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Olanzapine plus fluoxetine treatment alters mitochondrial respiratory chain activity in the rat brain

Published online by Cambridge University Press:  24 June 2014

Fabiano R. Agostinho
Affiliation:
Laboratório de Neurociências and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Gislaine Z. Réus
Affiliation:
Laboratório de Neurociências and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Roberto B. Stringari
Affiliation:
Laboratório de Neurociências and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Karine F. Ribeiro
Affiliation:
Laboratório de Neurociências and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Gabriela K. Ferreira
Affiliation:
Laboratório de Fisiopatologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Isabela C. Jeremias
Affiliation:
Laboratório de Fisiopatologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Giselli Scaini
Affiliation:
Laboratório de Fisiopatologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Gislaine T. Rezin
Affiliation:
Laboratório de Fisiopatologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
Emílio L. Streck
Affiliation:
Laboratório de Fisiopatologia Experimental and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
João Quevedo*
Affiliation:
Laboratório de Neurociências and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil
*
Professor João Quevedo, MD, PhD, Laboratório de Neurociências and Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Programa de Pós-Graduação em Ciências da Saúde, Unidade Acadêmica de Ciências da Saúde, Universidade do Extremo Sul Catarinense, Criciúma 88806-000, Santa Catarina, Brazil. Tel: +55 48 3443 4817; Fax: +55 48 3431 2736; E-mail: [email protected]

Extract

Agostinho FR, Réus GZ, Stringari RB, Ribeiro KF, Ferreira GK, Jeremias IC, Scaini G, Rezin GT, Streck EL, Quevedo J. Olanzapine plus fluoxetine treatment alters mitochondrial respiratory chain activity in the rat brain.

Background: Evidence is emerging for the role of dysfunctional mitochondria in pathophysiology and treatment of mood disorders. In this study, we evaluated the effects of acute and chronic administration of fluoxetine (FLX), olanzapine (OLZ) and the combination of FLX/OLZ on mitochondrial respiratory chain activity in the rat brain.

Methods: For acute treatment, Wistar rats received one single injection of OLZ (3 or 6 mg/kg) and/or FLX (12 or 25 mg/kg) and for chronic treatment, rats received daily injections of OLZ (3 or 6 mg/kg) and/or FLX (12 or 25 mg/kg) for 28 days and we evaluated the activity of mitochondrial respiratory chain complexes I, II, II–III and IV in prefrontal cortex, hippocampus and striatum.

Results: Our results showed that both acute and chronic treatments with FLX and OLZ alone or in combination altered respiratory chain complexes activity in the rat brain, but in combination we observed larger alterations.

Conclusions: Finally, these findings further support the hypothesis that metabolism energy could be involved in the treatment with antipsychotics and antidepressants in combination to mood disorders.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

