Involvement of NMDA receptors and l-arginine/nitric oxide/cyclic guanosine monophosphate pathway in the antidepressant-like effects of topiramate in mice forced swimming test

Brain Research Bulletin

Volumn 122, Issue , 2016, Pages 62-70

  Ostadhadi, Sattar ^a,b   Khan, Muhammad Imran ^a   Norouzi Javidan, Abbas ^b   Chamanara, Mohsen ^a   Jazaeri, Farahnaz ^a   Zolfaghari, Samira ^d   Dehpour, Ahmad Reza ^a,b,c  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Depression; Forced swimming test; Mice; Nitric oxide; NMDA; Topiramate

Indexed keywords

7 NITROINDAZOLE; ANTIDEPRESSANT AGENT; ARGININE; CYCLIC GMP; DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N(G) NITROARGININE METHYL ESTER; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; SILDENAFIL; TOPIRAMATE; ENZYME INHIBITOR; FRUCTOSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DEPRESSION; DRUG POTENTIATION; FORCED SWIM TEST; IMMOBILITY; LOCOMOTION; LOW DRUG DOSE; MALE; MOBILIZATION; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; OPEN FIELD TEST; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; IMMOBILIZATION; METABOLISM; SIGNAL TRANSDUCTION; SWIMMING;

ANIMALS; ANTIDEPRESSIVE AGENTS; ARGININE; BEHAVIOR, ANIMAL; CYCLIC GMP; DEPRESSION; ENZYME INHIBITORS; FRUCTOSE; HINDLIMB SUSPENSION; MALE; MICE; NITRIC OXIDE; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SWIMMING;

EID: 84962520809     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2016.03.004     Document Type: Article

References (84)

