Abstract
The present study investigated a possible antidepressant-like effect of ((4-tert-butylcyclohexylidene)methyl) (4-methoxystyryl) sulfide (BMMS) by using the forced swimming test (FST) and the tail suspension test (TST) in Swiss mice. The contribution of serotoninergic, glutamatergic and nitrergic systems in the antidepressant-like activity of BMMS was evaluated. We also examined the involvement of monoamine oxidase (MAO)-A, MAO-B and Na+, K+-ATPase activities in prefrontal cortex of mice. BMMS, (0.1–10 mg/kg, intragastrically (i.g.)) and fluoxetine (32 mg/kg, i.g.) decreased the immobility time in the FST and TST. The anti-immobility effect of BMMS (10 mg/kg, i.g.) in the TST was prevented by the pretreatment of mice with WAY100635 (0.1 mg/kg, subcutaneously (s.c.), a 5-HT1A receptor antagonist), ketanserin (5 mg/kg, intraperitoneal (i.p.), a 5-HT2A/2C receptor antagonist), and partially blocked by ondansetron (1 mg/kg, i.p., a 5-HT3 receptor antagonist). The anti-immobility effect of BMMS (10 mg / kg, i.g.) was not avoided by pretreatment with MK-801 (0.01 mg/kg, s.c. a non-competitive N-methyl D-Aspartate (NMDA) receptor) in the TST. Pretreatment with L-arginine (500 mg/kg, i.p., a nitric oxide precursor) reversed partially the reduction in the immobility time elicited by BMMS (10 mg/kg, i.g.) in TST. BMMS altered Na+,K+-ATPase and MAO-A activities in prefrontal cortex of mice, but was not able to change the MAO-B activity. In conclusion, BMMS exerted an antidepressant-like effect in mice and serotonergic and nitrergic systems are involved in the antidepressant-like action of compound. BMMS modulated MAO-A and Na+, K+- ATPase activities in prefrontal cortex of mice.
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Abreu TM, Monteiro VS, Martins ABS, Teles FB, da Conceição Rivanor R, Mota ÉF, Macedo DS, de Vasconcelos SMM, Júnior JERH, Benevides NMB (2018) Involvement of the dopaminergic system in the antidepressant-like effect of the lectin isolated from the red marine alga Solieria filiformis in mice. Int J Biol Macromol 111:534–541
Altamura AC, Dell'Osso B, Serati M, Ciabatti M, Buoli M (2008) Recent assessments on the neuro- biology of major depression: a critical review. Riv Psichiatr 43:185–207
Bogatko K, Poleszak E, Szopa A, Wyska E, Wlaź P, Świąder K, Wlaź A, Doboszewska U, Rojek K, Serefko A (2018) The influence of selective A1 and A2A receptor antagonists on the antidepressant-like activity of moclobemide, venlafaxine and bupropion in mice. J Pharm Pharmacol 70:1200–1208
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brocardo PS, Budni J, Kaster MP, Santos ARS, Rodrigues ALS (2008) Folic acid administration produces an antidepressant-like effect in mice: evidence for the involvement of the serotonertic and noradrenergic systems. Neuropharmacology 54:464–473
Brüning CA, Souza AC, Gai BM, Zeni G, Nogueira CW (2011) Antidepressant-like effect of m-trifluoromethyl-diphenyl diselenide in the mouse forced swimming test involves opioid and serotonergic systems. Eur J Pharmacol 658:145–149
Carfagna MA, Ponsler GD, Muhoberac BB (1996) Inhibition of ATPase activity in rat synaptic plasma membranes by simultaneous exposure to metals. Chem Biol Interact 8:53–65
Converge C (2015) Sparse whole-genome sequencing identifies two loci for major depressive disorder. Nature 523:588–591
