Local enhancement of cannabinoid CB1 receptor signalling in the dorsal hippocampus elicits an antidepressant-like effect

Behavioural Pharmacology

Volumn 18, Issue 5-6, 2007, Pages 431-438

  McLaughlin, Ryan J ^a   Hill, Matthew N ^a   Morrish, Anna C ^a   Gorzalka, Boris B ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

CB1 receptor; Depression; Endocannabinoids; Forced swim test; Hippocampus; Rat

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; ANTIDEPRESSANT AGENT; CANNABINOID 1 RECEPTOR; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; DEXANABINOL; DIMETHYL SULFOXIDE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; DRUG EFFECT; FORCED SWIMMING TEST; HIPPOCAMPUS; LOW DRUG DOSE; MALE; NONHUMAN; RAT; SPRAGUE DAWLEY RAT; SWIMMING;

ANALYSIS OF VARIANCE; ANIMALS; ANTIDEPRESSIVE AGENTS; BEHAVIOR, ANIMAL; BENZAMIDES; CARBAMATES; DENTATE GYRUS; DEPRESSION; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; HIPPOCAMPUS; MALE; PIPERIDINES; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; STRESS, PSYCHOLOGICAL; SWIMMING; TETRAHYDROCANNABINOL;

EID: 34548389394     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/FBP.0b013e3282ee7b44     Document Type: Article

References (66)

