Abstract
Rationale
There is a significant delay in the clinical response of antidepressant drugs, and antidepressant treatments produce side effects.
Objective
We examined the relationship between 17β-estradiol and topiramate in ovariectomized Wistar rats submitted to the forced swimming test (FST).
Methods
Topiramate was administered alone or combined with 17β-estradiol to ovariectomized rats submitted to the FST.
Results
Topiramate (20 mg/kg, P < 0.05; 30 mg/kg, P < 0.05) reduced immobility by increasing swimming; these effects were antagonized by finasteride (50 mg/kg). In interaction experiments, topiramate (10 mg/kg) plus 17β-estradiol (5 micrograms per rat; P < 0.05) reduced immobility by increasing swimming behavior. Besides, 17β-estradiol (2.5 micrograms per rat) shortened the onset of the antidepressant-like effects of topiramate (P < 0.05). In the open field test, topiramate alone or combined with 17β-estradiol (P < 0.05) reduced locomotion.
Conclusions
Topiramate alone or combined with 17β-estradiol produced antidepressant-like actions; and 17β-estradiol shortened the onset of the antidepressant-like effects of topiramate.
Similar content being viewed by others
References
Arnone D (2005) Review of the use of topiramate for treatment of psychiatric disorders. Ann Gen Psychiatr 4:5
Artigas F, Perez V, Alvarez E (1994) Pindolol induces a rapid improvement of depressed patients treated with serotonin reuptake inhibitors. Arch Gen Psychiatry 51:248–251
Bao A, Ji Y, Van Someren E, Hofman MA, Liu R, Zhou J (2004) Diurnal rhythms of free estradiol and cortisol during the normal menstrual cycle in women with major depression. Horm Behav 45:93–102
Barros HMT, Ferigolo M (1998) Ethopharmacology of imipramine in the forced-swimming test: gender differences. Neurosci Biobehav Rev 23:279–286
Bauer B, Bschor T, Kunz D, Berghöfer A, Ströhle S, Müller-Oerlinghausen B (2000) Double-blind, placebo-controlled trial of the use of lithium to augment antidepressant medication in continuation treatment of unipolar major depression. Am J Psychiatry 157:1429–1435
Bellido I, Gomez-Luque A, Garcia-Carrera P, Rius F, Sanchez de la Cuesta F (2003) Female rats show an increased sensibility to the forced swim test depressive-like stimulus in the hippocampus and frontal cortex 5-HT1A receptors. Neurosci Lett 350:145–148
Bernardi F, Stomati M, Luisi S, Pieri M, Labrie F, Genazzani A (2002) Effects of the new generation selective estrogen receptor modulator EM-652 and oral administration of estradiol valerate on circulating, brain, and adrenal β-endorphin and allopregnanolone levels in intact fertile and ovariectomized rats. Fertil Steril 77:1018–1027
Borsini F, Meli A (1988) Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology 94:147–160
Bourin M, Chenu F, Hascoët M (2009) The role of sodium channels in the mechanism of action of antidepressants and mood stabilizers. Curr Drug Targets 10:1052–1060
Brotto L, Barr A, Gorzalka B (2000) Sex differences in forced-swim and open-field test behaviours after chronic administration of melatonin. Eur J Pharmacol 402:87–93
Campbell T, Lin S, DeVries C, Lambert K (2003) Coping strategies in male and female rats exposed to multiple stressors. Physiol Behav 78:495–504
Castro E, Díaz A, Rodriguez-Gaztelumendi A, Del Olmo E, Pazos A (2008) WAY100635 prevents the changes induced by fluoxetine upon the 5-HT1A receptor functionality. Neuropharmacology 55:1391–1396
Chenu F, Guiard BP, Bourin M, Gardier AM (2006) Antidepressant-like activity of selective serotonin reuptake inhibitors combined with a NK1 receptor antagonist in the mouse forced swimming test. Behav Brain Res 172:256–263
