Ultralow doses of cannabinoid drugs protect the mouse brain from inflammation-induced cognitive damage

Journal of Neuroscience Research

Volumn 92, Issue 12, 2014, Pages 1669-1677

  Fishbein Kaminietsky, Miriam ^a   Gafni, Mikhal ^a   Sarne, Yosef ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Cannabinoids; Cognitive impairment; Cyclooxygenase; Neuroinflammation

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; 4 [4 (1,1 DIMETHYLHEPTYL) 2,6 DIMETHOXYPHENYL] 6,6 DIMETHYLBICYCLO[3.1.1]HEPT 2 EN 2 YLMETHANOL; ARACHIDONYL 2' CHLOROETHYLAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CYCLOOXYGENASE 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RIMONABANT; SR 141528; TETRAHYDROCANNABINOL; UNCLASSIFIED DRUG; 2-CHLORO-5-NITROBENZANILIDE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ANILIDE; ARACHIDONIC ACID DERIVATIVE; ARACHIDONYL-2-CHLOROETHYLAMIDE; BORNANE DERIVATIVE; CANNABINOID RECEPTOR AGONIST; DRONABINOL; LIPOPOLYSACCHARIDE; PTGS2 PROTEIN, MOUSE; PYRAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PROTECTION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG DOSE REGIMEN; DRUG EFFECT; ENCEPHALITIS; FRONTAL CORTEX; HIPPOCAMPUS; LOW DRUG DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECOGNITION; SINGLE DRUG DOSE; ANIMAL; BRAIN; CHEMICALLY INDUCED; COGNITION DISORDERS; COMPLICATION; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; METABOLISM; PATHOLOGY;

ANILIDES; ANIMALS; ARACHIDONIC ACIDS; BORNANES; BRAIN; CANNABINOID RECEPTOR AGONISTS; CANNABINOID RECEPTOR ANTAGONISTS; COGNITION DISORDERS; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRONABINOL; ENCEPHALITIS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED ICR; PPAR GAMMA; PYRAZOLES; RECOGNITION (PSYCHOLOGY);

EID: 84911989539     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23452     Document Type: Article

References (69)

