidence that axon-derived neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron 28:81-90.
23. Flores AI, Mallon BS, Matsui T, Ogawa W, Rosenzweig A, Okamoto T, Macklin WB (2000) Akt-mediated survival of oligodendrocytes induced by neuregulins. J Neurosci 20:7622-7630.
24. Galve-Roperh I, Sánchez C, Cortés ML, Gómez del Pulgar T, Izquierdo M, Guzmán M (2000) Antitumoral action of cannabinoids: Involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat Med 6:313-319.
25. Gard AL, Burrell MR, Pfeiffer SE, Rudge JS, Williams II WC (1995) Astroglial control of oligodendrocyte survival mediated by PDGF and leukemia inhibitory factor-like protein. Development 121:2187-2197.
26. Gómez del Pulgar T, Velasco G, Guzman M (2000) The CB1 cannabinoid receptor is coupled to the activation of protein kinase B/Akt. Biochem J 347:369-373.
27. Gu C, Cassacia-Bonnefil P, Srinivasan A, Chao MV (1999) Oligodendrocyte apoptosis mediated by caspase activation. J Neurosci 19:3043-3049.
28. 1 receptor. Proc Natl Acad Sci USA 98:3662-3665.
29. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study. J Neurosci 11:563-583.
30. Hetman M, Cavanaugh JE, Kimelman D, Xia Z (2000) Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J Neurosci 20:2567-2574.
31. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-202.
32. Huang CC, Lo SW, Hsu KS (2001) Presynaptic mechanism underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol (Lond) 532:731-748.
33. Keirstead HS, Blakemore WF (1999) The role of oligodendrocytes and oligodendrocyte progenitors in CNS remyelination. Adv Exp Med Biol 468:183-197.
34. Klein TW, Lane B, Newton CA, Friedman H (2000) The cannabinoid system and cytokine network. Proc Soc Exp Biol Med 225:1-8.
35. Lassmann H (1998) Neuropathology in multiple sclerosis: New concepts. Mult Scler 4:93-98.
36. Levine JM, Reynolds R, Fawcett JW (2001) The oligodendrocyte precursor cell in health and disease. Trends Neurosci 24:3947.
37. Lyman WD, Sonett JR, Brosnan CF, Elkin R, Bornstein MB (1989) Delta-9-tetrahydrocannabinol: A novel treatment for experimental autoimmune encephalomyelitis. J Neuroimmunol 23:73-81.
38. Mailleux P, Vanderhaeghen JJ (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: A comparative receptor-binding radioautography and in situ hybridization histochemistry. Neuroscience 48:655-668.
39. Matsuda LA, Lolait SJ, Brownstain MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561-564.
40. Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535-550.
41. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
42. Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR, Pertwee RJ, Griffin G, Bayewitch M, Barg, J Vogel Z (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83-90.
43. Moldrich G, Wenger T (2000) Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides 21:1735-1742.
44. Molina-Holgado E, Vela JM, Arévalo-Martín A, Guaza C (2001) LPS/IFN-γ cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the anti-inflammatory cytokine IL-10. Eur J Neurosci 13:493-502.
45. Molina-Holgado F, Molina-Holgado E, Guaza C, Rothwell NJ (2002) Role of CB1 and CB2 receptors in the inhibitory effects of cannabinoids on lipopolysaccharide-induced nitric oxide release. J Neurosci Res 67:829-836.
46. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61-65.
47. Nagayama T, Sinor AD, Simon RP, Chen J, Graham SH, Jin K, Greenberg DA (1999) Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J Neurosci 19:2987-2995.
48. Ong WY, Mackie K (1999) A light and electron microscopic study of the CB1 cannabinoid receptor in primate brain. Neuroscience 92:1177-1191.
49. Panikashvili D, Simeonidou C, Ben-Shabat S, Hanus L, Breuer A, Mechoulam R, Shohami E (2001) An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413:527-531.
50. Pap M, Cooper GM (2002) Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3β signaling pathway. Mol Cell Biol 22:578-586.
51. Pertwee RG (1997) Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol Ther 74:129-180.
52. Pertwee RG (2001) Cannabinoid receptors and pain. Prog Neurobiol 63:569-611.
53. Puffenbarger RA, Boothe AC, Cabral GA (2000) Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells. Glia 29:58-69.
54. Rinaldi-Carmona M, Barth F, Heaulme M, Shire D, Calandra B, Congy C, Martinez S, Maruani J, Neliat G, Caput D, Ferrara P, Soubrié P, Brelière JC, Le Fur G (1994) SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Lett 350:240-244.
55. Rodríguez JJ, Mackie K, Pickel VM (2001) Ultrastructural localization of the CB1 cannabinoid receptor in μ-opioid receptor patches of the rat caudate putamen nucleus. J Neurosci 21:823-833.
56. Sagan S, Venance L, Torrens Y, Cordier J, Glowinski J, Giaume C (1999) Anandamide and WIN 55212-2 inhibit cyclic AMP formation through G-protein-coupled receptors distinct from CB1 cannabinoid receptors in cultured astrocytes. Eur J Neurosci 11:691-699.
57. Shen M, Thayer SA (1998) Cannabinoid receptor agonists protect cultured rat hippocampal neurons from excitotoxicity. Mol Pharmacol 54:459-462.
58. Soane L, Cho H-J, Niculescu F, Rus H, Shin ML (2001) C5b-9 terminal complement complex protects oligodendrocytes from death by regulating Bad through phosphatidylinositol 3-kinase/Akt pathway. J Immunol 167:2305-2311.
59. Takano R, Hisahara S, Namikawa K, Kiyama H, Okano H, Miura M (2000) Nerve growth factor protects oligodendrocytes from tumor necrosis factor-α-induced injury through Akt-mediated signaling mechanism. J Biol Chem 275:16360-16365.
60. van der Stelt M, Veldhuis WB, van Haaften GW, Fezza F, Bisogno T, Bär PR, Veldink GA, Vliegenthart JFG, Di Marzo V, Nicolay K (2001) Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci 21:8765-8771.
61. Vela JM, González B, Castellano B (1998) Understanding glial abnormalities associated with myelin deficiency in the jimpy mutant mouse. Brain Res Rev 26:29-42.
62. Vemuri GS, McMorris FA (1996) Oligodendrocytes and their precursors require phosphatidylinositol 3-kinase signaling for survival. Development 122:2529-2537.
63. Williamson EM, Evans FJ (2000) Cannabinoids in clinical practice. Drugs 60:1303-1314.
64. Yasuda T, Grinspan J, Stern J, Franceschini B, Bannerman P, Pleasure D (1995) Apoptosis occurs in the oligodendroglial lineage and is prevented by basic fibroblast growth factor. J Neurosci Res 40:306-317.
65. Zhou L, Trapp BD, Miller RH (1998) Demyelination in the central nervous system mediated by an anti-oligodendrocyte antibody. J Neurosci Res 54:158-168.