Activation of cannabinoid CB2 receptor-mediated AMPK/CREB pathway reduces cerebral ischemic injury

American Journal of Pathology

Volumn 182, Issue 3, 2013, Pages 928-939

  Choi, In Young ^a   Ju, Chung ^a   Anthony Jalin, Angela M A ^a   Lee, Da In ^b   Prather, Paul L ^c   Kim, Won Ki ^a  

^a Korea University College of Medicine   (South Korea)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID 2 RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MANGANESE SUPEROXIDE DISMUTASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN BCL 2; PROTEIN KINASE B;

ANIMAL TISSUE; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; EMBRYO; ENZYME INDUCTION; IMMUNOREACTIVITY; MALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REOXYGENATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BRAIN INJURIES; BRAIN ISCHEMIA; BRAIN-DERIVED NEUROTROPHIC FACTOR; CATALASE; CELL DEATH; CEREBRAL CORTEX; CEREBRAL INFARCTION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FREE RADICAL SCAVENGERS; GLUCOSE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; OXIDATIVE STRESS; OXYGEN; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB2; SESQUITERPENES; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84874536805     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.11.024     Document Type: Article

References (68)

1. M.A. Moskowitz, E.H. Lo, and C. Iadecola The science of stroke: mechanisms in search of treatments Neuron 67 2010 181 198
2. C.J. Hillard Role of cannabinoids and endocannabinoids in cerebral ischemia Curr Pharm Des 14 2008 2347 2361
3. M. Zhang, B.R. Martin, M.W. Adler, R.J. Razdan, W. Kong, D. Ganea, and R.F. Tuma Modulation of cannabinoid receptor activation as a neuroprotective strategy for EAE and stroke J Neuroimmune Pharmacol 4 2009 249 259
4. G.A. Cabral, and L. Griffin-Thomas Emerging role of the cannabinoid receptor CB2 in immune regulation: therapeutic prospects for neuroinflammation Expert Rev Mol Med 11 2009 e3
5. C. Iadecola, and J. Anrather The immunology of stroke: from mechanisms to translation Nat Med 17 2011 796 808
6. S. Batkai, D. Osei-Hyiaman, H. Pan, O. El-Assal, M. Rajesh, P. Mukhopadhyay, F. Hong, J. Harvey-White, A. Jafri, G. Hasko, J.W. Huffman, B. Gao, G. Kunos, and P. Pacher Cannabinoid-2 receptor mediates protection against hepatic ischemia/reperfusion injury FASEB J 21 2007 1788 1800
7. M. Rajesh, H. Pan, P. Mukhopadhyay, S. Batkai, D. Osei-Hyiaman, G. Hasko, L. Liaudet, B. Gao, and P. Pacher Cannabinoid-2 receptor agonist HU-308 protects against hepatic ischemia/reperfusion injury by attenuating oxidative stress, inflammatory response, and apoptosis J Leukoc Biol 82 2007 1382 1389
8. F. Montecucco, S. Lenglet, V. Braunersreuther, F. Burger, G. Pelli, M. Bertolotto, F. Mach, and S. Steffens CB(2) cannabinoid receptor activation is cardioprotective in a mouse model of ischemia/reperfusion J Mol Cell Cardiol 46 2009 612 620
9. R.G. Pertwee Emerging strategies for exploiting cannabinoid receptor agonists as medicines Br J Pharmacol 156 2009 397 411
10. P. Pacher, and G. Hasko Endocannabinoids and cannabinoid receptors in ischaemia-reperfusion injury and preconditioning Br J Pharmacol 153 2008 252 262
