A cannabinoid type 2 receptor agonist attenuates blood-brain barrier damage and neurodegeneration in a murine model of traumatic brain injury

Journal of Neuroscience Research

Volumn 90, Issue 12, 2012, Pages 2293-2305

  Amenta, Peter S ^a   Jallo, Jack I ^a   Tuma, Ronald F ^b   Elliott, Melanie B ^a  

^a THOMAS JEFFERSON UNIVERSITY HOSPITAL   (United States)

^b TEMPLE UNIVERSITY   (United States)

Author keywords

Blood brain barrier; Cannabinoid 2 receptor; Controlled cortical impact; Endocannabinoid, traumatic brain injury; Microglia

Indexed keywords

0 1996; CANNABINOID RECEPTOR ANTAGONIST; CENTRAL NERVOUS SYSTEM AGENTS; FLUORESCEIN SODIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL COUNT; CONTROLLED STUDY; HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NERVE CELL DEGENERATION; NERVE DEGENERATION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; TRAUMATIC BRAIN INJURY;

ANIMALS; ANISOLES; BLOOD-BRAIN BARRIER; BRAIN INJURIES; DRUG EVALUATION, PRECLINICAL; EXPLORATORY BEHAVIOR; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; NERVE DEGENERATION; NEURONS; NEUROPROTECTIVE AGENTS; RECEPTOR, CANNABINOID, CB2; ROTAROD PERFORMANCE TEST; WOUNDS, NONPENETRATING;

EID: 84867744820     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23114     Document Type: Article

References (82)

