Elevation of endogenous anandamide impairs LTP, learning, and memory through CB1 receptor signaling in mice

Hippocampus

Volumn 24, Issue 7, 2014, Pages 808-818

  Basavarajappa, Balapal S ^a,b,c   Nagre, Nagaraja N ^a   Xie, Shan ^a   Subbanna, Shivakumar ^a  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c Department of Psychiatry College of Physicians and Surgeons Columbia University ^*  (United States)

Author keywords

Anandamide; CaMKIV phosphorylation; CB1 null mice; CREB; Fatty acid amide hydrolase; Long term potentiation; Mitogen activated protein kinase; URB597

Indexed keywords

2 ARACHIDONYL GLYCEROL; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; GLYCEROL DERIVATIVE; UNCLASSIFIED DRUG; 2-ARACHIDONYLGLYCEROL; ACYLGLYCEROL; AMIDASE; AMIDE; ARACHIDONIC ACID DERIVATIVE; BENZAMIDE DERIVATIVE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CARBAMIC ACID DERIVATIVE; CNR1 PROTEIN, RAT; CREB1 PROTEIN, MOUSE; CYCLOHEXYL CARBAMIC ACID 3'-CARBAMOYLBIPHENYL-3-YL ESTER; ENDOCANNABINOID; FATTY-ACID AMIDE HYDROLASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHORESIS; EVOKED RESPONSE; HIPPOCAMPUS; IMMUNOBLOTTING; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; MASS FRAGMENTOGRAPHY; MEMORY DISORDER; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SPATIAL MEMORY; TASK PERFORMANCE; WESTERN BLOTTING; Y-MAZE TEST; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DEFICIENCY; GENETICS; KNOCKOUT MOUSE; LEARNING; MAZE TEST; MEMORY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; BENZAMIDES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; CARBAMATES; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENDOCANNABINOIDS; GLYCERIDES; LEARNING; LONG-TERM POTENTIATION; MALE; MAP KINASE SIGNALING SYSTEM; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; POLYUNSATURATED ALKAMIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR, CANNABINOID, CB1; SPATIAL MEMORY;

EID: 84902535947     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22272     Document Type: Article

References (84)

