Cannabinoid receptor subtypes 1 and 2 mediate long-lasting neuroprotection and improve motor behavior deficits after transient focal cerebral ischemia

Neuroscience

Volumn 227, Issue , 2012, Pages 313-326

  Schmidt, W ^a,b   Schafer F ^a   Striggow, V ^a   Frohlich K ^a   Striggow, F ^a,b  

^a KeyNeurotek Pharmaceuticals AG   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

CB1 receptor; CB2 receptor; Cerebral ischemia; Endocannabinoid system; Neuroprotection

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 2 RECEPTOR; CANNABINOID 2 RECEPTOR AGONIST; CD45 ANTIGEN; ENDOTHELIN; KN 3872717; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CONTROLLED STUDY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MACROPHAGE ACTIVATION; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR DYSFUNCTION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; ANTIGENS, CD45; ARACHIDONIC ACIDS; BRAIN; BRAIN INFARCTION; CANNABINOIDS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ECTODYSPLASINS; ENDOCANNABINOIDS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; INDANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MOVEMENT DISORDERS; NEUROPROTECTIVE AGENTS; POLYUNSATURATED ALKAMIDES; PSYCHOMOTOR PERFORMANCE; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; SULFONIC ACIDS; TIME FACTORS;

EID: 84868522261     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.080     Document Type: Article

References (80)

