Skip to main content
SpringerLink
Log in

Chronic variable stress induces oxidative stress and decreases butyrylcholinesterase activity in blood of rats

  • Basic Neurosciences, Genetics and Immunology - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

Depressive disorders, including major depression, are serious and disabling, whose mechanisms are not clearly understood. Since life stressors contribute in some fashion to depression, chronic variable stress (CVS) has been used as an animal model of depression. In the present study we evaluated some parameters of oxidative stress [thiobarbituric acid reactive substances (TBARS), catalase (CAT), superoxide dismutase (SOD) and glutathione peroxidase (GPx)], and inflammatory markers (interleukin 6, C reactive protein, tumor necrosis factor-alpha and nitrites), as well as the activity of butyrylcholinesterase in blood of rats subjected to chronic stress. Homocysteine and folate levels also were measured. Stressed animals were submitted to different mild stressors for 40 days. After CVS, a reduction in weight gain was observed in the stressed group, as well as an increase in immobility time in the forced swimming test as compared with controls. Stressed animals presented a significant increase on TBARS and SOD/CAT ratio, but stress did not alter GPx activity and any inflammatory parameters studied. CVS caused a significant inhibition on serum butyrylcholinesterase activity. Stressed rats had higher plasmatic levels of homocysteine without differences in folate levels. Although it is difficult to extrapolate our findings to the human condition, the alterations observed in this work may be useful to help to understand, at least in part, the pathophysiology of depressive disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Alcantara VM, Chautard-Freire-Maia EA, Scartezini M, Cerci MS, Braun-Prado K, Picheth G (2002) Butyrylcholinesterase activity and risk factors for coronary artery disease. Scan J Clin Lab Invest 62:399–404

    Article  CAS  Google Scholar 

  • Alexopoulos P, Topalidis S, Irmisch G, Prehn K, Jung SU, Poppe K, Sebb H, Perneczky R, Kurz A, Bleich S, Herpertz SC (2010) Homocysteine and cognitive function in geriatric depression. Neuropsychobiology 61(2):97–104

    Article  CAS  PubMed  Google Scholar 

  • Bao AM, Meynena G, Swaab DF (2008) The stress system in depression and neurodegeneration: focus on the human hypothalamus. Brain Res Rev 57:531–553

    Article  CAS  PubMed  Google Scholar 

  • Belmaker RH, Agam G (2008) Major depressive disorder. N Engl J Med 358(1):55–68

    Article  CAS  PubMed  Google Scholar 

  • Bilici M, Efe H, Köroğlu MA, Uydu HA, Bekaroğlu M, Değer O (2001) Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 64(1):43–51

    Article  CAS  PubMed  Google Scholar 

  • Bottiglieri T, Laundy M, Crellin R, Toone BK, Carney MW, Reynolds EH (2000) Homocysteine, folate, methylation, and monoamine metabolism in depression. J Neurol Neurosurg Psychiatry 69:228–232

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cascalheira JF, Parreira MC, Viegas AN, Faria MC, Domingues FC (2008) Serum homocysteine: relationship with circulating levels of cortisol and ascorbate. Ann Nutr Metab 53(1):67–74

    Article  CAS  PubMed  Google Scholar 

  • Charney DS, Manji HK (2004) Life stress, genes, and depression: multiple pathways lead to increased risk and new opportunities for intervention. Sci. STKE 225:1–11

    Google Scholar 

  • Cumurcu BE, Ozyurt H, Etikan I, Demir S, Karlidag R (2009) Total antioxidant capacity and total oxidant status in patients with major depression: impact of antidepressant treatment. Psychiatry Clin Neurosci 63(5):639–645

    Article  CAS  PubMed  Google Scholar 

  • Dantzer R (2006) Cytokine, sickness behavior and depression. Neurol Clin 24(3):441–446

    Article  PubMed  Google Scholar 

  • Darvesh S, Hopkins DA, Geula C (2003) Neurobiology of butyrylcholinesterase. Nat Rev Neurosci 17:131–138

    Article  Google Scholar 

  • de Souza FG, Rodrigues MD, Tufik S, Nobrega JN, D’Almeida V (2006) Acute stressor-selective effects on homocysteine metabolism and oxidative stress parameters in female rats. Pharmacol Biochem Behav 85(2):400–407

    Article  PubMed  Google Scholar 

  • Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15:316–328

    Article  PubMed  Google Scholar 

  • Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Faraci FM, Lentz SR (2004) Hyperhomocysteinemia, oxidative stress, and cerebral vascular dysfunction. Stroke 35:345–347

