Cannabinoid receptor type-2 stimulation, blockade, and deletion alter the vascular inflammatory responses to traumatic brain injury

Journal of Neuroinflammation

Volumn 11, Issue 1, 2014, Pages

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

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cannabinoid; Controlled cortical impact; Inflammation; Intracellular adhesion molecule; Traumatic brain injury

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; CALCIUM BINDING PROTEIN; CANNABINOID; CANNABINOID 2 RECEPTOR; CANNABINOID 2 RECEPTOR AGONIST; FLUORESCEIN SODIUM; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; IONIZED CALCIUM BINDING ADAPTOR MOLECULE; MESSENGER RNA; O 1966; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BRAIN VASCULITIS; C57BL 6 MOUSE; CONTROLLED CORTICAL IMPACT INJURY; CONTROLLED STUDY; CRANIOTOMY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL BRAIN INJURY; FLUOROMETRY; GENE DELETION; GENE EXPRESSION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MACROPHAGE; MALE; MICROGLIA; MOUSE; NEUROMODULATION; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PROTEIN ANALYSIS; PROTEIN FUNCTION; RECEPTOR BLOCKING; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRAUMATIC BRAIN INJURY; WILD TYPE MOUSE; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN INJURIES; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; METABOLISM; RANDOMIZATION; TREATMENT OUTCOME; VASCULITIS, CENTRAL NERVOUS SYSTEM;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN INJURIES; CANNABINOID RECEPTOR AGONISTS; CANNABINOID RECEPTOR ANTAGONISTS; GENE DELETION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RANDOM ALLOCATION; RECEPTOR, CANNABINOID, CB2; TREATMENT OUTCOME; VASCULITIS, CENTRAL NERVOUS SYSTEM;

EID: 84988651258     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-014-0191-6     Document Type: Article

References (63)