1. Adhikary S, Li H, Heller J, Skarica M, Zhang M, Ganea D, Tuma RF.2011.Modulation of inflammatory responses by a cannabinoid-2-selective agonist after spinal cord injury.J Neurotrauma 28:2417-2427.
2. Arevalo-Martin A, Vela JM, Molina-Holgado E, Borrell J, Guaza C.2003.Therapeutic action of cannabinoids in a murine model of multiple sclerosis.J Neurosci 23:2511-2516.
3. 2 receptor antibodies.Br J Pharmacol 163:1113.
4. 2: a cannabinoid receptor with an identity crisis.Br J Pharmacol 160:467-479.
5. Baskaya M, Rao A, Dogan A, Donaldson D, Dempsey R.1997.The biphasic opening of the blood-brain barrier in the cortex and hippocampus after traumatic brain injury in rats.Neurosci Lett 226:33-36.
6. 2 receptor activation attenuates motor and autonomic function deficits in a mouse model of spinal cord injury.Clin Neurosurg 55:172-177.
7. Beaumont A, Marmarou A, Hayasaki K, Barzo P, Fatouros P, Corwin F, Marmarou C, Dunbar J.2000.The permissive nature of blood brain barrier (BBB) opening in edema formation following traumatic brain injury.Acta Neurochir Suppl 76:125-129.
8. Blaylock RL, Maroon J.2011.Immunoexcitotoxicity as a central mechanism in chronic traumatic encephalopathy-a unifying hypothesis.Surg Neurol Int 2:107.
9. Brown AJ.2007.Novel cannabinoid receptors.Br J Pharmacol 152:567-575.
10. 2 receptor.Eur J Pharmacol 396:141-149.
11. Bye N, Habgood MD, Callaway JK, Malakooti N, Potter A, Kossmann T, Morganti-Kossmann MC.2007.Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration.Exp Neurol 204:220-233.
12. 2 in immune regulation: therapeutic prospects for neuroinflammation.Expert Rev Mol Med 11:e3.
13. 2 receptors in the brain: role in central immune function.Br J Pharmacol 153:240-251.
14. 2 cannabinoid receptor by rodent macrophages and macrophage-like cells in relation to cell activation.Int Immunopharmacol 2:69-82.
15. Cernak I.2006.Recent advances in neuroprotection for treating traumatic brain injury.Expert Opin Invest Drugs 15:1371-1381.
16. Chen G, Zhang S, Shi J, Ai J, Qi M, Hang C.2009.Simvastatin reduces secondary brain injury caused by cortical contusion in rats: possible involvement of TLR4/NF-kappaB pathway.Exp Neurol 216:398-406.
17. Cole JT, Yarnell A, Kean WS, Gold E, Lewis B, Ren M, McMullen DC, Jacobowitz DM, Pollard HB, O'Neill JT, Grunberg NE, Dalgard CL, Frank JA, Watson WD.2011.Craniotomy: true sham for traumatic brain injury, or a sham of a sham?J Neurotrauma 28:359-369.
18. 2 receptor negatively regulates IL-12p40 production in murine macrophages: role of IL-10 and ERK1/2 kinase signaling.Br J Pharmacol 145:441-448.
19. Donkin JJ, Nimmo AJ, Cernak I, Blumbergs PC, Vink R.2009.Substance P is associated with the development of brain edema and functional deficits after traumatic brain injury.J Cereb Blood Flow Metab 29:1388-1398.
20. Elliott MB, Tuma RF, Amenta PS, Barbe MF, Jallo JI.2011.Acute effects of a selective cannabinoid-2 receptor agonist on neuroinflammation in a model of traumatic brain injury.J Neurotrauma 28:973-981.
21. Fraga D, Raborn ES, Ferreira GA, Cabral GA.2011.Cannabinoids inhibit migration of microglial-like cells to the HIV protein Tat.J Neuroimmune Pharmacol 6:566-577.
22. Franklin KB, Paxinos G.2008.The mouse brain in stereotaxic coordinates.New York:Academic Press.
23. Frey LC, Hellier J, Unkart C, Lepkin A, Howard A, Hasebroock K, Serkova N, Liang L, Patel M, Soltesz I, Staley K.2009.A novel apparatus for lateral fluid percussion injury in the rat.J Neurosci Methods 177:267-272.
24. 2 receptors: immunohistochemical localization in rat brain.Brain Res 1071:10-23.
25. Hailer NP.2008.Immunosuppression after traumatic or ischemic CNS damage: it is neuroprotective and illuminates the role of microglial cells.Prog Neurobiol 84:211-233.
26. Hall ED, Bryant YD, Cho W, Sullivan PG.2008.Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods.J Neurotrauma 25:235-247.
27. Hall KD, Lifshitz J.2010.Diffuse traumatic brain injury initially attenuates and later expands activation of the rat somatosensory whisker circuit concomitant with neuroplastic responses.Brain Res 1323:161-173.
28. Hoane MR KN, Vitek MP, McKenna SE.2009.COG1410 improves cognitive performance and reduces cortical neuronal loss in the traumatically injured brain.J Neurotrauma 26:121-129.
29. Homsi S, Federico F, Croci N, Palmier B, Plotkine M, Marchand-Leroux C, Jafarian-Tehrani M.2009.Minocycline effects on cerebral edema: relations with inflammatory and oxidative stress markers following traumatic brain injury in mice.Brain Res 1291:122-132.