Crema L, Schlabitz M, Tagliari B, Cunha A, Simao F, Krolow R, Pettenuzzo L, Salbego C, Vendite D, Wyse AT, Dalmaz C (2010) Na(+), K (+) ATPase activity is reduced in amygdala of rats with chronic stress-induced anxiety-like behavior. Neurochem Res 35:1787–1795
Cryan JF, Page ME, Lucki I (2005) Differential behavioral effects of the antidepressants reboxetine, fluoxetine, and moclobemide in a modified forced swim test following chronic treatment. Psychopharmacology 182:335–344
Da Silva FD, Pinz MP, Oliveira RL, Rodrigues KC, Silveira CC, Jesse CR, Roman SS, Wilhelm EA, Luchese C (2017) Organosulfur compound protects against memory decline induced by scopolamine through modulation of oxidative stress and Na+, K+- ATPase activity in mice. Metab Brain Dis 32:1819–1828
David DJ, Renard CE, Jolliet P, Hascoet M, Bourin M (2003) Antidepressant-like effects in various mice strains in the forced swimming test. Psychopharmacology 166:373–382
De Oliveira DR, da Silva DM, Florentino IF, de Brito AF, Fajemiroye JO, da Silva DPB, da Rocha FF, Costa EA, Galdino PM (2018) Monoamine involvement in the antidepressant-like effect of β-Caryophyllene. CNS Neurol Disord Drug Targets 17:309–320
De Vasconcellos AP, Zugno AI, Dos Santos AH, Nietto FB, Crema LM, Gonçalves M, Franzon R, de Souza Wyse AT, da Rocha ER, Dalmaz C (2005) Na+,K(+)-ATPase activity is reduced in hippocampus of rats submitted to an experimental model of depression: effect of chronic lithium treatment and possible involvement in learning deficits. Neurobiol Learn Mem 84:102–110
Elhwuegi AS (2004) Central monoamines and their role in major depression. Prog Neuro-Psychopharmacol Biol Psychiatry 228:435–451
Fajemiroye JO, Adam K, Jordan KZ, Alves CE, Aderoju AA (2018) Evaluation of anxiolytic and antidepressant-like activity of aqueous leaf extract of nymphaea lotus Linn. In mice. Iran J Pharm Res 17:613–626
Finberg JP, Rabey JM (2016) Inhibitors of MAO-A and MAO-B in psychiatry and neurology. Front Pharmacol 7:340
Fišar Z (2016) Drugs related to monoamine oxidase activity. Prog Neuro-Psychopharmacol Biol Psychiatry 69:112–124
Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400
Gamaro GD, Streck EL, Matte C, Prediger ME, Wyse AT, Dalmaz C (2003) Reduction of hippocampal Na+, K+-ATPase activity in rats subjected to an experimental model of depression. Neurochem Res 28:1339–1344
Goldstein I, Levy T, Galili D, Ovadia H, Yirmiya R, Rosen H, Lichtstein D (2006) Involvement of Na(+), K(+)-ATPase and endogenous digitalis-like compounds in depressive disorders. Biol Psychiatry 60:491–499
Goncalves AE, Burger C, Amoah SK, Tolardo R, Biavatti MW, de Souza MM (2012) The antidepressant-like effect of Hedyosmum brasiliense and its sesquiterpene lactone, podoandin in mice: evidence for the involvement of adrenergic, dopaminergic and serotonergic systems. Eur J Pharmacol 674:307–314
Grunewald M, Johnson S, Lu D, Wang Z, Lomberk G, Albert PR, Stockmeier CA, Meyer JH, Urrutia R, Miczek KA, Austin MC, Wang J, Paul IA, Woolverton WL, Seo S, Sittman DB, Ou XM (2012) Mechanistic role for a novel glucocorticoid-KLF11 (TIEG2) protein pathway in stress-induced monoamine oxidase a expression. J Biol Chem 287:24195–24206