Cipriani A, Barbui C, Salanti G, Rendell J, Brown R, Stockton S, Purgato M, Spineli L, Goodwin G, Geddes J (2011) Comparative efficacy and acceptability of antimanic drugs in acute mania: a multiple-treatments meta-analysis. Lancet 378:1306–1315
Contreras CM, Martínez-Mota L, Savedra M (1998) Desmethylimipramine restricts estral cycle oscillations in swimming. Prog Neuro-Psychopharmacol Biol Psychiatry 22:1121–1128
Dalla C, Antoniou K, Kokras N, Drossopoulou G, Papathanasiou G, Bekris S, Daskas S, Papadopoulou-Daifoti Z (2008) Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiol Behav 93:595–605
Dhir A, Kulkarni SK (2008) Antidepressant-like effect of 17beta-estradiol: involvement of dopaminergic, serotonergic, and (or) sigma-1 receptor systems. Can J Physiol Pharmacol 86:726–735
Ebert D, Jaspert A, Murata H, Kaschka WP (1995) Initial lithium augmentation improves the antidepressant effects of standard TCA treatment in nonresistant depressed patients. Psychopharmacology 118:223–225
Estrada-Camarena E, Fernandez-Guasti A, Lopez-Rubalcava L (2003) Antidepressant-like effect of different estrogenic compounds in the forced swimming test. Neuropsychopharmacology 28:830–838
Estrada-Camarena E, Fernández-Guasti A, López-Rubalcava C (2004) Interaction between estrogens and antidepressants in the FST in rats. Psychopharmacology 173:139–145
Estrada-Camarena E, Fernández Guasti A, López-Rubalcava C (2006) Participation of the 5-HT1A receptors in the antidepressant-like action of estrogens in the forced swimming test. Neuropsychopharmacology 31:247–255
Estrada-Camarena E, Vega-Rivera NM, Berlanga C, Fernández-Guasti A (2008) Reduction in the latency of action of antidepressants by 17 β-estradiol in the forced swimming test. Psychopharmacology 201:351–360
Farook J, Lewis B, Littleton J, Barron S (2009) Topiramate attenuates the stress-induced increase in alcohol consumption and preference in male C57BL/6 J mice. Physiol Behav 96:189–193
Frisone DF, Frye CA, Zimmerberg B (2002) Social isolation stress during the third week of life has age-dependent effects on spatial learning in rats. Behav Brain Res 128:153–160
Frye C, Walf A (2002) Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav 41:306–315
Gouveia A Jr, Afonseca TL, Maximino C, Dominguez R, Morato S (2008) Influence of gender and estrous cycle in the forced swim test in rats. Psychol Neurosci 1:191–197
Grosso S, Blardi P, Battaglini M, Franzoni E, De Lalla A, Mostardini R, Balestri P (2008) Topiramate effects on plasma serotonin levels in children with epilepsy. Epilepsy Res 81:148–154
Gutiérrez A, Contreras CM (2009) Stressors can affect immobility time and response to imipramine in the rat forced swim test. Pharmacol Biochem Behav 91:542–548
Hargreaves G, McGregor I (2007) Topiramate moderately reduces the motivation to consume alcohol and has a marked antidepressant effect in rats. Alcohol Clin Exp Res 31:1900–1907
Holsboer F (2001) Prospects for antidepressant drug discovery. Biol Psychol 57:47–65
Holsboer F, Lauer CJ, Schreiber W, Krieg JC (1995) Altered hypothalamic–pituitary–adrenocortical regulation in healthy subjects at high familial risk for affective disorders. Neuroendocrinology 62:340–347
Husum H, Van Kammen D, Termeer E, Bolwig G, Mathé A (2003) Topiramate normalizes hippocampal NPY-LI in flinders sensitive line ‘depressed’ rats and upregulates NPY, galanin, and CRH-LI in the hypothalamus: implications for mood-stabilizing and weight loss-inducing effects. Neuropsychopharmacology 28:1292–1299
IMS (2000) (Information Management Systems) National Disease Therapeutic Index (NDTI) Survey, December, 2000. Plymouth Meeting, PA: IMS Health
