Enhancement of cortical extracellular 5-HT by 5-HT1A and 5-HT2C receptor blockade restores the antidepressant-like effect of citalopram in non-responder mice

International Journal of Neuropsychopharmacology

Volumn 12, Issue 6, 2009, Pages 793-803

  Calcagno, Eleonora ^a   Guzzetti, Sara ^a   Canetta, Alessandro ^a   Fracasso, Claudia ^a   Caccia, Silvio ^a   Cervo, Luigi ^a   Invernizzi, Roberto W ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

5 HT1A receptors; 5 HT2C receptors; FST; Intracerebral microdialysis; SSRIs; TPH 2

Indexed keywords

6 CHLORO 5 METHYL 1 [[2 [(2 METHYL 3 PYRIDYL)OXY] 5 PYRIDYL]CARBAMOYL]INDOLINE; ANTIDEPRESSANT AGENT; CITALOPRAM; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; SEROTONIN 1A RECEPTOR; SEROTONIN 2C RECEPTOR; SEROTONIN UPTAKE INHIBITOR; AMINOPYRIDINE DERIVATIVE; INDOLE DERIVATIVE; PIPERAZINE DERIVATIVE; PYRIDINE DERIVATIVE; SEROTONIN; SEROTONIN ANTAGONIST;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG BRAIN LEVEL; DRUG EFFECT; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMOBILIZATION; MALE; MICRODIALYSIS; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; ANALYSIS OF VARIANCE; ANIMAL; BRAIN CORTEX; C57BL MOUSE; CYTOLOGY; DBA MOUSE; DRUG ANTAGONISM; DRUG INTERACTION; EXPLORATORY BEHAVIOR; EXTRACELLULAR FLUID; METABOLISM; METHODOLOGY;

AMINOPYRIDINES; ANALYSIS OF VARIANCE; ANIMALS; ANTIDEPRESSIVE AGENTS; CEREBRAL CORTEX; CITALOPRAM; DRUG INTERACTIONS; EXPLORATORY BEHAVIOR; EXTRACELLULAR FLUID; INDOLES; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICRODIALYSIS; PIPERAZINES; PYRIDINES; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTOR, SEROTONIN, 5-HT2C; SEROTONIN; SEROTONIN ANTAGONISTS;

EID: 68849105373     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145708009760     Document Type: Article

References (67)