30. Homsi S, Piaggio T, Croci N, Noble F, Plotkine M, Marchand-Leroux C, Jafarian-Tehrani M.2010.Blockade of acute microglial activation by minocycline promotes neuroprotection and reduces locomotor hyperactivity after closed head injury in mice: a twelve-week follow-up study.J Neurotrauma 27:911-921.
31. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S.1996.A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage.Biochem Biophys Res Commun 224:855-862.
32. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S.1998.Microglia-specific localisation of a novel calcium binding protein, Iba1.Brain Res Mol Brain Res 57:1-9.
33. Khan M, Sakakima H, Dhammu TS, Shunmugavel A, Im YB, Gilg AG, Singh AK, Singh I.2011.S-nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in rats.J Neuroinflammation 8:78.
34. Kigerl KA, Lai W, Rivest S, Hart RP, Satoskar AR, Popovich PG.2007.Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury.J Neurochem 102:37-50.
35. Kreutzberg GW.1996.Microglia: a sensor for pathological events in the CNS.Trends Neurosci 19:312-318.
36. Langlois JA, Rutland-Brown W, Wald MM.2006.The epidemiology and impact of traumatic brain injury: a brief overview.J Head Trauma Rehabil 21:375-378.
37. Lapter S MA, Meshorer A, Elmann A, Sharabi A, Vadai E, et al.2009.Amelioration of brain pathology and behavioral dysfunction in mice with lupus following treatment with a tolerogenic peptide.Arthritis Rheum 60:3744-3754.
38. Lenzlinger PM, Morganti-Kossmann MC, Laurer HL, McIntosh TK.2001.The duality of the inflammatory response to traumatic brain injury.Mol Neurobiol 24:169-181.
39. Leong S, Ling E.1992.Amoeboid and ramified microglia: their interrelationship and response to brain injury.Glia 7:9-18.
40. Li S, Kuroiwa T, Katsumata N, Ishibashi S, Sun LY, Endo S, Ohno K.2006.Transient vs. prolonged hyperlocomotion following lateral fluid percussion injury in mongolian gerbils.J Neurosci Res 83:292-300.
41. Liao H, Bu WY, Wang TH, Ahmed S, Xiao ZC.2005.Tenascin-R plays a role in neuroprotection via its distinct domains that coordinate to modulate the microglia function.J Biol Chem 280:8316-8323.
42. Lighthall JW.1988.Controlled cortical impact: a new experimental brain injury model.J Neurotrauma 5:1-15.
43. 2-selective ligands as immunosuppressive agents.Clin Immunol 122:259-270.
44. 9-tetrahydrocannabinol in rats.Pharmacol Biochem Behav 93:91-96.
45. 2 receptor in microglial cells in response to inflammatory stimuli.J Neurochem 95:437-445.
46. 2 or EDG-1.Eur J Pharmacol 489:21-27.
47. 2 cannabinoid receptor agonist JWH-015 modulates human monocyte migration through defined intracellular signaling pathways.Am J Physiol Heart Circ Physiol 294:H1145-H1155.
48. Munro S, Thomas KL, Abu-Shaar M.1993.Molecular characterization of a peripheral receptor for cannabinoids.Nature 365:61-65.
49. Onyszchuk G, Al-Hafez B, He YY, Bilgen M, Berman NE, Brooks WM.2007.A mouse model of sensorimotor controlled cortical impact: characterization using longitudinal magnetic resonance imaging, behavioral assessments and histology.J Neurosci Methods 160:187-196.
50. Pacher P, Batkai S, Kunos G.2006.The endocannabinoid system as an emerging target of pharmacotherapy.Pharmacol Rev 58:389-462.
51. 2 cannabinoid receptors are neuroprotective in Huntington's disease excitotoxicity.Brain 132:3152-3164.
52. 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.
53. Panikashvili D, Mechoulam R, Beni SM, Alexandrovich A, Shohami E.2005.CB1 cannabinoid receptors are involved in neuroprotection via NF-kappa B inhibition.J Cereb Blood Flow Metab 25:477-484.
54. Panikashvili D, Shein NA, Mechoulam R, Trembovler V, Kohen R, Alexandrovich A, Shohami E.2006.The endocannabinoid 2-AG protects the blood-brain barrier after closed head injury and inhibits mRNA expression of proinflammatory cytokines.Neurobiol Dis 22:257-264.
55. Phares TW, Fabis MJ, Brimer CM, Kean RB, Hooper DC.2007.A peroxynitrite-dependent pathway is responsible for blood-brain barrier permeability changes during a central nervous system inflammatory response: TNF-alpha is neither necessary nor sufficient.J Immunol 178:7334-7343.
56. Price DA, Martinez AA, Seillier A, Koek W, Acosta Y, Fernandez E, Strong R, Lutz B, Marsicano G, Roberts JL, Giuffrida A.2009.WIN55, 212-2, a cannabinoid receptor agonist, protects against nigrostriatal cell loss in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease.Eur J Neurosci 29:2177-2186.
