Synergistic effect of estradiol and fluoxetine in young adult and middle-aged female rats in two models of experimental depression

Behavioural Brain Research

Volumn 233, Issue 2, 2012, Pages 351-358

  Récamier Carballo, Soledad ^a   Estrada Camarena, Erika ^b   Reyes, Rebeca ^a   Fernández Guasti, Alonso ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b INSTITUTO NACIONAL DE PSIQUIATRÍA RAMÓN DE LA FUENTE MUÑIZ   (Mexico)

Author keywords

17 Estradiol; Chronic mild stress; Fluoxetine; Forced swimming test; Middle aged female rats; Young adult female rats

Indexed keywords

ESTRADIOL; FLUOXETINE; SUCROSE;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; CHRONIC STRESS; CLIMBING; DEPRESSION; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; DRUG SENSITIVITY; FEMALE; FORCED SWIMMING TEST; MIDDLE AGED; NONHUMAN; PRIORITY JOURNAL; RAT; SUGAR INTAKE;

AGING; ANALYSIS OF VARIANCE; ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; DEPRESSION; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; ESTRADIOL; FEMALE; FLUOXETINE; FOOD PREFERENCES; IMMOBILITY RESPONSE, TONIC; MOTOR ACTIVITY; OVARIECTOMY; RATS; STRESS, PSYCHOLOGICAL; SUCROSE; SWIMMING;

EID: 84862156770     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.05.034     Document Type: Article

References (64)

1. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry 2005, 62:593-602.
2. Murray C.J., Lopez A.D. Alternative projections of mortality and disability by cause 1990-2020: Global Burden of Disease Study. Lancet 1997, 349:1498-1504.
3. Deussing J.M. Animal models of depression. Drug Discovery Today: Disease Models 2006, 3:375-383.
4. Hasler G., Drevets W.C., Manji H.K., Charney D.S. Discovering endophenotypes for major depression. Neuropsychopharmacology 2004, 29:1765-1781.
5. Kessler R.C., McGonagle K.A., Swartz M., Blazer D.G., Nelson C.B. Sex and depression in the National Comorbidity Survey. I: Lifetime prevalence, chronicity and recurrence. Journal of Affective Disorders 1993, 29:85-96.
6. Hasin D.S., Goodwin R.D., Stinson F.S., Grant B.F. Epidemiology of major depressive disorder: results from the National Epidemiologic Survey on Alcoholism and Related Conditions. Archives of General Psychiatry 2005, 62:1097-1106.
7. Graziottin A., Serafini A. Depression and the menopause: why antidepressants are not enough. Menopause International 2009, 15:76-81.
8. Soares C.N., Almeida O.P., Joffe H., Cohen L.S. Efficacy of estradiol for the treatment of depressive disorders in perimenopausal women: a double-blind, randomized, placebo-controlled trial. Archives of General Psychiatry 2001, 58:529-534.
9. Cohen L.S., Soares C.N., Poitras J.R., Prouty J., Alexander A.B., Shifren J.L. Short-term use of estradiol for depression in perimenopausal and postmenopausal women: a preliminary report. American Journal of Psychiatry 2003, 160:1519-1522.
10. Estrada-Camarena E., Fernandez-Guasti A., Lopez-Rubalcava C. Antidepressant-like effect of different estrogenic compounds in the forced swimming test. Neuropsychopharmacology 2003, 28:830-838.
11. Li W., Li Q.J., An S.C. Preventive effect of estrogen on depression-like behavior induced by chronic restraint stress. Neuroscience Bulletin 2010, 26:140-146.
12. Walf A.A., Frye C.A. Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic-pituitary-adrenal axis activity. Neuropsychopharmacology 2005, 30:1288-1301.
13. Kiss A., Delattre A.M., Pereira S.I.R., Carolino R.G., Szawka R.E., Anselmo-Franci J.A., et al. 17β-Estradiol replacement in young, adult and middle-aged female ovariectomized rats promotes improvement of spatial reference memory and an antidepressant effect and alters monoamines and BDNF levels in memory- and depression-related brain areas. Behavioural Brain Research 2012, 227:100-108.
14. Stahl S.M. Basic psychopharmacology of antidepressants. Part 2: Estrogen as an adjunct to antidepressant treatment. Journal of Clinical Psychiatry 1998, 59(Suppl 4):15-24.
15. Estrada-Camarena E., Fernandez-Guasti A., Lopez-Rubalcava C. Interaction between estrogens and antidepressants in the forced swimming test in rats. Psychopharmacology (Berlin) 2004, 173:139-145.
16. Nowakowska E., Kus K. Antidepressant and memory affecting influence of estrogen and venlafaxine in ovariectomized rats. Arzneimittel-Forschung 2005, 55:153-159.
17. Morgan M.L., Cook I.A., Rapkin A.J., Leuchter A.F. Estrogen augmentation of antidepressants in perimenopausal depression: a pilot study. Journal of Clinical Psychiatry 2005, 66:774-780.
18. Soares C.N., Poitras J.R., Prouty J., Alexander A.B., Shifren J.L., Cohen L.S. Efficacy of citalopram as a monotherapy or as an adjunctive treatment to estrogen therapy for perimenopausal and postmenopausal women with depression and vasomotor symptoms. Journal of Clinical Psychiatry 2003, 64:473-479.
19. Estrada-Camarena E., Rivera N.M., Berlanga C., Fernandez-Guasti A. Reduction in the latency of action of antidepressants by 17 beta-estradiol in the forced swimming test. Psychopharmacology (Berlin) 2008, 201:351-360.
20. Ribeiro M.F., Ferigolo M., Reis F.M., Barros H.M., Spritzer P.M. Paradoxical effect of imipramine in hyperprolactinemic female rats exposed to the forced swimming test. Physiology and Behavior 2000, 68:619-623.
21. Joffe H., Groninger H., Soares C.N., Nonacs R., Cohen L.S. An open trial of mirtazapine in menopausal women with depression unresponsive to estrogen replacement therapy. Journal of Women's Health and Gender-Based Medicine 2001, 10:999-1004.