1. Adell A, Celada P, Abellan MT, Artigas F (2002). Origin and functional role of the extracellular serotonin in the midbrain raphe nuclei. Brain Research Brain Research Reviews 39, 154-180.
2. + conductance. Brain Research 305, 181-185. Artigas F, Celada P, Laruelle M, Adell A (2001). How does pindolol improve antidepressant action? Trends in Pharmacological Sciences 22, 224-228.
3. Artigas F, Romero L, de Montigny C, Blier P (1996). Acceleration of the effect of selected antidepressant drugs in major depression by 5-HT1A antagonists. Trends in Neurosciences 19, 378-383.
4. Azmitia EC, Segal M (1978). An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. Journal of Comparative Neurology 179, 641-667.
5. Beck SG, Pan YZ, Akanwa AC, Kirby LG (2004). Median and dorsal raphe neurons are not electrophysiologically identical. Journal of Neurophysiology 91, 994-1005.
6. Beyer CE, Cremers TI (2008). Do selective serotonin reuptake inhibitors acutely increase frontal cortex levels of serotonin? European Journal of Pharmacology 580, 350-354.
7. Blier P, Serrano A, Scatton B (1990). Differential responsiveness of the rat dorsal and median raphe 5-HT systems to 5-HT1 receptor agonists and p-chloroamphetamine. Synapse 5, 120-133.
8. Boothman L, Raley J, Denk F, Hirani E, Sharp T (2006a). In vivo evidence that 5-HT(2C) receptors inhibit 5-HT neuronal activity via a GABAergic mechanism. British Journal of Pharmacology 149, 861-869.
9. Boothman LJ, Mitchell SN, Sharp T (2006b). Investigation of the SSRI augmentation properties of 5-HT(2) receptor antagonists using in vivo microdialysis. Neuropharmacology 50, 726-732.
10. Bortolozzi A, Amargos-Bosch M, Toth M, Artigas F, Adell A (2004). In vivo efflux of serotonin in the dorsal raphe nucleus of 5-HT1A receptor knockout mice. Journal of Neurochemistry 88, 1373-1379.
11. Calcagno E, Canetta A, Guzzetti S, Cervo L, Invernizzi RW (2007). Strain differences in basal and post-citalopram extracellular 5-HT in the mouse medial prefrontal cortex and dorsal hippocampus: relation with tryptophan hydroxylase-2 activity. Journal of Neurochemistry 103, 1111-1120.
12. Ceci A, Baschirotto A, Borsini F (1994). The inhibitory effect of 8-OH-DPAT on the firing activity of dorsal raphe serotoninergic neurons in rats is attenuated by lesion of the frontal cortex. Neuropharmacology 33, 709-713.
13. Celada P, Puig MV, Casanovas JM, Guillazo G, Artigas F (2001). Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: Involvement of serotonin-1A, GABA(A), and glutamate receptors. Journal of Neuroscience 21, 9917-9929.
14. Cervo L, Canetta A, Calcagno E, Burbassi S, Sacchetti G, Caccia S, Fracasso C, Albani D, Forloni G, Invernizzi RW (2005). Genotype-dependent activity of tryptophan hydroxylase-2 determines the response to citalopram in a mouse model of depression. Journal of Neuroscience 25, 8165-8172.
15. Cremers TI, Giorgetti M, Bosker FJ, Hogg S, Arnt J, Mork A, Honig G, Bogeso KP, Westerink BH, den Boer H, Wikstrom HV, Tecott LH (2004). Inactivation of 5-HT(2C) receptors potentiates consequences of serotonin reuptake blockade. Neuropsychopharmacology 29, 1782-1789.
16. Cremers TI, Rea K, Bosker FJ, Wikstrom HV, Hogg S, Mork A, Westerink BH (2007). Augmentation of SSRI effects on serotonin by 5-HT2C antagonists: mechanistic studies. Neuropsychopharmacology 32, 1550-1557.
17. Delgado PL, Charney DS, Price LH, Aghajanian GK, Landis H, Heninger GR (1990). Serotonin function and the mechanism of antidepressant action. Reversal of antidepressant-induced remission by rapid depletion of plasma tryptophan. Archives of General Psychiatry 47, 411-418.
18. Di Matteo V, Di Giovanni G, Di Mascio M, Esposito E (2000). Biochemical and electrophysiological evidence that RO 60-0175 inhibits mesolimbic dopaminergic function through serotonin(2C) receptors. Brain Research 865, 85-90.
19. Englander MT, Dulawa SC, Bhansali P, Schmauss C (2005). How stress and fluoxetine modulate serotonin 2C receptor pre-mRNA editing. Journal of Neuroscience 25, 648-651.
20. Forster EA, Cliffe IA, Bill DJ, Dover GM, Jones D, Reilly Y, Fletcher A (1995). A pharmacological profile of the selective silent 5-HT1A receptor antagonist WAY-100635. European Journal of Pharmacology 281, 81-88.
21. Franklin KBJ, Paxinos G (1997). The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press. Fuller RW (1994). Uptake inhibitors increase extracellular serotonin concentration measured by brain microdialysis. Life Sciences 55, 163-167.
22. Gallager DW, Aghajanian GK (1976). Effect of antipsychotic drugs on the firing of dorsal raphe cells. II. Reversal by picrotoxin. European Journal of Pharmacology 39, 357-364.
23. Gartside SE, Umbers V, Hajos M, Sharp T (1995). Interaction between a selective 5-HT1A receptor antagonist and an SSRI in vivo: effects on 5-HT cell firing and extracellular 5-HT. British Journal of Pharmacology 115, 1064-1070.