1.Nelson, G, Hall, GB, Forchuk, C.Current and preferred housing of psychiatric consumers/survivors. Can J Commun Ment Health 2003;22:519.CrossRefGoogle ScholarPubMed
2.Konradi, C, Eaton, M, MacDonald, ML, Walsh, J, Benes, FM, Heckers, S.Molecular evidence for mitochondrial dysfunction in bipolar disorder. Arch Gen Psychiatry 2004; 61:300308.CrossRefGoogle ScholarPubMed
3.Belmaker, RH.Bipolar disorder. N Engl J Med 2004;351: 476486.CrossRefGoogle ScholarPubMed
4.Ustun, TB, Ayuso-Mateos, JL, Chatterji, S, Mathers, C, Murray, CJ.Global burden of depressive disorders in the year 2000. Br J Psychiatry 2004;84:386392.CrossRefGoogle Scholar
5.Kupfer, DJ.The increasing medical burden in bipolar disorder. JAMA 2005;293:25282530.CrossRefGoogle ScholarPubMed
6.Boekema, EJ, Braun, HP.Supramolecular structure of the mitochondrial oxidative phosphorylation system. J Biol Chem 2007;282:14.CrossRefGoogle ScholarPubMed
7.Fattal, O, Budur, K, Vaughan, AJ, Franco, K.Review of the literature on major mental disorders in adult patients with mitochondrial diseases. Psychosomatics 2006;47:17.CrossRefGoogle ScholarPubMed
8.Prabakaran, S, Swatton, JE, Ryan, MM et al. Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 2004;9:684687.CrossRefGoogle ScholarPubMed
9.Calabrese, V, Scapagnini, G, Giuffrida-Stella, AM, Bates, TE, Clark, JB.Mitochondrial involvement in brain function and dysfunction: relevance to aging, neurodegenerative disorders and longevity. Neurochem Res 2001;26: 739764.CrossRefGoogle ScholarPubMed
10.Armstrong, JS.The role of the mitochondrial permeability transition in cell death. Mitochondrion 2006;6:225234.CrossRefGoogle ScholarPubMed
11.Schapira, AH.Mitochondrial disease. Lancet 2006;368: 7082.CrossRefGoogle ScholarPubMed
12.Gur, RE, Resnick, SM, Alavi, A, Carrof, S, Kushner, M, Reivch, M.Regional brain function in schizophrenia II: repeated evaluation with positron emission tomography. Arch Gen Psychiatry 1987;44:126129.CrossRefGoogle ScholarPubMed
13.Castanier, C, Arnoult, D.Mitochondrial dynamics apoptosis. Med Sci 2010;26:830835.Google ScholarPubMed
14.Hung, CH, Ho, YS, Chang, RC.Modulation of mitochondrial calcium as a pharmacological target for Alzheimer's disease. Ageing Res Rev 2010;9:447456.CrossRefGoogle ScholarPubMed
15.Horn, D, Barrientos, A.Mitochondrial copper metabolism and delivery to cytochrome c oxidase. IUBMB Life 2008;60:421429.CrossRefGoogle ScholarPubMed
16.Madrigal, JLM, Olivenza, R, Moro, MA et al. Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 2001;24:420429.CrossRefGoogle ScholarPubMed
17.Shelton, RC.The return of fixed combinations in psychiatry: fluoxetine and olanzapine combination. Ther Clin Risk Manag 2006;2:187192.CrossRefGoogle ScholarPubMed
18.Tohen, M, Vieta, E, Calabrese, J.Efficacy of olanzapine and olanzapine-fluoxetine combination in the treatment of bipolar I depression. Arch Gen Psychiatry 2004;60: 10791088.CrossRefGoogle Scholar
19.Shelton, RC, Tollefson, GD, Tohen, M et al. A novel augmentation strategy for treating resistant major depression. Am J Psychiatry 2001;158:131134.CrossRefGoogle ScholarPubMed
20.Rezin, GT, Cardoso, MR, Gonçalves, CL et al. Inhibition of mitochondrial respiratory chain in brain of rats subjected to an experimental model of depression. Neurochem Int 2008;53:395400.CrossRefGoogle Scholar
21.Pittenger, C, Duman, RS.Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008;33:88109.CrossRefGoogle ScholarPubMed
22.Strakowski, SM, Delbello, MP, Adler, CM.The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 2005;10:105116.CrossRefGoogle ScholarPubMed
23.Agostinho, FR, Scaini, G, Ferreira, GK et al. Effects of olanzapine, fluoxetine and olanzapine/fluoxetine on creatine kinase activity in rat brain. Brain Res Bull 2009;80: 337340.CrossRefGoogle ScholarPubMed
24.Agostinho, FR, Réus, GZ, Stringari, RB et al. Treatment with olanzapine, fluoxetine and olanzapine/fluoxetine alters citrate synthase activity in rat brain. Neurosci Lett 2011;487: 278281.CrossRefGoogle ScholarPubMed
25.Lowry, OH, Rosebough, NG, Farr, AL, Randall, RJ.Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265275.CrossRefGoogle ScholarPubMed
26.Cassina, A, Radi, R.Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch Biochem Biophys 1996;328:309316.CrossRefGoogle ScholarPubMed
