Effects of the cannabinoid 1 receptor peptide ligands hemopressin, (m)RVD-hemopressin(α) and (m)VD-hemopressin(α) on memory in novel object and object location recognition tasks in normal young and Aβ1–42-treated mice

Neurobiology of Learning and Memory

Volumn 134, Issue , 2016, Pages 264-274

  Zhang, Rui san ^a,b   He, Zhen ^a   Jin, Wei dong ^a   Wang, Rui ^a  

^a LANZHOU UNIVERSITY   (China)

^b XI'AN MEDICAL UNIVERSITY   (China)

Author keywords

(m)RVD hemopressin( ); (m)VD hemopressin( ); Alzheimer's disease; Cannabinoid receptor; Hemopressin; Recognition memory

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; AMYLOID BETA PROTEIN[1-42]; CANNABINOID 1 RECEPTOR; NONAPEPTIDE; RVD HEMOPRESSIN; UNCLASSIFIED DRUG; VD HEMOPRESSIN ALPHA; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); BENZOXAZINE DERIVATIVE; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST; HEMOGLOBIN; HEMOPRESSIN; MORPHOLINE DERIVATIVE; NAPHTHALENE DERIVATIVE; OLIGOPEPTIDE; PEPTIDE FRAGMENT; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE; RVD-HEMOPRESSIN, HUMAN; VDPVNFKLLSH-OH;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; DRUG RESPONSE; LOCOMOTION; MALE; MEMORY; MEMORY ASSESSMENT; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NON-SPATIAL MEMORY TEST; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OBJECT LOCATION RECOGNITION TEST; TRAINING; AGONISTS; ALZHEIMER DISEASE; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; RECOGNITION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BEHAVIOR, ANIMAL; BENZOXAZINES; CANNABINOID RECEPTOR AGONISTS; CANNABINOID RECEPTOR ANTAGONISTS; DISEASE MODELS, ANIMAL; HEMOGLOBINS; INFUSIONS, INTRAVENTRICULAR; MALE; MEMORY DISORDERS; MICE; MORPHOLINES; NAPHTHALENES; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; RECOGNITION (PSYCHOLOGY);

EID: 84991094095     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2016.07.030     Document Type: Article

References (101)