24. Grignaschi G, Invernizzi RW, Fanelli E, Fracasso C, Caccia S, Samanin R (1998). Citalopram-induced hypophagia is enhanced by blockade of 5-HT(1A) receptors: role of 5-HT(2C) receptors. British Journal of Pharmacology 124, 1781-1787.
25. Guilloux JP, David DJ, Guiard BP, Chenu F, Reperant C, Toth M, Bourin M, Gardier AM (2006). Blockade of 5-HT1A receptors by (¡)-pindolol potentiates cortical 5-HT outflow, but not antidepressant-like activity of paroxetine: microdialysis and behavioral approaches in 5-HT1A receptor knockout mice. Neuropsychopharmacology 31, 2162-2172.
26. Gurevich I, Tamir H, Arango V, Dwork AJ, Mann JJ, Schmauss C (2002). Altered editing of serotonin 2C receptor pre-mRNA in the prefrontal cortex of depressed suicide victims. Neuron 34, 349-356.
27. Guzzetti S, Calcagno E, Canetta A, Sacchetti G, Fracasso C, Caccia S, Cervo L, Invernizzi RW (2008). Strain differences in paroxetine-induced reduction of immobility time in the forced swimming test in mice: role of serotonin. European Journal of Pharmacology 594, 117-124.
28. Hajos M, Hajos-Korcsok E, Sharp T (1999). Role of the medial prefrontal cortex in 5-HT1A receptor-induced inhibition of 5-HT neuronal activity in the rat. British Journal of Pharmacology 126, 1741-1750.
29. Hervas I, Queiroz CM, Adell A, Artigas F (2000). Role of uptake inhibition and autoreceptor activation in the control of 5-HT release in the frontal cortex and dorsal hippocampus of the rat. British Journal of Pharmacology 130, 160-166.
30. Hjorth S (1993). Serotonin 5-HT1A autoreceptor blockade potentiates the ability of the 5-HT reuptake inhibitor citalopram to increase nerve terminal output of 5-HT in vivo: a microdialysis study. Journal of Neurochemistry 60, 776-779.
31. Hjorth S, Auerbach SB (1994). Further evidence for the importance of 5-HT1A autoreceptors in the action of selective serotonin reuptake inhibitors. European Journal of Pharmacology 260, 251-255.
32. 3H]imipramine localization and relationship to serotonin transporter. Journal of Pharmacology and Experimental Therapeutics 252, 410-418.
33. Invernizzi R, Belli S, Samanin R (1992). Citalopram's ability to increase the extracellular concentrations of serotonin in the dorsal raphe prevents the drug's effect in the frontal cortex. Brain Research 584, 322-324.
34. Invernizzi R, Bramante M, Samanin R (1995). Extracellular concentrations of serotonin in the dorsal hippocampus after acute and chronic treatment with citalopram. Brain Research 696, 62-66.
35. Invernizzi R, Bramante M, Samanin R (1996). Role of 5-HT1A receptors in the effects of acute chronic fluoxetine on extracellular serotonin in the frontal cortex. Pharmacology Biochemistry and Behavior 54, 143-147.
36. Invernizzi R, Carli M, Di Clemente A, Samanin R (1991). Administration of 8-hydroxy-2-(Di-n-propylamino)tetralin in raphe nuclei dorsalis and medianus reduces serotonin synthesis in the rat brain: differences in potency and regional sensitivity. Journal of Neurochemistry 56, 243-247.
37. Invernizzi R, Velasco C, Bramante M, Longo A, Samanin R (1997). Effect of 5-HT1A receptor antagonists on citalopram-induced increase in extracellular serotonin in the frontal cortex, striatum and dorsal hippocampus. Neuropharmacology 36, 467-473.
38. Jacobs BL, Azmitia EC (1992). Structure and function of the brain serotonin system. Physiological Reviews 72, 165-229.
39. Jacobsen JP, Nielsen EO, Hummel R, Redrobe JP, Mirza N, Weikop P (2008). Insensitivity of NMRI mice to selective serotonin reuptake inhibitors in the tail suspension test can be reversed by co-treatment with 5-hydroxytryptophan. Psychopharmacology (Berlin) 199, 137-150.
40. Jans LA, Riedel WJ, Markus CR, Blokland A (2007). Serotonergic vulnerability and depression: assumptions, experimental evidence and implications. Molecular Psychiatry 12, 522-543.
41. Kennett GA, Lightowler S, de Biasi V, Stevens NC, Wood MD, Tulloch IF, Blackburn TP (1994). Effect of chronic administration of selective 5-hydroxytryptamine and noradrenaline uptake inhibitors on a putative index of 5-HT2C/2B receptor function. Neuropharmacology 33, 1581-1588.
42. Kennett GA, Wood MD, Bright F, Trail B, Riley G, Holland V, Avenell KY, Stean T, Upton N, Bromidge S, et al. (1997). SB 242084, a selective and brain penetrant 5-HT2C receptor antagonist. Neuropharmacology 36, 609-620.
43. Kosofsky BE, Molliver ME (1987). The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1, 153-168.
44. Lechin F, van der Dijs B, Hernandez-Adrian G (2006). Dorsal raphe vs. median raphe serotonergic antagonism. Anatomical, physiological, behavioral, neuroendocrinological, neuropharmacological and clinical evidences: relevance for neuropharmacological therapy. Progress in Neuropsychopharmacology and Biological Psychiatry 30, 565-585.