1. Albayram O., Alferink J., Pitsch J., Piyanova A., Neitzert K., Poppensieker K., Mauer D., Michel K., Legler A., Becker A., Monory K., Lutz B., Zimmer A., Bilkei-Gorzo A. Role of CB1 cannabinoid receptors on GABAergic neurons in brain aging. Proc Nat Acad Sci U S A 2011, 108:11256-11261.
2. Ashton J.C., Friberg D., Darlington C.L., Smith P.F. Expression of the cannabinoid CB2 receptor in the rat cerebellum: an immunohistochemical study. Neurosci Lett 2006, 396:113-116.
3. Ashton J.C., Rahman R.M.A., Nair S.M., Sutherland B.A., Glass M., Appleton I. Cerebral hypoxia-ischemia and middle cerebral artery occlusion induce expression of the cannabinoid CB2 receptor in the brain. Neurosci Lett 2007, 412:114-117.
4. Atwood B.K., Mackie K. CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 2010, 160:467-479.
5. Beltramo M., Bernardini N., Bertorelli R., Campanella M., Nicolussi E., Fredduzzi S., Reggiani A. CB2 receptor-mediated antihyperalgesia: possible direct involvement of neural mechanisms. Eur J Neurosci 2006, 23:1530-1538.
6. Benito C., Kim W.-K., Chavarría I., Hillard C.J., Mackie K., Tolón R.M., Williams K., Romero J. A glial endogenous cannabinoid system is upregulated in the brains of macaques with simian immunodeficiency virus-induced encephalitis. J Neurosci 2005, 25:2530-2536.
7. Benito C., Núñez E., Tolón R.M., Carrier E.J., Rábano A., Hillard C.J., Romero J. Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J Neurosci 2003, 23:11136-11141.
8. Brusco A., Tagliaferro P., Saez T., Onaivi E.S. Postsynaptic localization of CB2 cannabinoid receptors in the rat hippocampus. Synapse 2008, 62:944-949.
9. Buckley N.E., McCoy K.L., Mezey E., Bonner T., Zimmer A., Felder C.C., Glass M., Zimmer A. Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB2 receptor. Eur J Pharmacol 2000, 396:141-149.
10. Cabral G.A., Raborn E.S., Griffin L., Dennis J., Marciano-Cabral F. CB2 receptors in the brain: role in central immune function. Br J Pharmacol 2008, 153:240-251.
11. Campbell V.A., Gowran A. Alzheimer's disease: taking the edge off with cannabinoids?. Br J Pharmacol 2007, 152:655-662.
12. Carayon P., Marchand J., Dussossoy D., Derocq J.-M., Jbilo O., Bord A., Bouaboula M., Galiegue S., Mondiere P., Penarier G., Le Fur G., Defrance T., Casellas P. Modulation and functional involvement of CB2 peripheral cannabinoid receptors during B-cell differentiation. Blood 1998, 92:3605-3615.
13. Carlisle S.J., Marciano-Cabral F., Staab A., Ludwick C., Cabral G.A. Differential expression of the CB2 cannabinoid receptor by rodent macrophages and macrophage-like cells in relation to cell activation. Int Immunopharmacol 2002, 2:69-82.
14. Chavez A.E., Chiu C.Q., Castillo P.E. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat Neurosci 2010, 13:1511-1518.
15. Daniel H., Crepel F. Control of Ca2+ influx by cannabinoid and metabotropic glutamate receptors in rat cerebellar cortex requires K+ channels. J Physiol 2001, 537:793-800.
16. De Petrocellis L., Melck D., Ueda N., Maurelli S., Kurahashi Y., Yamamoto S., Marino G., Di Marzo V. Novel inhibitors of brain, neuronal, and basophilic anandamide amidohydrolase. Biochem Biophys Res Commun 1997, 231:82-88.
17. Derocq J.-M., Segui M., Marchand J., Le Fur G., Casellas P. Cannabinoids enhance human B-cell growth at low nanomolar concentrations. FEBS Lett 1995, 369:177-182.
18. Deutsch D.G., Omeir R., Arreaza G., Salehani D., Prestwich G.D., Huang Z., Howlett A. Methyl arachidonyl fluorophosphonate: a potent irreversible inhibitor of anandamide amidase. Biochem Pharmacol 1997, 53:255-260.
19. Di Marzo V. Targeting the endocannabinoid system: to enhance or reduce?. Nat Rev Drug Discov 2008, 7:438-455.
20. Di Marzo V. Endocannabinoid signaling in the brain: biosynthetic mechanisms in the limelight. Nat Neurosci 2011, 14:9-15.
21. Di Marzo V., Bifulco M., De Petrocellis L. The endocannabinoid system and its therapeutic exploitation. Nat Rev Drug Discov 2004, 3:771-784.
22. Dittel B.N. Direct suppression of autoreactive lymphocytes in the central nervous system via the CB2 receptor. Br J Pharmacol 2008, 153:271-276.