1. Ängehagen M., Ben-Menachem E., Shank R., Rönnbäck L., Hansson E. Topiramate modulation of kainate-induced calcium currents is inversely related to channel phosphorylation level. J. Neurochem. 2004, 88(2):320-325.
2. Appolinario J.C., Fontenelle L.F., Papelbaum M., Bueno J.R., Coutinho W. Topiramate use in obese patients with binge eating disorder: an open study. Can. J. Psychiatry 2002, 47(3):271-273.
3. Beavo J.A. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev. 1995, 75(4):725-748.
4. Bender A.T., Beavo J.A. Specific localized expression of cGMP PDEs in Purkinje neurons and macrophages. Neurochem. Int. 2004, 45(6):853-857.
5. Berman R.M., Cappiello A., Anand A., Oren D.A., Heninger G.R., Charney D.S., et al. Antidepressant effects of ketamine in depressed patients. Biol. Psychiatry 2000, 47(4):351-354.
6. Bourin M., Chenu F., Hascoët M. Topiramate and phenytoin anti-immobility effect in the mice forced swimming test is reversed by veratrine: implication for bipolar depression treatment. Behav. Brain Res. 2009, 205(2):421-425.
7. Boyce-Rustay J.M., Holmes A. Genetic inactivation of the NMDA receptor NR2A subunit has anxiolytic-and antidepressant-like effects in mice. Neuropsychopharmacology 2006, 31(11):2405-2414.
8. Boylan L., Flint L., Labovitz D., Jackson S., Starner K., Devinsky O. Depression but not seizure frequency predicts quality of life in treatment-resistant epilepsy. Neurology 2004, 62(2):258-261.
9. Calabrese J.R., Hirschfeld R.M., Frye M.A., Reed M.L. Impact of depressive symptoms compared with manic symptoms in bipolar disorder: results of a US community-based sample. J. Clin. Psychiatry 2004, 65(11):1499-1504.
10. Contestabile A. Roles of NMDA receptor activity and nitric oxide production in brain development. Brain Res. Rev. 2000, 32(2):476-509.
11. da Silva G.D., Matteussi A.S., dos Santos A.R.S., Calixto J.B., Rodrigues A.L.S. Evidence for dual effects of nitric oxide in the forced swimming test and in the tail suspension test in mice. Neuroreport 2000, 11(17):3699-3702.
12. Denninger J.W., Marletta M.A. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim. Biophys. Acta (BBA)-Bioenergetics 1999, 1411(2):334-350.
13. Dhir A., Kulkarni S. 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(4):921-925.
14. Dodgson S.J., Shank R.P., Maryanoff B.E. Topiramate as an inhibitor of carbonic anhydrase isoenzymes. Epilepsia 2000, 41(s1):35-39.
15. Du J., Creson T.K., Wu L.-J., Ren M., Gray N.A., Falke C., et al. The role of hippocampal GluR1 and GluR2 receptors in manic-like behavior. J. Neurosci. 2008, 28(1):68-79.
16. Eroglu L., Caglayan B. Anxiolytic and antidepressant properties of methylene blue in animal models. Pharmacol. Res. 1997, 36(5):381-385.
17. Esplugues J.V. NO as a signalling molecule in the nervous system. Br. J. Pharmacol. 2002, 135(5):1079-1095.
18. Ettinger A., Reed M., Cramer J. Depression and comorbidity in community-based patients with epilepsy or asthma. Neurology 2004, 63(6):1008-1014.
19. Förstermann U., Sessa W.C. Nitric oxide synthases: regulation and function. Eur. Heart J. 2012, 33(7):829-837.
20. Gao K., Gajwani P., Elhaj O., Calabrese J.R. Typical and atypical antipsychotics in bipolar depression. J. Clin. Psychiatry 2005, 66(11):1376-1385.
21. Garcia L.S., Comim C.M., Valvassori S.S., Réus G.Z., Barbosa L.M., Andreazza A.C., et al. Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Prog. Neuropsychopharmacol. Biol. Psychiatry 2008, 32(1):140-144.
22. 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(5):323-332.
23. Ghasemi M., Raza M., Dehpour A. NMDA receptor antagonists augment antidepressant-like effects of lithium in the mouse forced swimming test. J. Psychopharmacol. 2009, 24:585-594.
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 2009, 206(2):325-333.
25. Haj-Mirzaian A., Ostadhadi S., Kordjazy N., Dehpour A.R., Mehr S.E. Opioid/NMDA receptors blockade reverses the depressant-like behavior of foot shock stress in the mouse forced swimming test. Eur. J. Pharmacol. 2014, 735:26-31.
26. Haj-Mirzaian A., Kordjazy N., Haj-Mirzaian A., Ostadhadi S., Ghasemi M., Amiri S., et al. Evidence for the involvement of NMDA receptors in the antidepressant-like effect of nicotine in mouse forced swimming and tail suspension tests. Psychopharmacology 2015, 232(19):3551-3561.
27. Haj-Mirzaian A., Kordjazy N., Ostadhadi S., Amiri S., Haj-Mirzaian A., Dehpour A.-R. Fluoxetine reverses the behavioral despair induced by neurogenic stress in mice: role of N-methyl d-aspartate and opioid receptors. Can. J. Physiol. Pharmacol. 2016, (January).
28. Harden C.L. The co-morbidity of depression and epilepsy: epidemiology, etiology, and treatment. Neurology 2002, 59(6 Suppl. 4):S48-S55.
29. Hargreaves G.A., McGregor I.S. Topiramate moderately reduces the motivation to consume alcohol and has a marked antidepressant effect in rats. Alcohol.: Clin. Exp. Res. 2007, 31(11):1900-1907.