1. Asanuma M, Miyazaki I. 2008. Nonsteroidal anti-inflammatory drugs in experimental parkinsonian models and Parkinson's disease. Curr Pharm Des 14:1428-1434.
2. Assaf F, Fishbein M, Gafni M, Keren O, Sarne Y. 2011. Pre- and post-conditioning treatment with an ultralow dose of Delta9-tetrahydrocannabinol (THC) protects against pentylenetetrazole (PTZ)-induced cognitive damage. Behav Brain Res 220:194-201.
3. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM. 1999. PPARγ is required for placental, cardiac, and adipose tissue development. Mol Cell 4:585-595.
4. Bauer MK, Lieb K, Schulze-Osthoff K, Berger M, Gebicke-Haerter PJ, Bauer J, Fiebich BL. 1997. Expression and regulation of cyclooxygenase-2 in rat microglia. Eur J Biochem 243:726-731.
5. Borner C, Hollt V, Sebald W, Kraus J. 2007. Transcriptional regulation of the cannabinoid receptor type 1 gene in T cells by cannabinoids. J Leukoc Biol 81:336-343.
6. Bouaboula M, Hilairet S, Marchand J, Fajas L, Le Fur G, Casellas P. 2005. Anandamide induced PPARγ transcriptional activation and 3T3-L1 preadipocyte differentiation. Eur J Pharmacol 517:174-181.
7. Breder CD, Saper CB. 1996. Expression of inducible cyclooxygenase mRNA in the mouse brain after systemic administration of bacterial lipopolysaccharide. Brain Res 713:64-69.
8. Broussard GJ, Mytar J, Li RC, Klapstein GJ. 2012. The role of inflammatory processes in Alzheimer's disease. Inflammopharmacology 20:109-126.
9. Choi SH, Aid S, Bosetti F. 2009. The distinct roles of cyclooxygenase-1 and -2 in neuroinflammation: implications for translational research. Trends Pharmacol Sci 30:174-181.
10. Collino M, Patel NS, Lawrence KM, Collin M, Latchman DS, Yaqoob MM, Thiemermann C. 2005. The selective PPARγ antagonist GW9662 reverses the protection of LPS in a model of renal ischemia-reperfusion. Kidney Int 68:529-536.
11. Collins LM, Toulouse A, Connor TJ, Nolan YM. 2012. Contributions of central and systemic inflammation to the pathophysiology of Parkinson's disease. Neuropharmacology 62:2154-168.
12. Compton DR, Rice KC, De Costa BR, Razdan RK, Melvin LS, Johnson MR, Martin BR. 1993. Cannabinoid structure-activity relationships: correlation of receptor binding and in vivo activities. J Pharmacol Exp Ther 265:218-226.
13. Cunha C, Brambilla R, Thomas KL. 2010. A simple role for BDNF in learning and memory? Front Mol Neurosci 3:1.
14. Ellrichmann G, Reick C, Saft C, Linker RA. 2013. The role of the immune system in Huntington's disease. Clin Dev Immunol doi:10.1155/2013/541259.
15. Ennaceur A, Delacour J. 1988. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31:47-59.
16. Fakhfouri G, Ahmadiani A, Rahimian R, Grolla AA, Moradi F, Haeri A. 2012. WIN55212-2 attenuates amyloid-β-induced neuroinflammation in rats through activation of cannabinoid receptors and PPARγ pathway. Neuropharmacology 63:653-666.
17. Farooqui AA, Horrocks LA, Farooqui T. 2007. Modulation of inflammation in brain: a matter of fat. J Neurochem 101:577-599.
18. Fishbein M, Gov S, Assaf F, Gafni M, Keren O, Sarne Y. 2012. Long-term behavioral and biochemical effects of an ultralow dose of delta9-tetrahydrocannabinol (THC): neuroprotection and ERK signaling. Exp Brain Res 221:437-448.
19. Gao HM, Hong JS. 2008. Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol 29:357-365.
20. Gidday JM. 2006. Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci 7:437-448.
21. Gong JP, Onaivi ES, Ishiguro H, Liu QR, Tagliaferro PA, Brusco A, Uhl GR. 2006. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 1071:10-23.
22. Han J, Kesner P, Metna-Laurent M, Duan T, Xu L, Georges F, Koehl M, Abrous DN, Mendizabal-Zubiaga J, Grandes P, Liu Q, Bai G, Wang W, Xiong L, Ren W, Marsicano G, Zhang X. 2012. Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell 148:1039-1050.
23. Hausenloy DJ, Yellon DM. 2009. Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis 204:334-341.
