Restricted accessResearch articleFirst published online 2017-9
Opioid system contribution to the antidepressant-like action of m -trifluoromethyl-diphenyl diselenide in mice: A compound devoid of tolerance and withdrawal syndrome
Animal and clinical researches indicate that the opioid system exerts a crucial role in the etiology of mood disorders and is a target for intervention in depression treatment. This study investigated the contribution of the opioid system to the antidepressant-like action of acute or repeated m-trifluoromethyl-diphenyl diselenide administration to Swiss mice. m-Trifluoromethyl-diphenyl diselenide (50 mg/kg, intragastric) produced an antidepressant-like action in the forced swimming test from 30 min to 24 h after treatment. This effect was blocked by the µ and δ-opioid receptor antagonists, naloxonazine (10 mg/kg, intraperitoneally) and naltrindole (3 mg/kg, intraperitoneally), and it was potentiated by a κ-opioid receptor antagonist, norbinaltrophimine (1 mg/kg, subcutaneously). Combined treatment with subeffective doses of m-trifluoromethyl-diphenyl diselenide (10 mg/kg, intragastric) and morphine (1 mg/kg, subcutaneously) resulted in a synergistic antidepressant-like effect. The opioid system contribution to the m-trifluoromethyl-diphenyl diselenide antidepressant-like action was also demonstrated in the modified tail suspension test, decreasing mouse immobility and swinging time and increasing curling time, results similar to those observed using morphine, a positive control. Treatment with m-trifluoromethyl-diphenyl diselenide induced neither tolerance to the antidepressant-like action nor physical signs of withdrawal, which could be associated with the fact that m-trifluoromethyl-diphenyl diselenide did not change the mouse cortical and hippocampal glutamate uptake and release. m-Trifluoromethyl-diphenyl diselenide treatments altered neither locomotor nor toxicological parameters in mice. These findings demonstrate that m-trifluoromethyl-diphenyl diselenide elicited an antidepressant-like action by direct or indirect μ and δ-opioid receptor activation and the κ-opioid receptor blockade, without inducing tolerance, physical signs of withdrawal and toxicity.
Abdel-ZaherAOAbdel-RahmanMSELwaseiFM (2010) Blockade of nitric oxide overproduction and oxidative stress by Nigella sativa oil attenuates morphine-induced tolerance and dependence in mice. Neurochem Res35: 1557–1565.
2.
AlmatroudiAHusbandsSMBaileyCPet al. (2015) Combined administration of buprenorphine and naltrexone produces antidepressant-like effects in mice. J Psychopharmacol29: 812–821.
3.
BerrocosoEIkedaKSoraIet al. (2013) Active behaviours produced by antidepressants and opioids in the mouse tail suspension test. Int J Neuropsychopharmacol16: 151–162.
4.
BerrocosoEMicoJA (2009) Cooperative opioid and serotonergic mechanisms generate superior antidepressant-like effects in a mice model of depression. Int J Neuropsychopharmacol12: 1033–1044.
5.
BerrocosoESanchez-BlazquezPGarzonJet al. (2009) Opiates as antidepressants. Curr Pharm Des15: 1612–1622.
BodnarRJ (2017) Endogenous opiates and behavior: 2015. Peptides88: 126–188.
8.
BrocardoPSBudniJLobatoKRet al. (2009) Evidence for the involvement of the opioid system in the antidepressant-like effect of folic acid in the mouse forced swimming test. Behav Brain Res200: 122–127.
BruningCAMartiniFSoaresSMet al. (2015a) m-Trifluoromethyl-diphenyl diselenide, a multi-target selenium compound, prevented mechanical allodynia and depressive-like behavior in a mouse comorbid pain and depression model. Prog Neuropsychopharmacol Biol Psychiatry63: 35–46.
11.
BruningCAMartiniFSoaresSMet al. (2015b) Depressive-like behavior induced by tumor necrosis factor-alpha is attenuated by m-trifluoromethyl-diphenyl diselenide in mice. J Psychiatr Res 66–67: 75–83.
12.
BruningCAPrigolMRoehrsJAet al. (2010) Evidence for the involvement of mu-opioid and delta-opioid receptors in the antinociceptive effect caused by oral administration of m-trifluoromethyl-diphenyl diselenide in mice. Behav Pharmacol21: 621–626.
13.
BruningCASouzaACGaiBMet al. (2011) Antidepressant-like effect of m-trifluoromethyl-diphenyl diselenide in the mouse forced swimming test involves opioid and serotonergic systems. Eur J Pharmacol658: 145–149.
14.
CarrGVBangasserDABetheaTet al. (2010) Antidepressant-like effects of kappa-opioid receptor antagonists in Wistar Kyoto rats. Neuropsychopharmacology35: 752–763.