1. Aoyama, K., Matsubara, K., Fujikawa, Y., Nagahiro, Y., Shimizu, K., Umegae, N.,. Kobayashi, S., Nitration of manganese superoxide dismutase in cerebrospinal fluids is a marker for peroxynitrite-mediated oxidative stress in neurodegenerative diseases. Annals of Neurology 47 (2000), 524–527.
2. Arain, M., Khan, M., Craig, L., Nakanishi, S.T., Cannabinoid agonist rescues learning and memory after a traumatic brain injury. Annals of Clinical and Translational Neurology 2 (2015), 289–294.
3. Arseneault, L., Cannon, M., Poulton, R., Murray, R., Caspi, A., Moffitt, T.E., Cannabis use in adolescence and risk for adult psychosis: Longitudinal prospective study. British Medical Journal 325 (2002), 1212–1213.
4. Ashton, J.C., Friberg, D., Darlington, C.L., Smith, P.F., Expression of the cannabinoid CB2 receptor in the rat cerebellum: An immunohistochemical study. Neuroscience Letters 396 (2006), 113–116.
5. Aso, E., Juves, S., Maldonado, R., Ferrer, I., CB2 cannabinoid receptor agonist ameliorates Alzheimer-like phenotype in AbetaPP/PS1 mice. Journal of Alzheimers Disease 35 (2013), 847–858.
6. Aso, E., Palomer, E., Juves, S., Maldonado, R., Munoz, F.J., Ferrer, I., CB1 agonist ACEA protects neurons and reduces the cognitive impairment of AbetaPP/PS1 mice. Journal of Alzheimers Disease 30 (2012), 439–459.
7. Basavarajappa, B.S., Nagre, N.N., Xie, S., Subbanna, S., Elevation of endogenous anandamide impairs LTP, learning, and memory through CB1 receptor signaling in mice. Hippocampus 24 (2014), 808–818.
8. Bilkei-Gorzo, A., Racz, I., Valverde, O., Otto, M., Michel, K., Sastre, M., Zimmer, A., Early age-related cognitive impairment in mice lacking cannabinoid CB1 receptors. Proceedings of the National Academy of Sciences 102 (2005), 15670–15675.
9. Block, R.I., Ghoneim, M.M., Effects of chronic marijuana use on human cognition. Psychopharmacology (Berl) 110 (1993), 219–228.
10. Bomar, M.G., Galande, A.K., Modulation of the cannabinoid receptors by hemopressin peptides. Life Sciences 92 (2013), 520–524.
11. Campolongo, P., Morena, M., Scaccianoce, S., Trezza, V., Chiarotti, F., Schelling, G.,. Roozendaal, B., Novelty-induced emotional arousal modulates cannabinoid effects on recognition memory and adrenocortical activity. Neuropsychopharmacology 38 (2013), 1276–1286.
12. Castellano, C., Rossi-Arnaud, C., Cestari, V., Costanzi, M., Cannabinoids and memory: Animal studies. Current Drug Targets: CNS & Neurological Disorders 2 (2003), 389–402.
13. Cervino, C., Vicennati, V., Pasquali, R., Pagotto, U., Feeding disorders and obesity. Current Topics in Behavioral Neurosciences 1 (2009), 373–385.
14. Chacon, M.A., Barria, M.I., Soto, C., Inestrosa, N.C., Beta-sheet breaker peptide prevents Abeta-induced spatial memory impairments with partial reduction of amyloid deposits. Molecular Psychiatry 9 (2004), 953–961.
15. Chaperon, F., Thiebot, M.H., Behavioral effects of cannabinoid agents in animals. Critical Reviews in Neurobiology 13 (1999), 243–281.
16. Collins, D.R., Pertwee, R.G., Davies, S.N., The action of synthetic cannabinoids on the induction of long-term potentiation in the rat hippocampal slice. European Journal of Pharmacology 259 (1994), R7–R8.
17. Cotman, C.W., Berchtold, N.C., Exercise: A behavioral intervention to enhance brain health and plasticity. Trends in Neurosciences 25 (2002), 295–301.
18. Creer, D.J., Romberg, C., Saksida, L.M., van Praag, H., Bussey, T.J., Running enhances spatial pattern separation in mice. Proceedings of the National Academy of Sciences 107 (2010), 2367–2372.
19. Cui, J., Wang, Y., Dong, Q., Wu, S., Xiao, X., Hu, J.,. Zhang, Y., Morphine protects against intracellular amyloid toxicity by inducing estradiol release and upregulation of Hsp70. Journal of Neuroscience 31 (2011), 16227–16240.
20. Da, S., Takahashi, R.N., SR 141716A prevents delta 9-tetrahydrocannabinol-induced spatial learning deficit in a Morris-type water maze in mice. Progress in Neuro-Psychopharmacology and Biological Psychiatry 26 (2002), 321–325.