11. M. Zhang, M.W. Adler, M.E. Abood, D. Ganea, J. Jallo, and R.F. Tuma CB2 receptor activation attenuates microcirculatory dysfunction during cerebral ischemic/reperfusion injury Microvasc Res 78 2009 86 94
12. M. Zhang, B.R. Martin, M.W. Adler, R.K. Razdan, J.I. Jallo, and R.F. Tuma Cannabinoid CB(2) receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model J Cereb Blood Flow Metab 27 2007 1387 1396
13. M. Zhang, B.R. Martin, M.W. Adler, R.K. Razdan, D. Ganea, and R.F. Tuma Modulation of the balance between cannabinoid CB(1) and CB(2) receptor activation during cerebral ischemic/reperfusion injury Neuroscience 152 2008 753 760
14. S. Murikinati, E. Juttler, T. Keinert, D.A. Ridder, S. Muhammad, Z. Waibler, C. Ledent, A. Zimmer, U. Kalinke, and M. Schwaninger Activation of cannabinoid 2 receptors protects against cerebral ischemia by inhibiting neutrophil recruitment FASEB J 24 2010 788 798
15. J.G. Zarruk, D. Fernandez-Lopez, I. Garcia-Yebenes, M.S. Garcia-Gutierrez, J. Vivancos, F. Nombela, M. Torres, M.C. Burguete, J. Manzanares, I. Lizasoain, and M.A. Moro Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection Stroke 43 2012 211 219
16. J.C. Ashton, R.M. Rahman, S.M. Nair, B.A. Sutherland, M. Glass, and I. Appleton Cerebral hypoxia-ischemia and middle cerebral artery occlusion induce expression of the cannabinoid CB2 receptor in the brain Neurosci Lett 412 2007 114 117
17. N.H. Morgan, I.M. Stanford, and G.L. Woodhall Functional CB2 type cannabinoid receptors at CNS synapses Neuropharmacology 57 2009 356 368
18. E.S. Onaivi, H. Ishiguro, J.P. Gong, S. Patel, P.A. Meozzi, L. Myers, A. Perchuk, Z. Mora, P.A. Tagliaferro, E. Gardner, A. Brusco, B.E. Akinshola, B. Hope, J. Lujilde, T. Inada, S. Iwasaki, D. Macharia, L. Teasenfitz, T. Arinami, and G.R. Uhl Brain neuronal CB2 cannabinoid receptors in drug abuse and depression: from mice to human subjects PLoS One 3 2008 e1640
19. Z.X. Xi, X.Q. Peng, X. Li, R. Song, H.Y. Zhang, Q.R. Liu, H.J. Yang, G.H. Bi, J. Li, and E.L. Gardner Brain cannabinoid CB2 receptors modulate cocaine's actions in mice Nat Neurosci 14 2011 1160 1166
20. E.S. Onaivi, H. Ishiguro, J.P. Gong, S. Patel, A. Perchuk, P.A. Meozzi, L. Myers, Z. Mora, P. Tagliaferro, E. Gardner, A. Brusco, B.E. Akinshola, Q.R. Liu, B. Hope, S. Iwasaki, T. Arinami, L. Teasenfitz, and G.R. Uhl Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain Ann N Y Acad Sci 1074 2006 514 536
21. J.P. Gong, E.S. Onaivi, H. Ishiguro, Q.R. Liu, P.A. Tagliaferro, A. Brusco, and G.R. Uhl Cannabinoid CB2 receptors: immunohistochemical localization in rat brain Brain Res 1071 2006 10 23
22. M.D. Van Sickle, M. Duncan, P.J. Kingsley, A. Mouihate, P. Urbani, K. Mackie, N. Stella, A. Makriyannis, D. Piomelli, J.S. Davison, L.J. Marnett, V. Di Marzo, Q.J. Pittman, K.D. Patel, and K.A. Sharkey Identification and functional characterization of brainstem cannabinoid CB2 receptors Science 310 2005 329 332
23. J.L. Lanciego, P. Barroso-Chinea, A.J. Rico, L. Conte-Perales, L. Callen, E. Roda, V. Gomez-Bautista, I.P. Lopez, C. Lluis, J.L. Labandeira-Garcia, and R. Franco Expression of the mRNA coding the cannabinoid receptor 2 in the pallidal complex of Macaca fascicularis J Psychopharmacol 25 2011 97 104