15.
ChristieM (2008) Cellular neuroadaptations to chronic opioids: Tolerance, withdrawal and addiction. Br J Pharmacol154: 384–396.
CryanJFValentinoRJLuckiI (2005) Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev29: 547–569.
18.
FalconEMaierKRobinsonSAet al. (2015) Effects of buprenorphine on behavioral tests for antidepressant and anxiolytic drugs in mice. Psychopharmacology232: 907–915.
19.
FilhoCBDel FabbroLde GomesMGet al. (2013) Kappa-opioid receptors mediate the antidepressant-like activity of hesperidin in the mouse forced swimming test. Eur J Pharmacol698: 286–291.
20.
GaiBMBortolattoCFBruningCAet al. (2014) Depression-related behavior and mechanical allodynia are blocked by 3-(4-fluorophenylselenyl)-2,5-diphenylselenophene in a mouse model of neuropathic pain induced by partial sciatic nerve ligation. Neuropharmacology79: 580–589.
21.
GaoSGaoHFanYet al. (2016) Yiguanjian cataplasm attenuates opioid dependence in a mouse model of naloxone-induced opioid withdrawal syndrome. J Tradit Chin Med36: 464–470.
22.
GassawayMMRivesMLKruegelACet al. (2014) The atypical antidepressant and neurorestorative agent tianeptine is a mu-opioid receptor agonist. Transl Psychiatry4: e411.
23.
GlassMJKruzichPJKreekMJet al. (2004) Decreased plasma membrane targeting of NMDA-NR1 receptor subunit in dendrites of medial nucleus tractus solitarius neurons in rats self-administering morphine. Synapse53: 191–201.
24.
Haj-MirzaianAKordjazyNOstadhadiSet al. (2016) Fluoxetine reverses the behavioral despair induced by neurogenic stress in mice: Role of N-methyl-d-aspartate and opioid receptors. Can J Physiol Pharmacol94: 599–612.
HuXHuangFSzymusiakMet al. (2015) Curcumin attenuates opioid tolerance and dependence by inhibiting Ca2+/calmodulin-dependent protein kinase II α activity. J Pharmacol Exp Ther352: 420–428.
27.
JasinskiDRPevnickJSGriffithJD (1978) Human pharmacology and abuse potential of the analgesic buprenorphine: A potential agent for treating narcotic addiction. Arch Gen Psychiatry35: 501–516.
28.
JinLXinLGangPet al. (1999) Relationship between inhibition of agmatine on rat morphine physical dependence and opiate receptors. Chin J Drug Depend3: 178–181.
29.
KannetiRBhaveshDParamarDet al. (2011) Development and validation of a high-throughput and robust LC-MS/MS with electrospray ionization method for simultaneous quantitation of oseltamivir phosphate and its oseltamivir carboxylate metabolite in human plasma for pharmacokinetic studies. Biomed Chromatogr25: 727–733.
30.
KasterMPBudniJSantosARet al. (2007) Pharmacological evidence for the involvement of the opioid system in the antidepressant-like effect of adenosine in the mouse forced swimming test. Eur J Pharmacol576: 91–98.
31.
LinC-PKangK-HLinT-Het al. (2015) Role of spinal CXCL1 (GROα) in opioid tolerance: A human-to-rodent translational study. Anesthesiology122: 666.
MansouriMTNaghizadehBGhorbanzadehB (2014) Ellagic acid enhances morphine analgesia and attenuates the development of morphine tolerance and dependence in mice. Eur J Pharmacol741: 272–280.
35.
MaoJSungBJiRRet al. (2002) Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J Neurosci22: 8312–8323.
36.
MiguesPVLealRBMantovaniMet al. (1999) Synaptosomal glutamate release induced by the fraction Bc2 from the venom of the sea anemone Bunodosoma caissarum. Neuroreport10: 67–70.
37.
MulJDZhengJGoodyearLJ (2016) Validity assessment of 5 day repeated forced-swim stress to model human depression in young-adult C57BL/6J and BALB/cJ mice. eNeuro3: ENEURO. 0201–0216.2016.
38.
MurrayFHarrisonNJGrimwoodSet al. (2007) Nucleus accumbens NMDA receptor subunit expression and function is enhanced in morphine-dependent rats. Eur J Pharmacol562: 191–197.
39.
MurroughJWPerezAMPillemerSet al. (2013) Rapid and longer-term antidepressant effects of repeated ketamine infusions in treatment-resistant major depression. Biol Psychiatry74: 250–256.
40.
NogueiraCWRochaJB (2011) Toxicology and pharmacology of selenium: Emphasis on synthetic organoselenium compounds. Arch Toxicol85: 1313–1359.
