Cannabinoid receptor 2 attenuates microglial accumulation and brain injury following germinal matrix hemorrhage via ERK dephosphorylation in vivo and in vitro

Neuropharmacology

Volumn 95, Issue , 2015, Pages 424-433

  Tang, Jun ^a   Tao, Yihao ^a   Tan, Liang ^a   Yang, Liming ^a   Niu, Yin ^a   Chen, Qianwei ^a   Yang, Yunfeng ^a   Feng, Hua ^a   Chen, Zhi ^a   Zhu, Gang ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Cannabinoid receptor 2; MAPK pathway; Microglia; Neonatal stroke; Proliferation

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; CANNABINOID 2 RECEPTOR; CELL PROTEIN; IBA1 PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; THROMBIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; 1,3 BUTADIENE DERIVATIVE; CANNABINOID; INDOLE DERIVATIVE; IODOPRAVADOLINE; NITRILE; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN EDEMA; BRAIN INJURY; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GERMINAL MATRIX HEMORRHAGE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; WESTERN BLOTTING; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; IMMUNOMODULATION; INTRACRANIAL HEMORRHAGES; METABOLISM; NERVE DEGENERATION; OXIDATIVE STRESS; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RANDOMIZATION;

ANIMALS; BRAIN; BRAIN EDEMA; BUTADIENES; CANNABINOIDS; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; INDOLES; INTRACRANIAL HEMORRHAGES; MALE; MICROGLIA; NERVE DEGENERATION; NEUROIMMUNOMODULATION; NITRILES; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RANDOM ALLOCATION; RECEPTOR, CANNABINOID, CB2; THROMBIN;

EID: 84930943127     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.04.028     Document Type: Article

References (59)

