CB1 cannabinoid receptor activation rescues amyloid β-induced alterations in behaviour and intrinsic electrophysiological properties of rat hippocampal CA1 pyramidal neurones

Cellular Physiology and Biochemistry

Volumn 29, Issue 3-4, 2012, Pages 391-406

  Haghani, Masoud ^a   Shabani, Mohammad ^b   Javan, Mohammad ^c   Motamedi, Fereshteh ^a   Janahmadi, Mahyar ^a  

^a SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TARBIAT MODARES UNIVERSITY   (Iran)

Author keywords

After hyperpolarization; Alzheimer's disease; Neuronal excitability; Neurotoxicity

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; ACEA; AMYLOID BETA PROTEIN; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR AGONIST; CASPASE 3; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR CHANGE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HIPPOCAMPUS NERVE CELL; IN VIVO STUDY; MALE; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PATCH CLAMP; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

RATTUS;

EID: 84859912791     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000338494     Document Type: Article

References (92)

1. Koo EH, Lansbury PT Jr, Kelly JW: Amyloid diseases: abnormal protein aggregation in neurodegeneration. Proc Natl Acad Sci U S A 1999;96:9989-9990. (Pubitemid 29422496)
2. Carter J, Lippa CF: Beta-amyloid, neuronal death and Alzheimer's disease. Curr Mol Med 2001;1:733-737. (Pubitemid 33772946)
3. LaFerla FM: Calcium dyshomeostasis and intracellular signaling in Alzheimer's disease. Nat Rev Neurosci 2002;3:862-872.
4. Mattson MP: Pathways towards and away from Alzheimer's disease. Nature 2004;430:631-639. (Pubitemid 39061671)
5. Small DH: Dysregulation of calcium homeostasis in Alzheimer's disease. Neurochem Res 2009;4:1824-1829.
6. 2 + channels: a possible involvement of free radicals. J Neurochem 1997;68:265-271. (Pubitemid 26427316)
7. Price SA, Held B, Pearson HA: Amyloid beta protein increases Ca2+ currents in rat cerebellar granule neurones. Neuroreport 1998;9:539-545. (Pubitemid 28109219)
8. Lleo S, GreenbergM, Growdon JH: Current Pharmacotherapy for Alzheimer's Disease. Annu Rev Med 2006;57:513-533. (Pubitemid 43262005)
9. Terry RD: Cell death or synaptic loss in Alzheimer disease. J Neuropathol Exp Neurol 2000;59:1118-1119. (Pubitemid 32006314)
10. Garcia-Arencibia M, Gonzalez S, de Lago E, Ramos JA, Mechoulam R, Fernandez- Ruiz J: Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson's disease: importance of antioxidant and cannabinoid receptorindependent properties. Brain Res 2007;1134:162-170. (Pubitemid 46135535)
11. Sagredo O, Garcia-Arencibia M, de Lago E, Finetti S, Decio A, Fernandez-Ruiz J: Cannabinoids and neuroprotection in basal ganglia disorders. Mol Neurobiol 2007;36:82-91. (Pubitemid 351360353)
12. van der Stelt M, Mazzola C, Esposito G, Matias I, Petrosino S, De Filippis D. Micale V, Steardo L, Drago F, Iuvone T, Di Marzo V: Endocannabinoids and betaamyloid- induced neurotoxicity in vivo: effect of pharmacological elevation of endocannabinoid levels. Cell Mol Life Sci 2006;63:1410-1424. (Pubitemid 43939021)
13. Frick A, Magee J, Johnston D: LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 2004;7:126-135. (Pubitemid 38129788)
14. Yun SH, Gamkrelidze G, Stine WB, Sullivan PM, Pasternak JF, Ladu MJ, Trommer BL: Amyloid-beta1-42 reduces neuronal excitability in mouse dentate gyrus. Neurosci Lett 2006;403:162-165. (Pubitemid 43977795)
15. Minkeviciene R, Rheims S, Dobszay MB, Zilberter M, Hartikainen J, Fulop L, Penke B, Zilberter Y, Harkany T, Pitkanen A, Tanila H: Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J Neurosci 2009;9:3453-3462.