30. 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(3):207-213.
31. 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(4):274-281.
32. Hashimoto K., Sawa A., Iyo M. Increased levels of glutamate in brains from patients with mood disorders. Biol. Psychiatry 2007, 62(11):1310-1316.
33. 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(1):479-484.
34. Herrero A.I., Del Olmo N., González-Escalada J.R., Solís J.M. Two new actions of topiramate: inhibition of depolarizing GABA A-mediated responses and activation of a potassium conductance. Neuropharmacology 2002, 42(2):210-220.
35. Hesdorffer D.C., Hauser W.A., Annegers J.F., Cascino G. Major depression is a risk factor for seizures in older adults. Ann. Neurol. 2000, 47(2):246-249.
36. Hesdorffer D.C., Hauser W.A., Olafsson E., Ludvigsson P., Kjartansson O. Depression and suicide attempt as risk factors for incident unprovoked seizures. Ann. Neurol. 2006, 59(1):35-41.
37. Jackson M., Turkington D. Depression and anxiety in epilepsy. J. Neurol. Neurosurg. Psychiatry 2005, 76(Suppl. 1). i45-i7.
38. Joca S.R.L., Guimarães F.S. Inhibition of neuronal nitric oxide synthase in the rat hippocampus induces antidepressant-like effects. Psychopharmacology 2006, 185(3):298-305.
39. Kanner A.M. Depression and epilepsy: a new perspective on two closely related disorders. Epilepsy Curr. 2006, 6(5):141-146.
40. Karolewicz B., Paul I.A., Antkiewicz-Michaluk L. Effect of NOS inhibitor on forced swim test and neurotransmitters turnover in the mouse brain. Polish J. Pharmacol. 2001, 53(6):587-596.
41. Kaster M.P., Rosa A.O., Santos A.R., Rodrigues A.L.S. Involvement of nitric oxide-cGMP pathway in the antidepressant-like effects of adenosine in the forced swimming test. Int. J. Neuropsychopharmacol. 2005, 8(04):601-606.
42. 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(2):204-209.
43. Khan M.I., Ostadhadi S., Zolfaghari S., Mehr S.E., Hassanzadeh G., Dehpour A.-R. The involvement of NMDA receptor/NO/cGMP pathway in the antidepressant like effects of baclofen in mouse force swimming test. Neurosci. Lett. 2016, 612:52-61.
44. Kim M.J., Futai K., Jo J., Hayashi Y., Cho K., Sheng M. Synaptic accumulation of PSD-95 and synaptic function regulated by phosphorylation of serine-295 of PSD-95. Neuron 2007, 56(3):488-502.
45. Kimiskidis V.K., Triantafyllou N.I., Kararizou E., Gatzonis S.-S., Fountoulakis K.N., Siatouni A., et al. Depression and anxiety in epilepsy: the association with demographic and seizure-related variables. Ann. Gen. Psychiatry 2007, 6(1):28.
46. Kordjazy N., Haj-Mirzaian A., Amiri S., Ostadhadi S., Kordjazy M., Sharifzadeh M., et al. Elevated level of nitric oxide mediates the anti-depressant effect of rubidium chloride in mice. Eur. J. Pharmacol. 2015, 762:411-418.
47. Kordjazy N., Haj-Mirzaian A., Amiri S., Ostadhadi S., Amini-khoei H., Dehpour A.R. Involvement of N-methyl-d-aspartate receptors in the antidepressant-like effect of 5-hydroxytryptamine 3 antagonists in mouse forced swimming test and tail suspension test. Pharmacol. Biochem. Behav. 2015, 141:1-9.
48. Law A.J., Deakin J. Asymmetrical reductions of hippocampal NMDAR1 glutamate receptor mRNA in the psychoses. Neuroreport 2001, 12(13):2971-2974.
49. Ledo A., Frade J., Barbosa R.M., Laranjinha J. Nitric oxide in brain: diffusion, targets and concentration dynamics in hippocampal subregions. Mol. Aspects Med. 2004, 25(1):75-89.
50. Maidment I.D. The use of topiramate in mood stabilization. Ann. Pharmacother. 2002, 36(7/8):1277-1281.
51. Mantovani M., Pértile R., Calixto J.B., Santos A.R., Rodrigues A.L.S. Melatonin exerts an antidepressant-like effect in the tail suspension test in mice: evidence for involvement of N-methyl-d-aspartate receptors and the l-arginine-nitric oxide pathway. Neurosci. Lett. 2003, 343(1):1-4.
52. McElroy S.L., Suppes T., Keck P.E., Frye M.A., Denicoff K.D., Altshuler L.L., et al. Open-label adjunctive topiramate in the treatment of bipolar disorders. Biol. Psychiatry 2000, 47(12):1025-1033.
53. McIntyre R.S., Mancini D.A., McCann S., Srinivasan J., Sagman D., Kennedy S.H. Topiramate versus Bupropion SR when added to mood stabilizer therapy for the depressive phase of bipolar disorder: a preliminary single-blind study. Bipolar Disord. 2002, 4(3):207-213.
54. Meir A., Ginsburg S., Butkevich A., Kachalsky S.G., Kaiserman I., Ahdut R., et al. Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol. Rev. 1999, 79(3):1019-1088.
55. Molina-Hernández M., Téllez-Alcántara N.P., Olivera-Lopez J.I., Jaramillo M.T. 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 2010, 31(6):1184-1189.
56. Molina-Hernández M., Téllez-Alcántara N.P., Olivera-López J.I., Jaramillo M.T. The antidepressant-like effects of topiramate alone or combined with 17β-estradiol in ovariectomized Wistar rats submitted to the forced swimming test. Psychopharmacology 2014, 231(17):3343-3350.
