Plasticity of presynaptic and postsynaptic serotonin 1A receptors in an animal model of epilepsy-associated depression

Neuropsychopharmacology

Volumn 36, Issue 6, 2011, Pages 1305-1316

  Pineda, Eduardo A ^a   Hensler, Julie G ^b   Sankar, Raman ^a   Shin, Don ^a   Burke, Teresa F ^b   Mazarati, Andréy M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

comorbidity; depression; dorsal raphe; epilepsy; hypothalamo pituitary adrenocortical axis; serotonin 1A receptors

Indexed keywords

CORTICOSTERONE; DIAZEPAM; MIFEPRISTONE; PHENYTOIN; SEROTONIN 1A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTORADIOGRAPHY; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DISEASE ASSOCIATION; DOWN REGULATION; EPILEPTIC STATE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT;

ANIMALS; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EPILEPSY; MALE; NEURONAL PLASTICITY; RATS; RATS, WISTAR; RECEPTOR, SEROTONIN, 5-HT1A; SYNAPTIC MEMBRANES;

EID: 79954587698     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2011.18     Document Type: Article

References (73)

1. Aghajanian GK, Sprouse JS, Sheldon P, Rasmussen K (1990). Electrophysiology of the central serotonin system: receptor subtypes and transducer mechanisms. Ann N Y Acad Sci 600: 93-103; discussion 103.
2. Bellido I, Hansson AC, Gomez-Luque AJ, Andbjer B, Agnati LF, Fuxe K (2004). Corticosterone strongly increases the affinity of dorsal raphe 5-HT1A receptors. Neuroreport 15: 1457-1459. (Pubitemid 38925242)
3. Bunin MA, Wightman RM (1998). Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J Neurosci 18: 4854-4860. (Pubitemid 28285394)
4. Cavalheiro EA, Naffah-Mazzacoratti MG, Mello LE, Leite JP (2006). The pilocarpine model of seizures. In: Pitkanen A, Schwartzk-roin PA, Moshe SL (eds). Models of Seizures and Epilepsy. Elsevier: Amsterdam. pp 433-448.
5. 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. (Pubitemid 24178788)
6. Chaouloff F (2000). Serotonin, stress and corticoids. J Psychopharmacol 14: 139-151. (Pubitemid 30389487)
7. Chaput Y, de Montigny C, Blier P (1986). Effects of a selective 5-HT reuptake blocker, citalopram, on the sensitivity of 5-HT autoreceptors: electrophysiological studies in the rat brain. Naunyn Schmiedebergs Arch Pharmacol 333: 342-348. (Pubitemid 16023193)
8. Clark RD (2008). Glucocorticoid receptor antagonists. Curr Top Med Chem 8: 813-838. (Pubitemid 351982568)
9. Connor TJ, Kelliher P, Shen Y, Harkin A, Kelly JP, Leonard BE (2000). Effect of subchronic antidepressant treatments on behavioral, neurochemical, and endocrine changes in the forced-swim test. Pharmacol Biochem Behav 65: 591-597. (Pubitemid 30182501)
10. D'Ambrosio R, Hakimian S, Stewart T, Verley DR, Fender JS, Eastman CL et al (2009). Functional definition of seizure provides new insight into post-traumatic epileptogenesis. Brain 132: 2805-2821.
11. De Kloet ER, Sybesma H, Reul HM (1986). Selective control by corticosterone of serotonin1 receptor capacity in raphe-hippo-campal system. Neuroendocrinology 42: 513-521. (Pubitemid 16130110)
12. Dinan T (2001). Novel approaches to the treatment of depression by modulating the hypothalamic-pituitary-adrenal axis. Hum Psychopharmacol 16: 89-93.
13. Djavadian RL (2004). Serotonin and neurogenesis in the hippo-campal dentate gyrus of adult mammals. Acta Neurobiol Exp (Wars) 64: 189-200. (Pubitemid 38649380)
14. Dube C, Richichi C, Bender RA, Chung G, Litt B, Baram TZ (2006). Temporal lobe epilepsy after experimental prolonged febrile seizures: prospective analysis. Brain 129: 911-922.
15. Dudek FE, Bertram EH (2010). Counterpoint to 'What is epileptic seizure' by D'Ambrosio and Miller. Epilepsy Curr 10: 91-94.
