Fluoxetine facilitates fear extinction through amygdala endocannabinoids

Neuropsychopharmacology

Volumn 41, Issue 6, 2016, Pages 1598-1609

  Gunduz Cinar, Ozge ^a   Flynn, Shaun ^a   Brockway, Emma ^a   Kaugars, Katherine ^a   Baldi, Rita ^b   Ramikie, Teniel S ^b   Cinar, Resat ^a   Kunos, George ^a   Patel, Sachin ^b   Holmes, Andrew ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANANDAMIDE; CANNABINOID 1 RECEPTOR; CITALOPRAM; ENDOCANNABINOID; FATTY ACID AMIDASE; FLUOXETINE; AMIDASE; AMIDE; ANXIOLYTIC AGENT; ARACHIDONIC ACID DERIVATIVE; FATTY-ACID AMIDE HYDROLASE;

AMYGDALA; ANIMAL EXPERIMENT; ARTICLE; BIOCHEMICAL ANALYSIS; BRAIN REGION; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; ENZYME ACTIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEAR; FLUID INTAKE; IN VITRO STUDY; INFORMATION RETRIEVAL; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; ANIMAL; CHEMISTRY; DRUG EFFECTS; INBRED MOUSE STRAIN; METABOLISM; PHYSIOLOGY; REINFORCEMENT;

AMIDOHYDROLASES; AMYGDALA; ANIMALS; ANTI-ANXIETY AGENTS; ARACHIDONIC ACIDS; ENDOCANNABINOIDS; EXTINCTION, PSYCHOLOGICAL; FEAR; FLUOXETINE; MALE; MICE; MICE, INBRED STRAINS; POLYUNSATURATED ALKAMIDES;

EID: 84963522600     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.318     Document Type: Article

References (80)

1. Andero R, Ressler KJ. (2012). Fear extinction and BDNF: translating animal models of PTSD to the clinic. Genes Brain Behav 11: 503-512
2. Aronoff GR, Bergstrom RF, Pottratz ST, Sloan RS, Wolen RL, Lemberger L. (1984). Fluoxetine kinetics and protein binding in normal and impaired renal function. Clin Pharmacol Ther 36: 138-144
3. Aso E, Renoir T, Mengod G, Ledent C, Hamon M, Maldonado R, et al. (2009). Lack of CB1 receptor activity impairs serotonergic negative feedback. J Neurochem 109: 935-944
4. Atsak P, Hauer D, Campolongo P, Schelling G, Fornari RV, Roozendaal B. (2015). Endocannabinoid signaling within the basolateral amygdala integrates multiple stress hormone effects on memory consolidation. Neuropsychopharmacology 40: 1485-1494
5. Bambico FR, Cassano T, Dominguez-Lopez S, Katz N, Walker CD, Piomelli D, et al. (2010). Genetic deletion of fatty acid amide hydrolase alters emotional behavior and serotonergic transmission in the dorsal raphe, prefrontal cortex, and hippocampus. Neuropsychopharmacology 35: 2083-2100
6. Bisogno T, Melck D, De Petrocellis L, Bobrov M, Gretskaya NM, Bezuglov VV, et al. (1998). Arachidonoylserotonin and other novel inhibitors of fatty acid amide hydrolase. Biochem Biophys Res Commun 248: 515-522
7. Bissiere S, Humeau Y, Luthi A. (2003). Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 6: 587-592
8. Bortolato M, Mangieri RA, Fu J, Kim JH, Arguello O, Duranti A, et al. (2007). Antidepressant-like activity of the fatty acid amide hydrolase inhibitor URB597 in a rat model of chronic mild stress. Biol Psychiatry 62: 1103-1110
9. Bowers ME, Ressler KJ. (2015). Interaction between the cholecystokinin and endogenous cannabinoid systems in cued fear expression and extinction retention. Neuropsychopharmacology 40: 688-700
10. Bui E, Orr SP, Jacoby RJ, Keshaviah A, LeBlanc NJ, Milad MR, et al. (2013). Two weeks of pretreatment with escitalopram facilitates extinction learning in healthy individuals. Hum Psychopharmacol 28: 447-456
