Estradiol reduces depressive-like behavior through inhibiting nitric oxide/cyclic GMP pathway in ovariectomized mice

Hormones and Behavior

Volumn 63, Issue 2, 2013, Pages 361-369

  Heydarpour, Pouria ^a,b   Salehi Sadaghiani, Mohammad ^a   Javadi Paydar, Mehrak ^a,b   Rahimian, Reza ^a,b   Fakhfouri, Gohar ^c   Khosravi, Mohsen ^a   Khoshkish, Shayan ^a   Gharedaghi, Mohammad Hadi ^a,b   Ghasemi, Mehdi ^a,d   Dehpour, Ahmad Reza ^a,e  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Depression; Estradiol; Nitric oxide; Ovariectomy

Indexed keywords

7 NITROINDAZOLE; ARGININE; CYCLIC GMP; ESTRADIOL; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; SILDENAFIL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; FEMALE; FORCED SWIMMING TEST; HIPPOCAMPUS; HORMONE DETERMINATION; IMMOBILIZATION; LOCOMOTION; MOUSE; NONHUMAN; OPEN FIELD TEST; OVARIECTOMY; PRIORITY JOURNAL;

ANIMALS; ANTIDEPRESSIVE AGENTS; BEHAVIOR, ANIMAL; CYCLIC GMP; DEPRESSION; DOWN-REGULATION; ENZYME INHIBITORS; ESTRADIOL; FEMALE; MICE; MOTOR ACTIVITY; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OVARIECTOMY; SIGNAL TRANSDUCTION;

EID: 84872832464     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.12.005     Document Type: Article

References (75)

