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

Volumn 24, Issue 2, 2014, Pages 178-188

  Basavarajappa, Balapal S ^a,b   Subbanna, Shivakumar ^a  

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

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

CaMKIV; Cannabinoids; CB1 receptor null mice; LTP; MAPK, CREB; Phosphorylation

Indexed keywords

( 4 METHOXY 1 NAPHTHALENYL)( 1 PENTYL 1H INDOL 3 YL)METHANONE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; JWH 081; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RIMONABANT; UNCLASSIFIED DRUG;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; DRUG MEGADOSE; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECOGNITION; SIGNAL TRANSDUCTION; SPATIAL MEMORY; SPICE; SYNAPSE; TASK PERFORMANCE; WILD TYPE;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; CANNABINOID RECEPTOR ANTAGONISTS; CANNABINOIDS; CREB-BINDING PROTEIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; INDOLES; LEARNING DISORDERS; LONG-TERM POTENTIATION; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NAPHTHALENES; PHOSPHORYLATION; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION; SPACE PERCEPTION; SYNAPSES;

EID: 84892678351     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22213     Document Type: Article

References (74)

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. Aung MM, Griffin G, Huffman JW, Wu M, Keel C, Yang B, Showalter VM, Abood ME, Martin BR. 2000. Influence of the N-1 alkyl chain length of cannabimimetic indoles upon CB(1) and CB(2) receptor binding. Drug Alcohol Depend 60:133-140.
3. Auwarter V, Dresen S, Weinmann W, Muller M, Putz M, Ferreiros N. 2009. 'Spice' and other herbal blends: harmless incense or cannabinoid designer drugs? J Mass Spectrom 44:832-837.
4. Avdesh A, Hoe Y, Martins RN, Martin-Iverson MT. 2013. Pharmacological effects of cannabinoids on the reference and working memory functions in mice. Psychopharmacology (Berl) 225:483-494.
5. Basavarajappa BS, Ninan I, Arancio O. 2008. Acute ethanol suppresses glutamatergic neurotransmission through endocannabinoids in hippocampal neurons. J Neurochem 107:1001-1013.
6. 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.
7. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, Monory K, Marsicano G, Matteoli M, Canty A and others. 2007. Hardwiring the brain: Endocannabinoids shape neuronal connectivity. Science 316:1212-1216.
8. Bito H, Deisseroth K, Tsien RW. 1996. CREB phosphorylation and dephosphorylation: A Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
9. 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.
10. 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 312:637-6641.
11. Brents LK, Reichard EE, Zimmerman SM, Moran JH, Fantegrossi WE, Prather PL. 2011. Phase I hydroxylated metabolites of the K2 synthetic cannabinoid JWH-018 retain in vitro and in vivo cannabinoid 1 receptor affinity and activity. PLoS One 6:e21917.
12. Chin CN, Murphy JW, Huffman JW, Kendall DA. 1999. The third transmembrane helix of the cannabinoid receptor plays a role in the selectivity of aminoalkylindoles for CB2, peripheral cannabinoid receptor. J Pharmacol Exp Ther 291:837-844.
13. Collins DR, Pertwee RG, Davies SN. 1994. The action of synthetic cannabinoids on the induction of long-term potentiation in the rat hippocampal slice. Eur J Pharmacol 259:R7-R8.
14. 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.
15. 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 USA 95:8375-8380.
16. Deadwyler SA, Hampson RE, Mu J, Whyte A, Childers S. 1995. Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J Pharmacol Exp Ther 273:734-743.
17. 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.
18. Egashira N, Mishima K, Iwasaki K, Fujiwara M. 2002. Intracerebral microinjections of delta 9-tetrahydrocannabinol: search for the impairment of spatial memory in the eight-arm radial maze in rats. Brain Res 952:239-245.