11. Bukalo O, Pinard CR, Holmes A. (2014). Mechanisms to medicines: elucidating neural and molecular substrates of fear extinction to identify novel treatments for anxiety disorders. Br J Pharmacol 171: 4690-4718
12. Bukalo O, Pinard C, Silverstein S, Brehm C, Hartley N, Whittle N, et al. (2015). Prefrontal inputs to the amygdala instruct fear extinction memory formation. Sci Adv 1: e1500251
13. Burghardt NS, Bush DE, McEwen BS, LeDoux JE. (2007). Acute selective serotonin reuptake inhibitors increase conditioned fear expression: blockade with a 5-HT(2C) receptor antagonist. Biol Psychiatry 62: 1111-1118
14. Burghardt NS, Bauer EP. (2013). Acute and chronic effects of selective serotonin reuptake inhibitor treatment on fear conditioning: implications for underlying fear circuits. Neuroscience 247: 253-272
15. Camp MC, Macpherson KP, Lederle L, Graybeal C, Gaburro S, Debrouse LM, et al. (2012). Genetic strain differences in learned fear inhibition associated with variation in neuroendocrine, autonomic, and amygdala dendritic phenotypes. Neuropsychopharmacology 37: 1534-1547
16. Cassano T, Gaetani S, Macheda T, Laconca L, Romano A, Morgese MG, et al. (2011). Evaluation of the emotional phenotype and serotonergic neurotransmission of fatty acid amide hydrolase-deficient mice. Psychopharmacology (Berl) 214: 465-476
17. Crozatier C, Farley S, Mansuy IM, Dumas S, Giros B, Tzavara ET. (2007). Calcineurin (protein phosphatase 2B) is involved in the mechanisms of action of antidepressants. Neuroscience 144: 1470-1476
18. Cryan JF, O?Leary OF, Jin SH, Friedland JC, Ouyang M, Hirsch BR, et al. (2004). Norepinephrine-deficient mice lack responses to antidepressant drugs, including selective serotonin reuptake inhibitors. Proc Natl Acad Sci USA 101: 8186-8191
19. Deschaux O, Spennato G, Moreau JL, Garcia R. (2011). Chronic treatment with fluoxetine prevents the return of extinguished auditory-cued conditioned fear. Psychopharmacology (Berl) 215: 231-237
20. Deschaux O, Zheng X, Lavigne J, Nachon O, Cleren C, Moreau JL, et al. (2013). Post-extinction fluoxetine treatment prevents stressinduced reemergence of extinguished fear. Psychopharmacology (Berl) 225: 209-216
21. Dincheva I, Drysdale AT, Hartley CA, Johnson DC, Jing D, King EC, et al. (2015). FAAH genetic variation enhances fronto-amygdala function in mouse and human. Nat Commun 6: 6395
22. Dlugos A, Childs E, Stuhr KL, Hillard CJ, de Wit H. (2012). Acute stress increases circulating anandamide and other N-acylethanolamines in healthy humans. Neuropsychopharmacology 37: 2416-2427
23. Dubreucq S, Matias I, Cardinal P, Haring M, Lutz B, Marsicano G, et al. (2012). Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37: 1885-1900
24. Dulawa SC, Holick KA, Gundersen B, Hen R. (2004). Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 29: 1321-1330
25. Fitzgerald PJ, Whittle N, Flynn SM, Graybeal C, Pinard CR, Gunduz-Cinar O, et al. (2014). Prefrontal single-unit firing associated with deficient extinction in mice. Neurobiol Learn Mem 113: 69-81
26. 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 USA 102: 18620-18625
27. Godlewski G, Alapafuja SO, Batkai S, Nikas SP, Cinar R, Offertaler L, et al. (2010). Inhibitor of fatty acid amide hydrolase normalizes cardiovascular function in hypertension without adverse metabolic effects. Chem Biol 17: 1256-1266
