Role(s) of the 5-HT2C receptor in the development of maximal dentate activation in the hippocampus of anesthetized rats

CNS Neuroscience and Therapeutics

Volumn 20, Issue 7, 2014, Pages 651-661

  Orban, Gergely ^a,b   Bombardi, Cristiano ^c   Marino Gammazza, Antonella ^a,b   Colangeli, Roberto ^d   Pierucci, Massimo ^b,d   Pomara, Cristoforo ^d,e   Pessia, Mauro ^f   Bucchieri, Fabio ^a,b   Arcangelo, Benigno ^a   Smolders, Ilse ^g   De Deurwaerdère, Philippe ^h   Di Giovanni, Giuseppe ^b,d,i  

^a UNIVERSITY OF PALERMO   (Italy)

^b Istituto Euro mediterraneo di Scienza e Tecnologia (IEMeST)   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d UNIVERSITY OF MALTA   (Malta)

^e UNIVERSITY OF FOGGIA   (Italy)

^f UNIVERSITY OF PERUGIA   (Italy)

^g VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^h UNIVERSITÉ DE BORDEAUX   (France)

ⁱ CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Dentate gyrus; Depression; GABA; Memory; Serotonin receptors; Temporal lobe epilepsy

Indexed keywords

(3 CHLOROPHENYL)PIPERAZINE; 2 (6 CHLORO 5 FLUORO 1 INDOLYL) 1 METHYLETHYLAMINE; 6 CHLORO 5 METHYL 1 [[2 [(2 METHYL 3 PYRIDYL)OXY] 5 PYRIDYL]CARBAMOYL]INDOLINE; LORCASERIN; SEROTONIN 2C AGONIST; SEROTONIN 2C RECEPTOR; URETHAN; INTRAVENOUS ANESTHETIC AGENT; SEROTONIN 2 AGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPLEX PARTIAL SEIZURE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTOGENESIS; GABAERGIC SYSTEM; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTRACTABLE EPILEPSY; MALE; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; PROTEIN FUNCTION; TEMPORAL LOBE EPILEPSY; WESTERN BLOTTING; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; EPILEPSY, TEMPORAL LOBE; METABOLISM; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANESTHETICS, INTRAVENOUS; ANIMALS; DENTATE GYRUS; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT2C; SEROTONIN 5-HT2 RECEPTOR AGONISTS;

EID: 84902478392     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/cns.12285     Document Type: Article

References (58)