19. 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.
20. 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.
21. Government US. 2012. Synthetic Drug Abuse Prevention Act. In: 112th congress, Washington D.C: United State Government printing office. pp 138-139.
22. Grabowski PJ. 2005. Splicing-active nuclear extracts from rat brain. Methods 37:323-330.
23. Hampson RE, Deadwyler SA. 1999. Cannabinoids, hippocampal function and memory. Life Sci 65:715-723.
24. Herkenham M, Lynn AB, de Costa BR, Richfield EK. 1991. Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res. 547:267-274.
25. Hermanns-Clausen M, Kneisel S, Szabo B, Auwarter V. 2013. Acute toxicity due to the confirmed consumption of synthetic cannabinoids: Clinical and laboratory findings. Addiction 108:534-544.
26. Hillard CJ, Manna S, Greenberg MJ, DiCamelli R, Ross RA, Stevenson LA, Murphy V, Pertwee RG, Campbell WB. 1999. Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). J Pharmacol Exp Ther 289:1427-1433.
27. Hoffman AF, Macgill AM, Smith D, Oz M, Lupica CR. 2005. Species and strain differences in the expression of a novel glutamate-modulating cannabinoid receptor in the rodent hippocampus. Eur J Neurosci 22:2387-2391.
28. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D and others. 1998. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4:97-100.
29. Huffman JW, Dong D, Martin BR, Compton DR. 1994. Design, synthesis and pharmacology of cannabimimetic indoles. Bioorg Med Chem Lett 4:563-566.
30. Huffman JW, Thompson AL, Wiley JL, Martin BR. 2008. Synthesis and pharmacology of 1-deoxy analogs of CP-47, 497 and CP-55, 940. Bioorg Med Chem 16:322-335.
31. Huffman JW, Zengin G, Wu MJ, Lu J, Hynd G, Bushell K, Thompson AL, Bushell S, Tartal C, Hurst DP and others. 2005. Structure-activity relationships for 1-alkyl-3-(1-naphthoyl)indoles at the cannabinoid CB(1) and CB(2) receptors: Steric and electronic effects of naphthoyl substituents. New highly selective CB(2) receptor agonists. Bioorg Med Chem 13:89-112.
32. Kellogg R, Mackie K, Straiker A. 2009. Cannabinoid CB1 receptor-dependent long-term depression in autaptic excitatory neurons. J Neurophysiol 102:1160-1171.
33. Kesner RP, Rogers J. 2004. An analysis of independence and interactions of brain substrates that subserve multiple attributes, memory systems, and underlying processes. Neurobiol Learn Mem 82:199-215.
34. Kosiorek P, Hryniewicz A, Bialuk I, Zawadzka A, Winnicka MM. 2003. Cannabinoids alter recognition memory in rats. Pol J Pharmacol 55:903-910.
35. Lalonde R. 2002. The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26:91-104.
36. Lichtman AH, Dimen KR, Martin BR. 1995. Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology (Berl) 119:282-290.
37. Lichtman AH, Martin BR. 1996. Delta 9-tetrahydrocannabinol impairs spatial memory through a cannabinoid receptor mechanism. Psychopharmacology (Berl) 126:125-131.
38. Lubin FD, Sweatt JD. 2007. The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 55:942-957.
39. Mackie K, Hille B. 1992. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci USA 89:3825-3829.
40. Mackie K, Lai Y, Westenbroek R, Mitchell R. 1995. Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 15:6552.
41. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
42. Maurer HH, Sauer C, Theobald DS. 2006. Toxicokinetics of drugs of abuse: Current knowledge of the isoenzymes involved in the human metabolism of tetrahydrocannabinol, cocaine, heroin, morphine, and codeine. Ther Drug Monit 28:447-453.
43. 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.
44. Ohno-Shosaku T, Maejima T, Kano M. 2001. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminal. Neuron 29:729-738.
45. Pacher P, Batkai S, Kunos G. 2006. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58:389-462.
46. Pertwee RG. 2005. Pharmacological actions of cannabinoids. Handb Exp Pharmacol:1-51.