23. Edlich F., Weiwad M., Wildemann D., Jarczowski F., Kilka S., Moutty M.C., Jahreis G., Lucke C., Schmidt W., Striggow F., Fischer G. The specific FKBP38 inhibitor N-(N',N'-dimethylcarboxamidomethyl)cycloheximide has potent neuroprotective and neurotrophic properties in brain ischemia. J Biol Chem 2006, 281:14961-14970.
24. Eljaschewitsch E., Witting A., Mawrin C., Lee T., Schmidt P.M., Wolf S., Hoertnagl H., Raine C.S., Schneider-Stock R., Nitsch R., Ullrich O. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 2006, 49:67-79.
25. Fernandez-Ruiz J., Pazos M.R., Garcia-Arencibia M., Sagredo O., Ramos J.A. Role of CB2 receptors in neuroprotective effects of cannabinoids. Mol Cell Endocrinol 2008, 286:S91-S96.
26. Firsching R., Piek J., Skalej M., Rohde V., Schmidt U., Striggow F., The KN38-7271 study group Early survival of comatose patients after severe traumatic brain injury with the dual cannabinoid CB1/CB2 receptor agonist KN38-7271: a randomized, double-blind, placebo-controlled phase II trial. J Neurol Surg A Cent Eur Neurosurg 2012, 73:204-216.
27. Galiegue S., Mary S., Marchand J., Dussossoy D., Carriere D., Carayon P., Bouaboula M., Shire D., Le Fur G., Casellas P. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 1995, 232:54-61.
28. Gong J.-P., Onaivi E.S., Ishiguro H., Liu Q.-R., Tagliaferro P.A., Brusco A., Uhl G.R. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 2006, 1071:10-23.
29. Harvey B.S., Ohlsson K.S., Maag J.L.V., Musgrave I.F., Smid S.D. Contrasting protective effects of cannabinoids against oxidative stress and amyloid-ß evoked neurotoxicity in vitro. Neurotoxicology 2012, 33:138-146.
30. Hillard C.J., Manna S., Greenberg M.J., DiCamelli R., Ross R.A., Stevenson L.A., Murphy V., Pertwee R.G., Campbell W.B. Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). J Pharmacol Exp Ther 1999, 289:1427-1433.
31. Hohmann A.G., Suplita R.L., Bolton N.M., Neely M.H., Fegley D., Mangieri R., Krey J.F., Michael Walker J., Holmes P.V., Crystal J.D., Duranti A., Tontini A., Mor M., Tarzia G., Piomelli D. An endocannabinoid mechanism for stress-induced analgesia. Nature 2005, 435:1108-1112.
32. Huffman J.W., Liddle J., Yu S., Aung M.M., Abood M.E., Wiley J.L., Martin B.R. 3-(1',1'-Dimethylbutyl)-1-deoxy-delta8-THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg Med Chem 1999, 7:2905-2914.
33. Kathuria S., Gaetani S., Fegley D., Valino F., Duranti A., Tontini A., Mor M., Tarzia G., Rana G.L., Calignano A., Giustino A., Tattoli M., Palmery M., Cuomo V., Piomelli D. Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 2002, 9:76-81.
34. Katona I., Freund T.F. Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med 2008, 14:923-930.
35. Kawamura Y., Fukaya M., Maejima T., Yoshida T., Miura E., Watanabe M., Ohno-Shosaku T., Kano M. The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 2006, 26:2991-3001.
36. Klegeris A., Bissonnette C.J., McGeer P.L. Reduction of human monocytic cell neurotoxicity and cytokine secretion by ligands of the cannabinoid-type CB2 receptor. Br J Pharmacol 2003, 139:775-786.
37. Landucci E., Scartabelli T., Gerace E., Moroni F., Pellegrini-Giampietro D.E. CB1 receptors and post-ischemic brain damage: studies on the toxic and neuroprotective effects of cannabinoids in rat organotypic hippocampal slices. Neuropharmacol 2011, 60:674-682.
38. Maresz K., Pryce G., Ponomarev E.D., Marsicano G., Croxford J.L., Shriver L.P., Ledent C., Cheng X., Carrier E.J., Mann M.K., Giovannoni G., Pertwee R.G., Yamamura T., Buckley N.E., Hillard C.J., Lutz B., Baker D., Dittel B.N. Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells. Nat Med 2007, 13:492-497.
39. Marsicano G., Goodenough S., Monory K., Hermann H., Eder M., Cannich A., Azad S.C., Cascio M.G., Gutiérrez S.O., van der Stelt M., López-Rodriguez M.L., Casanova E., Schütz G., Zieglgänsberger W., Di Marzo V., Behl C., Lutz B. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 2003, 302:84-88.
40. Mauler F., Hinz V., Augstein K.H., Fassbender M., Horváth E. Neuroprotective and brain edema-reducing efficacy of the novel cannabinoid receptor agonist BAY 38-7271. Brain Res 2003, 989:99-111.