1. Abel E (1991). Gradient of alarm substance in the forced swimming test. Physiol Behav 49:321-323.
2. Abel E (1994). Behavioral and physiological effects of different water depths in the forced swim test. Physiol Behav 56:411-414.
3. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, et al. (2005). The endocannabinoid system drives neural progenitor proliferation. FASEB J 19:1704-1706.
4. Barna I, Zelena D, Arszovszki AC, Ledent C (2004). The role of endogenous cannabinoids in the hypothalamo-pituitary-adrenal axis regulation: in vivo and in vitro studies in CB1 receptor knockout mice. Life Sci 75:2959-2970.
5. Beylin AV, Shors TJ (2003). Glucocorticoids are necessary for enhancing the acquisition of associative memories after acute stressful experience. Horm Behav 43:124-131.
6. Bilang-Bleuel A, Ulricht S, Chandramohan Y, De Carli S, Droste SK, Reul JM (2005). Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: involvement in a glucocorticoid receptor-dependent behavioural response. Eur J Neurosci 22:1691-1700.
7. Borsini F, Meli A (1988). Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology 94:147-160.
8. Cannich A, Wotjak CT, Kamprath K, Herman H, Lutz B, Marsicano G (2004). CB1 cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice. Learn Mem 11:625-632.
9. Castane A, Maldonado R, Valverde O (2004). Role of different brain structures in the behavioural expression of WIN 55 212-2 withdrawal in mice. Br J Pharmacol 142:1309-1317.
10. Chen C, Bazan NG (2005). Lipid signaling: sleep, synaptic plasticity, and neuroprotection. Prostaglandins Lipid Mediat 77:65-76.
11. Cota D, Marsicano G, Tschop M, Grubler Y, Flachskamm C, Schubert M, et al. (2003). The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest 112:423-431.
12. Cota D, Steiner MA, Marsicano G, Cervino C, Herman JP, Grubler Y, et al. (2007). Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary-adrenal axis function. Endocrinology 148:1574-1581.
13. Cryan JF, Markou A, Lucki I (2002). Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23:238-245.
14. Degroot A, Nomikos GG (2007). In vivo neurochemical effects induced by changes in endocannabinoid neurotransmission. Curr Opin Pharmacol 7:62-68.
15. Derkinderen P, Valjent E, Toutant M, Corvol JC, Enslen H, Ledent C, et al. (2003). Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J Neurosci 23:2371-2382.
16. DeSanty KP, Dar MS (2001). Cannabinoid-induced motor incoordination through the cerebellar CB(1) receptor in mice. Pharmacol Biochem Behav 69:251-259.
17. Detke MJ, Rickels M, Lucki I (1995). Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 121:66-72.
18. Drew WG, Slagel DE (1973). Delta 9-THC: selective impairment of corticosterone uptake by limbic structures of the rat. Neuropharmacology 12:909-914.
19. Duncan GE, Knapp DJ, Johnson KB, Breese GR (1996). Functional classification of antidepressants based on antagonism of swim stress-induced fos-like immunoreactivity. J Pharmacol Exp Ther 277:1076-1089.
20. 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.
21. Eichenbaum H, Otto T, Cohen NJ (1992). The hippocampus: what does it do? Behav Neural Biol 57:2-36.
22. Freund TF, Katona I, Piomelli D (2003). Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066.
23. Gobbi G, Bambico FR, Mangieri R, Bortolato M, Campolongo P, Solinas M, et al. (2005). Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis. Proc Natl Acad Sci U S A 102:18620-18625.
24. Griebel G, Stemmelin J, Scatton B (2005). Effects of the cannabinoid CB1 receptor antagonist rimonabant in models of emotional reactivity in rodents. Biol Psychiatry 57:261-267.
25. Hampson RE, Deadwyler SA (1998). Role of cannabinoid receptors in memory storage. Neurobiol Dis 5:474-482.
26. Haring M, Marsicano G, Lutz B, Monoroy K (2007). Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice. Neuroscience 146:1212-1219.
27. Hasanein P, Parviz M, Keshavarz M, Javanmardi K (2007). CB1 receptor activation in the basolateral amygdala produces antinociception in animal models of acute and tonic nociception. Clin Exp Pharmacl Physiol 34:439-449.
28. Hebbar PB, Archer TK (2003). Chromatin remodeling by nuclear receptors. Chromosoma 111:495-504.
29. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991). Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583.
30. Herman JP, Mueller NK (2006). Role of the ventral subiculum in stress integration. Behav Brain Res 174:215-224.
31. Hill MN, Gorzalka BB (2005a). Pharmacological enhancement of cannabinoid CB1 receptor activity elicits an antidepressant-like response in the rat forced swim test. Eur Neuropsychopharmacol 15:593-599.
32. Hill MN, Gorzalka BB (2005b). Is there a role for the endocannabinoid system in the etiology and treatment of melancholic depression? Behav Pharmacol 16:333-352.
33. Hill MN, Froc DJ, Fox CJ, Gorzalka BB, Christie BR (2004). Prolonged cannabinoid treatment results in spatial working memory deficits and impaired long-term potentiation in the CA1 region of the hippocampus in vivo. Eur J Neurosci 20:859-863.
34. Hill MN, Patel S, Carrier EJ, Rademacher DJ, Ormerod BK, Hillard CJ, et al. (2005). Downregulation of endocannabinoid signaling in the hippocampus following chronic unpredictable stress. Neuropsychopharmacology 30:508-515.
