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On the effect of minocycline on the depressive-like behavior of mice repeatedly exposed to malathion: interaction between nitric oxide and cholinergic system

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Abstract

This study was performed to investigate the antidepressant-like effect of minocycline in mice exposed to organophosphate pesticide malathion and possible involvement of nitric oxide/cGMP pathway in this paradigm. Mice were administered specific doses of malathion once daily for 7 consecutive days. After induction of depression, different doses of minocycline were daily injected alone or combined with non-specific NOS inhibitor, L-NAME, specific inducible NOS inhibitor, AG, NO precursor, L-arginine, and PDE5I, sildenafil. After locomotion assessment in open-field test, immobility times were recorded in the FST and TST. Moreover, hippocampal nitrite concentrations and acetylcholinesterase activity were measured. The results showed that repeated exposure to malathion induces depressive-like behavior at dose of 250 mg/kg. Minocycline (160 mg/kg) significantly reduced immobility times in FST and TST (P < 0.001). Combination of sub-effective doses of minocycline (80 mg/kg) with either L-NAME (3 mg/kg) or AG (25 mg/kg) significantly exerted a robust antidepressant-like effect in FST and TST (P < 0.001). Furthermore, minocycline at the same dose which has antidepressant-like effect, significantly reduced hippocampal nitrite concentration. The investigation indicates the essential role for NO/cGMP pathway in malathion-induced depressive-like behavior and antidepressant-like effect of minocycline. Moreover, the interaction between nitrergic and cholinergic systems are suggested to be involved in malathion-induced depression.

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Abbreviations

NO:

Nitric oxide

cGMP:

Cyclic GMP

L-NAME:

Nω-nitro-L-arginine methyl ester

AG:

Aminoguanidine

NOS:

Nitric oxide synthhase

iNOS:

Inducible NOS

PDE5I:

Phosphodiesterase type 5 inhibitor

FST:

Forced swimming test

TST:

Tail suspension test

OFT:

Open-field test

AChE:

Acetylcholinesterase

OP:

Organophosphorous pesticide

References

  • Acker CI, Luchese C, Prigol M, Nogueira CW (2009) Antidepressant-like effect of diphenyldiselenide on rats exposed to malathion: involvement of Na+K+ ATPase activity. Neurosci Lett 455:168–172

    Article  CAS  PubMed  Google Scholar 

  • Ahmed R, Seth V, Pasha ST, Banerjee BD (2000) Influence of dietary ginger (ZingiberofficinalesRosc) on oxidative stress induced by malathion in rats. Food Chem Toxicol 38:443–450

    Article  CAS  PubMed  Google Scholar 

  • Almeida RC, Felisbino CS, López MG, Rodrigues ALS, Gabilan NH (2006) Evidence for the involvement of L-arginine-nitric oxide-cyclic guanosine monophosphate pathway in the antidepressant-like effect of memantine in mice. Behav Brain Res 168(2):318–322

    Article  CAS  PubMed  Google Scholar 

  • Antonenko YN, Rokitskaya TI, Cooper AJ, Krasnikov BF (2010) Minocycline chelates Ca2+, binds to membranes, and depolarizes mitochondria by formation of Ca2+-dependent ion channels. J Bioenerg Biomembr 42(2):151–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Araújo AV, Ferezin CZ, Gerson J, Rodrigues GJ, Lunardi CN, Vercesi JA, Grando MD, Bonaventura D, Bendhack LM (2011) Prostacyclin, not only nitric oxide, is a mediator of the vasorelaxation induced by acetylcholine in aortas from rats submitted to cecal ligation and perforation (CLP). Vasc Pharmacol 54:44–51

    Article  Google Scholar 

  • Armstrong GA, Rodgers CI, Money TG, Robertson RM (2009) Suppression of spreading depression-like events in locusts by inhibition of the NO/cGMP/PKG pathway. Neuroscience 29:8225–8235