16. Chen QS, Wei WZ, Shimahara T, Xie CW: Alzheimer amyloid beta-peptide inhibits the late phase of long-term potentiation through calcineurindependent mechanisms in the hippocampal dentate gyrus. Neurobiol Learn Mem 2002;77:354-371. (Pubitemid 34971647)
17. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L: Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007;55:697-711. (Pubitemid 47321079)
18. Palop JJ, Mucke L: Synaptic depression and aberrant excitatory network activity in Alzheimer's disease: two faces of the same coin? Neuromolecular Med 2010;12:48-55.
19. Walsh DM, Selkoe DJ: A beta oligomers - a decade of discovery. J Neurochem 2007;101:1172-1184.
20. Orban G, Volgyi K, Juhasz G, Penke B, Kekesi KA, Kardos J, Czurko A: Different electrophysiological actions of 24- and 72-hour aggregated amyloid-beta oligomers on hippocampal field population spike in both anesthetized and awake rats. Brain Res 2010;1354:227-235.
21. Shen M. Thayer SA: Cannabinoid receptor agonists protect cultured rat hippocampal neurons from excitotoxicity. Mol Pharmacol 1998;54:459-462. (Pubitemid 28442938)
22. 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. (Pubitemid 34026608)
23. Chemin J, Monteil A, Perez-Reyes E, Nargeot J, Lory P: Direct inhibition of T-type calcium channels by the endogenous cannabinoid anandamide. EMBO J 2001;20:7033-7040. (Pubitemid 34062295)
24. Gerdeman G, Lovinger DM: CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 2001;85:468-471. (Pubitemid 32062158)
25. Sade H, Muraki K, Ohya S, Hatano N, Imaizumi Y: Activation of largeconductance, Ca2+-activated K+ channels by cannabinoids. Am J Physiol Cell Physiol 2006;290:C77-86.
26. Shabani M, Hosseinmardi N, Haghani M, Shaibani V, Janahmadi M: Maternal exposure to the CB1 cannabinoid agonist WIN 55212-2 produces robust changes in motor function and intrinsic electrophysiological properties of cerebellar Purkinje neurons in rat offspring. Neurosci 2011;172:139-152.
27. Kowall NW, Beal MF, Busciglio J, Duffy LK, Yankner BA: An in vivo model for the neurodegenerative effects of beta amyloid and protection by substance P. Proc Natl Acad Sci U S A 1991;88:7247-7251. (Pubitemid 21915127)
28. Esposito G, Iuvone T, Savani C, Scuderi C, De Filippis D, Papa M, Di Marzo V, Steardo L: Opposing control of cannabinoid receptor stimulation on amyloid-beta-induced reactive gliosis: in vitro and in vivo evidence. J Pharmacol Exp Ther 2007;322:1144-1152. (Pubitemid 47295817)
29. Abdi A, Sadraie H, Dargahi L, Khalaj L, Ahmadiani A: Apoptosis inhibition can be threatening in A-induced neuroinflammation, through promoting cell proliferation.Neurochem Res 2011;36:39-48.
30. Nakamura S, Murayama N, Noshita T, Katsuragi R, Ohno T: Cognitive dysfunction induced by sequential injection of amyloid-beta and ibotenate into the bilateral hippocampus; protection by memantine and MK-801. Eur J Pharmacol 2006;548:115-22. (Pubitemid 44404130)
31. Stone TW: Neuropharmacology of quinolinic and kynurenic acids. Pharmacol Rev 1993;45:309-379. (Pubitemid 23292874)
32. Yoon KW, Covey DF, Rothman SM: Multiple mechanisms of picrotoxin block of GABA-induced currents in rat hippocampal neurons. J Physiol 1993;464:423-439. (Pubitemid 23169324)
33. Goldman-Rakic: Architecture of the prefrontal cortex and the central executive. Ann N Y Acad Sci 1995;769:71-83.
34. Shimamura AF: Memory and the prefrontal cortex. Ann N Y Acad Sci 1995;769:151-159.
35. Granon S, Poucet B: Involvement of the rat prefrontal cortex in cognitive functions: a central role for the prelimbic area. Psychobiology 2000;28:229-237. (Pubitemid 30480478)