Guimarães FS, Beijamini V, Moreira FA, Aguiar DC, De Lucca ACB (2005) Role of nitric oxide in brain regions related to defensive reactions. Neurosci Biobehav Rev 29:1313–1322
Haj-Mirzaian A, Amiri S, Kordjazy N, Rahimi-Balaei M, Haj-Mirzaian A, Marzban H, Aminzadeh A, Dehpour AR, Mehr SE (2015) Blockade of NMDA receptors reverses the depressant, but not anxiogenic effect of adolescence social isolation in mice. Eur J Pharmacol 750:160–166
Harkin A, Connor TJ, Walsh M, St John N, Kelly JP (2003) Serotonergic mediation of the antidepressant-like effects of nitric oxide synthase inhibitors. Neuropharmacology 44:616–623
Harris S, Johnson S, Duncan JW, Udemgba C, Meyer JH, Albert PR, Lomberk G, Urrutia R, Ou XM, Stockmeier CA, Wang JM (2015) Evidence revealing deregulation of the KLF11-MAO a pathway in association with chronic stress and depressive disorders. Neuropsychopharmacology 40:1373–1382
Higuchi Y, Soga T, Parhar IS (2017) Regulatory pathways of monoamine oxidase a during social stress. Front Neurosci 11:604
Ianiski FR, Alves CB, Bassaco MM, Silveira CC, Luchese C (2014) Protective effect of ((4-tert-butylcyclohexylidene) methyl) (4-methoxystyryl) sulfide, a novel unsymmetrical divinyl sulfide, on an oxidative stress model induced by sodium nitroprusside in mouse brain: involvement of glutathione peroxidase activity. J Pharm Pharmacol 66:1747–1754
Ianiski FR, Bassaco MM, Vogt AG, Reis AS, Pinz MP, Voss GT, De Oliveira RL, Silveira CC, Wilhelm EA, Luchese C (2017) Antinociceptive property of vinyl sulfides in spite of their weak antioxidant activity. Med Chem Res 1:1–6
Jesse CR, Savegnago L, Nogueira CW (2008) Spinal mechanisms of antinociceptive effect caused by oral administration of bis selenide in mice. Brain Res 1231:25–33
Jesse CR, Wilhelm EA, Bortolatto CF, Nogueira CW (2010) Evidence for the involvement of the serotonergic 5-HT2A/C and 5-HT3 receptors in the antidepressant-like effect caused by oral administration of bis selenide in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 34:294–302
Joca SR, Moreira FA, Wegener G (2015) Atypical neurotransmitters and the neurobiology of depression. CNS Neurol Disord Drug Targets 14:1001–1011
Johnson MD, Ma PM (1993) Localization of NADPH diaphorase activity in monoaminergic neurons of the rat brain. J Comp Neurol 332:391–406
Kahn D, Silver JM, Opler LA (1989) The safety of switching rapidly from tricyclic antidepressants to monoamine oxidase inhibitors. J Clin Psychopharmacol 9:198–202
Kaster MP, Rosa AO, Santos ARS, Rodrigues ALS (2005) Involvement of nitric oxide–cGMP pathway in the antidepressant-like effects of adenosine in the forced swimming test. Int J Neuropsychopharmacol 8:601–606
Kirshenbaum GS, Saltzman K, Rose B, Petersen J, Vilsen B, Roder JC (2011) Decreased neuronal Na+, K+ -ATPase activity in Atp1a3 heterozygous mice increases susceptibility to depression-like endophenotypes by chronic variable stress. Genes Brain Behav 10:542–550
Krajl MC (1965) A rapid microfluorimetric determination of monoamine oxidase. Biochem Pharmacol 14:1683–1685
Lesch KP, Aulakh CS, Wolozin BL, Tolliver TJ, Hill JL, Murphy DL (1993) Regional brain expression of serotonin transporter mRNA and its regulation by reuptake inhibiting antidepressants. Brain Res Mol Brain Res 17:31–35