16. Finn DP, Marti O, Harbuz MS, Valles A, Belda X, Marquez C et al (2003). Behavioral, neuroendocrine and neurochemical effects of the imidazoline I2 receptor selective ligand BU224 in naive rats and rats exposed to the stress of the forced swim test. Psychopharmacology (Berl) 167: 195-202. (Pubitemid 36628162)
17. Gould E (1999). Serotonin and hippocampal neurogenesis. Neuropsychopharmacology 21: 46S-51S. (Pubitemid 29396470)
18. Gould E, Tanapat P (1999). Stress and hippocampal neurogenesis. Biol Psychiatry 46: 1472-1479.
19. Gozlan H, Thibault S, Laporte AM, Lima L, Hamon M (1995). The selective 5-HT1A antagonist radioligand [3H]WAY 100635 labels both G-protein-coupled and free 5-HT1A receptors in rat brain membranes. Eur J Pharmacol 288: 173-186.
20. Gregus A, Wintink AJ, Davis AC, Kalynchuk LE (2005). Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav Brain Res 156: 105-114. (Pubitemid 39330441)
21. 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. Br J Pharmacol 126: 1741-1750. (Pubitemid 29213091)
22. Hensler J, Durgam H (2001). Regulation of 5-HT(1A) receptor-stimulated [35S]-GtpgammaS binding as measured by quantitative autoradiography following chronic agonist administration. Br J Pharmacol 132: 605-611. (Pubitemid 32142373)
23. Hensler JG, Advani T, Monteggia LM (2007). Regulation of serotonin-1A receptor function in inducible brain-derived neurotrophic factor knockout mice after administration of corticosterone. Biol Psychiatry 62: 521-529. (Pubitemid 47284023)
24. Hensler JG, Vogt MA, Gass P (2010). Regulation of cortical and hippocampal 5-HT(1A) receptor function by corticosterone in GR+/- mice. Psychoneuroendocrinology 35: 469-474.
25. Heydendael W, Jacobson L (2010). Widespread hypothalamic-pituitary- adrenocortical axis-relevant and mood-relevant effects of chronic fluoxetine treatment on glucocorticoid receptor gene expression in mice. Eur J Neurosci 31: 892-902.
26. Hokfelt T, Xu ZQ, Shi TJ, Holmberg K, Zhang X (1998). Galanin in ascending systems: focus on coexistence with 5-hydroxytrypta-mine and noradrenaline. Ann N Y Acad Sci 863: 252-263. (Pubitemid 29047780)
27. Holsboer F (1998). Current theories of the pathophysiology of mood disorders. In: Montgomery S, Halbreich U (eds). Pharmacotherapy of Mood and Cognition. American Psychiatric Press: Washington, DC.
28. Jackson BP, Dietz SM, Wightman RM (1995). Fast-scan cyclic voltammetry of 5-hydroxytryptamine. Anal Chem 67: 1115-1120.
29. Giovacchini G, Toczek MT, Bonwetsch R, Bagic A, Lang L, Fraser C et al (2005). 5-HT 1A receptors are reduced in temporal lobe epilepsy after partial-volume correction. J Nucl Med 46: 1128-1135. (Pubitemid 43741074)
30. Jobe PC (2003). Common pathogenic mechanisms between depression and epilepsy: an experimental perspective. Epilepsy Behav 4(Suppl 3): S14-S24. (Pubitemid 37428233)
31. Jobe PC, Dailey JW, Wernicke JF (1999). A noradrenergic and serotonergic hypothesis of the linkage between epilepsy and affective disorders. Crit Rev Neirobiol 13: 317-356.
32. Johnson SA, Fournier NM, Kalynchuk LE (2006). Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor. Behav Brain Res 168: 280-288. (Pubitemid 43201945)
33. Judge SJ, Ingram CD, Gartside SE (2004). Moderate differences in circulating corticosterone alter receptor-mediated regulation of 5-hydroxytryptamine neuronal activity. J Psychopharmacol 18: 475-483. (Pubitemid 39665115)
34. Kanner AM (2009a). Depression and epilepsy: a review of multiple facets of their close relation. Neurol Clin 27: 865-880.
35. Kanner AM (2009b). Depression and epilepsy: do glucocorticoids and glutamate explain their relationship? Curr Neurol Neurosci Rep 9: 307-312.