    Article  PubMed  Google Scholar 

  • Ferreira AG, Lima DD, Delwing D, Mackedanz V, Tagliari B, Kolling J, Schuck PF, Wajner M, Wyse AT (2010) Proline impairs energy metabolism in cerebral cortex of young rats. Metab Brain Dis 25(2):161–168

    Article  CAS  PubMed  Google Scholar 

  • Folstein M, Liu T, Peter I, Buel J, Arsenault L, Scott T, Qiu WW (2007) Homocysteine hypothesis of depression. Am J Psychiatry 16:861–867

    Article  Google Scholar 

  • Gamaro GD, Manoli LP, Torres ILS, Silveira R, Dalmaz C (2003) Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int 42:107–114

    Article  CAS  PubMed  Google Scholar 

  • Gamaro GD, Prediger ME, Bassani MG, Dalmaz C (2008) Fluoxetine alters feeding behavior and leptin levels in chronically-stressed rats. Pharmacol Biochem Behav 90:312–317

    Article  CAS  PubMed  Google Scholar 

  • Gillespie CF, Nemeroff CB (2005) Hypercortisolemia and depression. Psychosom Med 67:26–28

    Article  Google Scholar 

  • Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T, Yirmiya R (2008) Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry 13(7):717–728

    Article  CAS  PubMed  Google Scholar 

  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite and [15N]nitrate in biological fluids. Anal Biochem 126:131–138

    Article  CAS  PubMed  Google Scholar 

  • Haack M, Hinze-Selch D, Fenzel T, Kraus T, Kühn M, Schuld A, Pollmächer T (1999) Plasma levels of cytokines and soluble cytokine receptors in psychiatric patients upon hospital admission: effects of confounding factors and diagnosis. J Psychiatr Res 33:407–418

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97:1634–1658

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (2006) Free radicals in biology and medicine, 4th edn. Oxford University Press, Oxford

    Google Scholar 

  • Harro J, Tõnissaar M, Eller M, Kask A, Oreland L (2001) Chronic variable stress and partial 5-HT denervation by parachloroamphetamine treatment in the rat: effects on behavior and monoamine neurochemistry. Brain Res 899(1–2):227–239

    Article  CAS  PubMed  Google Scholar 

  • Jendricko T, Vidović A, Grubisić-Ilić M, Romić Z, Kovacić Z, Kozarić-Kovacić D (2009) Homocysteine and serum lipids concentration in male war veterans with posttraumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry 33(1):134–140

    Article  CAS  PubMed  Google Scholar 

  • Johnson AK, Grippo AJ (2006) Sadness and broken hearts: neurohumoral mechanisms and co-morbidity of ischemic heart disease and psychological depression. J Physiol Pharmacol 57(S11):5–29

    PubMed  Google Scholar 

  • Katz RJ, Hersh S (1981) Amitriptyline and scopolamine in an animal model of depression. Neurosci Biobehav Rev 5:265–271

    Article  CAS  PubMed  Google Scholar 

  • Kelly CB, McDonnell AP, Johnston TG, Mulholland C, Cooper SJ, McMaster D, Evans A, Whitehead AS (2004) The MTHFR C677T polymorphism is associated with depressive episodes in patients from Northern Ireland. J. Psychopharmacol 18(4):567–571

    Article  CAS  PubMed  Google Scholar 

  • Kelner MJ, Bagnell R, Montoya M, Estes L, Uglik SF, Cerutti P (1995) Transfection with human copper-zinc superoxide dismutase induces bidirectional alterations in other antioxidant enzymes, proteins, growth factor response, and paraquat resistance. Free Radic Biol Med 18:497–506

    Article  CAS  PubMed  Google Scholar 

  • Khanzode SD, Dakhale GN, Khanzode SS, Saoji A, Palasodkar R (2003) Oxidative damage and major depression: the potential antioxidant action of selective serotonin re-uptake inhibitors. Redox Rep 8(6):365–370

    Article  CAS  PubMed  Google Scholar 

  • Kim JM, Stewart R, Kim SW, Yang SJ, Shin IS, Yoon JS (2008) Predictive value of folate, vitamin B12 and homocysteine levels in latelife depression. Br J Psychiatry 192:268–274

    Article  PubMed  Google Scholar 

  • Konarska M, Stewart RE, McCarty R (1990) Predictability of chronic intermittent stress: effects on sympathetic-adrenal medullary responses of laboratory rats. Behav Neural Biol 53:231–243