1. Zaloshnja E, Miller T, Langlois JA, Selassie AW: Prevalence of long-term disability from traumatic brain injury in the civilian population of the United States, 2005. J Head Trauma Rehabil 2008, 23:394-400.
2. Langlois JA, Rutland-Brown W, Wald MM: The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil 2006, 21:375-378.
3. Erickson MA, Hartvigson PE, Morofuji Y, Owen JB, Butterfield DA, Banks WA: Lipopolysaccharide impairs amyloid beta efflux from brain: altered vascular sequestration, cerebrospinal fluid reabsorption, peripheral clearance and transporter function at the blood-brain barrier. J Neuroinflammation 2012, 9:150.
4. Tomkins O, Feintuch A, Benifla M, Cohen A, Friedman A, Shelef I: Blood-brain barrier breakdown following traumatic brain injury: a possible role in posttraumatic epilepsy. Cardiovasc Psychiatry Neurol 2011, 2011:765923.
5. Lenzlinger PM, Morganti-Kossmann MC, Laurer HL, McIntosh TK: The duality of the inflammatory response to traumatic brain injury. Mol Neurobiol 2001, 24:169-181.
6. Lagraoui M, Latoche JR, Cartwright NG, Sukumar G, Dalgard CL, Schaefer BC: Controlled cortical impact and craniotomy induce strikingly similar profiles of inflammatory gene expression, but with distinct kinetics. Front Neurol 2012, 3:155.
7. Dietrich JB: The adhesion molecule ICAM-1 and its regulation in relation with the blood-brain barrier. J Neuroimmunol 2002, 128:58-68.
8. Phares TW, Fabis MJ, Brimer CM, Kean RB, Hooper DC: A peroxynitritedependent 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 2007, 178:7334-7343.
9. Walker PA, Shah SK, Jimenez F, Gerber MH, Xue H, Cutrone R, Hamilton JA, Mays RW, Deans R, Pati S, Dash PK, Cox CS Jr: Intravenous multipotent adult progenitor cell therapy for traumatic brain injury: preserving the blood brain barrier via an interaction with splenocytes. Exp Neurol 2010, 225:341-352.
10. Hailer NP: Immunosuppression after traumatic or ischemic CNS damage: it is neuroprotective and illuminates the role of microglial cells. Prog Neurobiol 2008, 84:211-233.
11. Cherry JD, Olschowka JA, O'Banion MK: Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J Neuroinflammation 2014, 11:98.
12. Turtzo LC, Lescher J, Janes L, Dean DD, Budde MD, Frank JA: Macrophagic and microglial responses after focal traumatic brain injury in the female rat. J Neuroinflammation 2014, 11:82.
13. Cabral GA, Griffin-Thomas L: Emerging role of the cannabinoid receptor CB2 in immune regulation: therapeutic prospects for neuroinflammation. Expert Rev Mol Med 2009, 11:e3.
14. Cabral GA, Raborn ES, Griffin L, Dennis J, Marciano-Cabral F: CB2 receptors in the brain: role in central immune function. Br J Pharmacol 2008, 153:240-251.
15. Buckley NE, McCoy KL, Mezey E, Bonner T, Zimmer A, Felder CC, Glass M, Zimmer A: Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB(2) receptor. Eur J Pharmacol 2000, 396:141-149.
16. Fraga D, Raborn ES, Ferreira GA, Cabral GA: Cannabinoids inhibit migration of microglial-like cells to the HIV protein Tat. J Neuroimmune Pharmacol 2011, 6:566-577.
17. Munro S, Thomas KL, Abu-Shaar M: Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65.
18. Palazuelos J, Aguado T, Pazos MR, Julien B, Carrasco C, Resel E, Sagredo O, Benito C, Romero J, Azcoitia I, Fernández-Ruiz J, Guzmán M, Galve-Roperh I: Microglial CB2 cannabinoid receptors are neuroprotective in Huntington's disease excitotoxicity. Brain 2009, 132:3152-3164.
19. Elliott MB, Tuma RF, Amenta PS, Barbe MF, Jallo JI: Acute effects of a selective cannabinoid-2 receptor agonist on neuroinflammation in a model of traumatic brain injury. J Neurotrauma 2011, 28:973-981.
20. Zhang M, Adler MW, Abood ME, Ganea D, Jallo J, Tuma RF: CB2 receptor activation attenuates microcirculatory dysfunction during cerebral ischemic/reperfusion injury. Microvasc Res 2009, 78:86-94.
21. Zhang M, Martin BR, Adler MW, Razdan RK, Jallo JI, Tuma RF: Cannabinoid CB(2) receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model. J Cereb Blood Flow Metab 2007, 27:1387-1396.