24. Hayakawa K, Mishima K, Nozako M, Hazekawa M, Ogata A, Fujioka M, Harada K, Mishima S, Orito K, Egashira N, Iwasaki K, Fujiwara M. 2007. Delta9-tetrahydrocannabinol (delta9-THC) prevents cerebral infarction via hypothalamic-independent hypothermia. Life Sci 80:1466-1471.
25. Hewett SJ, Bell SC, Hewett JA. 2006. Contributions of cyclooxygenase-2 to neuroplasticity and neuropathology of the central nervous system. Pharmacol Ther 112:335-357.
26. Jaeschke H. 2003. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 284:G15-G26.
27. Jaturapatporn D, Isaac MG, McCleery J, Tabet N. 2012. Aspirin, steroidal, and nonsteroidal anti-inflammatory drugs for the treatment of Alzheimer's disease. Cochrane Database Syst Rev 2:CD006378.
28. Kumar A, Loane DJ. 2012. Neuroinflammation after traumatic brain injury: opportunities for therapeutic intervention. Brain Behav Immun 26:1191-1201.
29. Lin WY, Chang YC, Lee HT, Huang CC. 2009. CREB activation in the rapid, intermediate, and delayed ischemic preconditioning against hypoxic-ischemia in neonatal rat. J Neurochem 108:847-859.
30. Lipsky RH, Marini AM. 2007. Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Ann N Y Acad Sci 1122:130-143.
31. Lyman M, Lloyd DG, Ji X, Vizcaychipi MP, Ma D. 2013. Neuroinflammation: the role and consequences. Neurosci Res 79:1-12.
32. Marchalant Y, Cerbai F, Brothers HM, Wenk GL. 2008. Cannabinoid receptor stimulation is anti-inflammatory and improves memory in old rats. Neurobiol Aging 29:1894-1901.
33. Minghetti L. 2004. Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. J Neuropathol Exp Neurol 63:901-910.
34. Moore KJ, Rosen ED, Fitzgerald ML, Randow F, Andersson LP, Altshuler D, Milstone DS, Mortensen RM, Spiegelman BM, Freeman MW. 2001. The role of PPARγ in macrophage differentiation and cholesterol uptake. Nat Med 7:41-47.
35. Murry CE, Jennings RB, Reimer KA. 1986. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136.
36. Nagayama T, Sinor AD, Simon RP, Chen J, Graham SH, Jin K, Greenberg DA. 1999. Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J Neurosci 19:2987-2995.
37. Nakayama M, Uchimura K, Zhu RL, Nagayama T, Rose ME, Stetler RA, Isakson PC, Chen J, Graham SH. 1998. Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc Natl Acad Sci U S A 95:10954-10959.
38. Noble F, Rubira E, Boulanouar M, Palmier B, Plotkine M, Warnet JM, Marchand-Leroux C, Massicot F. 2007. Acute systemic inflammation induces central mitochondrial damage and mnesic deficit in adult Swiss mice. Neurosci Lett 424:106-110.
39. Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, Myers L, Mora Z, Tagliaferro P, Gardner E, Brusco A, Akinshola BE, Liu QR, Hope B, Iwasaki S, Arinami T, Teasenfitz L, Uhl GR. 2006. Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann N Y Acad Sci 1074:514-536.
40. O'Sullivan SE, Tarling EJ, Bennett AJ, Kendall DA, Randall MD. 2005. Novel time-dependent vascular actions of delta9-tetrahydrocannabinol mediated by peroxisome proliferator-activated receptor gamma. Biochem Biophys Res Commun 337:824-831.
41. Perry VH. 2004. The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun 18:407-413.
42. Pignataro G, Meller R, Inoue K, Ordonez AN, Ashley MD, Xiong Z, Gala R, Simon RP. 2008. In vivo and in vitro characterization of a novel neuroprotective strategy for stroke: ischemic postconditioning. J Cereb Blood Flow Metab 28:232-241.
43. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT. 2007. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453-462.
44. Rangwala SM, Lazar MA. 2004. Peroxisome proliferator-activated receptor gamma in diabetes and metabolism. Trends Pharmacol Sci 25:331-336.
45. Rees K, Stowe R, Patel S, Ives N, Breen K, Clarke CE, Ben-Shlomo Y. 2011. Nonsteroidal anti-inflammatory drugs as disease-modifying agents for Parkinson's disease: evidence from observational studies. Cochrane Database Syst Rev CD008454.
46. Rostami F, Oryan S, Ahmadiani A, Dargahi L. 2012. Morphine preconditioning protects against LPS-induced neuroinflammation and memory deficit. J Mol Neurosci 48:22-34.