21. Dale, C.S., Pagano, R.D.L., Rioli, V., Hyslop, S., Giorgi, R., Ferro, E.S., Antinociceptive action of hemopressin in experimental hyperalgesia. Peptides 26 (2005), 431–436.
22. Dao, A.T., Zagaar, M.A., Levine, A.T., Salim, S., Eriksen, J.L., Alkadhi, K.A., Treadmill exercise prevents learning and memory impairment in Alzheimer's disease-like pathology. Current Alzheimer Research 10 (2013), 507–515.
23. Dao, A.T., Zagaar, M.A., Salim, S., Eriksen, J.L., Alkadhi, K.A., Regular exercise prevents non-cognitive disturbances in a rat model of Alzheimer's disease. The International Journal of Neuropsychopharmacology 17 (2014), 593–602.
24. Darley, C.F., Tinklenberg, J.R., Roth, W.T., Atkinson, R.C., The nature of storage deficits and state-dependent retrieval under marihuana. Psychopharmacologia 37 (1974), 139–149.
25. Davies, S.N., Pertwee, R.G., Riedel, G., Functions of cannabinoid receptors in the hippocampus. Neuropharmacology 42 (2002), 993–1007.
26. Di Marzo, V., Petrosino, S., Endocannabinoids and the regulation of their levels in health and disease. Current Opinion in Lipidology 18 (2007), 129–140.
27. Dickson, D.W., Farlo, J., Davies, P., Crystal, H., Fuld, P., Yen, S.H., Alzheimer's disease. A double-labeling immunohistochemical study of senile plaques. American Journal of Pathology 132 (1988), 86–101.
28. Dief, Abeer E., Samy, Doaa M., Dowedar, Fatma I., Impact of exercise and vitamin b1 intake on hippocampal brain-derived neurotrophic factor and spatial memory performance in a rat model of stress. Journal of Nutritional Science and Vitaminology (Tokyo) 61 (2015), 1–7.
29. Dodd, G.T., Mancini, G., Lutz, B., Luckman, S.M., The peptide hemopressin acts through CB1 cannabinoid receptors to reduce food intake in rats and mice. Journal of Neuroscience 30 (2010), 7369–7376.
30. Elphick, M.R., Egertova, M., The neurobiology and evolution of cannabinoid signalling. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences 356 (2001), 381–408.
31. Erickson, K.I., Voss, M.W., Prakash, R.S., Basak, C., Szabo, A., Chaddock, L.,. Kramer, A.F., Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences 108 (2011), 3017–3022.
32. Ferrari, F., Ottani, A., Vivoli, R., Giuliani, D., Learning impairment produced in rats by the cannabinoid agonist HU 210 in a water-maze task. Pharmacology, Biochemistry and Behavior 64 (1999), 555–561.
33. Findeis, M.A., Peptide inhibitors of beta amyloid aggregation. Current Topics in Medicinal Chemistry 2 (2002), 417–423.
34. Giuliani, D., Ottani, A., Zaffe, D., Galantucci, M., Strinati, F., Lodi, R., Guarini, S., Hydrogen sulfide slows down progression of experimental Alzheimer's disease by targeting multiple pathophysiological mechanisms. Neurobiology of Learning and Memory 104 (2013), 82–91.
35. Gomes, I., Grushko, J.S., Golebiewska, U., Hoogendoorn, S., Gupta, A., Heimann, A.S., Devi, L.A., Novel endogenous peptide agonists of cannabinoid receptors. FASEB Journal 23 (2009), 3020–3029.
36. Goodman, J., Packard, M.G., Peripheral and intra-dorsolateral striatum injections of the cannabinoid receptor agonist WIN 55,212-2 impair consolidation of stimulus-response memory. Neuroscience 274 (2014), 128–137.
37. Goodman, J., Packard, M.G., The influence of cannabinoids on learning and memory processes of the dorsal striatum. Neurobiology of Learning and Memory 125 (2015), 1–14.
38. Gorzalka, B.B., Hill, M.N., Integration of endocannabinoid signaling into the neural network regulating stress-induced activation of the hypothalamic-pituitary-adrenal axis. Current Topics in Behavioral Neurosciences 1 (2009), 289–306.
39. Haghani, M., Shabani, M., Javan, M., Motamedi, F., Janahmadi, M., CB1 cannabinoid receptor activation rescues amyloid beta-induced alterations in behaviour and intrinsic electrophysiological properties of rat hippocampal CA1 pyramidal neurones. Cellular Physiology and Biochemistry 29 (2012), 391–406.
