Antagonism of cannabinoid 1 receptors reverses the anxiety-like behavior induced by central injections of corticotropin-releasing factor and cocaine withdrawal

Neuroscience

Volumn 204, Issue , 2012, Pages 125-133

  Kupferschmidt, D A ^a   Newman, A E ^b   Boonstra, R ^a   Erb, S ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Anxiety; Cocaine; Corticosterone; CRF; Endocannabinoid; Withdrawal

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID 1 RECEPTOR; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; BEHAVIORAL STRESS; BLOOD SAMPLING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DRUG MECHANISM; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LONG EVANS RAT; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RADIOIMMUNOASSAY; RAT; REVIEW;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; COCAINE; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DOPAMINE UPTAKE INHIBITORS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PIPERIDINES; PITUITARY-ADRENAL SYSTEM; PYRAZOLES; RATS; RATS, LONG-EVANS; RECEPTOR, CANNABINOID, CB1; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84857125718     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.07.022     Document Type: Review

References (78)

1. Ambrosio E., Sharpe L.G., Pilotte N.S. Regional binding to corticotropin releasing factor receptors in brain of rats exposed to chronic cocaine and cocaine withdrawal. Synapse 1997, 25:272-276.
2. Arévalo C., de Miguel R., Hernández-Tristán R. Cannabinoid effects on anxiety-related behaviours and hypothalamic neurotransmitters. Pharmacol Biochem Behav 2001, 70:123-131.
3. Auclair N., Otani S., Soubrie P., Crepel F. Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 2000, 83:3287-3293.
4. Baldwin H.A., Rassnick S., Rivier J., Koob G.F., Britton K.T. CRF antagonist reverses the "anxiogenic" response to ethanol withdrawal in the rat. Psychopharmacology (Berl) 1991, 103:227-232.
5. Basso A.M., Spina M., Rivier J., Vale W., Koob G.F. Corticotropin-releasing factor antagonist attenuates the "anxiogenic-like" effect in the defensive burying paradigm but not in the elevated plus-maze following chronic cocaine in rats. Psychopharmacology (Berl) 1999, 145:21-30.
6. Berridge C.W., Dunn A.J. CRF and restraint-stress decrease exploratory behavior in hypophysectomized mice. Pharmacol Biochem Behav 1989, 34:517-519.
7. Britton K.T., Lee G., Dana R., Risch S.C., Koob G.F. Activating and "anxiogenic" effects of corticotropin releasing factor are not inhibited by blockade of the pituitary-adrenal system with dexamethasone. Life Sci 1986, 39:1281-1286.
8. Campbell B.M., Morrison J.L., Walker E.L., Merchant K.M. Differential regulation of behavioral, genomic, and neuroendocrine responses by CRF infusions in rats. Pharmacol Biochem Behav 2004, 77:447-455.
9. Chiu C.Q., Puente N., Grandes P., Castillo P.E. Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 2010, 30:7236-7248.
10. Cota D., Steiner M.A., Marsicano G., Cervino C., Herman J.P., Grübler Y., Stalla J., Pasquali R., Lutz B., Stalla G.K., Pagotto U. Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary-adrenal axis function. Endocrinology 2007, 148:1574-1581.
11. Day H.E., Vittoz N.M., Oates M.M., Badiani A., Watson S.J., Robinson T.E., Akil H. A 6-hydroxydopamine lesion of the mesostriatal dopamine system decreases the expression of corticotropin releasing hormone and neurotensin mRNAs in the amygdala and bed nucleus of the stria terminalis. Brain Res 2002, 945:151-159.
12. de la Mora M.P., Gallegos-Cari A., Arizmendi-García Y., Marcellino D., Fuxe K. Role of dopamine receptor mechanisms in the amygdaloid modulation of fear and anxiety: structural and functional analysis. Prog Neurobiol 2010, 90:198-216.
13. DeVries A.C., Pert A. Conditioned increases in anxiogenic-like behavior following exposure to contextual stimuli associated with cocaine are mediated by corticotropin-releasing factor. Psychopharmacology (Berl) 1998, 137:333-340.
14. Di S., Malcher-Lopes R., Halmos K.C., Tasker J.G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 2003, 23:4850-4857.
15. Domenici M.R., Azad S.C., Marsicano G., Schierloh A., Wotjak C.T., Dodt H.U., Zieglgänsberger W., Lutz B., Rammes G. Cannabinoid receptor type 1 located on presynaptic terminals of principal neurons in the forebrain controls glutamatergic synaptic transmission. J Neurosci 2006, 26:5794-5799.
16. Dunn A.J., Berridge C.W. Physiological and behavioral responses to corticotropin-releasing factor administration: is CRF a mediator of anxiety or stress responses?. Brain Res Brain Res Rev 1990, 15:71-100.