Kornstein SG, Schneider RK (2001) Clinical features of treatment-resistant depression. J Clin Psychiatry 62:18–25
Kow LM, Devidze N, Pataky S, Shibuya I, Pfaff DW (2006) Acute estradiol application increases inward and decreases outward whole-cell currents of neurons in rat hypothalamic ventromedial nucleus. Brain Res 1116:1–11
Lam RW, Wan DD, Cohen NL, Kennedy SH (2002) Combining antidepressants for treatment-resistant depression: a review. J Clin Psychiatry 63:685–693
Lenzi E, Pluchino N, Begliuomini S, Casarosa E, Merlini S, Giannini A, Luisi M, Kumar N, Sitruk-Ware R, Genazzani A (2009) Central modifications of allopregnanolone and β-endorphin following subcutaneous administration of nestorone. J Steroid Biochem Mol Biol 116:15–20
Lucki I (1997) The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 8:523–532
Martínez-Mota L, Estrada-Camarena E, López C, Contreras CM, Fernández-Guasti A (2000) Interaction of desmethylimipramine with steroid hormones on experimental anxiety. Psychoneuroendocrinology 25:109–120
Martínez-Mota L, Ulloa RE, Herrera-Pérez J, Chavira R, Fernández-Guasti A (2011) Sex and age differences in the impact of the forced swimming test on the levels of steroid hormones. Physiol Behav 104:900–905
Mathé A, Husum H, El Khoury A, Jiménez-Vasquez P, Gruber S, Wörtwein G, Nikisch G, Baumann P, Ågren H, Andersson W, Södergren A, Angelucci F (2007) Search for biological correlates of depression and mechanisms of action of antidepressant treatment modalities. Do neuropeptides play a role? Physiol Behav 92:226–231
Miyaoka T, Wake R, Furuya M, Liaury K, Leda M, Kawakami K, Tsuchie K, Taki M, Ishihara K, Araki T, Horiguchi J (2012) Minocycline as adjunctive therapy for patients with unipolar psychotic depression: an open-label study. Progr Neuro-Psychopharmacol Biol Psychiatry 37:222–226
Molina M, Téllez-Alcántara P (2011) Fluoxetine, 17β-estradiol or folic acid combined with intra-lateral septal infusions of neuropeptide Y produced antidepressant-like actions in ovariectomized rats forced to swim. Peptides 32:2400–2406
Molina M, Tellez-Alcántara NP, Pérez J, Olivera JI, Jaramillo T (2004) Synergistic interaction between ketoconazole and several antidepressant drugs with allopregnanolone treatments in ovariectomized Wistar rats forced to swim. Progr Neuro-Psychopharmacol Biol Psychiatry 28:1337–1345
Molina M, Téllez-Alcántara NP, Pérez-García J, Olivera J, Jaramillo T (2005) Antidepressant-like actions of intra-accumbens infusions of allopregnanolone in ovariectomized Wistar rats. Pharmacol Biochem Behav 80:401–409
Molina M, Téllez-Alcántara NP, Olivera-Lopez JI, Jaramillo T (2009) Olanzapine plus 17β-estradiol produce antidepressant-like actions in rats forced to swim. Pharmacol Biochem Behav 93:491–497
Molina M, Téllez-Alcántara NP, Olivera J, Jaramillo T (2010) Antidepressant-like or anxiolytic-like actions of topiramate alone or co-administered with intra-lateral septal infusions of neuropeptide Y in male Wistar rats. Peptides 31:1184–1189
Molina M, Téllez-Alcántara NP, Olivera J, Jaramillo T (2011) The folic acid combined with 17β-estradiol produces antidepressant-like actions in ovariectomized rats forced to swim. Progr Neuro-Psychopharmacol Biol Psychiatry 35:60–66
Mora S, Dussaubat N, Díaz-Veliz G (1996) Effects of the estrus cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21:609–620
Moret C (2005) Combination/augmentation strategies for improving the treatment of depression. Neuropsychiatr Dis Treat 1:301–309
Mowla A, Kardeh E (2011) Topiramate augmentation in patients with resistant major depressive disorder: a double-blind placebo-controlled clinical trial. Progr Neuro-Psychopharmacol Biol Psychiatry 35:970–973