41. Mauler F., Horváth E., De Vry J., Jager R., Schwarz T., Sandmann S., Weinz C., Heinig R., Bottcher M. BAY 38-7271: a novel highly selective and highly potent cannabinoid receptor agonist for the treatment of traumatic brain injury. CNS Drug Rev 2003, 9:343-358.
42. Mauler F., Mittendorf J., Horváth E., de Vry J. Characterization of the diarylether sulfonylester (-)-(R)-3-(2-hydroxymethylindanyl-4-oxy)phenyl-4,4,4-trifluoro-1-sulfonate (BAY 38-7271) as a potent cannabinoid receptor agonist with neuroprotective properties. J Pharmacol Exp Ther 2002, 302:359-368.
43. McCoy K.L., Matveyeva M., Carlisle S.J., Cabral G.A. Cannabinoid inhibition of the processing of intact lysozyme by macrophages: evidence for CB2 receptor participation. J Pharmacol Exp Ther 1999, 289:1620-1625.
44. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., Gopher A., Almog S., Martin B.R., Compton D.R., Pertwee R.G., Griffin G., Bayewitch M., Barg J., Vogel Z. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 1995, 50:83-90.
45. Mechoulam R., Parker L.A. The endocannabinoid system and the brain. Ann Rev Psychol 2012, 10.1146/annurev-psych-113011-143739.
46. Metz G.A., Whishaw I.Q. Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 2002, 115:169-179.
47. Miller A.M., Stella N. CB2 receptor-mediated migration of immune cells: it can go either way. Br J Pharmacol 2008, 153:299-308.
48. Mor M., Rivara S., Lodola A., Plazzi P.V., Tarzia G., Duranti A., Tontini A., Piersanti G., Kathuria S., Piomelli D. Cyclohexylcarbamic acid 3'- or 4'-substituted biphenyl-3-yl esters as fatty acid amide hydrolase inhibitors: synthesis, quantitative structure-activity relationships, and molecular modeling studies. J Med Chem 2004, 47:4998-5008.
49. Murikinati S., Jüttler E., Keinert T., Ridder D.A., Muhammad S., Waibler Z., Ledent C., Zimmer A., Kalinke U., Schwaninger M. Activation of cannabinoid 2 receptors protects against cerebral ischemia by inhibiting neutrophil recruitment. FASEB J 2010, 24:788-798.
50. Nagayama T., Sinor A.D., Simon R.P., Chen J., Graham S.H., Jin K., Greenberg D.A. Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J Neurosci 1999, 19:2987-2995.
51. Onaivi E.S., Ishiguro H., Gong J.-P., Patel S., Meozzi P.A., Myers L., Perchuk A., Mora Z., Tagliaferro P.A., Gardner E., Brusco A., Akinshola B.E., Hope B., Lujilde J., Inada T., Iwasaki S., Macharia D., Teasenfitz L., Arinami T., Uhl G.R. Brain neuronal CB2 cannabinoid receptors in drug abuse and depression: from mice to human subjects. PLoS One 2008, 3:e1640.
52. Onaivi E.S., Ishiguro H., Gong J.-P., Patel S., Meozzi P.A., Myers L., Perchuk A., Mora Z., Tagliaferro P.A., Gardner E., Brusco A., Akinshola B.E., Liu Q.-R., Chirwa S.S., Hope B., Lujilde J., Inada T., Iwasaki S., Macharia D., Teasenfitz L., Arinami T., Uhl G.R. Functional expression of brain neuronal CB2 cannabinoid receptors are involved in the effects of drugs of abuse and in depression. Ann N Y Acad Sci 2008, 1139:434-449.
53. Panikashvili D., Simeonidou C., Ben-Shabat S., Hanus L., Breuer A., Mechoulam R., Shohami E. Nature 2001, 413:527-531.
54. Panikashvili D., Mechoulam R., Beni S.M., Alexandrovich A., Shohami E. CB1 cannabinoid receptors are involved in neuroprotection via NF-kappa B inhibition. J Cereb Blood Flow Metab 2005, 25:477-484.
55. Panikashvili D., Shein N.A., Mechoulam R., Trembovler V., Kohen R., Alexandrovich A., Shohami E. The endocannabinoid 2-AG protects the blood-brain barrier after closed head injury and inhibits mRNA expression of proinflammatory cytokines. Neurobiol Dis 2006, 22:257-264.
56. Paxinos G., Watson C. The rat brain in stereotoxic coordinates 2005, Elsevier Academic Press, San Diego, CA.
57. Pietr M., Kozela E., Levy R., Rimmerman N., Lin Y.H., Stella N., Vogel Z., Juknat A. Differential changes in GPR55 during microglial cell activation. FEBS Lett 2009, 583:2071-2076.
58. Price D.A., Martinez A.A., Seillier A., Koek W., Acosta Y., Fernandez E., Strong R., Lutz B., Marsicano G., Roberts J.L., 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.