24. M.T. Viscomi, S. Oddi, L. Latini, N. Pasquariello, F. Florenzano, G. Bernardi, M. Molinari, and M. Maccarrone Selective CB2 receptor agonism protects central neurons from remote axotomy-induced apoptosis through the PI3K/Akt pathway J Neurosci 29 2009 4564 4570
25. W.S. Sheng, S. Hu, X. Min, G.A. Cabral, J.R. Lokensgard, and P.K. Peterson Synthetic cannabinoid WIN55,212-2 inhibits generation of inflammatory mediators by IL-1beta-stimulated human astrocytes Glia 49 2005 211 219
26. J. Gertsch, M. Leonti, S. Raduner, I. Racz, J.Z. Chen, X.Q. Xie, K.H. Altmann, M. Karsak, and A. Zimmer Beta-caryophyllene is a dietary cannabinoid Proc Natl Acad Sci U S A 105 2008 9099 9104
27. Y.T. Tung, M.T. Chua, S.Y. Wang, and S.T. Chang Anti-inflammation activities of essential oil and its constituents from indigenous cinnamon (Cinnamomum osmophloeum) twigs Bioresour Technol 99 2008 3908 3913
28. G.F. Passos, E.S. Fernandes, F.M. da Cunha, J. Ferreira, L.F. Pianowski, M.M. Campos, and J.B. Calixto Anti-inflammatory and anti-allergic properties of the essential oil and active compounds from Cordia verbenacea J Ethnopharmacol 110 2007 323 333
29. S. Martin, E. Padilla, M.A. Ocete, J. Galvez, J. Jimenez, and A. Zarzuelo Anti-inflammatory activity of the essential oil of Bupleurum fruticescens Planta Med 59 1993 533 536
30. M.R. Loizzo, R. Tundis, F. Menichini, A.M. Saab, and G.A. Statti Antiproliferative effects of essential oils and their major constituents in human renal adenocarcinoma and amelanotic melanoma cells Cell Prolif 41 2008 1002 1012
31. E.S. Fernandes, G.F. Passos, R. Medeiros, F.M. da Cunha, J. Ferreira, M.M. Campos, L.F. Pianowski, and J.B. Calixto Anti-inflammatory effects of compounds alpha-humulene and (-)-trans-caryophyllene isolated from the essential oil of Cordia verbenacea Eur J Pharmacol 569 2007 228 236
32. A. Di Sotto, G. Mazzanti, F. Carbone, P. Hrelia, and F. Maffei Inhibition by beta-caryophyllene of ethyl methanesulfonate-induced clastogenicity in cultured human lymphocytes Mutat Res 699 2010 23 28
33. J.Y. Cho, H.J. Chang, S.K. Lee, H.J. Kim, J.K. Hwang, and H.S. Chun Amelioration of dextran sulfate sodium-induced colitis in mice by oral administration of beta-caryophyllene, a sesquiterpene Life Sci 80 2007 932 939
34. H.J. Chang, H.J. Kim, and H.S. Chun Quantitative structure-activity relationship (QSAR) for neuroprotective activity of terpenoids Life Sci 80 2007 835 841
35. I.Y. Choi, J.C. Lee, C. Ju, S. Hwang, G.S. Cho, H.W. Lee, W.J. Choi, L.S. Jeong, and W.K. Kim A3 adenosine receptor agonist reduces brain ischemic injury and inhibits inflammatory cell migration in rats Am J Pathol 179 2011 2042 2052
36. J.H. Lim, J.C. Lee, Y.H. Lee, I.Y. Choi, Y.K. Oh, H.S. Kim, J.S. Park, and W.K. Kim Simvastatin prevents oxygen and glucose deprivation/reoxygenation- induced death of cortical neurons by reducing the production and toxicity of 4-hydroxy-2E-nonenal J Neurochem 97 2006 140 150
37. Y. Choi, S.K. Kim, I.Y. Choi, C. Ju, K.W. Nam, S. Hwang, B.W. Kim, M.J. Yoon, M.H. Won, Y.K. Park, and W.K. Kim Amelioration of cerebral infarction and improvement of neurological deficit by a Korean herbal medicine, modified Bo-Yang-Hwan-O-Tang J Pharm Pharmacol 63 2011 695 706
38. I.Y. Choi, J.H. Lim, S. Hwang, J.C. Lee, G.S. Cho, and W.K. Kim Anti-ischemic and anti-inflammatory activity of (S)-cis-verbenol Free Radic Res 44 2010 541 551