1. Avis N.E., Brambilla D., Mckinlay S.M., Vass K. A longitudinal analysis of the association between menopause and depression. Results from the Massachusetts Women's Health Study. Ann. Epidemiol. 1994, 4:214-220.
2. Beavo J.A. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev. 1995, 75:725-748.
3. Bekku N., Yoshimura H., Araki H. Factors producing a menopausal depressive-like state in mice following ovariectomy. Psychopharmacology (Berl.) 2006, 187:170-180.
4. 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. Physiol. Behav. 1989, 45:1067-1068.
5. Cashen D.E., Macintyre D.E., Martin W.J. Effects of sildenafil on erectile activity in mice lacking neuronal or endothelial nitric oxide synthase. Br. J. Pharmacol. 2002, 136:693-700.
6. Chu H.P., Sarkar G., Etgen A.M. Estradiol and progesterone modulate the nitric oxide/cyclic gmp pathway in the hypothalamus of female rats and in GT1-1 cells. Endocrine 2004, 24:177-184.
7. Cohen L.S., Soares C.N., Vitonis A.F., Otto M.W., Harlow B.L. Risk for new onset of depression during the menopausal transition: the Harvard study of moods and cycles. Arch. Gen. Psychiatry 2006, 63:385-390.
8. Coker R.K., Laurent G.J. Pulmonary fibrosis: cytokines in the balance. Eur. Respir. J. 1998, 11:1218-1221.
9. da Silva G.D., Matteussi A.S., dos Santos A.R., Calixto J.B., Rodrigues A.L. Evidence for dual effects of nitric oxide in the forced swimming test and in the tail suspension test in mice. Neuroreport 2000, 11:3699-3702.
10. D'anglemont de Tassigny X., Campagne C., Steculorum S., Prevot V. Estradiol induces physical association of neuronal nitric oxide synthase with NMDA receptor and promotes nitric oxide formation via estrogen receptor activation in primary neuronal cultures. J. Neurochem. 2009, 109:214-224.
11. de Chaves G., Moretti M., Castro A.A., Dagostin W., da Silva G.G., Boeck C.R., Quevedo J., Gavioli E.C. Effects of long-term ovariectomy on anxiety and behavioral despair in rats. Physiol. Behav. 2009, 97:420-425.
12. Dhir A., Kulkarni S.K. Involvement of L-arginine-nitric oxide-cyclic guanosine monophosphate pathway in the antidepressant-like effect of venlafaxine in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31:921-925.
13. Dhir A., Kulkarni S.K. Involvement of nitric oxide (NO) signaling pathway in the antidepressant action of bupropion, a dopamine reuptake inhibitor. Eur. J. Pharmacol. 2007, 568:177-185.
14. Dhir A., Kulkarni S.K. Antidepressant-like effect of 17beta-estradiol: involvement of dopaminergic, serotonergic, and (or) sigma-1 receptor systems. Can. J. Physiol. Pharmacol. 2008, 86:726-735.
15. Dhir A., Kulkarni S.K. Nitric oxide and major depression. Nitric Oxide 2011, 24:125-131.
16. 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.
17. 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 (Berl.) 2008, 201:351-360.
18. Estrada-Camarena E., Lopez-Rubalcava C., Vega-Rivera N., Recamier-Carballo S., Fernandez-Guasti A. Antidepressant effects of estrogens: a basic approximation. Behav. Pharmacol. 2010, 21:451-464.
19. 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. J. Psychopharmacol. 2011, 25:1365-1377.
20. Freeman E.W. Associations of depression with the transition to menopause. Menopause 2010, 17:823-827.
21. Freeman E.W., Sammel M.D., Liu L., Gracia C.R., Nelson D.B., Hollander L. Hormones and menopausal status as predictors of depression in women in transition to menopause. Arch. Gen. Psychiatry 2004, 61:62-70.
22. Game X., Allard J., Escourrou G., Gourdy P., Tack I., Rischmann P., Arnal J.F., Malavaud B. Estradiol increases urethral tone through the local inhibition of neuronal nitric oxide synthase expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R851-R857.
23. Ghasemi M., Sadeghipour H., Mosleh A., Sadeghipour H.R., Mani A.R., Dehpour A.R. Nitric oxide involvement in the antidepressant-like effects of acute lithium administration in the mouse forced swimming test. Eur. Neuropsychopharmacol. 2008, 18:323-332.
24. Ghasemi M., Montaser-Kouhsari L., Shafaroodi H., Nezami B.G., Ebrahimi F., Dehpour A.R. NMDA receptor/nitrergic system blockage augments antidepressant-like effects of paroxetine in the mouse forced swimming test. Psychopharmacology (Berl.) 2009, 206:325-333.
25. Gingerich S., Krukoff T.L. Estrogen modulates endothelial and neuronal nitric oxide synthase expression via an estrogen receptor beta-dependent mechanism in hypothalamic slice cultures. Endocrinology 2005, 146:2933-2941.
26. Gingerich S., Krukoff T.L. Activation of ERbeta increases levels of phosphorylated nNOS and NO production through a Src/PI3K/Akt-dependent pathway in hypothalamic neurons. Neuropharmacology 2008, 55:878-885.
27. Gotti S., Martini M., Pradotto M., Viglietti-Panzica C., Panzica G. Rapid changes on nitrinergic system in female mouse hippocampus during the ovarian cycle. J. Chem. Neuroanat. 2009, 38:117-123.