36. Granon S, Vidal C, Thinus-Blanc C, Changeux JP, Poucet B: Working memory, response selection, and effortful processing in rats with medial prefrontal lesions. Behav Neurosci 1994;108:883-891. (Pubitemid 24322259)
37. Petrides M: Frontal lobes and behaviour. Curr Opin Neurobiol 1994;4:207-211. (Pubitemid 24126284)
38. Bilkey DK, Liu P: The effects of separate and combined perirhinal and prefrontal cortex lesions on spatial memory tasks in rats. Psychobiology 2000;28:12-20. (Pubitemid 30230898)
39. Swanson LW: A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res 1981;217:150-154. (Pubitemid 11072711)
40. Thierry AM, Gioanni Y, Degenetais E, Glowinski J: Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 2000;10:411-419.
41. Saint Marie RL, Miller EJ, Breier MR, Weber M, Swerdlow NR: Projections from ventral hippocampus to medial prefrontal cortex but not nucleus accumbens remain functional after fornix lesions in rats. Neuroscience 2010;168:498-504.
42. Gonzalo-Ruiz A, Sanz JM, Arevalo J, Geula C, Gonzalo P: Amyloid beta peptide-induced cholinergic fibres loss in the cerebral cortex of the rat is modified by diet high in lipids and by age. J Chem Neuroanat 2005;29:31-48. (Pubitemid 39602786)
43. Gonzalo-Ruiz A, Perez JL, Sanz JM, Geula C, Arevalo J: Effects of lipids and aging on the neurotoxicity and neuronal loss caused by intracerebral injections of the amyloid-beta peptide in the rat. Exp Neurol 2006;197:41-55. (Pubitemid 41817220)
44. Lue LF, Kuo YM, Roher AE, Brachova , Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J: Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 1999;155:853-862. (Pubitemid 29426831)
45. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ: Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002;416:535-539. (Pubitemid 34288854)
46. Rowan MJ, Klyubin I, Wang Q, Anwyl R: Synaptic plasticity disruption by amyloid beta protein: modulation by potential Alzheimer's disease modifying therapies. Biochem Soc Trans 2005;33:563-567. (Pubitemid 41160810)
47. Yamada K, Tanaka T, Mamiya T, Shiotani T, Kameyama T, Nabeshima T: Improvement by nefiracetam of betaamyloid-(1-42)-induced learning and memory impairments in rats. Br J Pharmacol 1999;126:235-244. (Pubitemid 29041763)
48. Grady CL, Furey ML, Pietrini P, Horwitz B, Rapoport SI: Altered brain functional connectivity and impaired short-term memory in Alzheimer's disease. Brain 2001;124:739-756. (Pubitemid 32303833)
49. Wei H, Xiong W, Yang S, Zhou Q, Liang C, Zeng BX, Xu L: Propofol facilitates the development of long-term depression (LTD) and impairs the maintenance of long-term potentiation (LTP) in the CA1 region of the hippocampus of anesthetized rats. Neurosci Lett 2001;324:181-184. (Pubitemid 34493864)
50. Chiang HC, Wang L, Xie Z, Yau A, Zhong Y: PI3 kinase signaling is involved in Abeta-induced memory loss in Drosophila. Proc Natl Acad Sci USA 2010;107:7060-7065.
51. Marin N, Romero B, Bosch-Morell F, Llansola M, Felipo V, Roma J, Romero FJ: Beta-amyloid-induced activation of caspase-3 in primary cultures of rat neurons. Mech Ageing Dev 2000;119:63-67.
52. Takuma H, Tomiyama T, Kuida K, Mori H: Amyloid beta peptide-induced cerebral neuronal loss is mediated by caspase-3 in vivo. J Neuropathol Exp Neurol 2004;63:255-261. (Pubitemid 38327945)
53. Lastres-Becker I, Molina-Holgado F, Ramos JA, Mechoulam R, Fernandez- Ruiz J: Cannabinoids provide neuroprotection against 6- hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson's disease. Neurobiol Dis 2005;19:96-107. (Pubitemid 40544727)