    CAS  PubMed  Google Scholar 

  • Assini FL, Zanette KD, Brocardo PS, Pandolfo P, Rodrigues ALS, Takahashi RN (2005) Behavioral effects and ChE measures after acute and repeated administration of malathion in rats. Environ Toxicol Pharmacol 20:443–449

    Article  CAS  PubMed  Google Scholar 

  • Azizi-Malekabadi H, Hosseini M, Soukhtanloo M, Sadeghian R, Fereidoni M, Khodabandehloo F (2012) Different effects of scopolamine on learning, memory, and nitric oxide metabolite levels in hippocampal tissues of ovariectomized and sham-operated rats. Arq Neuropsiquiatr 70(6):447–452

    Article  PubMed  Google Scholar 

  • Beseler CL, Stallones L, Hoppin JA, Alavanja MC, Blair A, Keefe T, Kamel F (2008) Depression and pesticide exposures among private pesticide applicators enrolled in the agricultural health study. Environ Health Pers 116:1713–1719

    Article  Google Scholar 

  • Bouchard MF, Bellinger DC, Wright RO, Weisskopf MG (2010) Attentiondeficit/hyperactivity disorder and urinary metabolites of organophosphate pesticides. Pediatrics 125:e1270–e1277

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1):248–254

    Article  CAS  PubMed  Google Scholar 

  • Carr RL, Chambers HW, Guarisco JA, Richardson JR, Tang J, Chambers JE (2001) Effects of repeated oral postnatal exposure to chlorpyrifos on open-field behavior in juvenile rats. Toxicol Sci 59:260

    Article  CAS  PubMed  Google Scholar 

  • Cheng PW, Lu PJ, Chen SR, Ho WY, Cheng WH, Hong LZ, Yeh TC, Sun GC, Wang LL, Hsiao M, Tseng CJ (2011) Central nicotinic acetylcholine receptor involved in Ca2+-calmodulin-endothelial nitric oxide synthase pathway modulated hypotensive effects. Br J Pharmacol 163:1203–1213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coker RK, Laurent GJ (1998) Pulmonary fibrosis: cytokines in the balance. Eur Respir J 11:1218–1221

  • Colosio C, Tiramani M, Maroni M (2003) Neurobehavioral effects of pesticides: state of the art. Neurotoxicology 24:577–591

    Article  CAS  PubMed  Google Scholar 

  • Da Silva GDL, Matteussi AS, dos Santos ARS, Calixto JB, Rodrigues AL (2000) Evidence for dual effects of nitric oxide in the forced swimming test and in the tail suspension test in mice. Neuroreport 11:3699–3702

    Article  PubMed  Google Scholar 

  • David DJP, Renard CE, Jolliet P, Hascoet M, Bourin M (2003) Antidepressant-like effects in various mice strains in the forced swimming test. J Psychopharmacol 166:373–382

    CAS  Google Scholar 

  • Delgado PL (2004) Common pathways of depression and pain. J Clin Psych 65(Suppl 12):16–19

    Google Scholar 

  • de Vente J, Markerink-van Ittersum M, Axer H, Steinbusch HWM (2001) Nitric-oxide-induced cGMP synthesis in cholinergic neurons in the rat brain. Exp Brain Res 136:480–491

  • de Vente J, Van Ittersum MM, Van Abeelen J, Emson PC, Axer H, Steinbusch HWM (2000) NO-mediated cGMP synthesis in cholinergic neurons in the rat forebrain: effects of lesioning dopaminergic or serotonergic pathways on nNOS and cGMP synthesis. Eur J Neurosci 12:507–519

  • Dhir A, Kulkarni S (2007) Involvement of l-arginine–nitric oxide–cyclic guanosine monophosphate pathway in the antidepressant-like effect of venlafaxine in mice. Prog. Neuro-Psychopharmacol Biol Psych 31:921–925