28. Harkin A.J., Bruce K.H., Craft B., Paul I.A. Nitric oxide synthase inhibitors have antidepressant-like properties in mice. 1. Acute treatments are active in the forced swim test. Eur. J. Pharmacol. 1999, 372:207-213.
29. Harkin A., Connor T.J., Burns M.P., Kelly J.P. Nitric oxide synthase inhibitors augment the effects of serotonin re-uptake inhibitors in the forced swimming test. Eur. Neuropsychopharmacol. 2004, 14:274-281.
30. Hayashi T., Yamada K., Esaki T., Muto E., Chaudhuri G., Iguchi A. Physiological concentrations of 17beta-estradiol inhibit the synthesis of nitric oxide synthase in macrophages via a receptor-mediated system. J. Cardiovasc. Pharmacol. 1998, 31:292-298.
31. Heiberg I.L., Wegener G., Rosenberg R. Reduction of cGMP and nitric oxide has antidepressant-like effects in the forced swimming test in rats. Behav. Brain Res. 2002, 134:479-484.
32. Herken H., Gurel A., Selek S., Armutcu F., Ozen M.E., Bulut M., Kap O., Yumru M., Savas H.A., Akyol O. Adenosine deaminase, nitric oxide, superoxide dismutase, and xanthine oxidase in patients with major depression: impact of antidepressant treatment. Arch. Med. Res. 2007, 38:247-252.
33. Hu Y., Wu D.L., Luo C.X., Zhu L.J., Zhang J., Wu H.Y., Zhu D.Y. Hippocampal nitric oxide contributes to sex difference in affective behaviors. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:14224-14229.
34. Inan S.Y., Yalcin I., Aksu F. Dual effects of nitric oxide in the mouse forced swimming test: possible contribution of nitric oxide-mediated serotonin release and potassium channel modulation. Pharmacol. Biochem. Behav. 2004, 77:457-464.
35. Joca S.R., Guimaraes F.S. Inhibition of neuronal nitric oxide synthase in the rat hippocampus induces antidepressant-like effects. Psychopharmacology (Berl.) 2006, 185:298-305.
36. Kalbasi Anaraki D., Sianati S., Sadeghi M., Ghasemi M., Paydar M.J., Ejtemaei Mehr S., Dehpour A.R. Modulation by female sex hormones of the cannabinoid-induced catalepsy and analgesia in ovariectomized mice. Eur. J. Pharmacol. 2008, 586:189-196.
37. Kandi P., Hayslett R.L. Nicotine and 17beta-estradiol produce an antidepressant-like effect in female ovariectomized rats. Brain Res. Bull. 2011, 84:224-228.
38. Kaster M.P., Ferreira P.K., Santos A.R., Rodrigues A.L. Effects of potassium channel inhibitors in the forced swimming test: possible involvement of L-arginine-nitric oxide-soluble guanylate cyclase pathway. Behav. Brain Res. 2005, 165:204-209.
39. Kim J.Y., Jo K.J., Kim O.S., Kim B.J., Kang D.W., Lee K.H., Baik H.W., Han M.S., Lee S.K. Parenteral 17beta-estradiol decreases fasting blood glucose levels in non-obese mice with short-term ovariectomy. Life Sci. 2010, 87:358-366.
40. Kiss A., Delattre A.M., Pereira S.I., Carolino R.G., Szawka R.E., Anselmo-Franci J.A., Zanata S.M., Ferraz A.C. 17beta-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. Behav. Brain Res. 2012, 227:100-108.
41. Knowles R.G., Palacios M., Palmer R.M., Moncada S. Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:5159-5162.
42. Kurata K., Takebayashi M., Morinobu S., Yamawaki S. Beta-estradiol, dehydroepiandrosterone, and dehydroepiandrosterone sulfate protect against N-methyl-D-aspartate-induced neurotoxicity in rat hippocampal neurons by different mechanisms. J. Pharmacol. Exp. Ther. 2004, 311:237-245.
43. Lagunas N., Calmarza-Font I., Diz-Chaves Y., Garcia-Segura L.M. Long-term ovariectomy enhances anxiety and depressive-like behaviors in mice submitted to chronic unpredictable stress. Horm. Behav. 2010, 58:786-791.
44. Ludka F.K., Zomkowski A.D., Cunha M.P., Dal-Cim T., Zeni A.L., Rodrigues A.L., Tasca C.I. Acute atorvastatin treatment exerts antidepressant-like effect in mice via the l-arginine-nitric oxide-cyclic guanosine monophosphate pathway and in creases BDNF levels. Eur. Neuropsychopharmacol. 2012, 10.1016/j.euroneuro.2012.05.005.
45. Lv X.H., Shi Da Z. Variations of serum estradiol and progesterone levels during consecutive reproductive states in Mongolian gerbils (Meriones unguiculatus). Exp. Anim. 2010, 59:231-237.
46. Macqueen G., Frodl T. The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research?. Mol. Psychiatry 2011, 16:252-264.
47. Malekinejad H., Hamidi M., Sadrkhanloo R.A, Ahmadi A. The effect of tamoxifen on the fetal and neonatal ovarian follicles development in rats. Iran. J. Basic Med. Sci. 2011, 14:240-248.
48. Mirbaha H., Tabaeizadeh M., Shaterian-Mohammadi H., Tahsili-Fahadan P., Dehpour A.R. Estrogen pretreatment modulates morphine-induced conditioned place preference in ovariectomized mice. Pharmacol. Biochem. Behav. 2009, 92:399-403.
49. Moretti M., Freitas A.E., Budni J., Fernandes S.C., Balen Gde O., Rodrigues A.L. Involvement of nitric oxide-cGMP pathway in the antidepressant-like effect of ascorbic acid in the tail suspension test. Behav. Brain Res. 2011, 225:328-333.