28. Gogolla N, Caroni P, Luthi A, Herry C. (2009). Perineuronal nets protect fear memories from erasure. Science 325: 1258-1261
29. Gunduz-Cinar O, Hill MN, McEwen BS, Holmes A. (2013a). Amygdala FAAH and anandamide: mediating protection and recovery from stress. Trends Pharmacol Sci 34: 637-644
30. Gunduz-Cinar O, Macpherson KP, Cinar R, Gamble-George J, Sugden K, Williams B, et al. (2013b). Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity. Mol Psychiatry 18: 813-823
31. Haring M, Marsicano G, Lutz B, Monory K. (2007). Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice. Neuroscience 146: 1212-1219
32. Hariri AR, Gorka A, Hyde LW, Kimak M, Halder I, Ducci F, et al. (2009). Divergent effects of genetic variation in endocannabinoid signaling on human threat-and reward-related brain function. Biol Psychiatry 66: 9-16
33. Hartley CA, McKenna MC, Salman R, Holmes A, Casey BJ, Phelps EA, et al. (2012). Serotonin transporter polyadenylation polymorphism modulates the retention of fear extinction memory. Proc Natl Acad Sci USA 109: 5493-5498
34. Hashimotodani Y, Ohno-Shosaku T, Kano M. (2007). Presynaptic monoacylglycerol lipase activity determines basal endocannabinoid tone and terminates retrograde endocannabinoid signaling in the hippocampus. J Neurosci 27: 1211-1219
35. Heifets BD, Chevaleyre V, Castillo PE. (2008). Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin. Proc Natl Acad Sci USA 105: 10250-10255
36. Herry C, Ciocchi S, Senn V, Demmou L, Muller C, Luthi A. (2008). Switching on and off fear by distinct neuronal circuits. Nature 454: 600-606
37. Hill MN, Bierer LM, Makotkine I, Golier JA, Galea S, McEwen BS, et al. (2013). Reductions in circulating endocannabinoid levels in individuals with post-traumatic stress disorder following exposure to the World Trade Center attacks. Psychoneuroendocrinology 38: 2952-2961
38. Hill MN, Ho WS, Hillard CJ, Gorzalka BB. (2008a). Differential effects of the antidepressants tranylcypromine and fluoxetine on limbic cannabinoid receptor binding and endocannabinoid contents. J Neural Transm 115: 1673-1679
39. Hill MN, McEwen BS. (2010). Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog Neuropsychopharmacol Biol Psychiatry 34: 791-797
40. Hill MN, Miller GE, Ho WS, Gorzalka BB, Hillard CJ. (2008b). Serum endocannabinoid content is altered in females with depressive disorders: a preliminary report. Pharmacopsychiatry 41: 48-53
41. Holmes A, Rodgers RJ. (2003). Prior exposure to the elevated plusmaze sensitizes mice to the acute behavioral effects of fluoxetine and phenelzine. Eur J Pharmacol 459: 221-230
42. Holmes A, Quirk GJ. (2010). Pharmacological facilitation of fear extinction and the search for adjunct treatments for anxiety disorders-the case of yohimbine. Trends Pharmacol Sci 31: 2-7
43. Holmes A, Singewald N. (2013). Individual differences in recovery from traumatic fear. Trends Neurosci 36: 23-31
44. Jiao J, Nitzke AM, Doukas DG, Seiglie MP, Dulawa SC. (2011). Antidepressant response to chronic citalopram treatment in eight inbred mouse strains. Psychopharmacology (Berl) 213: 509-520
45. John CS, Currie PJ. (2012). N-arachidonoyl-serotonin in the basolateral amygdala increases anxiolytic behavior in the elevated plus maze. Behav Brain Res 233: 382-388
46. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M. (2009). Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89: 309-380