    Article  CAS  Google Scholar 

  • Domek-Łopacińska K, Van De Waarenburg M, Markerink-van Ittersum M, Steinbusch HWM, de Vente J (2005) Nitric oxide-induced cGMP synthesis in the cholinergic system during the development and aging of the rat brain. Dev Brain Res 158:72–81

    Article  Google Scholar 

  • Eckeli AL, Dach F, Rodrigues ALS (2000) Acute treatments with GMP produce antidepressant-like effects in mice. Neuroreport 11:1839–1843

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL, Courtney KO, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95

    Article  CAS  PubMed  Google Scholar 

  • Elsheikha HM, Hussein HS, Rahbar MH (2008) Clinico-pathological effects of schistosomamansoni infection associated with simultaneous exposure to malathion in Swiss outbred albino mice. J Acta Torp 108:11–19

    Article  CAS  Google Scholar 

  • Esplugues JV (2002) NO as a signalling molecule in the nervous system. Br J Pharmacol 135:1079–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritze J (1993) The adrenergic-cholinergic imbalance hypothesis of depression: a review and a perspective. Rev Neurosci 41:63

    Google Scholar 

  • Garcia-Alloza M, Gil-Bea FJ, Diez-Ariza M, Chen CP, Francis PT, Lasheras B, Ramirez MJ (2005) Cholinergic-serotonergic imbalance contributes to cognitive and behavioral symptoms in Alzheimer’s disease. Neuropsychologia 43:442

    Article  CAS  PubMed  Google Scholar 

  • Gaur V, Kumar A (2010) Behavioral, biochemical and cellular correlates in the protective effect of sertraline against transient global ischemia induced behavioral despair: possible involvement of nitric oxide-cyclic guanosine monophosphate study pathway. Brain Res Bull 82:57–64

    Article  CAS  PubMed  Google Scholar 

  • Ghasemi M, Sadeghipour H, Mosleh A, Sadeghipour HR, Mani AR, Dehpour AR (2008) Nitric oxide involvement in the antidepressant-like effects of acute lithium administration in the mouse forced swimming test. Eur Neuropsychopharmacol 18:323–332

    Article  CAS  PubMed  Google Scholar 

  • Ghasemi M, Sadeghipour H, Poorheidari G, Dehpour AR (2009) A role for nitrergic system in the antidepressant-like effects of chronic lithium treatment in the mouse forced swimming test. Behav Brain Res 200:76–82

    Article  CAS  PubMed  Google Scholar 

  • Gieseler A, Schultze AT, Kupsch K, Haroon MF, Wolf G, Siemen D, Kreutzmann P (2009) Inhibitory modulation of the mitochondrial permeability transition by minocycline. Biochem Pharmacol 77:888–896

    Article  CAS  PubMed  Google Scholar 

  • Harkin A, Connor TJ, Burns MP, Kelly JP (2004a) Nitric oxide synthase inhibitors augment the effects of serotonin re-uptake inhibitors in the forced swimming test. Eur Neuropsychopharmacol 14:274–281

    Article  CAS  PubMed  Google Scholar 

  • Harkin A, Connor TJ, Burns MP, Kelly JP (2004b) Nitric oxide synthase inhibitors augment the effects of serotonin re-uptake inhibitors in the forced swimming test. Eur Neuropsychopharmacol 14:274–281

    Article  CAS  PubMed  Google Scholar 

  • Harkin AJ, Bruce KH, Craft B, Paul IA (1999) Nitric oxide synthase inhibitors have antidepressant-like properties in mice. 1. Acute treatments are active in the forced swim test. Eur J Pharmacol 372:207–213

    Article  CAS  PubMed  Google Scholar 

  • Harvey BH, Duvenhage I, Viljoen F, Scheepers N, Malan SF, Wegener G, et al. (2010) Role of monoamine oxidase, nitric oxide synthase and regional brain monoamines in the antidepressant-like effects of methylene blue and selected structural analogues. Biochem Pharmacol 80:1580–1591