1. J.C. Ashton, D. Friberg, C.L. Darlington, and P.F. Smith Expression of the cannabinoid CB2 receptor in the rat cerebellum: an immunohistochemical study Neurosci. Lett. 396 2006 113 116
2. P. Ballabh, A. Braun, and M. Nedergaard The blood-brain barrier: an overview: structure, regulation, and clinical implications Neurobiol. Dis. 16 2004 1 13
3. H. Bassan, C. Limperopoulos, K. Visconti, D.L. Mayer, H.A. Feldman, L. Avery, C.B. Benson, J. Stewart, S.A. Ringer, J.S. Soul, J.J. Volpe, and A.J. du Plessis Neurodevelopmental outcome in survivors of periventricular hemorrhagic infarction Pediatrics 120 2007 785 792
4. N.R. Bhat, P. Zhang, J.C. Lee, and E.L. Hogan Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures J. Neurosci. 18 1998 1633 1641
5. G.C. Brown, and J.J. Neher Inflammatory neurodegeneration and mechanisms of microglial killing of neurons Mol. Neurobiol. 41 2010 242 247
6. M.A. Burguillos, T. Deierborg, E. Kavanagh, A. Persson, N. Hajji, A. Garcia-Quintanilla, J. Cano, P. Brundin, E. Englund, J.L. Venero, and B. Joseph Caspase signalling controls microglia activation and neurotoxicity Nature 472 2011 319 324
7. Q. Chen, J. Zhang, J. Guo, J. Tang, Y. Tao, L. Li, H. Feng, and Z. Chen Chronic hydrocephalus and perihematomal tissue injury developed in a rat model of intracerebral hemorrhage with ventricular extension Transl. Stroke Res. 6 2015 125 132
8. S.H. Choi, D.Y. Lee, E.S. Chung, Y.B. Hong, S.U. Kim, and B.K. Jin Inhibition of thrombin-induced microglial activation and NADPH oxidase by minocycline protects dopaminergic neurons in the substantia nigra in vivo J. Neurochem. 95 2005 1755 1765
9. E.S. Chung, E. Bok, Y.C. Chung, H.H. Baik, and B.K. Jin Cannabinoids prevent lipopolysaccharide-induced neurodegeneration in the rat substantia nigra in vivo through inhibition of microglial activation and NADPH oxidase Brain Res. 1451 2012 110 116
10. G. Cui, T. Zuo, Q. Zhao, J. Hu, P. Jin, H. Zhao, J. Jing, J. Zhu, H. Chen, B. Liu, F. Hua, and X. Ye ROCK mediates the inflammatory response in thrombin induced microglia Neurosci. Lett. 554 2013 82 87
11. X.J. Dai, N. Li, L. Yu, Z.Y. Chen, R. Hua, X. Qin, and Y.M. Zhang Activation of BV2 microglia by lipopolysaccharide triggers an inflammatory reaction in PC12 cell apoptosis through a toll-like receptor 4-dependent pathway Cell Stress Chaperones 20 2015 321 331
12. F.M. Donovan, and D.D. Cunningham Signaling pathways involved in thrombin-induced cell protection J. Biol. Chem. 273 1998 12746 12752
13. J. Ehrhart, D. Obregon, T. Mori, H. Hou, N. Sun, Y. Bai, T. Klein, F. Fernandez, J. Tan, and R.D. Shytle Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation J. Neuroinflamm. 2 2005 29
14. E. Eljaschewitsch, A. Witting, C. Mawrin, T. Lee, P.M. Schmidt, S. Wolf, H. Hoertnagl, C.S. Raine, R. Schneider-Stock, R. Nitsch, and O. Ullrich The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells Neuron 49 2006 67 79
15. D. Fernandez-Lopez, J. Faustino, N. Derugin, M. Wendland, I. Lizasoain, M.A. Moro, and Z.S. Vexler Reduced infarct size and accumulation of microglia in rats treated with WIN 55,212-2 after neonatal stroke Neuroscience 207 2012 307 315
16. J. Fernandez-Ruiz, J. Romero, G. Velasco, R.M. Tolon, J.A. Ramos, and M. Guzman Cannabinoid CB2 receptor: a new target for controlling neural cell survival? Trends Pharmacol. Sci. 28 2007 39 45
17. D. Freyer, R. Manz, A. Ziegenhorn, M. Weih, K. Angstwurm, W.D. Docke, A. Meisel, R.R. Schumann, G. Schonfelder, U. Dirnagl, and J.R. Weber Cerebral endothelial cells release TNF-alpha after stimulation with cell walls of Streptococcus pneumoniae and regulate inducible nitric oxide synthase and ICAM-1 expression via autocrine loops J. Immunol. 163 1999 4308 4314
18. M. Fujii, P. Sherchan, Y. Soejima, Y. Hasegawa, J. Flores, D. Doycheva, and J.H. Zhang Cannabinoid receptor type 2 agonist attenuates apoptosis by activation of phosphorylated CREB-Bcl-2 pathway after subarachnoid hemorrhage in rats Exp. Neurol. 261 2014 396 403