47. Samuels IS, Saitta SC, Landreth GE. 2009. MAP'ing CNS development and cognition: an ERKsome process. Neuron 61:160-167.
48. Semmler A, Frisch C, Debeir T, Ramanathan M, Okulla T, Klockgether T, Heneka MT. 2007. Long-term cognitive impairment, neuronal loss, and reduced cortical cholinergic innervation after recovery from sepsis in a rodent model. Exp Neurol 204:733-740.
49. Shichita T, Sakaguchi R, Suzuki M, Yoshimura A. 2012. Postischemic inflammation in the brain. Front Immunol 3:132.
50. Shouman B, Fontaine RH, Baud O, Schwendimann L, Keller M, Spedding M, Lelievre V, Gressens P. 2006. Endocannabinoids potently protect the newborn brain against AMPA-kainate receptor-mediated excitotoxic damage. Br J Pharmacol 148:442-451.
51. Sivarajah A, McDonald MC, Thiemermann C. 2005. The cardioprotective effects of preconditioning with endotoxin, but not ischemia, are abolished by a peroxisome proliferator-activated receptor-γ antagonist. J Pharmacol Exp Ther 313:896-901.
52. Stella N. 2010. Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia 58:1017-1030.
53. Strauss KI, Barbe MF, Marshall RM, Raghupathi R, Mehta S, Narayan RK. 2000. Prolonged cyclooxygenase-2 induction in neurons and glia following traumatic brain injury in the rat. J Neurotrauma 17:695-711.
54. Sundararajan S, Jiang Q, Heneka M, Landreth G. 2006. PPARγ as a therapeutic target in central nervous system diseases. Neurochem Int 49:136-144.
55. Sweatt JD. 2004. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311-317.
56. Szanto A, Nagy L. 2008. The many faces of PPARγ: anti-inflammatory by any means? Immunobiology 213:789-803.
57. Thomas A, Baillie GL, Phillips AM, Razdan RK, Ross RA, Pertwee RG. 2007. Cannabidiol displays unexpectedly high potency as an antagonist of CB1 and CB2 receptor agonists in vitro. Br J Pharmacol 150:613-623.
58. Tourino C, Zimmer A, Valverde O. 2010. THC prevents mdma neurotoxicity in mice. PLoS One 5:e9143.
59. Truettner J, Busto R, Zhao W, Ginsberg MD, Perez-Pinzon MA. 2002. Effect of ischemic preconditioning on the expression of putative neuroprotective genes in the rat brain. Brain Res Mol Brain Res 103:106-115.
60. van der Stelt M, Veldhuis WB, Bar PR, Veldink GA, Vliegenthart JF, Nicolay K. 2001a. Neuroprotection by Delta9-tetrahydrocannabinol, the main active compound in marijuana, against ouabain-induced in vivo excitotoxicity. J Neurosci 21:6475-6479.
61. van der Stelt M, Veldhuis WB, van Haaften GW, Fezza F, Bisogno T, Bar PR, Veldink GA, Vliegenthart JF, Di Marzo V, Nicolay K. 2001b. Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci 21:8765-8771.
62. Vezzani A, Friedman A, Dingledine RJ. 2012. The role of inflammation in epileptogenesis. Neuropharmacology 69:16-24.
63. Waldman M, Hochhauser E, Fishbein M, Aravot D, Shainberg A, Sarne Y. 2013. An ultralow dose of tetrahydrocannabinol provides cardioprotection. Biochem Pharmacol 85:1626-1633.
64. Weberpals M, Hermes M, Hermann S, Kummer MP, Terwel D, Semmler A, Berger M, Schafers M, Heneka MT. 2009. NOS2 gene deficiency protects from sepsis-induced long-term cognitive deficits. J Neurosci 29:14177-14184.
65. Weggen S, Rogers M, Eriksen J. 2007. NSAIDs: small molecules for prevention of Alzheimer's disease or precursors for future drug development? Trends Pharmacol Sci 28:536-543.
66. Wever KE, Menting TP, Rovers M, van der Vliet JA, Rongen GA, Masereeuw R, Ritskes-Hoitinga M, Hooijmans CR, Warle M. 2012. Ischemic preconditioning in the animal kidney: a systematic review and meta-analysis. PLoS One 7:e32296.
67. Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF. 1993. Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11:371-386.
68. Yin JC, Tully T. 1996. CREB and the formation of long-term memory. Curr Opin Neurobiol 6:264-268.
69. Zeng Y, Xie K, Dong H, Zhang H, Wang F, Li Y, Xiong L. 2012. Hyperbaric oxygen preconditioning protects cortical neurons against oxygen-glucose deprivation injury: role of peroxisome proliferator-activated receptor-γ. Brain Res 1452:140-150.