47. Karlsson RM, Choe JS, Cameron HA, Thorsell A, Crawley JN, Holmes A, et al. (2008). The neuropeptide Y Y1 receptor subtype is necessary for the anxiolytic-like effects of neuropeptide Y, but not the antidepressant-like effects of fluoxetine, in mice. Psychopharmacology (Berl) 195: 547-557
48. Karpova NN, Pickenhagen A, Lindholm J, Tiraboschi E, Kulesskaya N, Agustsdottir A, et al. (2012). Fear erasure in mice requires synergy between antidepressant drugs and extinction training. Science 334: 1731-1734
49. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, et al. (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19: 4544-4558
50. Lemtiri-Chlieh F, Levine ES. (2010). BDNF evokes release of endogenous cannabinoids at layer 2/3 inhibitory synapses in the neocortex. J Neurophysiol 104: 1923-1932
51. Mato S, Vidal R, Castro E, Diaz A, Pazos A, Valdizan EM. (2010). Long-term fluoxetine treatment modulates cannabinoid type 1 receptor-mediated inhibition of adenylyl cyclase in the rat prefrontal cortex through 5-hydroxytryptamine 1A receptordependent mechanisms. Mol Pharmacol 77: 424-434
52. Micale V, Cristino L, Tamburella A, Petrosino S, Leggio GM, Drago F, et al. (2009). Anxiolytic effects in mice of a dual blocker of fatty acid amide hydrolase and transient receptor potential vanilloid type-1 channels. Neuropsychopharmacology 34: 593-606
53. Micale V, Di Marzo V, Sulcova A, Wotjak CT, Drago F. (2013). Endocannabinoid system and mood disorders: priming a target for new therapies. Pharmacol Ther 138: 18-37
54. Milad MR, Quirk GJ. (2012). Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63: 129-151
55. Milne RJ, Goa KL. (1991). Citalopram. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic potential in depressive illness. Drugs 41: 450-477
56. Navarria A, Tamburella A, Iannotti FA, Micale V, Camillieri G, Gozzo L, et al. (2014). The dual blocker of FAAH/TRPV1 N-arachidonoylserotonin reverses the behavioral despair induced by stress in rats and modulates the HPA-axis. Pharmacol Res 87: 151-159
57. Neumeister A, Normandin MD, Pietrzak RH, Piomelli D, Zheng MQ, Gujarro-Anton A, et al. (2013). Elevated brain cannabinoid CB receptor availability in post-traumatic stress disorder: a positron emission tomography study. Mol Psychiatry 18: 1034-1040
58. Neumeister A, Seidel J, Ragen BJ, Pietrzak RH. (2015). Translational evidence for a role of endocannabinoids in the etiology and treatment of posttraumatic stress disorder. Psychoneuroendocrinology 51: 577-584
59. Norcross M, Mathur P, Enoch AJ, Karlsson RM, Brigman JL, Cameron HA, et al. (2008). Effects of adolescent fluoxetine treatment on fear-, anxiety-or stress-related behaviors in C57BL/6J or BALB/cJ mice. Psychopharmacology (Berl) 200: 413-424
60. Papini S, Sullivan GM, Hien DA, Shvil E, Neria Y. (2015). Toward a translational approach to targeting the endocannabinoid system in posttraumatic stress disorder: a critical review of preclinical research. Biol Psychol 104C: 8-18
61. Patel S, Kingsley PJ, Mackie K, Marnett LJ, Winder DG. (2009). Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala. Neuropsychopharmacology 34: 2699-2709
62. Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ. (2010). Induction of fear extinction with hippocampal-infralimbic BDNF. Science 328: 1288-1290
63. 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