    Article  CAS  PubMed  Google Scholar 

  • Kubera M, Symbirtsev A, Basta-Kaim A, Borycz J, Roman A, Papp M, Claesson M (1996) Effect of chronic treatment with imipramine on interleukin 1 and interleukin 2 production by splenocytes obtained from rats subjected to a chronic mild stress model of depression. Pol J Pharmacol 48(5):503–506

    CAS  PubMed  Google Scholar 

  • Kunz M, Gama CS, Andreazza AC, Salvador M, Ceresér KM, Gomes FA, Belmonte-de-Abreu PS, Berk M, Kapczinski F (2008) Elevated serum superoxide dismutase and thiobarbituric acid reactive substances in different phases of bipolar disorder and in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 32(7):1677–1681

    Article  CAS  PubMed  Google Scholar 

  • Levine J, Timinsky I, Vishne T, Dwolatzky T, Roitman S, Kaplan Z, Kotler M, Sela BA, Spivak B (2008) Elevated serum homocysteine levels in male patients with PTSD. Depress Anxiety 25(11):E154–E157

    Article  PubMed  Google Scholar 

  • Lipton SA, Kim WK, Choi YB, Kumar S, D’Emilia DM, Rayudu PV, Arnelle DR, Stamler JS (1997) Neurotoxicity associated with dual actions of homocysteine at the N-methyl-d-aspartate receptor. Proc Natl Acad Sci USA 94:5923–5928

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–267

    CAS  PubMed  Google Scholar 

  • Lucca G, Comim CM, Valvassori SS, Réus GZ, Vuolo F, Petronilho F, Dal-Pizzol F, Gavioli EC, Quevedo J (2009) Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int 54:358–362

    Article  CAS  PubMed  Google Scholar 

  • Lucinio J, Wong ML (1999) The role of inflammatory mediators in the biology of major depression: central nervous system cytokines modulate the biological substrate of depressive symptoms, regulate stress-responsive systems, and contribute to neurotoxicity and neuroprotection. Mol Psychiatry 4:317–327

    Article  Google Scholar 

  • Madrigal JLM, Olivenza R, Moro MA, Lisasoain I, Lorenzo P, Rodrigo J, Leza JC (2001) Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 24(4):420–429

    Article  CAS  PubMed  Google Scholar 

  • Maes M, Yirmya R, Noraberg J, Brene S, Hibbeln J, Perinii G, Kubera M, Bob P, Lerer B, Maj M (2009) The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab Brain Dis 24:27–53

    Article  CAS  PubMed  Google Scholar 

  • Magera MJ, Lacey JM, Casetta B, Rinaldo P (1999) Method for the determination of total homocysteine in plasma and urine by stable isotope dilution and electrospray tandem mass spectrometry. Clin Chem 45:1517–1522

    CAS  PubMed  Google Scholar 

  • Maletic V, Robinson M, Oakes T, Iyengar S, Ball SG, Russel J (2007) Neurobiology of depression: an integrated view of key findings. Int J Clin Pract 61(12):2030–2040

    Article  CAS  Google Scholar 

  • Manji HK, Drevets WC, Charney DS (2001) The cellular neurobiology of depression. Nat Med 7(5):541–547

    Article  CAS  PubMed  Google Scholar 

  • Marin MT, Cruz FC, Planeta CS (2007) Chronic restraint or variable stresses differently affect the behavior, corticosterone secretion and body weight in rats. Physiol Behav 90(1):29–35

    Article  CAS  PubMed  Google Scholar 

  • Marklund S (1985) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 243–247

    Google Scholar 

  • Massoulié J, Pezzementi L, Bon S, Krejci E, Vallette FM (1993) Molecular and cellular biology of cholinesterases. Prog Neurobiol 41(1):31–91

    Article  PubMed  Google Scholar 

  • Matés JM, Pérez-Gomes C, De Castro IN (1999) Antioxidant enzymes and human diseases. Clin Biochem 32(8):595–603

    Article  PubMed  Google Scholar 

  • Matté C, Durigon E, Stefanello FM, Cipriani F, Wajner M, Wyse ATS (2006) Folic acid pretreatment prevents the reduction of Na(+),K(+)-ATPase and butyrylcholinesterase activities in rats subjected to acute hyperhomocysteinemia. Int J Dev Neurosci 24(1):3–8

    Article  PubMed  Google Scholar 

  • Matté C, Mackedanz V, Stefanello FM, Scherer EB, Andreazza AC, Zanotto C, Moro AM, Garcia SC, Gonçalves CA, Erdtmann B, Salvador M, Wyse ATS (2009) Chronic hyperhomocysteinemia alters antioxidant defenses and increases DNA damage in brain and blood of rats: protective effect of folic acid. Neurochem Int 54(1):7–13