22. Adhikary S, Li H, Heller J, Skarica M, Zhang M, Ganea D, Tuma RF: Modulation of inflammatory responses by a cannabinoid-2-selective agonist after spinal cord injury. J Neurotrauma 2011, 28:2417-2427.
23. Amenta PS, Jallo JI, Tuma RF, Elliott MB: A cannabinoid type 2 receptor agonist attenuates blood-brain barrier damage and neurodegeneration in a murine model of traumatic brain injury. J Neurosci Res 2012, 90:2293-22305.
24. 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: Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection. Stroke 2012, 43:211-219.
25. Price DA, Martinez AA, Seillier A, Koek W, Acosta Y, Fernandez E, Strong R, Lutz B, Marsicano G, Roberts JL, Giuffrida A: 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 2009, 29:2177-2186.
26. Cabral GA, Marciano-Cabral F: Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukoc Biol 2005, 78:1192-1197.
27. Romero-Sandoval EA, Horvath R, Landry RP, DeLeo JA: Cannabinoid receptor type 2 activation induces a microglial anti-inflammatory phenotype and reduces migration via MKP induction and ERK dephosphorylation. Mol Pain 2009, 5:25.
28. Gentleman SM, Leclercq PD, Moyes L, Graham DI, Smith C, Griffin WS, Nicoll JA: Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci Int 2004, 146:97-104.
29. Loane DJ, Byrnes KR: Role of microglia in neurotrauma. Neurotherapeutics 2010, 7:366-377.
30. Norden DM, Godbout JP: Review: microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathol Appl Neurobiol 2013, 39:19-34.
31. Lighthall JW: Controlled cortical impact: a new experimental brain injury model. J Neurotrauma 1988, 5:1-15.
32. Elliott MB, Oshinsky ML, Amenta PS, Awe OO, Jallo JI: Nociceptive neuropeptide increases and periorbital allodynia in a model of traumatic brain injury. Headache 2012, 52:966-984.
33. Wiley JL, Beletskaya ID, Ng EW, Dai Z, Crocker PJ, Mahadevan A, Razdan RK, Martin BR: Resorcinol derivatives: a novel template for the development of cannabinoid CB(1)/CB(2) and CB(2)-selective agonists. J Pharmacol Exp Ther 2002, 301:679-689.
34. Zhang M, Martin BR, Adler MW, Razdan RJ, Kong W, Ganea D, Tuma RF: Modulation of cannabinoid receptor activation as a neuroprotective strategy for EAE and stroke. J Neuroimmune Pharmacol 2009, 4:249-259.
35. Phares TW, Kean RB, Mikheeva T, Hooper DC: Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system. J Immunol 2006, 176:7666-7675.
36. Pertwee RG: Receptors and channels targeted by synthetic cannabinoid receptor agonists and antagonists. Curr Med Chem 2010, 17:1360-1381.
37. Fishbein-Kaminietsky M, Gafni M, Sarne Y: Ultralow doses of cannabinoid drugs protect the mouse brain from inflammation-induced cognitive damage. J Neurosci Res 2014, 92:1669-1677.
38. Ashton JC, Glass M: The cannabinoid CB2 receptor as a target for inflammation-dependent neurodegeneration. Curr Neuropharmacol 2007, 5:73-80.
39. 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: Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions. J Neurosci 2012, 32:4004-4016.
40. Reglero-Real N, Marcos-Ramiro B, Millan J: Endothelial membrane reorganization during leukocyte extravasation. Cell Mol Life Sci 2012, 69:3079-3099.
41. Harting MT, Jimenez F, Adams SD, Mercer DW, Cox CS Jr: Acute, regional inflammatory response after traumatic brain injury: implications for cellular therapy. Surgery 2008, 144:803-813.
42. Shein S, Shellington DK, Exo J, Jackson TC, Wisniewski SR, Jackson E, Vagni VA, Bayir H, Clark R, Dixon CE, Janesko-Feldman KL, Kochanek PM: Hemorrhagic shock shifts the serum cytokine profile from pro-to anti-inflammatory after experimental traumatic brain injury in mice. J Neurotrauma 2014, 31:1386-1395.
43. Li GZ, Zhang Y, Zhao JB, Wu GJ, Su XF, Hang CH: Expression of myeloid differentiation primary response protein 88 (Myd88) in the cerebral cortex after experimental traumatic brain injury in rats. Brain Res 2011, 1396:96-104.