Nakamura NH, McEwen BS (2005) Changes in interneuronal phenotypes regulated by estradiol in the adult rat hippocampus: a potential role for neuropeptide Y. Neuroscience 136:357–369
National Institutes of Health (1996) Guide for the care and use of laboratory animals. National Academy Press, Washington, DC
Nickel C, Lahmann C, Tritt K, Muehlbacher M, Kaplan P, Kettler C, Krawczyk J, Loew TH, Rother WK, Nickel MK (2005) Topiramate in treatment of depressive and anger symptoms in female depressive patients: a randomized, double-blind, placebo-controlled study. J Affect Disord 87:243–252
Pare W, Redei E (1993) Sex differences and stress response of WKY rats. Physiol Behav 54:1179–1185
Patchev VK, Shoaib M, Holsboer F, Almeida OFX (1994) The neurosteroid tetrahydroprogesterone counteracts corticotropin-releasing hormone-induced anxiety and alters the release and gene expression of corticotropin-releasing hormone in the rat hypothalamus. Neuroscience 62:265–271
Pinna G, Costa E, Guidotti A (2006) Fluoxetine and norfluoxetine stereospecifically and selectively increase brain neurosteroid content at doses that are inactive on 5-HT reuptake. Psychopharmacology 186:362–372
Porsolt RD, LePichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730–732
Romeo E, Ströhle A, Spalletta G, Di Michele F, Hermann B, Holsboer F, Pasini A, Rupprecht R (1998) Effects of antidepressant treatment on neuroactive steroids in major depression. Am J Psychiatry 155:910–913
Uzunov DP, Cooper TB, Costa E, Guidotti A (1996) Fluoxetine-induced changes in brain neurosteroid content measured by negative ion mass fragmentography. Proc Natl Acad Sci U S A 93:12599–12604
Uzunova V, Sheline Y, Davis JM, Rasmusson A, Uzunov DP, Costa E, Guidotti A (1998) Increase in the cerebrospinal fluid content of neurosteroids in patients with unipolar major depression who are receiving fluoxetine or fluvoxamine. Proc Natl Acad Sci U S A 95:3239–3244
Uzunova V, Ceci M, Kohler C, Uzunov DP, Wrynn AS (2003) Region-specific dysregulation of allopregnanolone brain content in the olfactory bulbectomized rat model of depression. Brain Res 976:1–8
Uzunova V, Wrynn AS, Kinnunen A, Ceci M, Kohler C, Uzunov DP (2004) Chronic antidepressants reverse cerebrocortical allopregnanolone decline in the olfactory-bulbectomized rat. Eur J Pharmacol 486:31–34
Uzunova V, Sampson L, Uzunov DP (2006) Relevance of endogenous 3α-reduced neurosteroids to depression and antidepressant action. Psychopharmacology 186:351–361
York DA, Singer L, Thomas S, Bray GA (2000) Effect of topiramate on body weight and body composition of osborne-mendel rats fed a high-fat diet: alterations in hormones, neuropeptide, and uncoupling-protein mRNAs. Nutrition 16:967–975
Zahra E, Ibtissam L, Abdelhalim M, Aboubakr EH, Ali O (2012) The Influence of gonadectomy on anxiolytic and antidepressant effects of melatonin in male and female Wistar rats: a possible implication of sex hormones. Neurosci Med 3:162–173
Acknowledgments
This study was supported by grant no. 52932 from the Consejo Nacional de Ciencia y Tecnología (CONACyT), México. We thank Warren Haid for revising the manuscript. We acknowledge the substantive and thoughtful suggestions offered by anonymous reviewers.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Molina-Hernández, M., Téllez-Alcántara, N.P., Olivera-López, J.I. et al. The antidepressant-like effects of topiramate alone or combined with 17β-estradiol in ovariectomized Wistar rats submitted to the forced swimming test. Psychopharmacology 231, 3343–3350 (2014). https://doi.org/10.1007/s00213-013-3251-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-013-3251-1