19. S. Fujimoto, H. Katsuki, T. Kume, and A. Akaike Thrombin-induced delayed injury involves multiple and distinct signaling pathways in the cerebral cortex and the striatum in organotypic slice cultures Neurobiol. Dis. 22 2006 130 142
20. S. Fujimoto, H. Katsuki, M. Ohnishi, M. Takagi, T. Kume, and A. Akaike Thrombin induces striatal neurotoxicity depending on mitogen-activated protein kinase pathways in vivo Neuroscience 144 2007 694 701
21. H.M. Gao, B. Liu, W. Zhang, and J.S. Hong Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson's disease FASEB J. 17 2003 1954 1956
22. J. Gertsch, R. Schoop, U. Kuenzle, and A. Suter Echinacea alkylamides modulate TNF-alpha gene expression via cannabinoid receptor CB2 and multiple signal transduction pathways FEBS Lett. 577 2004 563 569
23. A. Ghoshal, S. Das, S. Ghosh, M.K. Mishra, V. Sharma, P. Koli, E. Sen, and A. Basu Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis Glia 55 2007 483 496
24. F. Ginhoux, M. Greter, M. Leboeuf, S. Nandi, P. See, S. Gokhan, M.F. Mehler, S.J. Conway, L.G. Ng, E.R. Stanley, I.M. Samokhvalov, and M. Merad Fate mapping analysis reveals that adult microglia derive from primitive macrophages Science 330 2010 841 845
25. J. Guo, Q. Chen, J. Tang, J. Zhang, Y. Tao, L. Li, G. Zhu, H. Feng, and Z. Chen Minocycline-induced attenuation of iron overload and brain injury after experimental germinal matrix hemorrhage Brain Res. 1594 2015 115 124
26. M. Heron, P.D. Sutton, J. Xu, S.J. Ventura, D.M. Strobino, and B. Guyer Annual summary of vital statistics: 2007 Pediatrics 125 2010 4 15
27. C. Huang, R. Ma, S. Sun, G. Wei, Y. Fang, R. Liu, and G. Li JAK2-STAT3 signaling pathway mediates thrombin-induced proinflammatory actions of microglia in vitro J. Neuroimmunol. 204 2008 118 125
28. J.W. Huffman, J. Liddle, S. Yu, M.M. Aung, M.E. Abood, J.L. Wiley, and B.R. Martin 3-(1′,1′-Dimethylbutyl)-1-deoxy-delta8-THC and related compounds: synthesis of selective ligands for the CB2 receptor Bioorg. Med. Chem. 7 1999 2905 2914
29. T. Lekic, A. Manaenko, W. Rolland, N. Fathali, M. Peterson, J. Tang, and J.H. Zhang Protective effect of hydrogen gas therapy after germinal matrix hemorrhage in neonatal rats Acta Neurochir. Suppl. 111 2011 237 241
30. T. Lekic, A. Manaenko, W. Rolland, P.R. Krafft, R. Peters, R.E. Hartman, O. Altay, J. Tang, and J.H. Zhang Rodent neonatal germinal matrix hemorrhage mimics the human brain injury, neurological consequences, and post-hemorrhagic hydrocephalus Exp. Neurol. 236 2012 69 78
31. R. Mechoulam, E. Fride, and V. Di Marzo Endocannabinoids Eur. J. Pharmacol. 359 1998 1 18
32. T. Moller, U.K. Hanisch, and B.R. Ransom Thrombin-induced activation of cultured rodent microglia J. Neurochem. 75 2000 1539 1547
33. N. Morioka, H. Tanabe, A. Inoue, T. Dohi, and Y. Nakata Noradrenaline reduces the ATP-stimulated phosphorylation of p38 MAP kinase via beta-adrenergic receptors-cAMP-protein kinase A-dependent mechanism in cultured rat spinal microglia Neurochem. Int. 55 2009 226 234
34. F. Noorbakhsh, N. Vergnolle, M.D. Hollenberg, and C. Power Proteinase-activated receptors in the nervous system Nat. Rev. Neurosci. 4 2003 981 990
35. E. Nunez, C. Benito, M.R. Pazos, A. Barbachano, O. Fajardo, S. Gonzalez, R.M. Tolon, and J. Romero Cannabinoid CB2 receptors are expressed by perivascular microglial cells in the human brain: an immunohistochemical study Synapse 53 2004 208 213
36. M. Ohnishi, H. Katsuki, S. Fujimoto, M. Takagi, T. Kume, and A. Akaike Involvement of thrombin and mitogen-activated protein kinase pathways in hemorrhagic brain injury Exp. Neurol. 206 2007 43 52
37. M. Ohnishi, H. Katsuki, Y. Izumi, T. Kume, Y. Takada-Takatori, and A. Akaike Mitogen-activated protein kinases support survival of activated microglia that mediate thrombin-induced striatal injury in organotypic slice culture J. Neurosci. Res. 88 2010 2155 2164
38. M. Ohnishi, A. Monda, R. Takemoto, Y. Matsuoka, C. Kitamura, K. Ohashi, H. Shibuya, and A. Inoue Sesamin suppresses activation of microglia and p44/42 MAPK pathway, which confers neuroprotection in rat intracerebral hemorrhage Neuroscience 232 2013 45 52