40. Han, Z.L., Fang, Q., Wang, Z.L., Li, X.H., Li, N., Chang, X.M.,. Wang, R., Antinociceptive effects of central administration of the endogenous cannabinoid receptor type 1 agonist VDPVNFKLLSH-OH [(m)VD-hemopressin(alpha)], an N-terminally extended hemopressin peptide. Journal of Pharmacology and Experimental Therapeutics 348 (2014), 316–323.
41. Han, R.W., Xu, H.J., Zhang, R.S., Wang, P., Chang, M., Peng, Y.L.,. Wang, R., Neuropeptide S interacts with the basolateral amygdala noradrenergic system in facilitating object recognition memory consolidation. Neurobiology of Learning and Memory 107 (2014), 32–36.
42. Han, R.W., Zhang, R.S., Xu, H.J., Chang, M., Peng, Y.L., Wang, R., Neuropeptide S enhances memory and mitigates memory impairment induced by MK801, scopolamine or Abeta(1–42) in mice novel object and object location recognition tasks. Neuropharmacology 70 (2013), 261–267.
43. Hao, S., Avraham, Y., Mechoulam, R., Berry, E.M., Low dose anandamide affects food intake, cognitive function, neurotransmitter and corticosterone levels in diet-restricted mice. European Journal of Pharmacology 392 (2000), 147–156.
44. Heimann, A.S., Gomes, L., Dale, C.S., Pagano, R.L., Gupta, A., de Souza, L.L.,. Devi, L.A., Hemopressin is an inverse agonist of CB1 cannabinoid receptors. Proceedings of the National Academy of Sciences, USA 104 (2007), 20588–20593.
45. Hemming, M., Yellowlees, P.M., Effective treatment of Tourette's syndrome with marijuana. Journal of Psychopharmacology 7 (1993), 389–391.
46. Henquet, C., Krabbendam, L., Spauwen, J., Kaplan, C., Lieb, R., Wittchen, H.U., van Os, J., Prospective cohort study of cannabis use, predisposition for psychosis, and psychotic symptoms in young people. British Medical Journal 330 (2005), 11–14.
47. Herkenham, M., Lynn, A.B., Johnson, M.R., Melvin, L.S., Decosta, B.R., Rice, K.C., Characterization and localization of cannabinoid receptors in rat-brain – A quantitative invitro autoradiographic study. Journal of Neuroscience 11 (1991), 563–583.
48. Ikeda, H., Ikegami, M., Kai, M., Kamei, J., Cannabinoid functions in the amygdala contribute to conditioned fear memory in streptozotocin-induced diabetic mice: Interaction with glutamatergic functions. Experimental Neurology 269 (2015), 233–241.
49. Iuvone, T., Esposito, G., Esposito, R., Santamaria, R., Di Rosa, M., Izzo, A.A., Neuroprotective effect of cannabidiol, a non-psychoactive component from Cannabis sativa, on beta-amyloid-induced toxicity in PC12 cells. Journal of Neurochemistry 89 (2004), 134–141.
50. Iversen, L., Comparing cannabis with tobacco: Arithmetic does not add up. BMJ, 327, 2003, 165.
51. Janefjord, E., Maag, J.L., Harvey, B.S., Smid, S.D., Cannabinoid effects on beta amyloid fibril and aggregate formation, neuronal and microglial-activated neurotoxicity in vitro. Cellular and Molecular Neurobiology 34 (2014), 31–42.
52. Justinova, Z., Panlilio, L.V., Goldberg, S.R., Drug addiction. Current Topics in Behavioral Neuroscience 1 (2009), 309–346.
53. Kim, T.W., Kim, C.S., Kim, J.Y., Kim, C.J., Seo, J.H., Combined exercise ameliorates ovariectomy-induced cognitive impairment by enhancing cell proliferation and suppressing apoptosis. Menopause, 2015.
54. Lichtman, A.H., SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats. European Journal of Pharmacology 404 (2000), 175–179.
55. Lichtman, A.H., Dimen, K.R., Martin, B.R., Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology (Berl) 119 (1995), 282–290.
56. Marchalant, Y., Brothers, H.M., Wenk, G.L., Inflammation and aging: Can endocannabinoids help?. Biomedicine & Pharmacotherapy 62 (2008), 212–217.
57. Marchalant, Y., Brothers, H.M., Wenk, G.L., Cannabinoid agonist WIN-55,212-2 partially restores neurogenesis in the aged rat brain. Molecular Psychiatry 14 (2009), 1068–1069.
58. Marsicano, G., Lafenetre, P., Roles of the endocannabinoid system in learning and memory. Current Topics in Behavioral Neurosciences 1 (2009), 201–230.