47. Puighermanal E, Busquets-Garcia A, Maldonado R, Ozaita A. 2012. Cellular and intracellular mechanisms involved in the cognitive impairment of cannabinoids. Philos Trans R Soc Lond B Biol Sci 367:3254-3263.
48. Ranganathan M, D'Souza DC. 2006. The acute effects of cannabinoids on memory in humans: A review. Psychopharmacology (Berl) 188:425-444.
49. Razdan RK, Vemuri VK, Makriyannis A, Huffman JW. 2009. Cannabimimetic indoles, pyrroles, and indenes: structure-activity relationships and receptor interactions. In: Reggio PH, editor. Cannabinoid Receptor Ligands and Structure-Activity Relationships. Part I. Totowa: Humana Press. pp 3-94.
50. 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.
51. Robson P. 2001. Therapeutic aspects of cannabis and cannabinoids. Br J Psychiatry 178:107-115.
52. Rubino T, Parolaro D. 2008. Long lasting consequences of cannabis exposure in adolescence. Mol Cell Endocrinol 286:S108-S113.
53. 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.
54. 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.
55. 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 USA 97:14731-14736.
56. Seely KA, Brents LK, Radominska-Pandya A, Endres GW, Keyes GS, Moran JH, Prather PL. 2012. A major glucuronidated metabolite of JWH-018 is a neutral antagonist at CB1 receptors. Chem Res Toxicol 25:825-827.
57. Shen M, Piser TM, Seybold VS, Thayer SA. 1996. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 16:4322-4334.
58. 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.
59. Slanina KA, Roberto M, Schweitzer P. 2005. Endocannabinoids restrict hippocampal long-term potentiation via CB1. Neuropharmacology 49:660-668.
60. 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.
61. Suenaga T, Ichitani Y. 2008. Effects of hippocampal administration of a cannabinoid receptor agonist WIN 55, 212-2 on spontaneous object and place recognition in rats. Behav Brain Res 190:248-522.
62. Taura F, Sirikantaramas S, Shoyama Y, Morimoto S. 2007. Phytocannabinoids in Cannabis sativa: Recent studies on biosynthetic enzymes. Chem Biodivers 4:1649-1663.
63. 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.
64. 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 (Berl) 126:165-172.
65. Vardakou I, Pistos C, Spiliopoulou C. 2010. Spice drugs as a new trend: mode of action, identification and legislation. Toxicol Lett 197:157-162.
66. Varvel SA, Anum EA, Lichtman AH. 2005. Disruption of CB(1) receptor signaling impairs extinction of spatial memory in mice. Psychopharmacology (Berl) 179:863-872.
67. Varvel SA, Hamm RJ, Martin BR, Lichtman AH. 2001. Differential effects of delta 9-THC on spatial reference and working memory in mice. Psychopharmacology (Berl) 157:142-150.
68. 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 USA 99:13217-13221.
69. Wiebelhaus JM, Poklis JL, Poklis A, Vann RE, Lichtman AH, Wise LE. 2012. Inhalation exposure to smoke from synthetic "marijuana" produces potent cannabimimetic effects in mice. Drug Alcohol Depend 126:316-323.
70. Wilson RI, Nicoll RA. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
71. Wohlfarth A, Scheidweiler KB, Chen X, Liu HF, Huestis MA. 2013. Qualitative confirmation of 9 synthetic cannabinoids and 20 metabolites in human urine using LC-MS/MS and library search. Anal Chem 85:3730-3738.
72. Yim TT, Hong NS, Ejaredar M, McKenna JE, McDonald RJ. 2008. Post-training CB1 cannabinoid receptor agonist activation disrupts long-term consolidation of spatial memories in the hippocampus. Neuroscience 151:929-936.
73. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, Watanabe M. 2006. Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26:4740-4751.
74. Young AC, Schwarz E, Medina G, Obafemi A, Feng SY, Kane C, Kleinschmidt K. 2012. Cardiotoxicity associated with the synthetic cannabinoid, K9, with laboratory confirmation. Am J Emerg Med 30:e5-e7.