Protective Effects of Cannabidiol Against Hippocampal Cell Death and Cognitive Impairment Induced by Bilateral Common Carotid Artery Occlusion in Mice

Neurotoxicity Research

Volumn 26, Issue 4, 2014, Pages 307-316

  Schiavon, Angélica Pupin ^a   Soares, Lígia Mendes ^a   Bonato, Jéssica Mendes ^a   Milani, Humberto ^a   Guimarães, Francisco Silveira ^b   Weffort de Oliveira, Rúbia Maria ^a  

^a STATE UNIVERSITY OF MARINGÁ   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Bilateral common carotid artery occlusion; Cannabidiol; Hippocampus; Mice; Morris water maze

Indexed keywords

CANNABIDIOL; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROPROTECTIVE AGENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN ISCHEMIA; CAROTID ARTERY OBSTRUCTION; CELL SURVIVAL; COGNITIVE DEFECT; CONTROLLED STUDY; HIPPOCAMPUS; HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MACROGLIA; MALE; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NISSL STAINING; NONHUMAN; SPATIAL LEARNING; SPATIAL MEMORY; ANIMAL; ASTROCYTE; CAROTID ARTERY DISEASES; CELL DEATH; COGNITION DISORDERS; COMMON CAROTID ARTERY; COMPLICATION; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; MAZE TEST; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION;

CANNABIS SATIVA; MUS;

ANIMALS; ASTROCYTES; CANNABIDIOL; CAROTID ARTERY DISEASES; CAROTID ARTERY, COMMON; CELL DEATH; CELL SURVIVAL; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; NEURONS; NEUROPROTECTIVE AGENTS; RANDOM ALLOCATION;

EID: 84919385687     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-014-9457-0     Document Type: Article

References (58)