Liebenberg N, Joca S, Wegener G (2015) Nitric oxide involvement in the antidepressant-like effect of ketamine in the Flinders sensitive line rat model of depression. Acta Neuropsychiatr 27:90–96
Mann J (2003) Neurobiology of suicidal behaviour. Nature Reviews 4:819–828
Matsumoto T, Furuta T, Nimura Y, Suzuki O (1984) 3-(p-Hydroxyphenyl) propionic acid as a new fluorogenic reagent for amine oxidase assays. Anal Biochem 138:133–136
McKenna MT, Michaud CM, Murray CJ, Marks JS (2015) Assessing the burden of disease in the United States using disability adjusted life years. Am J Prev Med 28:415–423
Medvedev AE, Ivanov AS, Veselovsky AV, Skvortsov VS, Archakov AI (1996) QSAR analysis of indole analogues as monoamine oxidase inhibitors. J Chem Inf Comput Sci 36:664–671
Menard C, Hodes GE, Russo SJ (2015) Pathogenesis of depression: insights from human and rodent studies. Neurosci 321:138–162
Meyer JH, Ginovart N, Boovariwala A, Sagrati S, Hussey D, Garcia A, Young T, Praschak-Rieder N, Wilson AA, Houle S (2006) Elevated monoamine oxidase a levels in the brain: an explanation for the monoamine imbalance of major depression. Arch Gen Psychiatry 63:1209–1216
Meyer JH, Wilson AA, Sagrati S, Miler L, Rusjan P, Bloomfield PM, Clark M, Sacher J, Voineskos AN, Houle S (2009) Brain monoamine oxidase a binding in major depressive disorder. Arch Gen Psychiatry 66:1304–1312
Moretti M, Ribeiro CM, Neis VB, Bettio LEB, Rosa PB, Rodrigues ALS (2018) Evidence for the involvement of opioid system in the antidepressant-like effect of ascorbic acid. Naunyn Schmiedeberg's Arch Pharmacol 391:169–176
Ostadhadi S, Imran Khanc M, Norouzi-Javidan A, Chamanara M, Jazaeri F, Zolfagharie S, Dehpoura AR (2016) 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 Res Bull 122:62–70
Parcell S (2002) Sulfur in human nutrition and applications in medicine. Altern Med Rev 7:22–44
Pesarico AP, Stangherlin EC, Mantovani AC, Zeni G, Nogueira CW (2015) 7-Fluoro-1,3-diphenylisoquinoline-1-amine aboleishes depressive- like behavior and prefrontal cortical oxidative damage induced by acute restraint stress in mice. Physiol Behav 149:294–302
Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730–732
Réus GZ, Abelaira HM, Tuon T, Titus SE, Ignácio ZM, Rodrigues AL, Quevedo J (2016) Glutamatergic NMDA receptor as therapeutic target for depression. Adv Protein Chem Struct Biol 103:169–202
Ripoll N, David DJ, Dailly E, Hascoet M, Bourin M (2003) Antidepressant-like effects in various mice strains in the tail suspension test. Behav Brain Res 143:193–200
Rosa AO, Lin J, Calixto JB, Santos AR, Rodrigues AL (2003) Involvement of NMDA receptors and L-arginine-nitric oxide pathway in the antidepressant-like effects of zinc in mice. Behav Brain Res 144:87–93
Sanacora G, Zarate CA, Krystal JH, Manji HK (2008) Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nature Rev Drug Disc 7:426–437
Sartim AG, Brito BM, Gobira PH, Joca SRL (2019) Attenuation of glutamatergic and nitrergic system contributes to the antidepressant-like effect induced by capsazepine in the forced swimming test. Behav Pharmacol 30:59–66
Shamraj OI, Lingrel JB (1994) A putative fourth Na+,K(+)-ATPase alpha-subunit gene is expressed in testis. Proc Natl Acad Sci 91:12952–12956
Shih JC, Chen K, Ridd MJ (1999) Monoamine oxidase: from genes to behavior. Annu Rev Neurosci 22:197–217