35. Hill MN, Ho WS, Sinopoli KJ, Viau V, Hillard CJ, Gorzalka BB (2006). Involvement of the endocannabinoid system in the ability of long-term tricyclic antidepressant treatment to suppress stress-induced activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 31:2591-2599.
36. Hill MN, Karacabeyli ES, Gorzalka BB (2007). Estrogen recruits the endocannabinoid system to modulate emotionality. Psychoneuroendocrinology 32:350-357.
37. Howlett AC (2002). The cannabinoid receptors. Prostaglandins Lipid Mediat 68-69:619-631.
38. Jacobson L, Sapolsky R (1991). The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118-134.
39. Jiang W, Zhang Y, Xiao L, Van Cleemput J, Ji SP, Bai G, et al. (2005). Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic and antidepressant-like effects. J Clin Invest 115:3104-3116.
40. Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO, et al. (2004). Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 66:204-208.
41. Karanian DA, Brown QB, Makriyannis A, Bahr BA (2005). Blocking cannabinoid activation of FAK and ERK1/2 compromises synaptic integrity in hippocampus. Eur J Pharmacol 508:47-56.
42. Korte SM, De Kloet ER, Buwalda B, Bouman SD, Bohus B (1996). Antisense to the glucocorticoid receptor in hippocampal dentate gyrus reduces immobility in forced swim test. Eur J Pharmacol 301:19-25.
43. Lichtman AH, Dimen KR, Martin BR (1995). Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology 119:282-290.
44. Ligresti A, Cascio MG, Di Marzo V (2005). Endocannabinoid metabolic pathways and enzymes. Curr Drug Targets CNS Neurol Disord 4:615-623.
45. Lin HC, Mao SC, Gean PW (2006). Effects of intra-amygdala infusion of CB1 receptor agonists on the reconsolidation of fear-potentiated startle. Learn Mem 13:316-321.
46. Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O (2002). Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology 159:379-387.
47. McGaugh JL, Roozendaal B (2002). Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205-210.
48. Molina VA, Heyser CJ, Spear LP (1994). Chronic variable stress or chronic morphine facilitates immobility in a forced swim test: reversal by naloxone. Psychopharmacology 114:433-440.
49. Olson AK, Hill MN, Carrier EJ, Morrish AC, Gorzalka BB, Christie BR, et al. (2006). Voluntary exercise up-regulates endocannabinoid signaling in the hippocampus. Soc Neurosci [Abstract]; 791.8.
50. Padley JR, Li Q, Pilowsky PM, Goodchild AK (2003). Cannabinoid receptor activation in the rostral ventrolateral medulla oblongata evokes cardiorespiratory effects in anaesthetised rats. Br J Pharmacol 140:384-394.
51. Palazzo E, de Novellis V, Petrosino S, Marabese I, Vita D, Giordano C, et al. (2006). Neuropathic pain and the endocannabinoid system in the dorsal raphe: pharmacological treatment and interactions with the serotonergic system. Eur J Neurosci 24:2011-2020.
52. Patel S, Roelke CT, Rademacher DJ, Cullinan WE, Hillard CJ (2004). Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 145: 5431-5438.
53. Paxinos G, Watson C (1998). The rat brain in stereotaxic coordinates. 4th ed. San Diego: Academic Press.
54. Piomelli D, Tarzia G, Duranti A, Tontini A, Mor M, Compton TR, et al. (2006). Pharmacological profile of the selective FAAH inhibitor KDS-4103 (URB597). CNS Drug Rev 12:21-38.
55. Porsolt RD, Anton G, Blavet N, Jalfre M (1978). Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379-391.
56. Realini N, Guidali C, Perletti G, Parolaro D, Rubino T (2006). Role of endocannabinoids in the modulation of anxious states in rat prefrontal cortex. 16th Annual Symposium on the Cannabinoids. 138.
57. Rodriguez de Fonseca F, Del Arco I, Bermudez-Silva FJ, Bilbao A, Cippitelli A, Navarro M (2005). The endocannabinoid system: physiology and pharmacology. Alcohol Alcohol 40:2-14.
58. Roohbakhsh A, Moghaddam AH, Massoudi R, Zarrindast MR (2007). Role of dorsal hippocampal cannabinoid receptors and nitric oxide in anxiety like behaviours in rats using the elevated plus-maze test. Clin Exp Pharmacol Physiol 34:223-229.
59. Rutkowska M, Jachimczuk O (2004). Antidepressant-like properties of ACEA (arachidonyl-2-chloroethylamide), the selective agonist of CB1 receptors. Acta Pol Pharm 61:165-167.
60. Schlicker E, Kathmann M (2001). Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 22:565-572.
61. Shearman LP, Rosko KM, Fleischer R, Wang J, Xu S, Tong XS, et al. (2003). Antidepressant-like and anorectic effects of the cannabinoid CB1 receptor inverse agonist AM251 in mice. Behav Pharmacol 14:573-582.
62. Shiriyama Y, Chen AC, Nakagawa S, Russell DS, Duman RS (2002). Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 22:3251-3261.
63. Solinas M, Panlilio LV, Tanda G, Makriyannis A, Matthews SA, Goldberg SR (2005). Cannabinoid agonists but not inhibitors of endogenous cannabinoid transport or metabolism enhance the reinforcing efficacy of heroin in rats. Neuropsychopharmacology 30:2046-2057.
64. Tzavara ET, Davis RJ, Perry KW, Li X, Salhoff C, Bymaster FP, et al. (2003). The CB1 receptor antagonist SR141716A selectively increases monoaminergic neurotransmission in the medial prefrontal cortex: implications for therapeutic actions. Br J Pharmacol 138: 544-553.
65. Vinod KY, Hungund BL (2006). Role of the endocannabinoid system in depression and suicide. Trends Pharmacol Sci 27:539-545.
66. Witkin JM, Tzavara ET, Davis RJ, Li X, Nomikos GG (2005). A therapeutic role for cannabinoid CB1 receptor antagonists in major depressive disorders. Trends Pharmacol Sci 26:609-617.