22. Amsterdam J., Garcia-Espana F., Fawcett J., Quitkin F., Reimherr F., Rosenbaum J., et al. Fluoxetine efficacy in menopausal women with and without estrogen replacement. Journal of Affective Disorders 1999, 55:11-17.
23. Romano-Torres M., Fernandez-Guasti A. Estradiol valerate elicits antidepressant-like effects in middle-aged female rats under chronic mild stress. Behavioural Pharmacology 2010, 21:104-111.
24. Sell S.L., Craft R.M., Seitz P.K., Stutz S.J., Cunningham K.A., Thomas M.L. Estradiol-sertraline synergy in ovariectomized rats. Psychoneuroendocrinology 2008, 33:1051-1060.
25. Estrada-Camarena E., Lopez-Rubalcava C., Vega-Rivera N., Recamier-Carballo S., Fernandez-Guasti A. Antidepressant effects of estrogens: a basic approximation. Behavioural Pharmacology 2010, 21:451-464.
26. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berlin) 1995, 121:66-72.
27. Martinez-Mota L., Cruz-Martinez J.J., Marquez-Baltazar S., Fernandez-Guasti A. Estrogens participate in the antidepressant-like effect of desipramine and fluoxetine in male rats. Pharmacology Biochemistry and Behavior 2008, 88:332-340.
28. Papp M., Willner P., Muscat R. An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology (Berlin) 1991, 104:255-259.
29. Moreau J.L., Scherschlicht R., Jenck F., Martin J.R. Chronic mild stress-induced anhedonia model of depression; sleep abnormalities and curative effects of electroshock treatment. Behavioural Pharmacology 1995, 6:682-687.
30. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berlin) 1997, 134:319-329.
31. Montgomery S.A., Loft H., Sanchez C., Reines E.H., Papp M. Escitalopram (S-enantiomer of citalopram): clinical efficacy and onset of action predicted from a rat model. Pharmacology and Toxicology 2001, 88:282-286.
32. Bekris S., Antoniou K., Daskas S., Papadopoulou-Daifoti Z. Behavioural and neurochemical effects induced by chronic mild stress applied to two different rat strains. Behavioural Brain Research 2005, 161:45-59.
33. Grippo A.J., Sullivan N.R., Damjanoska K.J., Crane J.W., Carrasco G.A., Shi J., et al. Chronic mild stress induces behavioral and physiological changes, and may alter serotonin 1A receptor function, in male and cycling female rats. Psychopharmacology (Berlin) 2005, 179:769-780.
34. Herrera-Pérez J.J., Martinez-Mota L., Fernandez-Guasti A. Aging increases the susceptibility to develop anhedonia in male rats. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2008, 32:1798-1803.
35. Muscat R., Towell A., Willner P. Changes in dopamine autoreceptor sensitivity in an animal model of depression. Psychopharmacology (Berlin) 1988, 94:545-550.
36. Ayensu W.K., Pucilowski O., Mason G.A., Overstreet D.H., Rezvani A.H., Janowsky D.S. Effects of chronic mild stress on serum complement activity, saccharin preference, and corticosterone levels in Flinders lines of rats. Physiology and Behavior 1995, 57:165-169.
37. Willner P., Moreau J.L., Nielsen C.K., Papp M., Sluzewska A. Decreased hedonic responsiveness following chronic mild stress is not secondary to loss of body weight. Physiology and Behavior 1996, 60:129-134.
38. Récamier-Carballo S., Fernández-Guasti A. Forced swimming and chronic mild stress as animal models of depression. Behavioral Animal Models 2012, 123-137. Research Signpost, Kerala, India. J.C. Sara Cruz, Pedro Arriaga-Ramírez (Eds.).
39. Herrera-Pérez J.J., Martínez-Mota L., Fernandez-Guasti A. Testosterone prevents but not reverses anhedonia in middle-aged males and lacks an effect on stress vulnerability in young adults. Hormones and Behavior 2012, 61:623-630.
40. Martinez-Mota L., Estrada-Camarena E., Lopez-Rubalcava C., Contreras C.M., Fernandez-Guasti A. Interaction of desipramine with steroid hormones on experimental anxiety. Psychoneuroendocrinology 2000, 25:109-120.
41. Muscat R., Papp M., Willner P. Reversal of stress-induced anhedonia by the atypical antidepressants, fluoxetine and maprotiline. Psychopharmacology (Berlin) 1992, 109:433-438.
42. de Chaves G., Moretti M., Castro A.A., Dagostin W., da Silva G.G., Boeck C.R., et al. Effects of long-term ovariectomy on anxiety and behavioral despair in rats. Physiology and Behavior 2009, 97:420-425.
43. Estrada-Camarena E., Lopez-Rubalcava C., Hernandez-Aragon A., Mejia-Mauries S., Picazo O. Long-term ovariectomy modulates the antidepressant-like action of estrogens, but not of antidepressants. Journal of Psychopharmacology 2011, 25:1365-1377.