    Article  CAS  PubMed  Google Scholar 

  • Heiberg IL, Wegener G, Rosenberg R (2002) Reduction of cGMP and nitric oxide has antidepressant-like effects in the forced swimming test in rats. Behav Brain Res 134:479–484

    Article  CAS  PubMed  Google Scholar 

  • Herken H, Gurel A, Selek S, Armutcu F, Ozen ME, Bulut M, Kap O, Yumru M, Savas HA, Akyol O (2007) Adenosine deaminase, nitric oxide, superoxide dismutase, and xanthine oxidase in patients with major depression: impact of antidepressant treatment. Arch Med Res 38:247–252

    Article  CAS  PubMed  Google Scholar 

  • Hope BT, Michael GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH diapborase is a nitric oxide synthase. Proc Natl Acad Sci 88:2811–2814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Wu DL, Luo CX, Zhu LJ, Zhang J, Wu HY, Zhu DY (2012) Hippocampal nitric oxide contributes to sex difference in affective behaviors. Proc Natl Acad Sci 109:14224–14229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang CC, Hsu KS (2010) Activation of muscarinic acetylcholine receptors induces a nitric oxide–dependent long-term depression in rat medial prefrontal cortex. Cereb Cortex 20:982–996

    Article  PubMed  Google Scholar 

  • Ikenouchi-Sugita A, Toyohira Y, Yoshimura R, Ueno S, Tsutsui M, Nakamura J, Yanagihara N (2009) Opposite effects of milnacipran, a serotonin norepinephrine reuptake inhibitor, on the levels of nitric oxide and brain-derived neurotrophic factor in mouse brain cortex. Naunyn Schmie-Debergs Arch Pharmacol 380(6):479–486

    Article  CAS  Google Scholar 

  • Jaga K, Dharmani C (2007) Dharmani, the interrelation between organophosphate toxicity and the epidemiology of depression and suicide. Rev Environ Health 22:57–73

    Article  CAS  PubMed  Google Scholar 

  • Kamimura Y, Fujii T, Kojima H, Nagano T, Kawashima K (2003) Nitric oxide (NO) synthase mRNA expression and NO production via muscarinic acetylcholine receptor-mediated pathways in the CEM, human leukemic T-cell line. Life Sci 72:2151–2154

    Article  CAS  PubMed  Google Scholar 

  • Kayanm Y, Ogawa T (1987) Electrophysiology of ascending, possibly cholinergic neuron ~ in the rat laterodorsal tegmental nucleus: comparison with monoamine neurons. Neuroscience 77:277–282

    Google Scholar 

  • Kessler RC, Merikangas KR, Wang PS (2007) Prevalence, comorbidity, and service utilization for mood disorders in the United States at the beginning of the twenty-first century. Ann Rev Clin Psychol 3:137–158

    Article  Google Scholar 

  • Kilinc E, Yetik G, Dalbasti T, Ozsoz M (2002) Comparison of electrochemical detection of acetylcholine-induced nitric oxide release (NO) and contractile force measurement of rabbit isolated carotid artery endothelium. J Pharmaceut Biomed Anal 28:345–354

    Article  CAS  Google Scholar 

  • Kulkarni SK, Dhir A (2007) Possible involvement of L-arginine-nitric oxide (NO)-cyclic guanosine monophosphate (cGMP) signaling pathway in the antidepressant activity of berberine chloride. Eur J Pharmacol 569:77–83

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Gupta RC, Goad JT, Karanth S, Pope C (2007) Modulation of parathion toxicity by glucose feeding: is nitric oxide Involved? Toxicol Appl Pharmacol 219:106–113

    Article  CAS  PubMed  Google Scholar 

  • Mantovani M, Pértile R, Calixto JB, Santos AR, Rodrigues ALS (2003) 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 343:1–4