1. Atwood BK, Huffman J, Straiker A, Mackie K. 2010. JWH018, a common constituent of 'Spice' herbal blends, is a potent and efficacious cannabinoid CB receptor agonist. Br J Pharmacol 160:585-593.
2. Barros DM, Carlis V, Maidana M, Silva ES, Baisch AL, Ramirez MR, Izquierdo I. 2004. Interactions between anandamide-induced anterograde amnesia and post-training memory modulatory systems. Brain Res 1016:66-71.
3. Basavarajappa BS, Arancio O. 2008. Synaptic plasticity: Emerging role for endocannabinoid system.In: Kaiser TF, Peters FJ, editors. Synaptic Plasticity: New Research. NY, USA: Nova Science. pp 77-112.
4. 35S] GTPgS binding in synaptic plasma membrane from chronic ethanol exposed mouse. Brain Res 815:89-97.
5. Basavarajappa BS, Subbanna S. 2014. CB1 Receptor-mediated signaling underlies the hippocampal synaptic, learning and memory deficits following treatment with JWH-081, a new component of spice/K2 preparations. Hippocampus 24:178-188.
6. Basavarajappa BS, Cooper TB, Hungund BL. 1998. Chronic ethanol administration down-regulates cannabinoid receptors in mouse brain synaptic plasma membrane. Brain Res 793:212-218.
7. Basavarajappa BS, Saito M, Cooper TB, Hungund BL. 2003. Chronic ethanol inhibits the anandamide transport and increases extracellular anandamide levels in cerebellar granule neurons. Eur J Pharmacol 466:73-83.
8. Basavarajappa BS, Yalamanchili R, Cravatt BF, Cooper TB, Hungund BL. 2006. Increased ethanol consumption and preference and decreased ethanol sensitivity in female FAAH knockout mice. Neuropharmacology 50:834-844.
9. Basavarajappa BS, Ninan I, Arancio O. 2008. Acute ethanol suppresses glutamatergic neurotransmission through endocannabinoids in hippocampal neurons. J Neurochem 107:1001-1013.
10. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, Monory K, Marsicano G, Matteoli M, Canty A, Irving, A. J. Katona I, Yanagawa Y, Rakic P, Lutz B, Mackie K, Harkany T. 2007. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316:1212-1216.
11. Bito H, Deisseroth K, Tsien RW. 1996. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-14.
12. Bohme GA, Laville M, Ledent C, Parmentier M, Imperato A. 2000. Enhanced long-term potentiation in mice lacking cannabinoid CB1 receptors. Neuroscience 95:5-7.
13. Bouaboula M, Poinot-Chazel C, Bourrie B, Canat X, Calandra B, Rinaldi-Carmona M, Le Fur G, Casellas P. 1995. Activation of mitogen-activated protein kinases by stimulation of the central cannabinoid receptor CB1. Biochem J 312(Pt 2):637-641.
14. Brodkin J, Moerschbaecher JM. 1997. SR141716A antagonizes the disruptive effects of cannabinoid ligands on learning in rats. J Pharmacol Exp Ther. 282:1526-1532.
15. Busquets-Garcia A, Puighermanal E, Pastor A, de la Torre R, Maldonado R, Ozaita A. 2011. Differential role of anandamide and 2-arachidonoylglycerol in memory and anxiety-like responses. Biol Psychiatry 70:479-486.
16. Caiati MD, Sivakumaran S, Lanore F, Mulle C, Richard E, Verrier D, Marsicano G, Miles R, Cherubini E. 2012. Developmental regulation of CB1-mediated spike-time dependent depression at immature mossy fiber-CA3 synapses. Sci Rep 2:285.
17. Castellano C, Cabib S, Palmisano A, Di Marzo V, Puglisi-Allegra S. 1997. The effects of anandamide on memory consolidation in mice involve both D1 and D2 dopamine receptors. Behav Pharmacol 8:707-712.
18. Chait LD, Pierri J. 1992. Effects of smoked marijuana on human performance.In: Murphy L, Bartke A, editors. A Critical Review, in Marijuana/Cannabinoids: Neurobiology and Neurophysiology. Boca Raton, FL: CRC Press. pp 387-423.
19. Chavez AE, Chiu CQ, Castillo PE. 2010. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat Neurosci 13:1511-1518.
20. Clarke JR, Rossato JI, Monteiro S, Bevilaqua LR, Izquierdo I, Cammarota M. 2008. Posttraining activation of CB1 cannabinoid receptors in the CA1 region of the dorsal hippocampus impairs object recognition long-term memory. Neurobiol Learn Mem 90:374-381.