1. Di Giovanni G, Esposito E, Di Matteo V, eds. 5-HT2C Receptors in the Pathophysiology of CNS Disease. The Receptors. New York: Springer/Humana Press, 2011; 1-557.
2. Higgins GA, Sellers EM, Fletcher PJ. From obesity to substance abuse: therapeutic opportunities for 5-HT2C receptor agonists. Trends Pharmacol Sci 2013;34:560-570.
3. De Deurwaerdere P, Lagiere M, Bosc M, Navailles S. Multiple controls exerted by 5-HT2C receptors upon basal ganglia function: from physiology to pathophysiology. Exp Brain Res 2013;230:477-511.
4. Hoyer D, Hannon JP, Martin GR. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 2002;71:533-554.
5. Di Giovanni G, Di Matteo V, Pierucci M, Benigno A, Esposito E. Central serotonin2C receptor: from physiology to pathology. Curr Top Med Chem 2006;6:1909-1925.
6. Navailles S, Lagiere M, Guthrie M, De Deurwaerdere P. Serotonin2c receptor constitutive activity: in vivo direct and indirect evidence and functional significance. Cent Nerv Syst Agents Med Chem 2013;13:98-107.
7. Crunelli V, Di Giovanni G. Monoamine modulation of tonic GABAA inhibition. Rev Neurosci 2014;00:1-12.
8. Jakus R, Bagdy G. The Role of 5-HT2C Receptor in Epilepsy. In: Di Giovanni G, Esposito E, Di Matteo V, editors. 5-HT2C Receptors in the Pathophysiology of CNS Disease. New York: Humana Press, 2011; 429-444.
9. Isaac M. Serotonergic 5-HT2C receptors as a potential therapeutic target for the design antiepileptic drugs. Curr Top Med Chem 2005;5:59-67.
10. Pompeiano M, Palacios JM, Mengod G. Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res Mol Brain Res 1994;23:163-178.
11. Abramowski D, Rigo M, Duc D, Hoyer D, Staufenbiel M. Localization of the 5-hydroxytryptamine2C receptor protein in human and rat brain using specific antisera. Neuropharmacology 1995;34:1635-1645.
12. Li QH, Nakadate K, Tanaka-Nakadate S, Nakatsuka D, Cui YL, Watanabe Y. Unique expression patterns of 5-HT2A and 5-HT2C receptors in the rat brain during postnatal development: western blot and immunohistochemical analyses. J Comp Neurol 2004;469:128-140.
13. Clemett DA, Punhani T, Duxon MS, Blackburn TP, Fone KCF. Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS. Neuropharmacology 2000;39:123-132.
14. Tecott LH, Logue SF, Wehner JM, Kauer JA. Perturbed dentate gyrus function in serotonin 5-HT2C receptor mutant mice. Proc Natl Acad Sci USA 1998;95:15026-15031.
15. Sorman E, Wang D, Hajos M, Kocsis B. Control of hippocampal theta rhythm by serotonin: role of 5-HT2c receptors. Neuropharmacology 2011;61:489-494.
16. Brennan TJ, Seeley WW, Kilgard M, Schreiner CE, Tecott LH. Sound-induced seizures in serotonin 5-HT2c receptor mutant mice. Nat Genet 1997;16:387-390.
17. Tecott LH, Sun LM, Akana SF, et al. Eating disorder and epilepsy in mice lacking 5-HT2c serotonin receptors. Nature 1995;374:542-546.
18. Krishnakumar A, Nandhu MS, Paulose CS. Upregulation of 5-HT2C receptors in hippocampus of pilocarpine-induced epileptic rats: antagonism by Bacopa monnieri. Epilepsy Behav 2009;16:225-230.
19. Bagdy G, Kecskemeti V, Riba P, Jakus R. Serotonin and epilepsy. J Neurochem 2007;100:857-873.
20. Orban G, Pierucci M, Benigno A, et al. High dose of 8-OH-DPAT decreases maximal dentate gyrus activation and facilitates granular cell plasticity in vivo. Exp Brain Res 2013;230:441-451.
21. Stringer JL, Lothman EW. Maximal dentate activation: a tool to screen compounds for activity against limbic seizures. Epilepsy Res 1990;5:169-176.
22. Di Giovanni G, García I, Colangeli R, et al. N-(furan-2-ylmethyl)-N-methylprop-2-yn-1-amine (F2MPA): a Potential Cognitive Enhancer with MAO Inhibitor Properties. CNS Neurosci Ther 2014;???:???-???. In Press.
23. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York: Academic Press, 2007.
24. Stringer JL, Williamson JM, Lothman EW. Induction of paroxysmal discharges in the dentate gyrus: frequency dependence and relationship to afterdischarge production. J Neurophysiol 1989;62:126-135.
25. Hoyer D. Functional correlates of serotonin 5-HT1 recognition sites. J Recept Res 1988;8:59-81.
26. Hamik A, Peroutka SJ. 1-(m-chlorophenyl)piperazine (mCPP) interactions with neurotransmitter receptors in the human brain. Biol Psychiatry 1989;25:569-575.
27. Chan EW, He Y, Chui CS, Wong AY, Lau WC, Wong IC. Efficacy and safety of lorcaserin in obese adults: a meta-analysis of 1-year randomized controlled trials (RCTs) and narrative review on short-term RCTs. Obes Rev 2013;14:383-392.
28. Martin JR, Bos M, Jenck F, et al. 5-HT2C receptor agonists: pharmacological characteristics and therapeutic potential. J Pharmacol Exp Ther 1998;286:913-924.
29. Di Matteo V, Di Giovanni G, Esposito E. SB 242084: a Selective 5-HT2C Receptor Antagonist. CNS Drug Rev 2000;6:195-205.
30. Beyeler A, Kadiri N, Navailles S, et al. Stimulation of serotonin2C receptors elicits abnormal oral movements by acting on pathways other than the sensorimotor one in the rat basal ganglia. Neuroscience 2010;169:158-170.
31. Di Matteo V, Pierucci M, Esposito E. Selective stimulation of serotonin2C receptors blocks the enhancement of striatal and accumbal dopamine release induced by nicotine administration. J Neurochem 2004;89:418-429.