17. Dunn A.J., File S.E. Corticotropin-releasing factor has an anxiogenic action in the social interaction test. Horm Behav 1987, 21:193-202.
18. Eaves M., Thatcher-Britton K., Rivier J., Vale W., Koob G.F. Effects of corticotropin releasing factor on locomotor activity in hypophysectomized rats. Peptides 1985, 6:923-926.
19. Eliava M., Yilmazer-Hanke D., Asan E. Interrelations between monoaminergic afferents and corticotropin-releasing factor-immunoreactive neurons in the rat central amygdaloid nucleus: ultrastructural evidence for dopaminergic control of amygdaloid stress systems. Histochem Cell Biol 2003, 120:183-197.
20. Erb S., Borkowski S., Funk D., Watson S.J., Akil H. Effects of chronic cocaine on CRH and CRH-BP mRNA expression in the extended amygdala following drug-free periods of up to 28 days. Soc Neurosci Abstr 2003, 856.1.
21. Evanson N.K., Tasker J.G., Hill M.N., Hillard C.J., Herman J.P. Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 2010, 151:4811-4819.
22. Evanson N.K., Ulrich-Lai Y.M., Furay A.R., Tasker J.G., Herman J.P. Hypothalamic paraventricular cannabinoid receptor signaling in fast feedback inhibition of the hypothalamus-pituitary-adrenal axis response to acute restraint stress. Soc Neurosci Abstr 2007, 197:195.
23. Griebel G., Stemmelin J., Scatton B. Effects of the cannabinoid CB1 receptor antagonist rimonabant in models of emotional reactivity in rodents. Biol Psychiatry 2005, 57:261-267.
24. Hall B.J., Pearson L.S., Buccafusco J.J. Effect of the use-dependent, nicotinic receptor antagonist BTMPS in the forced swim test and elevated plus maze after cocaine discontinuation in rats. Neurosci Lett 2010, 474:84-87.
25. Haller J., Varga B., Ledent C., Freund T.F. CB1 cannabinoid receptors mediate anxiolytic effects: convergent genetic and pharmacological evidence with CB1-specific agents. Behav Pharmacol 2004, 15:299-304.
26. Heinrichs S.C., Menzaghi F., Schulteis G., Koob G.F., Stinus L. Suppression of corticotropin-releasing factor in the amygdala attenuates aversive consequences of morphine withdrawal. Behav Pharmacol 1995, 6:74-80.
27. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 1991, 11:563-583.
28. Hermann H., Lutz B. Coexpression of the cannabinoid receptor type 1 with the corticotropin-releasing hormone receptor type 1 in distinct regions of the adult mouse forebrain. Neurosci Lett 2005, 375:13-18.
29. Hermes G.L., Delgado B., Tretiakova M., Cavigelli S.A., Krausz T., Conzen S.D., McClintock M.K. Social isolation dysregulates endocrine and behavioral stress while increasing malignant burden of spontaneous mammary tumors. Proc Natl Acad Sci U S A 2009, 106:22393-22398.
30. Hill M.N., McEwen B.S. Involvement of the endocannabinoid system in the neurobehavioral effects of stress and glucocorticoids. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:791-797.
31. Hill M.N., McLaughlin R.J., Morrish A.C., Viau V., Floresco S.B., Hillard C.J., Gorzalka B.B. Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 2009, 34:2733-2745.
32. Hill M.N., McLaughlin R.J., Viau V., Gorzalka B.B., Hillard C.J. Stress-induced alterations in limbic endocannabinoid content in the rat: correlations to HPA axis activation. 17th Annual Symposium of the International Cannabinoid Research Society 2007, Vol. 23.
33. Katona I., Rancz E.A., Acsady L., Ledent C., Mackie K., Hajos N., Freund T.F. Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 2001, 21:9506-9518.
34. Kupferschmidt D.A., Wang T., Singh A., Erb S. Endocannabinoids and CRF interact to mediate the expression of anxiety and reinstatement of cocaine seeking. Soc Neurosci Abstr 2010, 164.5.
35. Lafenêtre P., Chaouloff F., Marsicano G. The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacol Res 2007, 56:367-381.
36. Maj M., Turchan J., Smiałowska M., Przewłocka B. Morphine and cocaine influence on CRF biosynthesis in the rat central nucleus of amygdala. Neuropeptides 2003, 37:105-110.
37. Meloni E.G., Gerety L.P., Knoll A.T., Cohen B.M., Carlezon W.A. Behavioral and anatomical interactions between dopamine and corticotropin-releasing factor in the rat. J Neurosci 2006, 26:3855-3863.