36. Klink R, Robichaud M, Debonnel G (2002). Gender and gonadal status modulation of dorsal raphe nucleus serotonergic neurons. Part II. Regulatory mechanisms. Neuropharmacology 43: 1129-1138. (Pubitemid 36009366)
37. Kondziella D, Alvestad S, Vaaler A, Sonnewald U (2007). Which clinical and experimental data link temporal lobe epilepsy with depression? J Neurochem 103: 2136-2152. (Pubitemid 350173563)
38. Kornblum HI, Sankar R, Shin DH, Wasterlain CG, Gall CM (1997). Induction of brain derived neurotrophic factor mRNA by seizures in neonatal and juvenile rat brain. Mol Brain Res 44: 219-228. (Pubitemid 27100089)
39. LaFrance Jr WC, Kanner AM, Hermann B (2008). Psychiatric comorbidities in epilepsy. Int Rev Neurobiol 83: 347-383.
40. Lanfumey L, Mongeau R, Cohen-Salmon C, Hamon M (2008). Corticosteroid-serotonin interactions in the neurobiological mechanisms of stress-related disorders. Neurosci Biobehav Rev 32: 1174-1184.
41. Le Poul E, Laaris N, Doucet E, Laporte AM, Hamon M, Lanfumey L (1995). Early desensitization of somato-dendritic 5-HT1A autoreceptors in rats treated with fluoxetine or paroxetine. Naunyn Schmiedebergs Arch Pharmacol 352: 141-148.
42. Lemonde S, Turecki G, Bakish D, Du L, Hrdina PD, Bown CD et al (2003). Impaired repression at a 5-hydroxytryptamine 1A receptor gene polymorphism associated with major depression and suicide. J Neurosci 23: 8788-8799. (Pubitemid 37176660)
43. Lothe A, Didelot A, Hammers A, Costes N, Saoud M, Gilliam F et al (2008). Comorbidity between temporal lobe epilepsy and depression: a [18F]MPPF PET study. Brain 131: 2765-2782.
44. Lu X, Barr AM, Kinney JW, Sanna P, Conti B, Behrens MM et al (2005). A role for galanin in antidepressant actions with a focus on the dorsal raphe nucleus. Proc Natl Acad Sci USA 102: 874-879. (Pubitemid 40282758)
45. Man MS, Young AH, McAllister-Williams RH (2002). Corticoster-one modulation of somatodendritic 5-HT1A receptor function in mice. J Psychopharmacol 16: 245-252. (Pubitemid 34983081)
46. Manji HK, Drevets WC, Charney DS (2001). The cellular neurobiology of depression. Nat Med 7: 541-547. (Pubitemid 32448319)
47. Mann JJ, Arango V, Marzuk PM, Theccanat S, Reis DJ (1989). Evidence for the 5-HT hypothesis of suicide. A review of postmortem studies. Br J Psychiatry Suppl 7-14.
48. Martinez-Mota L, Contreras CM, Saavedra M (1999). Progesterone reduces immobility in rats forced to swim. Arch Med Res 30: 286-289. (Pubitemid 29486680)
49. Maudhuit C, Prevot E, Dangoumau L, Martin P, Hamon M, Adrien J (1997). Antidepressant treatment in helpless rats: effect on the electrophysiological activity of raphe dorsalis serotonergic neurons. Psychopharmacology (Berl) 130: 269-275. (Pubitemid 27170360)
50. Mazarati A, Siddarth P, Baldwin RA, Shin D, Caplan R, Sankar R (2008). Depression after status epilepticus: behavioural and biochemical deficits and effects of fluoxetine. Brain 131: 2071-2083.
51. Mazarati AM, Baldwin RA, Shinmei S, Sankar R (2005). In vivo interaction between serotonin and galanin receptors types 1 and 2 in the dorsal raphe: implication for limbic seizures. J Neurochem 95: 1495-1503. (Pubitemid 41779272)
52. Mazarati AM, Pineda E, Shin D, Tio D, Taylor AN, Sankar R (2010). Comorbidity between epilepsy and depression: role of hippocampal interleukin-1beta. Neurobiol Dis 37: 461-467.
53. Mazarati AM, Shin D, Kwon YS, Bragin A, Pineda E, Tio D et al (2009). Elevated plasma corticosterone level and depressive behavior in experimental temporal lobe epilepsy. Neurobiol Dis 34: 457-461.
54. Oitzl MS, Fluttert M, Sutanto W, de Kloet ER (1998). Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. Eur J Neurosci 10: 3759-3766. (Pubitemid 29073932)
55. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17: 3727-3738. (Pubitemid 27200597)
56. Parsey RV, Oquendo MA, Ogden RT, Olvet DM, Simpson N, Huang YY et al (2006). Altered serotonin 1A binding in major depression: a [carbonyl-C-11] WAY100635 positron emission tomography study. Biol Psychiatry 59: 106-113. (Pubitemid 43117499)
57. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates. Academic Press: San Diego.
58. Plotsky PM, Owens MJ, Nemeroff CB (1998). Psychoneuroendo-crinology of depression. Hypothalamic-pituitary-adrenal axis. Psychiatr Clin North Am 21: 293-307.
59. Pohorecky LA, Baumann MH, Benjamin D (2004). Effects of chronic social stress on neuroendocrine responsiveness to challenge with ethanol, dexamethasone and corticotropin-releasing hormone. Neuroendocrinology 80: 332-342. (Pubitemid 40470241)
60. Racine RJ (1972). Modification of seizure activity by electrical stimulation. II. Motor seizures. Electroencephalogr Clin Neurophysiol 32: 281-294.
61. Riad M, Garcia S, Watkins KC, Jodoin N, Doucet E, Langlois X et al (2000). Somatodendritic localization of 5-HT1A and preterminal axonal localization of 5-HT1B serotonin receptors in adult rat brain. J Comp Neurol 417: 181-194. (Pubitemid 30038263)
62. Robichaud M, Debonnel G (2005). Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J Neuroendocrinol 17: 179-185. (Pubitemid 40553017)
63. Rossi DV, Burke TF, McCasland M, Hensler JG (2008). Serotonin-1A receptor function in the dorsal raphe nucleus following chronic administration of the selective serotonin reuptake inhibitor sertraline. J Neurochem 105: 1091-1099. (Pubitemid 351590776)
64. Rossi DV, Valdez M, Gould GG, Hensler JG (2006). Chronic administration of venlafaxine fails to attenuate 5-HT1A receptor function at the level of receptor-G protein interaction. Int J Neuropsychopharmacol 9: 393-406. (Pubitemid 43979699)
65. Saavedra M, Contreras CM, Azamar-Arizmendi G, Hernandez-Lozano M (2006). Differential progesterone effects on defensive burying and forced swimming tests depending upon a gradual decrease or an abrupt suppression schedules. Pharmacol Biochem Behav 83: 130-135.
66. Sah R, Pritchard LM, Richtand NM, Ahlbrand R, Eaton K, Sallee FR et al (2005). Expression of the glucocorticoid-induced receptor mRNA in rat brain. Neuroscience 133: 281-292. (Pubitemid 40694177)
67. Sargent PA, Kjaer KH, Bench CJ, Rabiner EA, Messa C, Meyer J et al (2000). Brain serotonin1A receptor binding measured by positron emission tomography with [11C]WAY-100635: effects of depression and antidepressant treatment. Arch Gen Psychiatry 57: 174-180. (Pubitemid 30075269)
68. Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S (2005). Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 192: 348-356. (Pubitemid 40347259)
69. Schmidt-Kastner R, Humpel C, Wetmore C, Olson L (1996). Cellular hybridization for BDNF, trkB, and NGF mRNAs and BDNF-immunoreactivity in rat forebrain after pilocarpine-induced status epilepticus. Exp Brain Res 107: 331-347. (Pubitemid 26024967)
70. Sprouse JS, Aghajanian GK (1987). Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1: 3-9. (Pubitemid 17114243)
71. Wrona MZ, Dryhurst G (1987). Oxidation chemistry of 5-hydroxytryptamine. 1. Mechanism and products formed at micromolar concentrations. J Org Chem 52: 2817-2825.
72. Yu S, Holsboer F, Almeida OF (2008). Neuronal actions of glucocorticoids: focus on depression. J Steroid Biochem Mol Biol 108: 300-309. (Pubitemid 351179642)
73. Zobel A, Wellmer J, Schulze-Rauschenbach S, Pfeiffer U, Schnell S, Elger C et al (2004). Impairment of inhibitory control of the hypothalamic pituitary adrenocortical system in epilepsy. Eur Arch Psychiatry Clin Neurosci 254: 303-311. (Pubitemid 39312824)