1. Anderson CA, Arciniegas DB (2010) Cognitive sequelae of hypoxic-ischemic brain injury: a review. Neurorehabilitation 26(1):47–63
2. Auriel E, Bornstein NM (2010) Neuroprotection in acute ischemic stroke-current status. J Cell Mol Med 4(9):2200–2202
3. Bachevalier J, Meunier M (1996) Cerebral ischemia: are the memory deficits associated with hippocampal cell loss? Hippocampus 6(5):553–560
4. Blum S, Luchsinger JA, Manly JJ, Schupf N, Stern Y, Brown TR, DeCarli C, Small SA, Mayeux R, Brickman AM (2012) Memory after silent stroke: hippocampus and infarcts both matter. Neurology 78(1):38–46
5. Bora KS, Arora S, Shri R (2011) Role of Ocimum basilicum L. in prevention of ischemia and reperfusion-induced cerebral damage, and motor dysfunctions in mice brain. J Ethnopharmacol 137(3):1360–1365
6. Braida D, Pegorini S, Arcidiacono MV, Consalez GG, Croci L, Sala M (2003) Post-ischemic treatment with cannabidiol prevents electroencephalographic flattening, hyperlocomotion and neuronal injury in gerbils. Neurosci Lett 346(1–2):61–64
7. Campos AC, Moreira FA, Gomes FV, Del Bel EA, Guimarães FS (2012) Multiple mechanisms involved in the large-spectrum therapeutic potential of cannabidiol in psychiatric disorders. Philos Trans R Soc Lond B 367(1607):3364–3378
8. Campos AC, Ortega Z, Palazuelos J, Fogaça MV, Aguiar DC, Díaz-Alonso J, Ortega-Gutiérrez S, Vázquez-Villa H, Moreira FA, Guzmán M, Galve-Roperh I, Guimarães FS (2013) The anxiolytic effect of cannabidiol on chronically stressed mice depends on hippocampal neurogenesis: involvement of the endocannabinoid system. Int J Neuropsychopharmacol 16(6):1407–1419. doi:10.1017/S1461145712001502
9. Carty ML, Wixey JA, Kesby J, Reinebrant HE, Colditz PB, Gobe G (2010) Long-term losses of amygdala corticotropin-releasing factor neurons are associated with behavioural outcomes following neonatal hypoxia–ischemia. Behav Brain Res 208:609–618
10. Caruana DA, Nesbitt C, Mumby DG, Chapman CA (2008) Seizure activity in the rat hippocampus, perirhinal and prefrontal cortex associated with transient global cerebral ischemia. J Neural Transm 115(3):401–411
11. Castillo A, Tolón MR, Fernández-Ruiz J, Romero J, Martinez-Orgado J (2010) The neuroprotective effect of cannabidiol in an in vitro model of newborn hypoxic-ischemic brain damage in mice is mediated by CB(2) and adenosine receptors. Neurobiol Dis 37(2):434–440
12. Cheung WM, Wang CK, Kuo JS, Lin TN (1999) Changes in the level of glial fibrillary acidic protein (GFAP) after mild and severe focal cerebral ischemia. Chin J Physiol 42(4):227–235
13. Colangelo AM, Cirillo G, Lavitrano ML, Alberghina L, Papa M (2012) Targeting reactive astrogliosis by novel biotechnological strategies. Biotechnol Adv 30(1):261–271
14. Corbett D, Crooks P (1997) Ischemic preconditioning: a long term survival study using behavioural and histological endpoints. Brain Res. 760(1–2):129–136
15. Corbett D, Nurse S (1998) The problem of assessing effective neuroprotection in experimental cerebral ischemia. Prog Neurobiol. 54(5):531–548
16. de la Tremblaye PB, Plamondon H (2011) Impaired conditioned emotional response and object recognition are concomitant to neuronal damage in the amygdala and perirhinal cortex in middle-aged ischemic rats. Behav Brain Res 219(2):227–233
17. Duan YL, Wang SY, Zeng QW, Su DS, Li W, Wang XR, Zhao Z (2011) Astroglial reaction to delta opioid peptide [D-Ala2, D-Leu5] enkephalin confers neuroprotection against global ischemia in the adult rat hippocampus. Neuroscience 192:81–90
18. Esposito G, Scuderi C, Valenza M, Togna GI, Latina V, De Filippis D, Cipriano M, Carratù MR, Iuvone T, Steardo L (2011) Cannabidiol reduces Aβ-induced neuroinflammation and promotes hippocampal neurogenesis through PPARγ involvement. PLoS One 6(12):e28668
19. Fernández-Ruiz J, Sagredo O, Pazos MR, García C, Pertwee R, Mechoulam R, Martínez-Orgado J (2013) Cannabidiol for neurodegenerative disorders: important new clinical applications for this phytocannabinoid? Br J Clin Pharmacol 75(2):323–333
20. Franklin KBJ, Paxinos G (1997) The mouse brain in stereotaxic coordinates, 2nd edn. Editora Academic Press, San Diego
21. Garcia C, Palomo-Garo C, Garcia-Arencibia M, Ramos J, Pertwee R, Fernández-Ruiz J (2011) Symptom-relieving and neuroprotective effects of the phytocannabinoid D9-THCV in animal modeks of Parkinson’s disease. Br J Pharmacol 164(7):1495–1506
22. Harvey BS, Ohlsson KS, Mååg JL, Musgrave IF, Smid SD (2012) Contrasting protective effects of cannabinoids against oxidative stress and amyloid-β evoked neurotoxicity in vitro. Neurotoxicology 33(1):138–146
23. Hayakawa K, Mishima K, Irie K, Hazekawa M, Mishima S, Fujioka M, Orito K, Egashira N, Katsurabayashi S, Takasaki K, Iwasaki K, Fujiwara M (2008) Cannabidiol prevents a post-ischemic injury progressively induced by cerebral ischemia via a high-mobility group box1-inhibiting mechanism. Neuropharmacology 55(8):1280–1286
24. Hayakawa K, Irie K, Sano K, Watanabe T, Higuchi S, Enoki M, Nakano T, Harada K, Ishikane S, Ikeda T, Fujioka M, Orito K, Iwasaki K, Mishima K, Fujiwara M (2009) Therapeutic time window of cannabidiol treatment on delayed ischemic damage via high-mobility group box1-inhibiting mechanism. Biol Pharm Bull 32(9):1538–1544
25. Iuvone T, Esposito G, Esposito R, Santamaria R, Di Rosa M, Izzo AA (2004) Neuroprotective effect of cannabidiol, a non-psychoactive component from Cannabis sativa, on beta-amyloid-induced toxicity in PC12 cells. J Neurochem 89(1):134–141