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki M, Kayama Y, Kihara T, Kawasaki K, Yamaguchi E, Wada Y (1996) Possible release of nitric oxide from cholinergic axons in the thalamus by stimulation of the rat laterodorsal tegmental nucleus as measured with voltammetry. J Chem Neuroanat 10:203–207

    Article  CAS  PubMed  Google Scholar 

  • Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002) Neurobiology of depression. Neuron 34:13

    Article  CAS  PubMed  Google Scholar 

  • Nikodemova M, Duncan ID, Watters JJ (2006) Minocycline exerts inhibitory effects on multiple mitogen activated protein kinases and IκBα degradation in a stimulus specific manner in microglia. J Neurochem 96:314–323

    Article  CAS  PubMed  Google Scholar 

  • Porsolt RD, Bertin A, Jalfre M (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327–336

    CAS  PubMed  Google Scholar 

  • Puzzo D, Sapienza S, Arancio O, Palmeri A (2008) Role of phosphodiesterase 5 in synaptic plasticity and memory. J Neuropsych Dis Treat 4:371

    Article  CAS  Google Scholar 

  • Rauh VA, Garfinkel R, Perera R, Andrews H, Hoepner L, Barr D, Whitehead D, Tang D, Whyatt RM (2006) Impact of prenatal chlorpyrifos exposure on neurodevelopment in the first 3 years of life among inner-city children. Pediatrics 118:1845–1859

    Article  Google Scholar 

  • Reidy TJ, Bowler RM, Rauch SS, Pedroza GI (1992) Pesticide exposure and neuropsychological impairment in migrant farm workers. Arch Clin Neuropsychol 7:85

    Article  CAS  PubMed  Google Scholar 

  • Rosa AO, Kaster MP, Binfaré RW, Morales S, Martín-Aparicio E, Navarro-Rico ML, Rodrigues ALS (2008) Antidepressant-like effect of the novel thiadiazolidinone NP031115 in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 32(6):1549–1556

    Article  CAS  Google Scholar 

  • Sadaghiani MS, Javadi-Paydar M, Gharedaghi MH, Yousefzadeh Farda Y, Dehpour AR (2011) 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 224:336–343

    Article  CAS  PubMed  Google Scholar 

  • Satoh K, Fibiger HC (1986) Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J Comp Neurol 253:277–302

    Article  CAS  PubMed  Google Scholar 

  • Scarabelli TM, Stephanou A, Pasini E, Gitti G, Townsend P, Lawrence K, Gardin J (2004) Minocycline inhibits caspase activation and reactivation, increases the ratio of XIAP to smac/DIABLO, and reduces the mitochondrial leakage of cytochrome C and smac/DIABLO. J Am Coll Cardiol 43(5):865–874

    Article  CAS  PubMed  Google Scholar 

  • Schulz R, Drayer RA, Rollman BL (2002) Depression as a risk factor for non-suicide mortality in the elderly. Biol sych 52:205–225

    Google Scholar 

  • Sharma VK, Goyal A, Ganti SS (2010) Minocycline, an antibiotic and a neuroprotective: justifying role in Alzheimer’s disease. Asian J Pharm Clin Res 3(3):142–145

    CAS  Google Scholar 

  • Steru L, Chermat R, Thierry B, Simon P (1985) The tail suspension test: a new method for screening antidepressants in mice. J Psychopharmacol 85:367–370

    Article  CAS  Google Scholar 

  • Suzuki E, Yagi G, Nakaki T, Kanba S, Asai M (2001) Elevated plasma nitrate levels in depressive states. J Aff Dis 63:221–224

    Article  CAS  Google Scholar 

  • Teng YD, Choi H, Onario RC, Zhu S, Desilets FC, Lan S, Friedlander RM (2004) Minocycline inhibits contusion-triggered mitochondrial cytochrome c release and mitigates functional deficits after spinal cord injury. Proc Natl Acad Sci 101(9):3071–3076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tikka T, Fiebich BL, Goldsteins G, Keinänen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. Neuroscience 21(8):2580–2588