21. Collins DR, Pertwee RG, Davies SN. 1995. Prevention by the cannabinoid antagonist, SR141716A, of cannabinoid-mediated blockade of long-term potentiation in the rat hippocampal slice. Br J Pharmacol 115:869-870.
22. Da S, Takahashi RN. 2002. SR 141716A prevents delta 9-tetrahydrocannabinol-induced spatial learning deficit in a Morris-type water maze in mice. Prog Neuropsychopharmacol Biol Psychiatry 26:321-325.
23. Daigle TL, Kearn CS, Mackie K. 2008. Rapid CB1 cannabinoid receptor desensitization defines the time course of ERK1/2 MAP kinase signaling. Neuropharmacology 54:36-44.
24. De Petrocellis L, Melck D, Palmisano A, Bisogno T, Laezza C, Bifulco M, Di Marzo V. 1998. The endogenous cannabinoid anandamide inhibits human breast cancer cell proliferation. Proc Natl Acad Sci U S A 95:8375-8380.
25. Dellu F, Mayo W, Cherkaoui J, Le Moal M, Simon H. 1992. A two-trial memory task with automated recording: Study in young and aged rats. Brain Res 588:132-139.
26. Dember WN, Fowler H. 1958. Spontaneous alternation behavior. Psychol Bull 55:412-428.
27. Derkinderen P, Valjent E, Toutant M, Corvol JC, Enslen H, Ledent C, Trzaskos J, Caboche J, Girault JA. 2003. Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J Neurosci 23:2371-2382.
28. Di Marzo V, De Petrocellis L. 2010. Endocannabinoids as regulators of transient receptor potential (TRP) channels: A further opportunity to develop new endocannabinoid-based therapeutic drugs. Curr Med Chem 17:1430-1449.
29. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, Piomelli D. 1994. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372:686-691.
30. Di Marzo V, Petrosino S. 2007. Endocannabinoids and the regulation of their levels in health and disease. Curr Opin Lipidol 18:129-140.
31. Egertova M, Elphick MR. 2000. Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422:159-171.
32. Ennaceur A, Delacour J. 1988. A new one-trial test for neurobiological studies of memory in rats. I. Behavioral data. Behav Brain Res 31:47-59.
33. Galve-Roperh I, Sanchez C, Cortes ML, Gomez del Pulgar T, Izquierdo M, Guzman M. 2000. Anti-tumoral action of cannabinoids: involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat Med 6:313-319.
34. Goonawardena AV, Sesay J, Sexton CA, Riedel G, Hampson RE. 2011. Pharmacological elevation of anandamide impairs short-term memory by altering the neurophysiology in the hippocampus. Neuropharmacology 61(5-6):1016-1025.
35. Grabowski PJ. 2005. Splicing-active nuclear extracts from rat brain. Methods 37:323-330.
36. Hampson RE, Deadwyler SA. 1999. Cannabinoids, hippocampal function and memory. Life Sci 65(6-7):715-723.
37. Hansen HS. 2010. Palmitoylethanolamide and other anandamide congeners. Proposed role in the diseased brain. Exp Neurol 224:48-55.
38. Heifets BD, Castillo PE. 2009. Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol 71:283-306.
39. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC. 1990. Cannabinoid receptor localization in brain. Proc Natl Acad Sci U S A 87:1932-1936.
40. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Cost BR, Rice KC. 1991. Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study. J Neurosci 16:8057-8066.
41. Heyser CJ, Hampson RE, Deadwyler SA. 1993. Effects of delta-9-tetrahydrocannabinol on delayed match to sample performance in rats: alterations in short-term memory associated with changes in task specific firing of hippocampal cells. J Pharmacol Exp Ther 264:294-307.
42. Ho WS, Barrett DA, Randall MD. 2008. 'Entourage' effects of N-palmitoylethanolamide and N-oleoylethanolamide on vasorelaxation to anandamide occur through TRPV1 receptors. Br J Pharmacol 155:837-846.
43. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders, S. Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K. 1998. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4:97-100.
44. Huestis MA, Gorelick DA, Heishman SJ, Preston KL, Nelson RA, Moolchan ET, Frank RA. 2001. Blockade of effects of smoked marijuana by the CB1-selective cannabinoid receptor antagonist SR141716. Arch Gen Psychiatry 58:322-328.
45. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M. 2009. Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309-380.
46. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A, Mor M, Tarzia G, La Rana G, Calignano A, Giustino A, Tattoli M, Palmery M, Cuomo V, Piomelli D. 2003. Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9:76-81.
47. Katona I, Urban GM, Wallace M, Ledent C, Jung KM, Piomelli D, Mackie K, Freund TF. 2006. Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26:5628-5637.
48. Kawahara H, Drew GM, Christie MJ, Vaughan CW. 2011. Inhibition of fatty acid amide hydrolase unmasks CB1 receptor and TRPV1 channel-mediated modulation of glutamatergic synaptic transmission in midbrain periaqueductal grey. Br J Pharmacol 163:1214-1222.
49. Kosiorek P, Hryniewicz A, Bialuk I, Zawadzka A, Winnicka MM. 2003. Cannabinoids alter recognition memory in rats. Pol J Pharmacol 55:903-910.
50. Lichtman AH. 2000. SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats. Eur J Pharmacol 404:175-179.
51. Lichtman AH, Martin BR. 1996. Delta 9-tetrahydrocannabinol impairs spatial memory through a cannabinoid receptor mechanism. Psychopharmacology (Berlin) 126:125-131.
52. Lichtman AH, Dimen KR, Martin BR. 1995. Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology (Berlin) 119:282-290.
53. Logothetis NK, Sheinberg DL. 1996. Visual object recognition. Annu Rev Neurosci 19:577-621.
54. Mallet PE, Beninger RJ. 1998. The cannabinoid CB1 receptor antagonist SR141716A attenuates the memory impairment produced by delta9-tetrahydrocannabinol or anandamide. Psychopharmacology (Berlin) 140:11-19.
55. Marsch R, Foeller E, Rammes G, Bunck M, Kossl M, Holsboer F, Zieglgansberger W, Landgraf R, Lutz B, Wotjak CT. 2007. Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 27:832-839.
56. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
57. Mazzola C, Medalie J, Scherma M, Panlilio LV, Solinas M, Tanda G, Drago F, Cadet JL, Goldberg SR, Yasar S. 2009. Fatty acid amide hydrolase (FAAH) inhibition enhances memory acquisition through activation of PPAR-alpha nuclear receptors. Learn Mem 16:332-337.
58. Monory K, Blaudzun H, Massa F, Kaiser N, Lemberger T, Schutz G, Wotjak CT, Lutz B, Marsicano G. 2007. Genetic dissection of behavioural and autonomic effects of Delta(9)-tetrahydrocannabinol in mice. PLoS Biol 5:e269.
59. Murillo-Rodriguez E, Sanchez-Alavez M, Navarro L, Martinez-Gonzalez D, Drucker-Colin R, Prospero-Garcia O. 1998. Anandamide modulates sleep and memory in rats. Brain Res 812:270-274.
60. Ning Y, O'Neill K, Lan H, Pang L, Shan LX, Hawes BE, Hedrick JA. 2008. Endogenous and synthetic agonists of GPR119 differ in signalling pathways and their effects on insulin secretion in MIN6c4 insulinoma cells. Br J Pharmacol 155:1056-1065.
61. Nowicky AV, Teyler TJ, Vardaris RM. 1987. The modulation of long-term potentiation by delta-9-tetrahydrocannabinol in the rat hippocampus, in vitro. Brain Res Bull 19:663-672.
62. Nyiri G, Cserep C, Szabadits E, Mackie K, Freund TF. 2005. CB1 cannabinoid receptors are enriched in the perisynaptic annulus and on preterminal segments of hippocampal GABAergic axons. Neuroscience 136:811-822.
63. Paton GS, Pertwee RG, Davies SN. 1998. Correlation between cannabinoid mediated effects on paired pulse depression and induction of long term potentiation in the rat hippocampal slice. Neuropharmacology 37:1123-1130.
64. Piomelli D. 2003. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873-884.