26. Kartsounis LD, Rudge P, Stevens JM (1995) Bilateral lesions of CA1 and CA2 fields of the hippocampus are sufficient to cause a severe amnesic syndrome in humans. J Neurol Neurosurg Psychiatry 59(1):95–98
27. Kindy MS, Bhat AN, Bhat NR (1992) Transient ischemia stimulates glial fibrillary acid protein and vimentin gene expression in the gerbil neocortex, striatum and hippocampus. Brain Res Mol Brain Res 13(3):199–206
28. Kumaran D, Udayabanu M, Kumar M, Aneja R, Katyal A (2008) Involvement of angiotensin converting enzyme in cerebral hypoperfusion induced anterograde memory impairment and cholinergic dysfunction in rats. Neuroscience 155(3):626–639
29. Lafuente H, Alvarez FJ, Pazos MR, Alvarez A, Rey-Santano MC, Mielgo V, Murgia-Esteve X, Hilario E, Martinez-Orgado J (2011) Cannabidiol reduces brain damage and improves functional recovery after acute hypoxia–ischemia in newborn pigs. Pediatr Res 70(3):272–277
30. Lee TH, Kato H, Kogure K, Itoyama Y (1996) Temporal profile of nerve growth factor like immunoreactivity after transient focal cerebral ischemia in rats (1996). Brain Res 713:199–210
31. Mao X, Yin W, Liu M, Ye M, Liu P, Liu J, Xu S, Pi R (2011) Osthole, a natural coumarin, improves neurobehavioral functions and reduces infarct volume and matrix metalloproteinase-9 activity after transient focal cerebral ischemia in rats. Brain Res 1385:275–280
32. Mateen FJ, Josephs KA, Trenerry MR, Felmlee-Devine MD, Weaver AL, Carone M, White RD (2011) Long-term cognitive outcomes following out-of-hospital cardiac arrest: a population-based study. Neurology 77(15):1438–1445
33. Mechoulam R, Shohami E (2007) Endocannabinoids and traumatic brain injury. Mol Neurobiol 36(1):68–74
34. Moulaert VR, Wachelder EM, Verbunt JA, Wade DT, van Heugten CM (2010) Determinants of quality of life in survivors of cardiac arrest. J Rehabil Med 42(6):553–558
35. Neumann JT, Cohan CH, Dave KR, Wright CB, Perez-Pinzon MA (2013) Global cerebral ischemia: synaptic and cognitive dysfunction. Curr Drug Targets 14(1):20–35
36. Nikonenko AG, Radenovic L, Andjus PR, Skibo GG (2009) Structural features of ischemic damage in the hippocampus. Anat Rec (Hoboken) 292(12):1914–1921
37. Norenberg MD (1996) Astrocytic-ammonia interactions in hepatic encephalopathy. Semin Liver Dis 16(3):245–253
38. Pazos MR, Cinquina V, Gómez A, Layunta R, Santos M, Fernández-Ruiz J, Martínez-Orgado J (2012) Cannabidiol administration after hypoxia–ischemia to newborn rats reduces long-term brain injury and restores neurobehavioral function. Neuropharmacology 63(5):776–783
39. 2 receptors. Neuropharmacology 71:282–291
40. Pekny M, Pekna M (2004) Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol. 204(4):428–437
41. Pekny M, Nilsson M (2005) Astrocyte activation and reactive gliosis. Glia 50(4):427–434
42. Peskine A, Picq C, Pradat-diehl P (2010) Neurological sequelae after cerebral anoxia. Brain Inj 24(5):755–761
43. Petito CK, Halaby IA (1993) Relationship between ischemia and ischemic neuronal necrosis to astrocyte expression of glial fibrillary acidic protein. Int J Dev Neurosci 11(2):239–247
44. Prediger RD, Fernandes MS, Rial D, Wopereis S, Pereira VS, Bosse TS, Da Silva CB, Carradore RS, Machado MS, Cechinel-Filho V, Costa-Campos L (2008) Effects of acute administration of the hydroalcoholic extract of mate tea leaves (Ilex paraguariensis) in animal models of learning and memory. J Ethnopharmacol 120(3):465–473
45. Ridet JL, Malhotra SK, Privat A, Gage FH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20(12):570–577
46. Robel S, Berninger B, Götz M (2011) The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12(2):88–104
47. Sachdev PS, Chen X, Joscelyne A, Wen W, Brodaty H (2007) Amygdala in stroke/transient ischemic attack patients and its relationship to cognitive impairment and psychopathology: the Sydney stroke study. Am J Geriatr Psychiatry 15:487–496
48. Sagredo O, Pazos MR, Satta V, Ramos JA, Pertwee RG, Fernández-Ruiz J (2011) Neuroprotective effects of phytocannabinoid-based medicines in experimental models of Huntington’s disease. J Neurosci Res 89(9):1509–1518
49. Schmued LC, Stowers CC, Scallet AC, Xu L (2005) Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res 1035(1):24–31
50. Seif el Nasr M, Nuglisch J, Krieglstein J (1992) Prevention of ischemia-induced cerebral hypothermia by controlling the environmental temperature. J Pharmacol Toxicol Methods 27(1):23–26
51. Shinjyo N, Di Marzo V (2013) The effect cannabichromene on adult neural stem/progenitor cells. Neurochem 63(5):432–437
52. Soares LM, Schiavon AP, Milani H, de Oliveira RM (2013) Cognitive impairment and persistent anxiety-related responses following bilateral common carotid artery occlusion in mice. Behav Brain Res 249:28–37
53. Stoll G, Jander S, Schroeter M (1998) Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56(2):149–171
54. Szydlowska K, Gozdz A, Dabrowski M, Zawadzka M, Kaminska B (2010) Prolonged activation of ERK triggers glutamate-induced apoptosis of astrocytes: neuroprotective effect of FK506. J Neurochem 113(4):904–918
55. Takuma K, Baba A, Matsuda T (2004) Astrocyte apoptosis: implications for neuroprotection. Prog Neurobiol 72(2):111–127
56. 2 receptors. ACS Chem Neurosci 3(5):400–406
57. Zhang L, Fu F, Zhang X, Zhu M, Wang T, Fan H (2010) Escin attenuates cognitive deficits and hippocampal injury after transient global cerebral ischemia in mice via regulating certain inflammatory genes. Neurochem Int 57(2):119–127
58. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the Hippocampus. J Neurosci 6(10):2950–2967