39. P. Pacher, S. Batkai, and G. Kunos The endocannabinoid system as an emerging target of pharmacotherapy Pharmacol. Rev. 58 2006 389 462
40. B.G. Ramirez, C. Blazquez, D.P.T. Gomez, M. Guzman, and M.L. de Ceballos Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation J. Neurosci. 25 2005 1904 1913
41. R.M. Ransohoff, and V.H. Perry Microglial physiology: unique stimuli, specialized responses Annu. Rev. Immunol. 27 2009 119 145
42. E.A. Romero-Sandoval, R. Horvath, R.P. Landry, and J.A. DeLeo Cannabinoid receptor type 2 activation induces a microglial anti-inflammatory phenotype and reduces migration via MKP induction and ERK dephosphorylation Mol. Pain 5 2009 25
43. K. Saijo, A. Crotti, and C.K. Glass Regulation of microglia activation and deactivation by nuclear receptors Glia 61 2013 104 111
44. K.P. Sarker, S. Obara, M. Nakata, I. Kitajima, and I. Maruyama Anandamide induces apoptosis of PC-12 cells: involvement of superoxide and caspase-3 FEBS Lett. 472 2000 39 44
45. J.N. Sharma, A. Al-Omran, and S.S. Parvathy Role of nitric oxide in inflammatory diseases Inflammopharmacology 15 2007 252 259
46. A.H. Shennan, and S. Bewley Why should preterm births be rising? BMJ 332 2006 924 925
47. J. Strahle, H.J. Garton, C.O. Maher, K.M. Muraszko, R.F. Keep, and G. Xi Mechanisms of hydrocephalus after neonatal and adult intraventricular hemorrhage Transl. Stroke Res. 3 2012 25 38
48. F. Striggow, M. Riek, J. Breder, P. Henrich-Noack, K.G. Reymann, and G. Reiser The protease thrombin is an endogenous mediator of hippocampal neuroprotection against ischemia at low concentrations but causes degeneration at high concentrations Proc. Natl. Acad. Sci. U.S.A. 97 2000 2264 2269
49. V. Supramaniam, R. Vontell, L. Srinivasan, J. Wyatt-Ashmead, H. Hagberg, and M. Rutherford Microglia activation in the extremely preterm human brain Pediatr. Res. 73 2013 301 309
50. V. Supramaniam, R. Vontell, L. Srinivasan, J. Wyatt-Ashmead, H. Hagberg, and M. Rutherford Microglia activation in the extremely preterm human brain Pediatr. Res. 73 2013 301 309
51. L. Tan, H. Ge, J. Tang, C. Fu, W. Duanmu, Y. Chen, R. Hu, J. Sui, X. Liu, and H. Feng Amantadine preserves dopamine level and attenuates depression-like behavior induced by traumatic brain injury in rats Behav. Brain Res. 279 2015 274 282
52. Y. Tao, J. Tang, Q. Chen, J. Guo, L. Li, L. Yang, H. Feng, G. Zhu, and Z. Chen Cannabinoid CB2 receptor stimulation attenuates brain edema and neurological deficits in a germinal matrix hemorrhage rat model Brain Res. 1602 2015 127 135
53. J.R. Weinstein, M. Zhang, M. Kutlubaev, R. Lee, C. Bishop, H. Andersen, U.K. Hanisch, and T. Moller Thrombin-induced regulation of CD95(Fas) expression in the N9 microglial cell line: evidence for involvement of proteinase-activated receptor(1) and extracellular signal-regulated kinase 1/2 Neurochem. Res. 34 2009 445 452
54. J. Wu, S. Yang, G. Xi, S. Song, G. Fu, R.F. Keep, and Y. Hua Microglial activation and brain injury after intracerebral hemorrhage Acta Neurochir. Suppl. 105 2008 59 65
55. G. Xi, R.F. Keep, and J.T. Hoff Mechanisms of brain injury after intracerebral haemorrhage Lancet Neurol. 5 2006 53 63
56. G. Xi, G. Reiser, and R.F. Keep The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury: deleterious or protective? J. Neurochem. 84 2003 3 9
57. G. Xi, K.R. Wagner, R.F. Keep, Y. Hua, G.M. de Courten-Myers, J.P. Broderick, T.G. Brott, and J.T. Hoff Role of blood clot formation on early edema development after experimental intracerebral hemorrhage Stroke 29 1998 2580 2586
58. A. Yarilina, K. Xu, C. Chan, and L.B. Ivashkiv Regulation of inflammatory responses in tumor necrosis factor-activated and rheumatoid arthritis synovial macrophages by JAK inhibitors Arthritis Rheum. 64 2012 3856 3866
59. M.A. Yenari, T.M. Kauppinen, and R.A. Swanson Microglial activation in stroke: therapeutic targets Neurotherapeutics 7 2010 378 391