27.Fischer, JC, Ruitenbeek, W, Berden, JA et al. Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 1995;153:2326.CrossRefGoogle Scholar
28.Rustin, P, Chretien, D, Bourgeron, T et al. Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 1994;228:3551.CrossRefGoogle ScholarPubMed
29.Marco, R, Pestana, A, Sebastian, J, Sols, A.Oxaloacetate metabolic crossroads in liver. Enzyme compartmentation and regulation of gluconeogenesis. Mol Cell Biochem. 1974;3:5370.CrossRefGoogle ScholarPubMed
30.Ben-Shachar, D, Karry, R.Neuroanatomical pattern of mitochondrial complex I pathology varies between schizophrenia, bipolar disorder and major depression. PLoS One 2008;3:3676.CrossRefGoogle ScholarPubMed
31.Quiroz, JA, Gray, AN, Kato, T, Manji, HK.Mitochondrially mediated plasticity in the pathophysiology and treatment of bipolar disorder. Neuropsychopharmacology 2008; 33:25512565.CrossRefGoogle ScholarPubMed
32.Iwamoto, K, Bundo, M, Kato, T.Altered expression of mitochondria-related genes in postmortem brains of patients with bipolar disorder or schizophrenia, as revealed by large-scale DNA microarray analysis. Hum Mol Genet 2005;14: 241253.CrossRefGoogle ScholarPubMed
33.Kato, T.Mitochondrial dysfunction in bipolar disorder: from 31P-magnetic resonance spectroscopic findings to their molecular mechanisms. Int Rev Neurobiol 2005;63:2140.CrossRefGoogle ScholarPubMed
34.Andreazza, AC, Shao, L, Wang, JF, Young, LT.Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch Gen Psychiatry 2010;67: 360368.CrossRefGoogle ScholarPubMed
35.Corrêa, C, Amboni, G, Assis, LC et al. Effects of lithium and valproate on hippocampus citrate synthase activity in an animal model of mania. Prog Neuropsychopharmacol Biol Psychiatry 2007;31:887891.CrossRefGoogle Scholar
36.Wang, FJ, Shao, L, Sun, X, Young, LT.Glutathione S-transferase is a novel target for mood stabilizing drugs in primary cultured neuron. J Neurochem 2004;88:14771484.CrossRefGoogle Scholar
37.Dror, E, Klein, R, Karry, A et al. State-dependent alterations in mitochondrial complex I activity in platelets: a potential peripheral marker for schizophrenia. Mol Psychiatry 2002;7:9951001.CrossRefGoogle ScholarPubMed
38.Prince, JA, Blennow, K, Gottfries, CG, Karlsson, I, Oreland, L.Mitochondrial function is differentially altered in the basal ganglia of chronic schizophrenics. Europsychopharmacology 1999;21:372379.CrossRefGoogle ScholarPubMed
39.Streck, EL, Rezin, GT, Barbosa, LM, Assis, LC, Grandi, E, Quevedo, J.Effect of antipsychotics on succinate dehydrogenase and cytochrome oxidase activities in rat brain. Naunyn Schmiedebergs Arch Pharmacol 2007;376:127133.CrossRefGoogle ScholarPubMed
40.Burkhardt, C, Kelly, JP, Lim, YH, Filley, CM, Parker, WDNeuroleptic medications inhibit complex I of the electron transport chain. Ann Neurol 1993;33:512517.CrossRefGoogle ScholarPubMed
41.Modica-Napolitano, JS, Lagace, CJ, Brennan, WA, Aprille, JR.Differential effects of typical and atypical neuroleptics on mitochondrial function in vitro. Arch Pharm Res 2003;26:951–559.CrossRefGoogle ScholarPubMed
42.Maurer, I, Moller, HJ.Inhibition of complex I by neuroleptics in normal human brain cortex parallels the extrapyramidal toxicity of neuroleptics. Mol Cell Biochem 1997;174:255259.CrossRefGoogle ScholarPubMed
43.Ji, B, La, Y, Gao, L et al. A comparative proteomics analysis of rat mitochondria from the cerebral cortex and hippocampus in response to antipsychotic medications. J Proteome Res 2009;8:36333641.CrossRefGoogle ScholarPubMed
44.Wu, Y, Wu, S, Lee, W, Wei, Y.Mitochondrial respiratory dysfunction-elicited oxidative stress and posttranslational protein modification in mitochondrial diseases. Ann N Y Acad Sci 2010;1201:147156.CrossRefGoogle ScholarPubMed
45.Płoszaj, T, Robaszkiewicz, A, Witas, H.Oxidative damage of mitochondrial DNA: the result or consequence of enhanced generation of reactive oxygen species. Postepy Biochem 2010;56:139146.Google ScholarPubMed
46.Padurariu, M, Ciobica, A, Dobrin, I, Stefanescu, C.Evaluation of antioxidant enzymes activities and lipid peroxidation in schizophrenic patients treated with typical and atypical antipsychotics. Neurosci Lett 2010;479: 317320.CrossRefGoogle ScholarPubMed