    CAS  PubMed  Google Scholar 

  • Trullas R, Folio T, Young A, Miller R, Boje K, Skolnick P (1991) L-aminocyclopropanecarboxylates exhibit antidepressant and anxiolytic actions in animal models. Eur J Pharmacol 203:379–385

    Article  CAS  PubMed  Google Scholar 

  • Vincent SR, Satoh K, Armstrong DM, Panula P, Vale W, Fibiger HC (1986) Neuropeptides and NADPH-diaphorase activity in the ascending cholinergic reticular system of the rat. Neuroscience 17:167–182

    Article  CAS  PubMed  Google Scholar 

  • Wang SZ, Sheng ZZ, El-Fakahany EE (1994) Efficient coupling of M5 muscarinic acetylcholine receptors to activation of nitric oxide synthase. J Pharmacol Exp Ther 268:552–557

    CAS  PubMed  Google Scholar 

  • Ward TR, Mundy WR (1996) Organophosphorous compounds preferentially affect second messenger systems coupled to M2/M4 receptors in rat frontal cortex. Brain Res Bull 39(1):49–55

    Article  CAS  PubMed  Google Scholar 

  • Wiklund CU, Wiklund NP, Gustafsson LE (1993) Modulation of neuroeffector transmission by endogenous nitric oxide: a role for acetylcholine receptor-activated nitric oxide formation, as indicated by measurements of nitric oxide/nitrite release. Eur J Pharmacol 240:235–242

    Article  CAS  PubMed  Google Scholar 

  • Woolf NJ, Butcher LL (1986) Choliuergic systems in the rat brain: III. Projections from the pontomesencephalictegmentum to the thalamus, rectum, basal ganglia, and basal forebrain. Brain Res Bull 16:603–637

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Tong C, Eisenach JC (1996) Acetylcholine stimulates the release of nitric oxide from rat spinal cord. Anesthesiology 85:107–111

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Huang XY, Ye ML, Luo CX, Wu HY, Hu Y, Zhu DY (2010) Neuronal nitric oxide synthase alteration accounts for the role of 5-HT1A receptor in modulating anxiety-related behaviors. Neurosci 30(7):2433–2441

    Article  Google Scholar 

  • Zhuo M, Meller ST, Gebhart GF (1993) Endogenous nitric oxide is required for tonic cholinergic inhibition of spinal mechanical transmission. Pain 54:71–78

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, P.O. Box: 13145-784, Tehran, Iran

    Seyed Soheil Saeedi Saravi, Alireza Arefidoust, Rahele Yaftian & Ahmad Reza Dehpour

  2. Experimental Medicine Research Center, Tehran University of Medical Sciences, Tehran, Iran

    Seyed Soheil Saeedi Saravi, Alireza Arefidoust, Rahele Yaftian & Ahmad Reza Dehpour

  3. Department of Toxicology-Pharmacology, Faculty of Pharmacy, Guilan University of Medical Sciences, Rasht, Iran

    Seyed Soheil Saeedi Saravi

  4. Department of Toxicology-Pharmacology, Faculty of Pharmacy, Mazandaran University of Medical Sciences, Sari, Iran

    Roya Amirkhanloo, Seyed Sobhan Saeedi Saravi & Mohammad Shokrzadeh

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  1. Seyed Soheil Saeedi Saravi
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  2. Roya Amirkhanloo
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Seyed Soheil Saeedi Saravi and Roya Amirkhanloo authors contributed equally to this paper as first author.

Mohammad Shokrzadeh and Ahmad Reza Dehpour contributed in the article equally as corresponding author.

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Saeedi Saravi, S.S., Amirkhanloo, R., Arefidoust, A. et al. On the effect of minocycline on the depressive-like behavior of mice repeatedly exposed to malathion: interaction between nitric oxide and cholinergic system. Metab Brain Dis 31, 549–561 (2016). https://doi.org/10.1007/s11011-015-9764-z

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