38. Navarro M., Hernández E., Muñoz R.M., del Arco I., Villanúa M.A., Carrera M.R., Rodríguez de Fonseca F. Acute administration of the CB1 cannabinoid receptor antagonist SR 141716A induces anxiety-like responses in the rat. Neuroreport 1997, 8:491-496.
39. Onaivi E.S. An endocannabinoid hypothesis of drug reward and drug addiction. Ann N Y Acad Sci 2008, 1139:412-421.
40. Onaivi E.S., Chakrabarti A., Gwebu E.T., Chaudhuri G. Neurobehavioral effects of delta 9-THC and cannabinoid (CB1) receptor gene expression in mice. Behav Brain Res 1995, 72:115-125.
41. Patel S., Cravatt B.F., Hillard C.J. Synergistic interactions between cannabinoids and environmental stress in the activation of the central amygdala. Neuropsychopharmacology 2005, 30:497-507.
42. Patel S., Hillard C.J. Pharmacological evaluation of cannabinoid receptor ligands in a mouse model of anxiety: further evidence for an anxiolytic role for endogenous cannabinoid signaling. J Pharmacol Exp Ther 2006, 318:304-311.
43. Patel S., Roelke C.T., Rademacher D.J., Hillard C.J. Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur J Neurosci 2005, 21:1057-1069.
44. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1997, Academic Press, New York.
45. Pertwee R.G. Inverse agonism and neutral antagonism at cannabinoid CB1 receptors. Life Sci 2005, 76:1307-1324.
46. Phelix C.F., Liposits Z., Paull W.K. Catecholamine-CRF synaptic interaction in a septal bed nucleus: afferents of neurons in the bed nucleus of the stria terminalis. Brain Res Bull 1994, 33:109-119.
47. Pich E.M., Heinrichs S.C., Rivier C., Miczek K.A., Fisher D.A., Koob G.F. Blockade of pituitary-adrenal axis activation induced by peripheral immunoneutralization of corticotropin-releasing factor does not affect the behavioral response to social defeat stress in rats. Psychoneuroendocrinology 1993, 18:495-507.
48. Pillolla G., Melis M., Perra S., Muntoni A.L., Gessa G.L., Pistis M. Medial forebrain bundle stimulation evokes endocannabinoid-mediated modulation of ventral tegmental area dopamine neuron firing in vivo. Psychopharmacology (Berl) 2007, 191:843-853.
49. Racz I., Bilkei-Gorzo A., Toth Z.E., Michel K., Palkovits M., Zimmer A. A critical role for the cannabinoid CB1 receptors in alcohol dependence and stress-stimulated ethanol drinking. J Neurosci 2003, 23:2453-2458.
50. Rademacher D.J., Meier S.E., Shi L., Ho W.S., Jarrahian A., Hillard C.J. Effects of acute and repeated restraint stress on endocannabinoid content in the amygdala, ventral striatum, and medial prefrontal cortex in mice. Neuropharmacology 2008, 54:108-116.
51. Rassnick S., Heinrichs S.C., Britton K.T., Koob G.F. Microinjection of a corticotropin-releasing factor antagonist into the central nucleus of the amygdala reverses anxiogenic-like effects of ethanol withdrawal. Brain Res 1993, 605:25-32.
52. Richter R.M., Weiss F. In vivo CRF release in rat amygdala is increased during cocaine withdrawal in self-administering rats. Synapse 1999, 32:254-261.
53. Rodaros D., Caruana D.A., Amir S., Stewart J. Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience 2007, 150:8-13.
54. Rodgers R.J., Evans P.M., Murphy A. Anxiogenic profile of AM251, a selective cannabinoid CB1 receptor antagonist, in plus-maze-naïve and plus-maze-experienced mice. Behav Pharmacol 2005, 16:405-413.
55. Roohbakhsh A., Moghaddam A.H., Massoudi R., Zarrindast M.R. 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 2007, 34:223-229.
56. Rubino T., Guidali C., Vigano D., Realini N., Valenti M., Massi P., Parolaro D. CB1 receptor stimulation in specific brain areas differently modulate anxiety-related behaviour. Neuropharmacology 2008, 54:151-160.
57. Rubino T., Realini N., Castiglioni C., Guidali C., Viganó D., Marras E., Petrosino S., Perletti G., Maccarrone M., Di Marzo V., Parolaro D. Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex. Cereb Cortex 2008, 18:1292-1301.
58. Rubino T., Sala M., Viganò D., Braida D., Castiglioni C., Limonta V., Guidali C., Realini N., Parolaro D. Cellular mechanisms underlying the anxiolytic effect of low doses of peripheral Delta9-tetrahydrocannabinol in rats. Neuropsychopharmacology 2007, 32:2036-2045.