47.Réus, GZ, Stringari, RB, Souza, B et al. Harmine and imipramine promote antioxidant activities in prefrontal cortex and hippocampus. Oxid Med Cell Longev 2010;3: 325331.CrossRefGoogle ScholarPubMed
48.Valvassori, SS, Petronilho, FC, Réus, GZ et al. Effect of N-acetylcysteine and/or deferoxamine on oxidative stress and hyperactivity in an animal model of mania. Prog Neuropsychopharmacol Biol Psychiatry 2008;32:10641068.CrossRefGoogle ScholarPubMed
49.Polydoro, M, Schröder, N, Lima, MN et al. Haloperidol- and clozapine-induced oxidative stress in the rat brain. Pharmacol Biochem Behav 2004;78:751756.CrossRefGoogle ScholarPubMed
50.Reinke, A, Martins, MR, Lima, MS, Moreira, JC, Dal-Pizzol, F, Quevedo, J.Haloperidol and clozapine, but not olanzapine, induces oxidative stress in rat brain. Neurosci Lett 2004;372:157160.CrossRefGoogle Scholar
51.Lohr, JB, Cadet, JL, Lohr, MA et al. Vitamin E in the treatment of tardive dyskinesia: the possible involvement of free radical mechanisms. Schizophr Bull 1988;14:291296.CrossRefGoogle ScholarPubMed
52.Peet, M, Laugharne, J, Rangarajan, N.Tardive dyskinesia, lipid peroxidation, and sustained amelioration with vitamin E treatment. Int Clin Psychopharmacol 1993;8: 151153.CrossRefGoogle ScholarPubMed
53.Andreassen, OA, Ferrante, RJ, Beal, MF, Jorgensen, HA.Oral dyskinesias and striatal lesions in rats after long-term co-treatment with haloperidol and 3-nitropropionic acid. Neuroscience 1998;87:639648.CrossRefGoogle Scholar
54.Park, SW, Lee, CH, Lee, JG et al. Protective effects of atypical antipsychotic drugs against MPP+-induced oxidative stress in PC12 cells. Neurosci Res 2011;69:283290.CrossRefGoogle ScholarPubMed
55.Gałecki, P, Szemraj, J, Bieńkiewicz, M, Florkowski, A, Gałecka, E.Lipid peroxidation and antioxidant protection in patients during acute depressive episodes and in remission after fluoxetine treatment. Pharmacol Rep 2009;61: 436447.CrossRefGoogle ScholarPubMed
56.Kirkova, M, Tzvetanova, E, Vircheva, S, Zamfirova, R, Grygier, B, Kubera, M.Antioxidant activity of fluoxetine: studies in mice melanoma model. Cell Biochem Funct 2010; 28:497502.CrossRefGoogle ScholarPubMed
57.Chung, YC, Kim, SR, Park, JY et al. Fluoxetine prevents MPTP-induced loss of dopaminergic neurons by inhibiting microglial activation. Neuropharmacology 2011;60: 963974.CrossRefGoogle ScholarPubMed
58.Streck, EL, Amboni, G, Scaini, G et al. Brain creatine kinase activity in an animal model of mania. Life Sci 2008; 82:424429.CrossRefGoogle Scholar
59.Assis, IC, Rezin, GT, Comim, CM et al. Effect of acute administration of ketamine and imipramine on creatine kinase activity in the brain of rats. Rev Bras Psiquiatr 2009;31:247252.CrossRefGoogle ScholarPubMed
60.Santos, PM, Scaini, G, Rezin, GT et al. Brain creatine kinase activity is increased by chronic administration of paroxetine. Brain Res Bull 2009;80:327330.CrossRefGoogle ScholarPubMed
61.Rezin, GT, Gonçalves, CL, Daufenbach, JF et al. Acute administration of ketamine reverses the inhibition of mitochondrial respiratory chain induced by chronic mild stress. Brain Res Bull 2009;79:418421.CrossRefGoogle ScholarPubMed
62.Hroudova, J, Fisar, Z.Activities of respiratory chain complexes and citrate synthase influenced by pharmacologically different antidepressants and mood stabilizers. Neuro Endocrinol Lett 2010;31:336342.Google ScholarPubMed
63.Hirschfeld, RM, Montgomery, SA, Aguglia, E.Partial response and nonresponse to antidepressant therapy: current approaches and treatment options. J Clin Psychiatry 2002;63:826837.CrossRefGoogle ScholarPubMed
64.Fava, M.New approaches to the treatment of refractory depression. J Clin Psychiatry 2000;61:2632.Google Scholar
65.Morishita, S.Clonazepam as a therapeutic adjunct to improve the management of depression: a brief review. Hum Psychopharmacol 2009;24:191198.CrossRefGoogle ScholarPubMed
66.Schatzberg, AF.New approaches to managing psychotic depression. J Clin Psychiatry 2003;64:1923.Google ScholarPubMed
67.Matthews, JD, Bottonari, KA, Polania, LM.An open study of olanzapine and fluoxetine for psychotic major depressive disorder: interim analyses. J Clin Psychiatry 2002;63:11641170.CrossRefGoogle ScholarPubMed