44. Moretti M., de Souza A.G., de Chaves G., de Andrade V.M., Romao P.R.T., Gavioli E.C., et al. Emotional behavior in middle-aged rats: implications for geriatric psychopathologies. Physiology and Behavior 2011, 102:115-120.
45. Dalla C., Antoniou K., Drossopoulou G., Xagoraris M., Kokras N., Sfikakis A., et al. Chronic mild stress impact: are females more vulnerable?. Neuroscience 2005, 135:703-714.
46. Galea L.A., Wide J.K., Barr A.M. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behavioural Brain Research 2001, 122:1-9.
47. Estrada-Camarena E., Lopez-Rubalcava C., Fernandez-Guasti A. Facilitating antidepressant-like actions of estrogens are mediated by 5-HT1A and estrogen receptors in the rat forced swimming test. Psychoneuroendocrinology 2006, 31:905-914.
48. Walf A.A., Paris J.J., Frye C.A. Chronic estradiol replacement to aged female rats reduces anxiety-like and depression-like behavior and enhances cognitive performance. Psychoneuroendocrinology 2009, 34:909-916.
49. Rubinow D.R., Schmidt P.J., Roca C.A. Estrogen-serotonin interactions: implications for affective regulation. Biological Psychiatry 1998, 44:839-850.
50. Epperson C.N., Wisner K.L., Yamamoto B. Gonadal steroids in the treatment of mood disorders. Psychosomatic Medicine 1999, 61:676-697.
51. Detke M.J., Lucki I. Detection of serotonergic and noradrenergic antidepressants in the rat forced swimming test: the effects of water depth. Behavioural Brain Research 1996, 73:43-46.
52. Page M.E., Detke M.J., Dalvi A., Kirby L.G., Lucki I. Serotonergic mediation of the effects of fluoxetine, but not desipramine, in the rat forced swimming test. Psychopharmacology (Berlin) 1999, 147:162-167.
53. Estrada-Camarena E., Fernandez-Guasti A., Lopez-Rubalcava C. Participation of the 5-HT1A receptor in the antidepressant-like effect of estrogens in the forced swimming test. Neuropsychopharmacology 2006, 31:247-255.
54. Shores M.M., White S.S., Veith R.C., Szot P. Tyrosine hydroxylase mRNA is increased in old age and norepinephrine uptake transporter mRNA is decreased in middle age in locus coeruleus of Brown-Norway rats. Brain Research 1999, 826:143-147.
55. Estes K.S., Simpkins J.W. Catecholamine levels and activity change at different rates in discrete brain regions of aging female rats. Federation Proceedings 1981, 40:509.
56. Maines L.W., Keck B.J., Smith J.E., Lakoski J.M. Corticosterone regulation of serotonin transporter and 5-HT1A receptor expression in the aging brain. Synapse 1999, 32:58-66.
57. Olivier B., Soudijn W., van Wijngaarden I. Serotonin, dopamine and norepinephrine transporters in the central nervous system and their inhibitors. Progress in Drug Research 2000, 54:59-119.
58. Jin M., Jin F., Zhang L., Chen Z., Huang H. Two estrogen replacement therapies differentially regulate expression of estrogen receptors alpha and beta in the hippocampus and cortex of ovariectomized rat. Brain Research. Molecular Brain Research 2005, 142:107-114.
59. Barha C.K., Dalton G.L., Galea L.A. Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats. Neuropsychopharmacology 2010, 35:547-559.
60. Drossopoulou G., Antoniou K., Kitraki E., Papathanasiou G., Papalexi E., Dalla C., et al. Sex differences in behavioral, neurochemical and neuroendocrine effects induced by the forced swim test in rats. Neuroscience 2004, 126:849-857.
61. Bernardi M., Vergoni A.V., Sandrini M., Tagliavini S., Bertolini A. Influence of ovariectomy, estradiol and progesterone on the behavior of mice in an experimental model of depression. Physiology and Behavior 1989, 45:1067-1068.
62. Okada M., Hayashi N., Kometani M., Nakao K., Inukai T. Influences of ovariectomy and continuous replacement of 17beta-estradiol on the tail skin temperature and behavior in the forced swimming test in rats. Japanese Journal of Pharmacology 1997, 73:93-96.
63. Rachman I.M., Unnerstall J.R., Pfaff D.W., Cohen R.S. Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:13941-13946.
64. Herrera-Perez J.J., Martinez-Mota L., Fernandez-Guasti A. Aging impairs the antidepressant-like response to citalopram in male rats. European Journal of Pharmacology 2010, 633:39-43.