44. Giambelluca MS, Rollet-Labelle E, Bertheau-Mailhot G, Laflamme C, Pouliot M: Post-transcriptional regulation of tumor necrosis factor alpha biosynthesis: relevance to pathophysiology of rheumatoid arthritis. OA Inflammation 2013, 1:3.
45. Landry RP, Martinez E, Deleo JA, Romero-Sandoval EA: Spinal cannabinoid receptor type 2 agonist reduces mechanical allodynia and induces mitogen-activated protein kinase phosphatases in a rat model of neuropathic pain. J Pain 2012, 13:836-848.
46. Bayir H, Kagan VE, Borisenko GG, Tyurina YY, Janesko KL, Vagni VA, Billiar TR, Williams DL, Kochanek PM: Enhanced oxidative stress in iNOS-deficient mice after traumatic brain injury: support for a neuroprotective role of iNOS. J Cereb Blood Flow Metab 2005, 25:673-684.
47. Foley LM, Hitchens TK, Ho C, Janesko-Feldman KL, Melick JA, Bayir H, Kochanek PM: Magnetic resonance imaging assessment of macrophage accumulation in mouse brain after experimental traumatic brain injury. J Neurotrauma 2009, 26:1509-1519.
48. Hang CH, Shi JX, Li JS, Wu W, Yin HX: Concomitant upregulation of nuclear factor-kB activity, proinflammatory cytokines and ICAM-1 in the injured brain after cortical contusion trauma in a rat model. Neurol India 2005, 53:312-317.
49. Khan M, Im YB, Shunmugavel A, Gilg AG, Dhindsa RK, Singh AK, Singh I: Administration of S-nitrosoglutathione after traumatic brain injury protects the neurovascular unit and reduces secondary injury in a rat model of controlled cortical impact. J Neuroinflammation 2009, 6:32.
50. Fabis MJ, Phares TW, Kean RB, Koprowski H, Hooper DC: Blood-brain barrier changes and cell invasion differ between therapeutic immune clearance of neurotrophic virus and CNS autoimmunity. Proc Natl Acad Sci U S A 2008, 105:15511-15516.
51. Nag S: Pathophysiology of blood-brain barrier breakdown. Methods Mol Med 2003, 89:97-119.
52. Neuwelt EA, Bauer B, Fahlke C, Fricker G, Iadecola C, Janigro D, Leybaert L, Molnar Z, O'Donnell ME, Povlishock JT, Saunders NR, Sharp F, Stanimirovic D, Watts RJ, Drewes LR: Engaging neuroscience to advance translational research in brain barrier biology. Nat Rev Neurosci 2011, 12:169-182.
53. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD: Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 2006, 1:223-236.
54. Sacerdote P, Massi P, Panerai AE, Parolaro D: In vivo and in vitro treatment with the synthetic cannabinoid CP55, 940 decreases the in vitro migration of macrophages in the rat: involvement of both CB1 and CB2 receptors. J Neuroimmunol 2000, 109:155-163.
55. Walter L, Stella N: Cannabinoids and neuroinflammation. Br J Pharmacol 2004, 141:775-785.
56. Montecucco F, Burger F, Mach F, Steffens S: CB2 cannabinoid receptor agonist JWH-015 modulates human monocyte migration through defined intracellular signaling pathways. Am J Physiol Heart Circ Physiol 2008, 294:H1145-H1155.
57. Correa F, Mestre L, Docagne F, Guaza C: Activation of cannabinoid CB2 receptor negatively regulates IL-12p40 production in murine macrophages: role of IL-10 and ERK1/2 kinase signaling. Br J Pharmacol 2005, 145:441-448.
58. Lombard C, Nagarkatti M, Nagarkatti P: CB2 cannabinoid receptor agonist, JWH-015, triggers apoptosis in immune cells: potential role for CB2-selective ligands as immunosuppressive agents. Clin Immunol 2007, 122:259-270.
59. Maresz K, Carrier EJ, Ponomarev ED, Hillard CJ, Dittel BN: Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli. J Neurochem 2005, 95:437-445.
60. Ashton JC: Knockout controls and the specificity of cannabinoid CB2 receptor antibodies. Br J Pharmacol 2011, 163:1113.
61. Ashton JC: The use of knockout mice to test the specificity of antibodies for cannabinoid receptors. Hippocampus 2012, 22:643-644.
62. Atwood BK, Mackie K: CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 2010, 160:467-479.
63. Lopez-Rodriguez AB, Siopi E, Finn DP, Marchand-Leroux C, Garcia-Segura LM, Jafarian-Tehrani M, Viveros MP: CB1 and CB2 cannabinoid receptor antagonists prevent minocycline-induced neuroprotection following traumatic brain injury in mice. Cereb Cortex 2013. doi:10.1093/cercor/bht202