65. Reibaud M, Obinu MC, Ledent C, Parmentier M, Bohme GA, Imperato A. 1999. Enhancement of memory in cannabinoid CB1 receptor knock-out mice. Eur J Pharmacol 379:R1-R2.
66. Robinson L, Goonawardena AV, Pertwee RG, Hampson RE, Riedel G. 2007. The synthetic cannabinoid HU210 induces spatial memory deficits and suppresses hippocampal firing rate in rats. Br J Pharmacol 151:688-700.
67. Rubino T, Parolaro D. 2008. Long lasting consequences of cannabis exposure in adolescence. Mol Cell Endocrinol 286(1-2 Suppl 1):S108-S113.
68. Rubino T, Sala M, Vigano D, Braida D, Castiglioni C, Limonta V, Guidali C, Realini N, Parolaro D. 2007. Cellular mechanisms underlying the anxiolytic effect of low doses of peripheral Delta9-tetrahydrocannabinol in rats. Neuropsychopharmacology 32:2036-2045.
69. Sadrian B, Subbanna S, Wilson DA, Basavarajappa BS, Saito M. 2012. Lithium prevents long-term neural and behavioral pathology induced by early alcohol exposure. Neuroscience 206:122-135.
70. Sarnyai Z, Sibille EL, Pavlides C, Fenster RJ, McEwen BS, Toth M. 2000. Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin(1A) receptors. Proc Natl Acad Sci U S A 97:14731-14736.
71. Seillier A, Advani T, Cassano T, Hensler JG, Giuffrida A. 2010. Inhibition of fatty-acid amide hydrolase and CB1 receptor antagonism differentially affect behavioural responses in normal and PCP-treated rats. Int J Neuropsychopharmacol 13:373-386.
72. Sik A, van Nieuwehuyzen P, Prickaerts J, Blokland A. 2003. Performance of different mouse strains in an object recognition task. Behav Brain Res 147:49-54.
73. Slanina KA, Roberto M, Schweitzer P. 2005. Endocannabinoids restrict hippocampal long-term potentiation via CB1. Neuropharmacology 49:660-668.
74. Stella N, Schweitzer P, Piomelli D. 1997. A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773-778.
75. Subbanna S, Shivakumar M, Psychoyos D, Xie S, Basavarajappa BS. 2013. Anandamide-CB1 receptor signaling contributes to postnatal ethanol-induced neonatal neurodegeneration, adult synaptic and memory deficits. J Neuosci 33:6350-6366.
76. Terranova JP, Michaud JC, Le Fur G, Soubrie P. 1995. Inhibition of long-term potentiation in rat hippocampal slices by anandamide and WIN55212-2: Reversal by SR141716 A, a selective antagonist of CB1 cannabinoid receptors. Naunyn Schmiedebergs Arch Pharmacol 352:576-579.
77. Terranova JP, Storme JJ, Lafon N, Perio A, Rinaldi-Carmona M, Le Fur G, Soubrie P. 1996. Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology (Berlin) 126:165-172.
78. Varvel SA, Lichtman AH. 2002. Evaluation of CB1 receptor knockout mice in the Morris water maze. J Pharmacol Exp Ther 301:915-924.
79. Varvel SA, Hamm RJ, Martin BR, Lichtman AH. 2001. Differential effects of delta 9-THC on spatial reference and working memory in mice. Psychopharmacology (Berlin) 157:142-150.
80. Varvel SA, Anum E, Niyuhire F, Wise LE, Lichtman AH. 2005. Delta(9)-THC-induced cognitive deficits in mice are reversed by the GABA(A) antagonist bicuculline. Psychopharmacology (Berlin) 178:317-327.
81. Varvel SA, Cravatt BF, Engram AE, Lichtman AH. 2006. Fatty acid amide hydrolase (-/-) mice exhibit an increased sensitivity to the disruptive effects of anandamide or oleamide in a working memory water maze task. J Pharmacol Exp Ther 317:251-257.
82. Vitolo O, Gong B, Cao Z, Ishii H, Jaracz S, Nakanishi K, Arancio O, Dzyuba SV, Lefort R, Shelanski M. 2009. Protection against beta-amyloid induced abnormal synaptic function and cell death by Ginkgolide J. Neurobiol Aging 30:257-265.
83. Vitolo OV, Sant'Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M. 2002. Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci U S A 99:13217-13221.
84. Wise LE, Cannavacciulo R, Cravatt BF, Martin BF, Lichtman AH. 2008. Evaluation of fatty acid amides in the carrageenan-induced paw edema model. Neuropharmacology 54:181-188.