39. D. Huang, B. Ou, M. Hampsch-Woodill, J.A. Flanagan, and E.K. Deemer Development and validation of oxygen radical absorbance capacity assay for lipophilic antioxidants using randomly methylated beta-cyclodextrin as the solubility enhancer J Agric Food Chem 50 2002 1815 1821
40. Y. Cai, G.S. Cho, C. Ju, S.L. Wang, J.H. Ryu, C.Y. Shin, H.S. Kim, K.W. Nam, A.M. Jalin, W. Sun, I.Y. Choi, and W.K. Kim Activated microglia are less vulnerable to hemin toxicity due to nitric oxide-dependent inhibition of JNK and p38 MAPK activation J Immunol 187 2011 1314 1321
41. E.V. Golanov, and D.J. Reis Contribution of cerebral edema to the neuronal salvage elicited by stimulation of cerebellar fastigial nucleus after occlusion of the middle cerebral artery in rat J Cereb Blood Flow Metab 15 1995 172 174
42. F.S. den Boon, P. Chameau, Q. Schaafsma-Zhao, W. van Aken, M. Bari, S. Oddi, C.G. Kruse, M. Maccarrone, W.J. Wadman, and T.R. Werkman Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors Proc Natl Acad Sci U S A 109 2012 3534 3539
43. L. Mikasova, L. Groc, D. Choquet, and O.J. Manzoni Altered surface trafficking of presynaptic cannabinoid type 1 receptor in and out synaptic terminals parallels receptor desensitization Proc Natl Acad Sci U S A 105 2008 18596 18601
44. S.J. Carlisle, F. Marciano-Cabral, A. Staab, C. Ludwick, and G.A. Cabral Differential expression of the CB2 cannabinoid receptor by rodent macrophages and macrophage-like cells in relation to cell activation Int Immunopharmacol 2 2002 69 82
45. A. Almeida, M. Delgado-Esteban, J.P. Bolanos, and J.M. Medina Oxygen and glucose deprivation induces mitochondrial dysfunction and oxidative stress in neurones but not in astrocytes in primary culture J Neurochem 81 2002 207 217
46. N.R. Sims, and H. Muyderman Mitochondria, oxidative metabolism and cell death in stroke Biochim Biophys Acta 1802 2010 80 91
47. K. Niizuma, H. Yoshioka, H. Chen, G.S. Kim, J.E. Jung, M. Katsu, N. Okami, and P.H. Chan Mitochondrial and apoptotic neuronal death signaling pathways in cerebral ischemia Biochim Biophys Acta 1802 2010 92 99
48. P. Derkinderen, E. Valjent, M. Toutant, J.C. Corvol, H. Enslen, C. Ledent, J. Trzaskos, J. Caboche, and J.A. Girault Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus J Neurosci 23 2003 2371 2382
49. K.P. Sarker, K.K. Biswas, M. Yamakuchi, K.Y. Lee, T. Hahiguchi, M. Kracht, I. Kitajima, and I. Maruyama ASK1-p38 MAPK/JNK signaling cascade mediates anandamide-induced PC12 cell death J Neurochem 85 2003 50 61
50. F. Molina-Holgado, E. Pinteaux, L. Heenan, J.D. Moore, N.J. Rothwell, and R.M. Gibson Neuroprotective effects of the synthetic cannabinoid HU-210 in primary cortical neurons are mediated by phosphatidylinositol 3-kinase/AKT signaling Mol Cell Neurosci 28 2005 189 194
51. D.R. Sagar, S. Kelly, P.J. Millns, C.T. O'Shaughnessey, D.A. Kendall, and V. Chapman Inhibitory effects of CB1 and CB2 receptor agonists on responses of DRG neurons and dorsal horn neurons in neuropathic rats Eur J Neurosci 22 2005 371 379
52. K. Kitagawa CREB and cAMP response element-mediated gene expression in the ischemic brain FEBS J 274 2007 3210 3217