50. Morgan M.A., Pfaff D.W. Estrogen's effects on activity, anxiety, and fear in two mouse strains. Behav. Brain Res. 2002, 132:85-93.
51. Oliveira R.M., Guimaraes F.S., Deakin J.F. Expression of neuronal nitric oxide synthase in the hippocampal formation in affective disorders. Braz. J. Med. Biol. Res. 2008, 41:333-341.
52. Ostlund H., Keller E., Hurd Y.L. Estrogen receptor gene expression in relation to neuropsychiatric disorders. Ann. N. Y. Acad. Sci. 2003, 1007:54-63.
53. Panzica G.C., Viglietti-Panzica C., Sica M., Gotti S., Martini M., Pinos H., Carrillo B., Collado P. Effects of gonadal hormones on central nitric oxide producing systems. Neuroscience 2006, 138:987-995.
54. Payandemehr B., Bahremand A., Rahimian R., Ziai P., Amouzegar A., Sharifzadeh M., Dehpour A.R. 5-HT(3) receptor mediates the dose-dependent effects of citalopram on pentylenetetrazole-induced clonic seizure in mice: Involvement of nitric oxide. Epilepsy Res. 2012, 101:217-227.
55. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 1977, 229:327-336.
56. Puzzo D., Sapienza S., Arancio O., Palmeri A. Role of phosphodiesterase 5 in synaptic plasticity and memory. Neuropsychiatr. Dis. Treat. 2008, 4:371-387.
57. 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. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13941-13946.
58. Reyna-Neyra A., Sarkar G., Etgen A.M. Regulation of soluble guanylyl cyclase activity by oestradiol and progesterone in the hypothalamus but not hippocampus of female rats. J. Neuroendocrinol. 2007, 19:418-425.
59. Richette P., Dumontier M.F., Tahiri K., Widerak M., Torre A., Benallaoua M., Rannou F., Corvol M.T., Savouret J.F. Oestrogens inhibit interleukin 1beta-mediated nitric oxide synthase expression in articular chondrocytes through nuclear factor-kappa B impairment. Ann. Rheum. Dis. 2007, 66:345-350.
60. Rocha B.A., Fleischer R., Schaeffer J.M., Rohrer S.P., Hickey G.J. 17 Beta-estradiol-induced antidepressant-like effect in the forced swim test is absent in estrogen receptor-beta knockout (BERKO) mice. Psychopharmacology (Berl.) 2005, 179:637-643.
61. Sadaghiani M.S., Javadi-Paydar M., Gharedaghi M.H., Fard Y.Y., Dehpour A.R. Antidepressant-like effect of pioglitazone in the forced swimming test in mice: the role of PPAR-gamma receptor and nitric oxide pathway. Behav. Brain Res. 2011, 224:336-343.
62. Sadeghi M., Sianati S., Anaraki D.K., Ghasemi M., Paydar M.J., Sharif B., Mehr S.E., Dehpour A.R. Study of morphine-induced dependence in gonadectomized male and female mice. Pharmacol. Biochem. Behav. 2009, 91:604-609.
63. Salehi-Sadaghiani M., Javadi-Paydar M., Gharedaghi M.H., Zandieh A., Heydarpour P., Yousefzadeh-Fard Y., Dehpour A.R. NMDA receptor involvement in antidepressant-like effect of pioglitazone in the forced swimming test in mice. Psychopharmacology (Berl.) 2012.
64. Sapolsky R.M. The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death. Biol. Psychiatry 2000, 48:755-765.
65. Snyder S.H., Bredt D.S. Nitric oxide as a neuronal messenger. Trends Pharmacol. Sci. 1991, 12:125-128.
66. Stefano G.B., Prevot V., Beauvillain J.C., Cadet P., Fimiani C., Welters I., Fricchione G.L., Breton C., Lassalle P., Salzet M., Bilfinger T.V. Cell-surface estrogen receptors mediate calcium-dependent nitric oxide release in human endothelia. Circulation 2000, 101:1594-1597.
67. Stoffel E.C., Craft R.M. Ovarian hormone withdrawal-induced "depression" in female rats. Physiol. Behav. 2004, 83:505-513.
68. Tahsili-Fahadan P., Yahyavi-Firouz-abadi N., Orandi A.H., Esmaeili B., Basseda Z., Dehpour A.R. Rewarding properties of sildenafil citrate in mice: role of the nitric oxide-cyclic GMP pathway. Psychopharmacology (Berl.) 2006, 185:201-207.
69. 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.
70. Walf A.A., Frye C.A. Estradiol reduces anxiety- and depression-like behavior of aged female mice. Physiol. Behav. 2010, 99:169-174.
71. Wang D., An S.C., Zhang X. Prevention of chronic stress-induced depression-like behavior by inducible nitric oxide inhibitor. Neurosci. Lett. 2008, 433:59-64.
72. Yildiz F., Erden B.F., Ulak G., Utkan T., Gacar N. Antidepressant-like effect of 7-nitroindazole in the forced swimming test in rats. Psychopharmacology (Berl.) 2000, 149:41-44.
73. Zhang J., Huang X.Y., Ye M.L., Luo C.X., Wu H.Y., Hu Y., Zhou Q.G., Wu D.L., Zhu L.J., Zhu D.Y. Neuronal nitric oxide synthase alteration accounts for the role of 5-HT1A receptor in modulating anxiety-related behaviors. J. Neurosci. 2010, 30:2433-2441.
74. Zhou Q.G., Hu Y., Hua Y., Hu M., Luo C.X., Han X., Zhu X.J., Wang B., Xu J.S., Zhu D.Y. Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis. J. Neurochem. 2007, 103:1843-1854.
75. Zhou Q.G., Zhu L.J., Chen C., Wu H.Y., Luo C.X., Chang L., Zhu D.Y. Hippocampal neuronal nitric oxide synthase mediates the stress-related depressive behaviors of glucocorticoids by downregulating glucocorticoid receptor. J. Neurosci. 2011, 31:7579-7590.