64. Popova D, Agustsdottir A, Lindholm J, Mazulis U, Akamine Y, Castren E, et al. (2014). Combination of fluoxetine and extinction treatments forms a unique synaptic protein profile that correlates with long-term fear reduction in adult mice. Eur Neuropsychopharmacol 24: 1162-1174
65. Ramikie TS, Nyilas R, Bluett RJ, Gamble-George JC, Hartley ND, Mackie K, et al. (2014). Multiple mechanistically distinct modes of endocannabinoid mobilization at central amygdala glutamatergic synapses. Neuron 81: 1111-1125
66. Riddle MC, McKenna MC, Yoon YJ, Pattwell SS, Santos PM, Casey BJ, et al. (2013). Caloric restriction enhances fear extinction learning in mice. Neuropsychopharmacology 38: 930-937
67. Roozendaal B, McEwen BS, Chattarji S. (2009). Stress, memory and the amygdala. Nat Rev Neurosci 10: 423-433
68. Rose TM, Reilly CA, Deering-Rice CE, Brewster C. (2014). Inhibition of FAAH, TRPV1, and COX2 by NSAID-serotonin conjugates. Bioorg Med Chem Lett 24: 5695-5698
69. Sanchez C, Hyttel J. (1999). Comparison of the effects of antidepressants and their metabolites on reuptake of biogenic amines and on receptor binding. Cell Mol Neurobiol 19: 467-489
70. Shonesy BC, Bluett RJ, Ramikie TS, Báldi R, Hermanson DJ, Kingsley PJ, et al. (2014). Genetic disruption of 2-arachidonoylglycerol synthesis reveals a key role for endocannabinoid signaling in anxiety modulation. Cell Rep 9: 1644-1653
71. Singewald N, Schmuckermair C, Whittle N, Holmes A, Ressler KJ. (2015). Pharmacology of cognitive enhancers for exposure-based therapy of fear, anxiety and trauma-related disorders. Pharmacol Ther 149: 150-190
72. Spennato G, Zerbib C, Mondadori C, Garcia R. (2008). Fluoxetine protects hippocampal plasticity during conditioned fear stress and prevents fear learning potentiation. Psychopharmacology (Berl) 196: 583-589
73. Tovote P, Fadok JP, Luthi A. (2015). Neuronal circuits for fear and anxiety. Nat Rev Neurosci 16: 317-331
74. Trouche S, Sasaki JM, Tu T, Reijmers LG. (2013). Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses. Neuron 80: 1054-1065
75. Umathe SN, Manna SS, Jain NS. (2011). Involvement of endocannabinoids in antidepressant and anti-compulsive effect of fluoxetine in mice. Behav Brain Res 223: 125-134
76. Yoshida T, Uchigashima M, Yamasaki M, Katona I, Yamazaki M, Sakimura K, et al. (2011). Unique inhibitory synapse with particularly rich endocannabinoid signaling machinery on pyramidal neurons in basal amygdaloid nucleus. Proc Natl Acad Sci USA 108: 3059-3064
77. Zarate J, Churruca I, Echevarria E, Casis L, Lopez de Jesus M, Saenz del Burgo L, et al. (2008). Immunohistochemical localization of CB1 cannabinoid receptors in frontal cortex and related limbic areas in obese Zucker rats: effects of chronic fluoxetine treatment. Brain Res 1236: 57-72
78. Zhang G, Asgeirsdottir HN, Cohen SJ, Munchow AH, Barrera MP, Stackman RW Jr. (2013). Stimulation of serotonin 2A receptors facilitates consolidation and extinction of fear memory in C57BL/6J mice. Neuropharmacology 64: 403-413
79. Zhong P, Liu Y, Hu Y, Wang T, Zhao YP, Liu QS. (2015). BDNF interacts with endocannabinoids to regulate cocaine-induced synaptic plasticity in mouse midbrain dopamine neurons. J Neurosci 35: 4469-4481
80. Zhu PJ, Lovinger DM. (2005). Retrograde endocannabinoid signaling in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. J Neurosci 25: 6199-6207