57. Moncada S., Bolaños J.P. Nitric oxide, cell bioenergetics and neurodegeneration. J. Neurochem. 2006, 97(6):1676-1689.
58. Nowak G., Ordway G.A., Paul I.A. Alterations in the N-methyl-d-asparatate (NMDA) receptor complex in the frontal cortex of suicide victims. Brain Res. 1995, 675(1):157-164.
59. Ostadhadi S., Haj-Mirzaian A., Nikoui V., Kordjazy N., Dehpour A.R. Involvement of opioid system in antidepressant-like effect of the cannabinoid CB1 receptor inverse agonist AM-251 after physical stress in mice. Clin. Exp. Pharmacol. Physiol. 2015, 43:203-212.
60. Ostadhadi S., Kordjazy N., Haj-Mirzaian A., Ameli S., Akhlaghipour G., Dehpour A. Involvement of NO/cGMP pathway in the antidepressant-like effect of gabapentin in mouse forced swimming test. Naunyn Schmiedebergs Arch. Pharmacol. 2016, 1-10.
61. Patil C.S., Singh V.P., Kulkarni S.K. Peripheral and central activation of nitric oxide-cyclic GMP pathway by sildenafil. Inflammopharmacology 2005, 13(5-6):467-478.
62. Paul I.A., Skolnick P. Glutamate and depression. Ann. N. Y. Acad. Sci. 2003, 1003(1):250-272.
63. Porsolt R., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Thér. 1977, 229(2):327-336.
64. Qian J., Noebels J.L. Topiramate alters excitatory synaptic transmission in mouse hippocampus. Epilepsy Res. 2003, 55(3):225-233.
65. Rawls S.M., Thomas T., Adeola M., Patil T., Raymondi N., Poles A., et al. Topiramate antagonizes NMDA-and AMPA-induced seizure-like activity in planarians. Pharmacol. Biochem. Behav. 2009, 93(4):363-367.
66. Rogóz Z., Skuza G., Maj J., Danysz W. Synergistic effect of uncompetitive NMDA receptor antagonists and antidepressant drugs in the forced swimming test in rats. Neuropharmacology 2002, 42(8):1024-1030.
67. Rosa A.O., Lin J., Calixto J.B., Santos A.R.S., Rodrigues A.L.S. Involvement of NMDA receptors and l-arginine-nitric oxide pathway in the antidepressant-like effects of zinc in mice. Behav. Brain Res. 2003, 144(1):87-93.
68. Sanacora G., Zarate C.A., Krystal J.H., Manji H.K. Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat. Rev. Drug Discov. 2008, 7(5):426-437.
69. + channel-mediated release of [3H] glutamate in hippocampal nerve endings. Neuropharmacology 2007, 52(2):598-605.
70. Skolnick P. Antidepressants for the new millennium. Eur. J. Pharmacol. 1999, 375(1):31-40.
71. + current fractions by the new anticonvulsant topiramate. J. Pharmacol. Exp. Ther. 1999, 288(3):960-968.
72. Van Staveren W.C., Steinbusch H.W., Markerink-van Ittersum M., Behrends S., De Vente J. Species differences in the localization of cGMP-producing and NO-responsive elements in the mouse and rat hippocampus using cGMP immunocytochemistry. Eur. J. Neurosci. 2004, 19(8):2155-2168.
73. Volke V., Wegener G., Bourin M., Vasar E. Antidepressant-and anxiolytic-like effects of selective neuronal NOS inhibitor 1-(2-trifluoromethylphenyl)-imidazole in mice. Behav. Brain Res. 2003, 140(1):141-147.
74. Von Seggern R.L., Mannix L.K., Adelman J.U. Efficacy of topiramate in migraine prophylaxis: a retrospective chart analysis, headache. J. Head Face Pain 2002, 42(8):804-809.
75. Wegener G., Volke V., Harvey B.H., Rosenberg R. Local, but not systemic, administration of serotonergic antidepressants decreases hippocampal nitric oxide synthase activity. Brain Res. 2003, 959(1):128-134.
76. White H.S., Brown S.D., Woodhead J.H., Skeen G.A., Wolf H.H. Topiramate enhances GABA-mediated chloride flux and GABA-evoked chloride currents in murine brain neurons and increases seizure threshold. Epilepsy Res. 1997, 28(3):167-179.
77. White H.S., Brown S.D., Woodhead J., Skeen G.A., Wolf H.H. Topiramate modulates GABA-evoked currents in murine cortical neurons by a nonbenzodiazepine mechanism. Epilepsia 2000, 41(s1):17-20.
78. White H.S. Molecular pharmacology of topiramate: managing seizures and preventing migraine, headache. J. Head Face Pain 2005, 45(s1):S48-S56.
79. Yatham L.N. Newer anticonvulsants in the treatment of bipolar disorder. J. Clin. Psychiatry 2004, 65:28-35.
80. 2+ homeostasis in pentylentetrazol-induced epilepsy of rats. J. Recept. Signal Transduct. 2011, 31(2):173-179.
81. Zarate C.A., Singh J.B., Carlson P.J., Brutsche N.E., Ameli R., Luckenbaugh D.A., et al. A randomized trial of an N-methyl-d-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiatry 2006, 63(8):856-864.
82. 2+ currents in CA1 pyramidal neurons in vitro. Epilepsia 1998, 39(Suppl. 6):44.
83. Zhang Xl, Velumian A.A., Jones O.T., Carlen P.L. Modulation of high-voltage-activated calcium channels in dentate granule cells by topiramate. Epilepsia 2000, 41(s1):52-60.
84. Zomkowski A.D., Engel D., Gabilan N.H., Rodrigues A.L.S. Involvement of NMDA receptors and l-arginine-nitric oxide-cyclic guanosine monophosphate pathway in the antidepressant-like effects of escitalopram in the forced swimming test. Eur. Neuropsychopharmacol. 2010, 20(11):793-801.