45. Liu R, Jolas T, Aghajanian G (2000). Serotonin 5-HT(2) receptors activate local GABA inhibitory inputs to serotonergic neurons of the dorsal raphe nucleus. Brain Research 873, 34-45.
46. Lorens SA, Guldberg HC (1974). Regional 5-hydroxytryptamine following selective midbrain raphe lesions in the rat. Brain Research 78, 45-56.
47. Miquel MC, Doucet E, Riad M, Adrien J, Verge D, Hamon M (1992). Effect of the selective lesion of serotoninergic neurons on the regional distribution of 5-HT1A receptor mRNA in the rat brain. Brain Research Molecular Brain Research 14, 357-362.
48. Moser PC, Sanger DJ (1999). 5-HT1A receptor antagonists neither potentiate nor inhibit the effects of fluoxetine and befloxatone in the forced swim test in rats. European Journal of Pharmacology 372, 127-134.
49. O'Neill MF, Conway MW (2001). Role of 5-HT(1A) and 5-HT(1B) receptors in the mediation of behavior in the forced swim test in mice. Neuropsychopharmacology 24, 391-398.
50. Pazos A, Cortes R, Palacios JM (1985). Quantitative autoradiographic mapping of serotonin receptors in the rat brain. II. Serotonin-2 receptors. Brain Research 346, 231-249.
51. ++ currents in central 5-HT-containing neurons: 5-HT1A receptors may play a role in hallucinogenesis. Journal of Pharmacology and Experimental Therapeutics 269, 1160-1165.
52. Pineyro G, Blier P (1999). Autoregulation of serotonin neurons: role in antidepressant drug action. Pharmacological Reviews 51, 533-591.
53. Porsolt RD, Bertin A, Jalfre M (1977). Behavioral despair in mice: a primary screening test for antidepressants. Archives Internationales de Pharmacodynamie et de Therapie 229, 327-336.
54. Pozzi L, Acconcia S, Ceglia I, Invernizzi RW, Samanin R (2002). Stimulation of 5-hydroxytryptamine (5-HT(2C)) receptors in the ventrotegmental area inhibits stress-induced but not basal dopamine release in the rat prefrontal cortex. Journal of Neurochemistry 82, 93-100.
55. Quérée P, Sharp T (2006). Electrophysiological evidence for 5-HT2C receptor-mediated control of 5-HT cell firing in the anaesthetised rat. Proceedings of the British Pharmacological Society (http://www.pA2online.org/ abstracts/Vol4Issue2abst050P.pdf). Accessed 2 December 2008.
56. Robinson TE, Whishaw IQ (1988). Normalization of extracellular dopamine in striatum following recovery from a partial unilateral 6-OHDA lesion of the substantia nigra: a microdialysis study in freely moving rats. Brain Research 450, 209-224.
57. Romero L, Artigas F (1997). Preferential potentiation of the effects of serotonin uptake inhibitors by 5-HT1A receptor antagonists in the dorsal raphe pathway: role of somatodendritic autoreceptors. Journal of Neurochemistry 68, 2593-2603.
58. Serrats J, Mengod G, Cortes R (2005). Expression of serotonin 5-HT2C receptors in GABAergic cells of the anterior raphe nuclei. Journal of Chemical Neuroanatomy 29, 83-91. Sharp T, Boothman L, Raley J, Quérée P (2007). Important messages in the 'post': recent discoveries in 5-HT neurone feedback control. Trends in Pharmacological Sciences 28, 629-636.
59. Shopsin B, Friedman E, Gershon S (1976). Parachlorophenylalanine reversal of tranylcypromine effects in depressed patients. Archives of General Psychiatry 33, 811-819.
60. Sinton CM, Fallon SL (1988). Electrophysiological evidence for a functional differentiation between subtypes of the 5-HT1 receptor. European Journal of Pharmacology 157, 173-181.
61. Tatarczynska E, Klodzinska A, Stachowicz K, Chojnacka-Wojcik E (2004). Effect of combined administration of 5-HT1A or 5-HT1B/1D receptor antagonists and antidepressants in the forced swimming test. European Journal of Pharmacology 487, 133-142.
62. Trillat AC, Malagie I, Mathe-Allainmat M, Anmela MC, Jacquot C, Langlois M, Gardier AM (1998). Effects of WAY 100635 and (-)-5-Me-8-OH-DPAT, a novel 5-HT1A receptor antagonist, on 8-OH-DPAT responses. European Journal of Pharmacology 347, 41-49.
63. Walther DJ, Peter JU, Bashammakh S, Hortnagl H, Voits M, Fink H, Bader M (2003). Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299, 76.
64. Wang QP, Ochiai H, Nakai Y (1992). GABAergic innervation of serotonergic neurons in the dorsal raphe nucleus of the rat studied by electron microscopy double immunostaining. Brain Research Bulletin 29, 943-948.
65. Weissmann-Nanopoulos D, Mach E, Magre J, Demassey Y, Pujol J-F (1985). Evidence for the localization of 5-HT1A binding sites on serotonin containing neurons in the raphe dorsalis and raphe centralis nuclei of the rat brain. Neurochemistry International 7, 1061-1072.
66. Zhang X, Beaulieu JM, Sotnikova TD, Gainetdinov RR, Caron MG (2004). Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 305, 217.
67. Zhang X, Gainetdinov RR, Beaulieu JM, Sotnikova TD, Burch LH, Williams RB, Schwartz DA, Krishnan KR, Caron MG (2005). Loss-of-function mutation in tryptophan hydroxylase-2 identified in unipolar major depression. Neuron 45, 11-16.