59. Puente N., Cui Y., Lassalle O., Lafourcade M., Georges F., Venance L., Grandes P., Manzoni O.J. Polymodal activation of the endocannabinoid system in the extended amygdala. Nat Neurosci 2011, 14:1542-1547.
60. Sanchez A.J., Garca-Merino A. Neuroprotective agents: cannabinoids. Clin Immunol 2012, 142:57-67.
61. Schatz A.R., Lee M., Condie R.B., Pulaski J.T., Kaminski N.E. Cannabinoid receptors CB1 and CB2: a characterization of expression and adenylate cyclase modulation within the immune system. Toxicol Appl Pharmacol 1997, 142:278-287.
62. Schlicker E., Kathmann M. Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 2001, 22:565-572.
63. Sharkey J., Butcher S.P. Characterisation of an experimental model of stroke produced by intracerebral microinjection of endothelin-1 adjacent to the rat middle cerebral artery. J Neurosci Methods 1995, 60:125-131.
64. Shen M., Thayer S.A. Cannabinoid receptor agonists protect cultured rat hippocampal neurons from excitotoxicity. Mol Pharmacol 1998, 54:459-462.
65. Shohami E., Cohen-Yeshurun A., Magid L., Algali M., Mechoulam R. Endocannabinoids and traumatic brain injury. Br J Pharmacol 2011, 163:1402-1410.
66. Sinor A.D., Irvin S.M., Greenberg D.A. Endocannabinoids protect cerebral cortical neurons from in vitro ischemia in rats. Neurosci Lett 2000, 278:157-160.
67. Skaper S.D., Buriani A., Dal Toso R., Petrelli L., Romanello S., Facci L., Leon A. The ALIAmide palmitoylethanolamide and cannabinoids, but not anandamide, are protective in a delayed postglutamate paradigm of excitotoxic death in cerebellar granule neurons. Proc Natl Acad Sci U S A 1996, 93:3984-3989.
68. Stella N. Cannabinoid signaling in glial cells. Glia 2004, 48:267-277.
69. Stella N. Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia 2010, 58:1017-1030.
70. Stella N., Schweitzer P., Piomelli D. A second endogenous cannabinoid that modulates long-term potentiation. Nature 1997, 388:773-778.
71. Striggow F., Röhnert P., Reymann K.G. Telomics - tissue-based screening for target validation and preclinical drug development. New Drugs 2002, 1:30-36.
72. Sugiura T., Kondo S., Sukagawa A., Nakane S., Shinoda A., Itoh K., Yamashita A., Waku K. 2-Arachidonoylgylcerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 1995, 215:89-97.
73. Sutherland C.A., Amin D. Relative activities of rat and dog platelet phospholipase A2 and diglyceride lipase. Selective inhibition of diglyceride lipase by RHC 80267. J Biol Chem 1982, 257:14006-14010.
74. Szabo B., Urbanski M.J., Bisogno T., Marzo V.D., Mendiguren A., Baer W.U., Freiman I. Depolarization-induced retrograde synaptic inhibition in the mouse cerebellar cortex is mediated by 2-arachidonoylglycerol. J Physiol 2006, 577:263-280.
75. Tarzia G., Duranti A., Tontini A., Piersanti G., Mor M., Rivara S., Plazzi P.V., Park C., Kathuria S., Piomelli D. Design, synthesis, and structure-activity relationships of alkylcarbamic acid aryl esters, a new class of fatty acid amide hydrolase inhibitors. J Med Chem 2003, 46:2352-2360.
76. Van Sickle M.D., Duncan M., Kingsley P.J., Mouihate A., Urbani P., Mackie K., Stella N., Makriyannis A., Piomelli D., Davison J.S., Marnett L.J., Di Marzo V., Pittman Q.J., Patel K.D., Sharkey K.A. Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 2005, 310:329-332.
77. Walter L., Franklin A., Witting A., Wade C., Xie Y., Kunos G., Mackie K., Stella N. Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J Neurosci 2003, 23:1398-1405.
78. Wolf S.A., Tauber S., Ullrich O. CNS immune surveillance and neuroinflammation: endocannabinoids keep control. Curr Pharm Des 2008, 14:2266-2278.
79. Zhang M., Martin B.R., Adler M.W., Razdan R.K., Jallo J.I., Tuma R.F. Cannabinoid CB2 receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model. J Cereb Blood Flow Metab 2007, 27:1387-1396.
80. Zurolo E., Iyer A.M., Spliet W.G., Van Rijen P.C., Troost D., Gorter J.A., Aronica E. CB1 and CB2 cannabinoid receptor expression during development and in epileptogenic developmental pathologies. Neuroscience 2010, 170:28-41.