Silveira CC, Rinaldi F, Bassaco MM, Guadagnin RC, Kaufman TS (2011) Synthesis of (diphenylphosphinoyl) methyl vinyl sulfides, symmetric and asymmetric divinyl sulfides from bis[(diphenylphosphinoyl)methyl] sulfide. Synthesis 8:1233–1242
Soto-Otero R, Méndez-Alvarez E, Hermida-Ameijeiras A, Sánchez-Sellero I, Cruz-Landeira A, Lamas ML (2001) Inhibition of brain monoamine oxidase activity by the generation of hydroxyl radicals: potential implications in relation to oxidative stress. Life Sci 69:879–889
Steru L, Chermat R, Thierry B, Simon P (1985) The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology 85:367–370
Tagliaferro P, Ramos AJ, Lopez-Costa JJ, Lopez EM, Saavedra JP, Brusco A (2001) Increased nitric oxide synthase activity in a model of serotonin depletion. Brain Res Bull 54:199–205
Tochigi M, Iwamoto K, Bundo M, Sasaki T, Kato N, Kato T (2008) Gene expression profiling of major depression and suicide in the prefrontal cortex of postmortem brains. Neurosci Res 60:184–191
Trivedi MH, Rush AJ, Wisniewski SR, Nierenberg AA, Warden D, Ritz L, Norquist G, Howland RH, Lebowitz B, McGrath PJ, Shores-Wilson K, Biggs MM, Balasubramani GK, Fava M (2006) Evaluation of outcomes with citalopram for depression using measurement-based care in STAR*D: implications for clinical practice. Am J Psychiatry 163:28–40
Tsugeno Y, Ito A (1997) A key amino acid responsible for substrate selectivity of monoamine oxidase a and B. J Biol Chem 272:14033–14036
Tsugeno Y, Hirashiki I, Ogata F, Ito A (1995) Regions of the molecule responsible for substrate specificity of monoamine oxidase a and B: a chimeric enzyme analysis. J Biochem 118:974–980
Velasquez D, Quines C, Pistóia R, Zeni G, Nogueira CW (2017) Selective inhibition of MAO-A activity results in an antidepressant-like action of 2-benzoyl 4-iodoselenophene in mice. Physiol Behav 170:100–105
Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83:482–504
Wong ML, Licinio J (2001) Research and treatment approaches to depression. Nat Rev Neurosci 2:343–351
World Health Organization - WHO (2010) Mental health. IOP Publishing PhysicsWeb. http://www.who.int/topics/mental_health/en. Accessed 19 September 2017
Zomkowski ADE, Rosa AO, Lin J, Santos AR, Calixto JB, Rodrigues LS (2004) Evidence for serotonin receptor subtypes involvement in agmatine antidepressant like-effect in the mouse forced swimming test. Brain Res 1023:253–263
Acknowledgments
We are grateful for the financial support and scholarships from the Brazilian agencies CNPq (UNIVERSAL 408874/2016-3), FAPERGS (PRONEM 16/2551-0000240-1, PRONUPEQ 16/2551-0000526-5 and PqG 17/2551-0001013-2). CNPq is also acknowledged for the fellowship to C.C.S., E.A.W. and C. L. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível superior – Brasil (CAPES) - Finance Code 001.
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de Oliveira, R.L., Voss, G.T., Paltian, J.J. et al. Contribution of serotonergic and nitrergic pathways, as well as monoamine oxidase-a and Na+, K+-ATPase enzymes in antidepressant-like action of ((4-tert-butylcyclohexylidene) methyl) (4-methoxystyryl) sulfide (BMMS). Metab Brain Dis 34, 1313–1324 (2019). https://doi.org/10.1007/s11011-019-00436-x
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DOI: https://doi.org/10.1007/s11011-019-00436-x