53. K. Tanaka Alteration of second messengers during acute cerebral ischemia: adenylate cyclase, cyclic AMP-dependent protein kinase, and cyclic AMP response element binding protein Prog Neurobiol 65 2001 173 207
54. Z. Kokaia, G. Andsberg, Q. Yan, and O. Lindvall Rapid alterations of BDNF protein levels in the rat brain after focal ischemia: evidence for increased synthesis and anterograde axonal transport Exp Neurol 154 1998 289 301
55. K. Niizuma, H. Endo, and P.H. Chan Oxidative stress and mitochondrial dysfunction as determinants of ischemic neuronal death and survival J Neurochem 109 Suppl 1 2009 133 138
56. V. Nadler, R. Mechoulam, and M. Sokolovsky Blockade of 45Ca2+ influx through the N-methyl-D-aspartate receptor ion channel by the non-psychoactive cannabinoid HU-211 Brain Res 622 1993 79 85
57. N. Eshhar, S. Striem, R. Kohen, O. Tirosh, and A. Biegon Neuroprotective and antioxidant activities of HU-211, a novel NMDA receptor antagonist Eur J Pharmacol 283 1995 19 29
58. E.S. Onaivi, H. Ishiguro, S. Gu, and Q.R. Liu CNS effects of CB2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity J Psychopharmacol 26 2012 92 103
59. B.K. Atwood, and K. Mackie CB2: a cannabinoid receptor with an identity crisis Br J Pharmacol 160 2010 467 479
60. Y. Dagon, Y. Avraham, Y. Ilan, R. Mechoulam, and E.M. Berry Cannabinoids ameliorate cerebral dysfunction following liver failure via AMP-activated protein kinase FASEB J 21 2007 2431 2441
61. Q.R. Liu, C.H. Pan, A. Hishimoto, C.Y. Li, Z.X. Xi, A. Llorente-Berzal, M.P. Viveros, H. Ishiguro, T. Arinami, E.S. Onaivi, and G.R. Uhl Species differences in cannabinoid receptor 2 (CNR2 gene): identification of novel human and rodent CB2 isoforms, differential tissue expression and regulation by cannabinoid receptor ligands Genes Brain Behav 8 2009 519 530
62. P. Weisova, D. Davila, L.P. Tuffy, M.W. Ward, C.G. Concannon, and J.H. Prehn Role of 5′-adenosine monophosphate-activated protein kinase in cell survival and death responses in neurons Antioxid Redox Signal 14 2011 1863 1876
63. S. Ramamurthy, and G.V. Ronnett Developing a head for energy sensing: AMP-activated protein kinase as a multifunctional metabolic sensor in the brain J Physiol 574 Pt 1 2006 85 93
64. C. Culmsee, J. Monnig, B.E. Kemp, and M.P. Mattson AMP-activated protein kinase is highly expressed in neurons in the developing rat brain and promotes neuronal survival following glucose deprivation J Mol Neurosci 17 2001 45 58
65. L.D. McCullough, Z. Zeng, H. Li, L.E. Landree, J. McFadden, and G.V. Ronnett Pharmacological inhibition of AMP-activated protein kinase provides neuroprotection in stroke J Biol Chem 280 2005 20493 20502
66. J. Li, Z. Zeng, B. Viollet, G.V. Ronnett, and L.D. McCullough Neuroprotective effects of adenosine monophosphate-activated protein kinase inhibition and gene deletion in stroke Stroke 38 2007 2992 2999
67. T. Sasaki, H. Takemori, Y. Yagita, Y. Terasaki, T. Uebi, N. Horike, H. Takagi, T. Susumu, H. Teraoka, K. Kusano, O. Hatano, N. Oyama, Y. Sugiyama, S. Sakoda, and K. Kitagawa SIK2 is a key regulator for neuronal survival after ischemia via TORC1-CREB Neuron 69 2011 106 119
68. D.M. Thomson, S.T. Herway, N. Fillmore, H. Kim, J.D. Brown, J.R. Barrow, and W.W. Winder AMP-activated protein kinase phosphorylates transcription factors of the CREB family J Appl Physiol 104 2008 429 438