41.
NogueiraCWZeniGRochaJBT (2004) Organoselenium and organotellurium compounds: Toxicology and pharmacology. Chem Rev104: 6255–6285.
42.
PaulmierC (1986) Selenoorganic functional groups. In: PaulmierC (ed.) Selenium Reagents and Intermediates in Organic Synthesis. 1st ed. Oxford: Pergamon Press, pp. 25–51.
43.
PorsoltRDBertinAJalfreM (1977a) Behavioral despair in mice: Primary screening-test for antidepressants. Arch Int Pharmacodyn Ther229: 327–336.
44.
PorsoltRDLepichonMJalfreM (1977b) Depression: New animal-model sensitive to antidepressant treatments. Nature266: 730–732.
45.
QuinesCBRosaSGVelasquezDet al. (2016) Diphenyl diselenide elicits antidepressant-like activity in rats exposed to monosodium glutamate: A contribution of serotonin uptake and Na(+), K(+)-ATPase activity. Behav Brain Res301: 161–167.
46.
RehniAKBhatejaPSinghTGet al. (2008) Nuclear factor-kappa-B inhibitor modulates the development of opioid dependence in a mouse model of naloxone-induced opioid withdrawal syndrome. Behav Pharmacol19: 265–269.
47.
RobinsonSAEricksonRLBrowneCAet al. (2017) A role for the mu opioid receptor in the antidepressant effects of buprenorphine. Behav Brain Res319: 96–103.
48.
RuhéHGvan RooijenGSpijkerJet al. (2012) Staging methods for treatment resistant depression. A systematic review. J Affect Disord137: 35–45.
49.
SaitohASugiyamaANemotoTet al. (2011) The novel delta opioid receptor agonist KNT-127 produces antidepressant-like and antinociceptive effects in mice without producing convulsions. Behav Brain Res223: 271–279.
50.
SamuelsBANautiyalKMKruegelACet al. (2017) The Behavioral Effects of the Antidepressant Tianeptine Require the Mu-Opioid Receptor. Neuropsychopharmacology. Epub ahead of print 19April2017. doi: 10.1038/npp.2017.60.
51.
SavegnagoLJesseCRNogueiraCW (2009) Structural modifications into diphenyl diselenide molecule do not cause toxicity in mice. Environ Toxicol Pharmacol27: 271–276.
52.
ShirayamaYIshidaHIwataMet al. (2004) Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J Neurochem90: 1258–1268.
53.
SigginsGRMartinGRobertoMet al. (2003) Glutamatergic transmission in opiate and alcohol dependence. Ann NY Acad Sci1003: 196–211.
54.
SongLWuCZuoY (2015) Melatonin prevents morphine-induced hyperalgesia and tolerance in rats: role of protein kinase C and N-methyl-D-aspartate receptors. BMC Anesthesiol15: 12.
55.
SteruLChermatRThierryBet al. (1985) The tail suspension test: A new method for screening antidepressants in mice. Psychopharmacology85: 367–370.
56.
StollALRueterS (1999) Treatment augmentation with opiates in severe and refractory major depression. Am J Psychiatry156: 2017.
57.
Tejedor-RealPMicoJAMaldonadoRet al. (1995) Implication of endogenous opioid system in the learned helplessness model of depression. Pharmacol Biochem Behav52: 145–152.
58.
ThomaziAPGodinhoGFRSRodriguesJMet al. (2004) Ontogenetic profile of glutamate uptake in brain structures slices from rats: Sensitivity to guanosine. Mech Ageing Dev125: 475–481.
59.
TompkinsDASmithMTMintzerMZet al. (2014) A double blind, within subject comparison of spontaneous opioid withdrawal from buprenorphine versus morphine. J Pharmacol Exp Ther348: 217–226.
60.
WalshRNCumminsRA (1976) The open-field test: A critical review. Psychol Bull83: 482–504.
61.
WangFRQiaoMQXueLet al. (2015) Possible involvement of mu opioid receptor in the antidepressant-like effect of shuyu formula in restraint stress-induced depression-like rats. Evid Based Complement Alternat Med2015: 452412.
62.
WangXFWuNSuRBet al. (2011) Agmatine modulates neuroadaptations of glutamate transmission in the nucleus accumbens of repeated morphine-treated rats. Eur J Pharmacol650: 200–205.
63.
WeiELohHHWayEL (1973) Quantitative aspects of precipitated abstinence in morphine-dependent rats. J Pharmacol Exp Ther184: 398–403.
ZomkowskiADESantosARSRodriguesALS (2005) Evidence for the involvement of the opioid system in the agmatine antidepressant-like effect in the forced swimming test. Neuroscience Letters381: 279–283.
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