57. Ramirez BG, Blazquez C, Gomez del Pulgar T, Guzman M, de Ceballos ML.2005.Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation.J Neurosci 25:1904-1913.
58. Ramirez SH, Hasko J, Skuba A, Fan S, Dykstra H, McCormick R, Reichenbach N, Krizbai I, Mahadevan A, Zhang M, Tuma R, Son YJ, Persidsky Y.2012.Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions.J Neurosci 32:4004-4016.
59. Saatman KE, Feeko KJ, Pape RL, Raghupathi R.2006.Differential behavioral and histopathological responses to graded cortical impact injury in mice.J Neurotrauma 23:1241-1253.
60. 2 receptors.J Neuroimmunol 109:155-163.
61. Sanchez Mejia RO, Ona VO, Li M, Friedlander RM.2001.Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction.Neurosurgery 48:1393-1401.
62. Sandhir R, Onyszchuk G, Berman NE.2008.Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury.Exp Neurol 213:372-380.
63. Schmued LC SC, Scallet AC, Xu L.2005.Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons.Brain Res 1035:24-31.
64. Schwarzbold ML, Rial D, De Bem T, Machado DG, Cunha MP, dos Santos AA, dos Santos DB, Figueiredo CP, Farina M, Goldfeder EM, Rodrigues AL, Prediger RD, Walz R.2010.Effects of traumatic brain injury of different severities on emotional, cognitive, and oxidative stress-related parameters in mice.J Neurotrauma 27:1883-1893.
65. Simard AR, Rivest S.2007.Neuroprotective effects of resident microglia following acute brain injury.J Comp Neurol 504:716-729.
66. Stokely ME, Bhat MA, Koulen P.2007.Microfluorimetry defines early axonal damage in a rat model of optic neuritis: a novel method targeting early CNS autoimmunity.J Neurosci Methods 166:217-228.
67. Tremblay ME, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A.2011.The role of microglia in the healthy brain.J Neurosci 31:16064-16069.
68. van der Stelt M, Veldhuis WB, Maccarrone M, Bar PR, Nicolay K, Veldink GA, Di Marzo V, Vliegenthart JF.2002.Acute neuronal injury, excitotoxicity, and the endocannabinoid system.Mol Neurobiol 26:317-346.
69. 2 receptors.Science 310:329-332.
70. Wagner AK, Postal BA, Darrah SD, Chen X, Khan AS.2007.Deficits in novelty exploration after controlled cortical impact.J Neurotrauma 24:1308-1320.
71. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J.2009.Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals.J Neurosci 29:3974-3980.
72. Walker PA, Shah SK, Jimenez F, Gerber MH, Xue H, Cutrone R, Hamilton JA, Mays RW, Deans R, Pati S, Dash PK, Cox CSJr.2010.Intravenous multipotent adult progenitor cell therapy for traumatic brain injury: preserving the blood brain barrier via an interaction with splenocytes.Exp Neurol 225:341-352.
73. Walter L, Franklin A, Witting A, Wade C, Xie Y, Kunos G, Mackie K, Stella N.2003.Nonpsychotropic cannabinoid receptors regulate microglial cell migration.J Neurosci 23:1398-1405.
74. Wieseler J, Ellis A, Sprunger D, Brown K, McFadden A, Mahoney J, Rezvani N, Maier SF, Watkins LR.2010.A novel method for modeling facial allodynia associated with migraine in awake and freely moving rats.J Neurosci Methods 185:236-245.
75. 2-selective agonists.J Pharmacol Exp Ther 301:679-689.
76. Zaloshnja E, Miller T, Langlois JA, Selassie AW.2008.Prevalence of long-term disability from traumatic brain injury in the civilian population of the United States, 2005.J Head Trauma Rehabil 23:394-400.
77. Zarruk JG, Fernandez-Lopez D, Garcia-Yebenes I, Garcia-Gutierrez MS, Vivancos J, Nombela F, Torres M, Burguete MC, Manzanares J, Lizasoain I, Moro MA.2012.Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection.Stroke 43:211-219.
78. Zhang M, Martin BR, Adler MW, Razdan RK, Jallo JI, Tuma RF.2007.Cannabinoid CB(2) receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model.J Cereb Blood Flow Metab 27:1387-1396.
79. 2 receptor activation during cerebral ischemic/reperfusion injury.Neuroscience 152:753-760.
80. 2 receptor activation attenuates microcirculatory dysfunction during cerebral ischemic/reperfusion injury.Microvasc Res 78:86-94.
81. Zhang M, Martin BR, Adler MW, Razdan RJ, Kong W, Ganea D, Tuma RF.2009b.Modulation of cannabinoid receptor activation as a neuroprotective strategy for EAE and stroke.J Neuroimmune Pharmacol 4:249-259.
82. Zweckberger K, Stoffel M, Baethmann A, Plesnila N.2003.Effect of decompression craniotomy on increase of contusion volume and functional outcome after controlled cortical impact in mice.J Neurotrauma 20:1307-1314.