32. Invernizzi RW, Pierucci M, Calcagno E, et al. Selective activation of 5-HT(2C) receptors stimulates GABA-ergic function in the rat substantia nigra pars reticulata: a combined in vivo electrophysiological and neurochemical study. Neuroscience 2007;144:1523-1535.
33. Navailles S, Lagiere M, Le Moine C, De Deurwaerdere P. Role of 5-HT2C receptors in the enhancement of c-Fos expression induced by a 5-HT2B/2C inverse agonist and 5-HT 2 agonists in the rat basal ganglia. Exp Brain Res 2013;230:525-535.
34. Di Giovanni G, Di Matteo V, Pierucci M, Esposito E. Serotonin-dopamine interaction: electrophysiological evidence. Prog Brain Res, 2008; 172:45-71.
35. Di Matteo V, Di Giovanni G, Pierucci M, Esposito E. Serotonin control of central dopaminergic function: focus on in vivo microdialysis studies. Prog Brain Res 2008;172:7-44.
36. White HS. Animal models of epileptogenesis. Neurology 2002;59(9 Suppl 5):S7-S14.
37. Loscher W. Strategies for antiepileptogenesis: Antiepileptic drugs versus novel approaches evaluated in post-status epilepticus models of temporal lobe epilepsy, 2012.
38. De Deurwaerdere P, Navailles S, Berg KA, Clarke WP, Spampinato U. Constitutive activity of the serotonin2C receptor inhibits in vivo dopamine release in the rat striatum and nucleus accumbens. J Neurosci 2004;24:3235-3241.
39. Upton N, Stean T, Middlemiss D, Blackburn T, Kennett G. Studies on the role of 5-HT2C and 5-HT2B receptors in regulating generalised seizure threshold in rodents. Eur J Pharmacol 1998;359:33-40.
40. Martinez A, Finegersh A, Cannon DM, et al. The 5-HT1A receptor and 5-HT transporter in temporal lobe epilepsy. Neurology 2013;80:1465-1471.
41. Thomsen WJ, Grottick AJ, Menzaghi F, et al. Lorcaserin, a novel selective human 5-hydroxytryptamine2C agonist: in vitro and in vivo pharmacological characterization. J Pharmacol Exp Ther 2008;325:577-587.
42. Dalton GL, Lee MD, Kennett GA, Dourish CT, Clifton PG. mCPP-induced hyperactivity in 5-HT2C receptor mutant mice is mediated by activation of multiple 5-HT receptor subtypes. Neuropharmacology 2004;46:663-671.
43. Higgins GA, Fletcher PJ. Serotonin and drug reward: focus on 5-HT2C receptors. Eur J Pharmacol 2003;480:151-162.
44. Navailles S, Lagiere M, Roumegous A, et al. Serotonin2C ligands exhibiting full negative and positive intrinsic activity elicit purposeless oral movements in rats: distinct effects of agonists and inverse agonists in a rat model of Parkinson's disease. Int J Neuropsychopharmacol 2013;16:593-606.
45. Damjanoska KJ, Muma NA, Zhang Y, et al. Neuroendocrine evidence that (S)-2-(chloro-5-fluoro-indol- l-yl)-1-methylethylamine fumarate (Ro 60-0175) is not a selective 5-hydroxytryptamine(2C) receptor agonist. J Pharmacol Exp Ther 2003;304:1209-1216.
46. Aguiar CC, Almeida AB, Araujo PV, et al. Anticonvulsant effects of agomelatine in mice. Epilepsy Behav 2012;24:324-328.
47. O'Dell LE, Kreifeldt MJ, George FR, Ritz MC. Serotonin(2C) receptors appear to mediate genetic sensitivity to cocaine-induced convulsions. Psychopharmacology 1999;146:313-319.
48. O'Dell LE, Kreifeldt MJ, George FR, Ritz MC. The role of serotonin(2) receptors in mediating cocaine-induced convulsions. Pharmacol Biochem Behav 2000;65:677-681.
49. Shirasaka Y, Wasterlain CG. The effect of urethane anesthesia on evoked potentials in dentate gyrus. Eur J Pharmacol 1995;282:11-17.
50. Stringer JL, Lothman EW. Use of maximal dentate activation to study the effect of drugs on kindling and kindled responses. Epilepsy Res 1990;6:180-186.
51. Bough KJ, Schwartzkroin PA, Rho JM. Calorie restriction and ketogenic diet diminish neuronal excitability in rat dentate gyrus in vivo. Epilepsia 2003;44:752-760.
52. Stringer JL, Agarwal KS, Dure LS. Is cell death necessary for hippocampal mossy fiber sprouting? Epilepsy Res 1997;27:67-76.
53. Mengod G. Serotonin 5-HT2C Receptors: Chemical Neuronatomy in the Mammalian Brain. In: Di Giovanni G, Esposito E, Di Matteo V, editors. 5-HT2C Receptors in the Pathophysiology of CNS Disease. New York: Humana Press, 2011; 17-27.
54. Sloviter RS, Bumanglag AV. Defining "epileptogenesis" and identifying "antiepileptogenic targets" in animal models of acquired temporal lobe epilepsy is not as simple as it might seem. Neuropharmacology 2013;69:3-15.
55. Sloviter RS, Damiano BP. Sustained electrical stimulation of the perforant path duplicates kainate-induced electrophysiological effects and hippocampal damage in rats. Neurosci Lett 1981;24:279-284.
56. Stringer JL. Repeated seizures increase GFAP and vimentin in the hippocampus. Brain Res 1996;717:147-153.
57. Di Giovanni G, De Deurwaerdere P, Di Mascio M, Di Matteo V, Esposito E, Spampinato U. Selective blockade of serotonin-2C/2B receptors enhances mesolimbic and mesostriatal dopaminergic function: a combined in vivo electrophysiological and microdialysis study. Neuroscience 1999;91:587-597.
58. Shen RY, Andrade R. 5-Hydroxytryptamine2 receptor facilitates GABAergic neurotransmission in rat hippocampus. J Pharmacol Exp Ther 1998;285:805-812.