54. Fernandez-Ruiz J, Romero J, Velasco G, Tolon RM, Ramos JA, Guzman M: Cannabinoid CB2 receptor: a new target for controlling neural cell survival? Trends Pharmacol Sci 2007;28:39-45. (Pubitemid 46038536)
55. Martinez-Orgado J, Fernandez-Lopez D, Lizasoain I, Romero J: The seek of neuroprotection: introducing cannabinoids. Recent Pat CNS Drug Discov 2007;2:131-139. (Pubitemid 46952450)
56. Jackson SJ, Pryce G, Diemel LT, Cuzner ML, Baker D: Cannabinoid-receptor 1 null mice are susceptible to neurofilament damage and caspase 3 activation. Neurosci 2005;134:261-268. (Pubitemid 40943652)
57. Harkany T, Abraham I, Timmerman W, Laskay G, Toth B, Sasvari M, Konya C, Sebens JB, Korf J, Nyakas C, Zarandi M, Soos K, Penke B, Luiten PG: Betaamyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis Eur J Neurosci 2000;12:2735-2745.
58. Brecht S, Gelderblom M, Srinivasan A, Mielke K, Dityateva G, Herdegen T: Caspase-3 activation and DNA fragmentation in primary hippocampal neurons following glutamate excitotoxicity. Brain Res Mol Brain Res 2001;94:25-34. (Pubitemid 32964743)
59. Shen M, Piser TM, Seybold VS, Thayer SA: Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 1996;16:4322-4334. (Pubitemid 26243028)
60. Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, Garcia-Alloza M, Micheva KD, Smith SJ, Kim ML, Lee VM, Hyman BT, Spires- Jones TL: Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci U S A 2009;106:4012-4017.
61. Bayer TA, Wirths O: Intracellular accumulation of amyloid-Beta - a predictor for synaptic dysfunction and neuron loss in Alzheimer's disease. Front Aging Neurosci 2010;2:8.
62. Palop JJ, Mucke L: Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 2010;13:812-818.
63. Tong L, Balazs R, Thornton PL, Cotman CW: Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J Neurosci 2004;24:6799-6809. (Pubitemid 38993902)
64. Rowan MJ, Klyubin I, Cullen WK, Anwyl R: Synaptic plasticity in animal models of early Alzheimer's disease. Philos Trans R Soc Lond B Biol Sci 2003;358:821-828. (Pubitemid 36536714)
65. Funk GD, Parkis MA, Selvaratnam SR, Robinson DM, Miles GB, Peebles KC: Synaptic control of motoneuron excitability in rodents: from months to milliseconds. Clin Exp Pharmacol Physiol 2000;27:120-125. (Pubitemid 30104102)
66. Antri M, Fenelon K, Dubuc R: The contribution of synaptic inputs to sustained depolarizations in reticulospinal neurons. J Neurosci 2009;29:1140-1151.
67. Schulz DJ, Baines RA, Hempel CM, Li L, Liss B, Misonou H: Cellular excitability and the regulation of functional neuronal identity: from gene expression to neuromodulation. J Neurosci 2006;26:10362-10367. (Pubitemid 44564584)
68. Wang Y, Zhang G, Zhou H, Barakat A, Querfurth H: Opposite effects of low and high doses of Abeta42 on electrical network and neuronal excitability in the rat prefrontal cortex. PLoS One 2009;4:e8366.
69. Zou X, Coyle D, Wong-Lin K, Maguire L: Computational study of hippocampalseptal theta rhythm changes due to Betaamyloid- altered ionic channels. PLoS One 2011;6:e21579.
70. Sanchez-Vives MV, Nowak LG, McCormick DA: Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro. J Neurosci 2000;20:4286-4299. (Pubitemid 30365699)
71. Seroussi Y, Brosh I, Barkai E: Learninginduced reduction in post-burst afterhyperpolarization (AHP) is mediated by activation of PKC. Eur J Neurosci 2002;16:965-969. (Pubitemid 35463588)
72. Cohen AS, Coussens CM, Raymond CR, Abraham WC: Longlasting increase in cellular excitability associated with thepriming of LTP induction in rat hippocampus. J Neurophysiol 1999;82,3139-3148. (Pubitemid 30017440)