59. Rubio M., Fernández-Ruiz J., de Miguel R., Maestro B., Michael Walker J., Ramos J.A. CB1 receptor blockade reduces the anxiogenic-like response and ameliorates the neurochemical imbalances associated with alcohol withdrawal in rats. Neuropharmacology 2008, 54:976-988.
60. Sahuque L.L., Kullberg E.F., Mcgeehan A.J., Kinder J.R., Hicks M.P., Blanton M.G., Janak P.H., Olive M.F. Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: role of CRF receptor subtypes. Psychopharmacology (Berl) 2006, 186:122-132.
61. Sajdyk T.J., Schober D.A., Gehlert D.R., Shekhar A. Role of corticotropin-releasing factor and urocortin within the basolateral amygdala of rats in anxiety and panic responses. Behav Brain Res 1999, 100:207-215.
62. Sarnyai Z., Bíró E., Gardi J., Vecsernyés M., Julesz J., Telegdy G. Brain corticotropin-releasing factor mediates "anxiety-like" behavior induced by cocaine withdrawal in rats. Brain Res 1995, 675:89-97.
63. Sarnyai Z., Shaham Y., Heinrichs S.C. The role of corticotropin-releasing factor in drug addiction. Pharmacol Rev 2001, 53:209-243.
64. Savinainen J.R., Saario S.M., Niemi R., Järvinen T., Laitinen J.T. An optimized approach to study endocannabinoid signaling: evidence against constitutive activity of rat brain adenosine A1 and cannabinoid CB1 receptors. Br J Pharmacol 2003, 140:1451-1459.
65. Sawchenko P.E., Imaki T., Potter E., Kovács K., Imaki J., Vale W. The functional neuroanatomy of corticotropin-releasing factor. Ciba Found Symp 1993, 172:5-21. discussion: 21-29.
66. Sciolino N.R., Bortolato M., Eisenstein S.A., Fu J., Oveisi F., Hohmann A.G., Piomelli D. Social isolation and chronic handling alter endocannabinoid signaling and behavioral reactivity to context in adult rats. Neuroscience 2010, 168:371-386.
67. Sithisarn T., Bada H.S., Dai H., Randall D.C., Legan S.J. Effects of perinatal cocaine exposure on open field behavior and the response to corticotropin releasing hormone (CRH) in rat offspring. Brain Res 2011, 1370:136-144.
68. Spina M.G., Merlo-Pich E., Akwa Y., Balducci C., Basso A.M., Zorrilla E.P., Britton K.T., Rivier J., Vale W.W., Koob G.F. Time-dependent induction of anxiogenic-like effects after central infusion of urocortin or corticotropin-releasing factor in the rat. Psychopharmacology (Berl) 2002, 160:113-121.
69. Stewart J., Horton C., Robinson B., Amir S. Unilateral loss of dopaminergic innervation suppresses the expression of CRF-IR in the ipsilateral oval nucleus of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in the rat. Soc Neurosci Abstr 2008, 767.21.
70. Suchecki D., Tiba P.A., Tufik S. Hormonal and behavioural responses of paradoxical sleep-deprived rats to the elevated plus maze. J Neuroendocrinol 2002, 14:549-554.
71. Toth M., Mikics E., Tulogdi A., Aliczki M., Haller J. Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm Behav 2011, 60:28-36.
72. Walker D.L., Miles L.A., Davis M. Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:1291-1308.
73. Wanat M.J., Hopf F.W., Stuber G.D., Phillips P.E., Bonci A. Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 2008, 586:2157-2170.
74. Zarrindast M.R., Sarahroodi S., Arzi A., Khodayar M.J., Taheri-Shalmani S., Rezayof A. Cannabinoid CB1 receptors of the rat central amygdala mediate anxiety-like behavior: interaction with the opioid system. Behav Pharmacol 2008, 19:716-723.
75. Zhou Y., Maiya R., Norris E.H., Kreek M.J., Strickland S. Involvement of tissue plasminogen activator in stress responsivity during acute cocaine withdrawal in mice. Stress 2010, 13:481-490.
76. Zhou Y., Spangler R., Ho A., Kreek M.J. Increased CRH mRNA levels in the rat amygdala during short-term withdrawal from chronic "binge" cocaine. Brain Res Mol Brain Res 2003, 114:73-79.
77. Zhou Y., Spangler R., LaForge K.S., Maggos C.E., Ho A., Kreek M.J. Corticotropin-releasing factor and type 1 corticotropin-releasing factor receptor messenger RNAs in rat brain and pituitary during "binge"-pattern cocaine administration and chronic withdrawal. J Pharmacol Exp Ther 1996, 279:351-358.
78. Zorrilla E.P., Valdez G.R., Weiss F. Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacology (Berl) 2001, 158:374-381.