59. Martin-Moreno, A.M., Brera, B., Spuch, C., Carro, E., Garcia-Garcia, L., Delgado, M.,. de Ceballos, M.L., Prolonged oral cannabinoid administration prevents neuroinflammation, lowers beta-amyloid levels and improves cognitive performance in Tg APP 2576 mice. Journal of Neuroinflammation, 9, 2012.
60. Martin-Moreno, A.M., Reigada, D., Ramirez, B.G., Mechoulam, R., Innamorato, N., Cuadrado, A., de Ceballos, M.L., Cannabidiol and other cannabinoids reduce microglial activation in vitro and in vivo: Relevance to Alzheimer's disease. Molecular Pharmacology 79 (2011), 964–973.
61. Matsuda, L.A., Bonner, T.I., Lolait, S.J., Localization of cannabinoid receptor mRNA in rat brain. Journal of Comparative Neurology 327 (1993), 535–550.
62. Matsuda, L.A., Lolait, S.J., Brownstein, M.J., Young, A.C., Bonner, T.I., Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346 (1990), 561–564.
63. McGeer, P.L., Itagaki, S., Tago, H., McGeer, E.G., Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neuroscience Letters 79 (1987), 195–200.
64. Miller, L.L., Branconnier, R.J., Cannabis: Effects on memory and the cholinergic limbic system. Psychological Bulletin 93 (1983), 441–456.
65. Munro, S., Thomas, K.L., Abu-Shaar, M., Molecular characterization of a peripheral receptor for cannabinoids. Nature 365 (1993), 61–65.
66. Murray, E.A., Bussey, T.J., Hampton, R.R., Saksida, L.M., The parahippocampal region and object identification. Annals of the New York Academy of Sciences 911 (2000), 166–174.
67. Nitta, A., Itoh, A., Hasegawa, T., Nabeshima, T., Beta-Amyloid protein-induced Alzheimer's disease animal model. Neuroscience Letters 170 (1994), 63–66.
68. Nowicky, A.V., Teyler, T.J., Vardaris, R.M., The modulation of long-term potentiation by delta-9-tetrahydrocannabinol in the rat hippocampus, in vitro. Brain Research Bulletin 19 (1987), 663–672.
69. Nunez, E., Benito, C., Pazos, M.R., Barbachano, A., Fajardo, O., Gonzalez, S.,. Romero, J., Cannabinoid CB2 receptors are expressed by perivascular microglial cells in the human brain: An immunohistochemical study. Synapse (New York, N. Y.) 53 (2004), 208–213.
70. Okamura, N., Garau, C., Duangdao, D.M., Clark, S.D., Jungling, K., Pape, H.C., Reinscheid, R.K., Neuropeptide S enhances memory during the consolidation phase and interacts with noradrenergic systems in the brain. Neuropsychopharmacology 36 (2011), 744–752.
71. Onaivi, E.S., Ishiguro, H., Gong, J.P., Patel, S., Meozzi, P.A., Myers, L.,. Uhl, G.R., Functional expression of brain neuronal CB2 cannabinoid receptors are involved in the effects of drugs of abuse and in depression. Annals of the New York Academy of Sciences 1139 (2008), 434–449.
72. Orr, A.L., Hanson, J.E., Li, D., Klotz, A., Wright, S., Schenk, D.,. Madison, D.V., Beta-amyloid inhibits E-S potentiation through suppression of cannabinoid receptor 1-dependent synaptic disinhibition. Neuron 82 (2014), 1334–1345.
73. Pan, J.X., Wang, Z.L., Li, N., Han, Z.L., Li, X.H., Tang, H.H.,. Wang, R., Analgesic tolerance and cross-tolerance to the cannabinoid receptors ligands hemopressin, VD-hemopressin(alpha) and WIN55,212-2 at the supraspinal level in mice. Neuroscience Letters 578 (2014), 187–191.
74. Patel, S., Hillard, C.J., Role of endocannabinoid signaling in anxiety and depression. Current Topics in Behavioral Neurosciences 1 (2009), 347–371.
75. Paxinos, G., Franklin, K.B.J., Franklin, K.B.J., The mouse brain in stereotaxic coordinates. 2nd ed., 2001, Academic Press, San Diego.
76. Price, D.L., Sisodia, S.S., Mutant genes in familial Alzheimer's disease and transgenic models. Annual Review of Neuroscience 21 (1998), 479–505.
77. Ramirez, B.G., Blazquez, C., Gomez del Pulgar, T., Guzman, M., de Ceballos, M.L., Prevention of Alzheimer's disease pathology by cannabinoids: Neuroprotection mediated by blockade of microglial activation. Journal of Neuroscience 25 (2005), 1904–1913.
78. Ranganathan, M., D'Souza, D.C., The acute effects of cannabinoids on memory in humans: A review. Psychopharmacology (Berl) 188 (2006), 425–444.