73. Disterhoft JF, Oh MM: Alterations in intrinsic neuronal excitability during normal aging. Aging Cell 2007;6:327-336. (Pubitemid 46785138)
74. Storm JF: Action potential repolarization and a fast afterhyperpolarization in rat hippocampal pyramidal cells. J Physiol 1987;385:733-759. (Pubitemid 17048959)
75. Shao LR., Halvorsrud R, Borg-Graham L, Storm JF: The role of BK type Ca2+ dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J Physiol 1999;521:135-146.
76. Lockridge A, Yuan LL: Spatial learning deficits in mice lacking A-type K+ channel subunits. Hippocampus 2011;21:1152-1156.
77. Kim J, Wei DS, Hoffman DA: Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 2005;569:41-57. (Pubitemid 41701375)
78. Storm JF: Potassium currents in hippocampal pyramidal cells. Prog Brain Res 1990;83:161-187. (Pubitemid 20205278)
79. Byrne JH, Shapiro E, Dieringer N, Koester J: Biophysical mechanisms contributing to inking behavior in Aplysia. J Neurophysiol 1979;42:1233-1250. (Pubitemid 10229762)
80. Bekkers JM, Delaney AJ: Modulation of excitability by -dendrotoxin-sensitive potassium channels in neocortical pyramidal neurons. J Neurosci 2001;21:6553-6560. (Pubitemid 32781099)
81. Plant LD, Webster NJ, Boyle JP, Ramsden M, Freir DB, Peers C, Pearson HA: Amyloid beta peptide as a physiological modulator of neuronal 'A'-type K+ current. Neurobiol Aging 2006;27:1673-1683. (Pubitemid 44344847)
82. Ramsden M, Plant LD, Webster NJ, Vaughan PF, Henderson Z, Pearson HA: Differential effects of unaggregated and aggregated amyloid beta protein (1-40) on K+ channel currents in primary cultures of rat cerebellar granule and cortical neurones. J Neurochem 2001;79:699-712. (Pubitemid 33029943)
83. Wacnik PW, Luhr KM, Hill RH, Ljunggren HG, Kristensson K, Svensson M: Cannabinoids affect dendritic cell (DC) potassium channel function and modulate DC T cell stimulatory capacity. J Immunol 2008;181:3057-3066.
84. Svensson M, Chen P, Hammarfjord O: Dendritic cell regulation by cannabinoidbased drugs. Pharmaceuticals 2010;3:2733-2750.
85. Smith IF, Green KN, LaFerla FM: Calcium dysregulation in Alzheimer's disease: recent advances gained from genetically modified animals. Cell Calcium 2005;38:427-437. (Pubitemid 41283281)
86. Kawahara M, Arispe N, Kuroda Y, Rojas E: Alzheimer's disease amyloid beta-protein forms Zn2+-sensitive, cation-selective channels across excised membrane patches from hypothalamic neurons. Biophys J 1997;73:67-75. (Pubitemid 27274105)
87. Davidson RM, Shajenko L, Donta TS: Amyloid beta-peptide (A beta P) potentiates a nimodipine-sensitive Ltype barium conductance in N1E-115 neuroblastoma cells. Brain Res 1994;643:324-327.
88. Kasparova J, Lisa V, Tucek S, Dolezal V: Chronic exposure of NG108-15 cells to amyloid beta peptide (A beta (1-42)) abolishes calcium influx via N-type calcium channels. Neurochem Res 2001;26:1079-1084. (Pubitemid 33021433)
89. Furukawa K, Barger SW, Blalock EM, Mattson MP: Activation of K+ channels and suppression of neuronal activity bysecreted beta-amyloid-precursor protein. Nature 1996;379:74-78. (Pubitemid 26008138)
90. Pan X, Ikeda SR, Lewis DL: Rat brain cannabinoid receptor modulates N-type Ca2+ channels in a neuronal expression system. Mol Pharmacol 1996;49:707-714.
91. Twitchell W, Brown S, Mackie K: Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 1997;78:43-50. (Pubitemid 27318909)
92. Guo J, Ikeda SR: Endocannabinoids modulate N-type calcium channels and G-protein-coupled inwardly rectifying potassium channels via CB1 cannabinoid receptors heterologously expressed in mammalian neurons. Mol Pharmacol 2004;65:665-674. (Pubitemid 38264034)