79. Reibaud, M., Obinu, M.C., Ledent, C., Parmentier, M., Bohme, G.A., Imperato, A., Enhancement of memory in cannabinoid CB1 receptor knock-out mice. European Journal of Pharmacology 379 (1999), R1–R2.
80. Riedel, G., Davies, S.N., Cannabinoid function in learning, memory and plasticity. Handbook of Experimental Pharmacology, 2005, 445–477.
81. Rioli, V., Gozzo, F.C., Heimann, A.S., Linardi, A., Krieger, J.E., Shida, C.S.,. Ferro, E.S., Novel natural peptide substrates for endopeptidase 24.15, neurolysin, and angiotensin-converting enzyme. Journal of Biological Chemistry 278 (2003), 8547–8555.
82. Roberts, A.J., Hedlund, P.B., The 5-HT(7) receptor in learning and memory. Hippocampus 22 (2012), 762–771.
83. Romero, J., Garcia, L., Cebeira, M., Zadrozny, D., Fernandez-Ruiz, J.J., Ramos, J.A., The endogenous cannabinoid receptor ligand, anandamide, inhibits the motor behavior: Role of nigrostriatal dopaminergic neurons. Life Sciences 56 (1995), 2033–2040.
84. Sagar, D.R., Jhaveri, M., Chapman, V., Targeting the cannabinoid system to produce analgesia. Current Topics in Behavioral Neurosciences 1 (2009), 275–287.
85. Sandyk, R., Awerbuch, G., Marijuana and Tourette's syndrome. Journal of Clinical Psychopharmacology 8 (1988), 444–445.
86. Soderstrom, K., Johnson, F., Zebra finch CB1 cannabinoid receptor: Pharmacology and in vivo and in vitro effects of activation. Journal of Pharmacology and Experimental Therapeutics 297 (2001), 189–197.
87. Stella, N., Cannabinoid signaling in glial cells. Glia 48 (2004), 267–277.
88. Stella, N., Schweitzer, P., Piomelli, D., A second endogenous cannabinoid that modulates long-term potentiation. Nature 388 (1997), 773–778.
89. Sun, X., Dey, S.K., Cannabinoid/Endocannabinoid signaling impact on early pregnancy events. Current Topics in Behavioral Neurosciences 1 (2009), 255–273.
90. Terranova, J.P., Michaud, J.C., Le Fur, G., Soubrie, P., 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-Schmiedeberg's Archives of Pharmacology 352 (1995), 576–579.
91. Terranova, J.P., Storme, J.J., Lafon, N., Perio, A., Rinaldi-Carmona, M., Le Fur, G., Soubrie, P., Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology (Berl) 126 (1996), 165–172.
92. Tsou, K., Brown, S., Sanudo-Pena, M.C., Mackie, K., Walker, J.M., Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83 (1998), 393–411.
93. van der Stelt, M., Mazzola, C., Esposito, G., Matias, I., Petrosino, S., De Filippis, D.,. Di Marzo, V., Endocannabinoids and beta-amyloid-induced neurotoxicity in vivo: Effect of pharmacological elevation of endocannabinoid levels. Cellular and Molecular Life Sciences 63 (2006), 1410–1424.
94. van Praag, H., Shubert, T., Zhao, C., Gage, F.H., Exercise enhances learning and hippocampal neurogenesis in aged mice. Journal of Neuroscience 25 (2005), 8680–8685.
95. Van Sickle, M.D., Duncan, M., Kingsley, P.J., Mouihate, A., Urbani, P., Mackie, K.,. Sharkey, K.A., Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310 (2005), 329–332.
96. Volk, D.W., Lewis, D.A., The role of endocannabinoid signaling in cortical inhibitory neuron dysfunction in schizophrenia. Biological Psychiatry 79:7 (2016), 595–603.
97. Williams, C.M., Kirkham, T.C., Anandamide induces overeating: Mediation by central cannabinoid (CB1) receptors. Psychopharmacology (Berl) 143 (1999), 315–317.
98. Wilson, R.I., Nicoll, R.A., Endocannabinoid signaling in the brain. Science 296 (2002), 678–682.
99. Wu, J., Bie, B., Yang, H., Xu, J.J., Brown, D.L., Naguib, M., Activation of the CB2 receptor system reverses amyloid-induced memory deficiency. Neurobiology of Aging 34 (2013), 791–804.
100. Wu, N., Rao, X., Gao, Y., Wang, J., Xu, F., Amyloid-beta deposition and olfactory dysfunction in an Alzheimer's disease model. Journal of Alzheimers Disease 37 (2013), 699–712.
101. Zhang, R.S., Xu, H.J., Jiang, J.H., Han, R.W., Chang, M., Peng, Y.L.,. Wang, R., Endomorphin-1 attenuates Abeta42 induced impairment of novel object and object location recognition tasks in mice. Brain Research 1629 (2015), 210–220.