    Article  PubMed  Google Scholar 

  • Mattson MP, Shea TB (2003) Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders. Trends Neurosci 26:137–146

    Article  CAS  PubMed  Google Scholar 

  • Mesulam MM, Guillozet A, Shaw P, Levey A, Duysen EG, Lockridge O (2002) Acethylcolynesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyse acetylcholine. Neuroscience 110:627–639

    Article  CAS  PubMed  Google Scholar 

  • Miller AH, Maletic V, Raison CL (2009) Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 65(9):732–741

    Article  CAS  PubMed  Google Scholar 

  • Mormède C, Castanon N, Médina C, Moze E, Lestage J, Leveu PJ, Dantzer R (2003) Chronic mild stress in mice decreases peripheral cytokine and increases central cytokine expression independently of IL-10 regulation of the cytokine network. Neuroimmunomodulation 10:359–366

    Google Scholar 

  • Ng F, Berk M, Dean O, Bush AI (2008) Oxidative stress in psychiatric disorders: evidence base and therapeutic implications. Int J Neuropsychopharmacol 21:1–26

    Google Scholar 

  • Ni Y, Su M, Lin J, Wang X, Qiu Y, Zhao A, Chen T, Jia W (2008) Metabolic profiling reveals disorder of amino acid metabolism in four brain regions from a rat model of chronic unpredictable mild stress. FEBS Lett 582(17):2627–2636

    Article  CAS  PubMed  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  • Olivenza R, Moro MA, Lisasoain I, Lorenzo P, Fernandez AP, Rodrigo J, Boscá L, Leza JC (2000) Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex. J Neurochem 74:785–791

    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 

  • Rada P, Colasante C, Skirzewski M, Hernandez L, Hoebel B (2006) Behavioral depression in the swim test causes a biphasic, long-lasting change in accumbens acetylcholine release, with partial compensation by acetylcholinesterase and muscarinic-1 receptors. Neuroscience 141:67–76

    Article  CAS  PubMed  Google Scholar 

  • Refsum H, Nurk E, Smith AD, Ueland PM, Gjesdal CG, Bjelland I, Tverdal A, Tell GS, Nygård O, Vollset SE (2006) The Hordaland homocysteine study: a community-based study of homocysteine, its determinants, and associations with disease. J Nutr 136(6):1731S–1740S

    CAS  PubMed  Google Scholar 

  • Reif A, Schneider MF, Kamolz S, Pfuhlmann B (2003) Homocysteinemia in psychiatric disorders: association with dementia and depression, but not schizophrenia in female patients. J Neural Transm 110:1401–1411

    Article  CAS  PubMed  Google Scholar 

  • Resler G, Lavie R, Campos J, Mata S, Urbina M, García A, Apitz R, Lima L (2008) Effect of folic acid combined with fluoxetine in patients with major depression on plasma homocysteine and vitamin B12, and serotonin levels in lymphocytes. Neuroimmunomodulation 15(3):145–152

    Article  CAS  PubMed  Google Scholar 

  • Röhrdanz E, Obertrifter B, Ohler S, Tran-Thi Q, Kahl R (2000) Influence of Adriamycin and paraquat on antioxidant enzyme expression in primary rat hepatocytes. Arch Toxicol 74:231–237

    Article  PubMed  Google Scholar 

  • Sapolsky RM (1996) Why stress is bad for your brain. Science 273:749–750

    Article  CAS  PubMed  Google Scholar 

  • Schallreuter KU, Elwary S (2007) Hydrogen peroxide regulates the cholinergic signal in a concentration dependent manner. Life Sci 80(24–25):2221–2226

    Article  CAS  PubMed  Google Scholar 

  • Scherer EB, Stefanello FM, Mattos C, Netto CA, Wyse ATS (2007) Homocysteine reduces cholinesterase activity in rat and human serum. Int J Dev Neurosci 25(4):201–205

    Article  CAS  PubMed  Google Scholar 

  • Schiepers OJ, Wichers MC, Maes M (2005) Cytokines and major depression. Prog Neuropsychopharmacol Biol Psychiatry 29(2):201–217

    Article  CAS  PubMed  Google Scholar 

  • Stefanello FM, Franzon R, Tagliari B, Wannmacher C, Wajner M, Wyse ATS (2005) Reduction of butyrylcholinesterase activity in rat serum subjected to hyperhomocysteinemia. Metab Brain Dis 20(2):97–103

    Article  CAS  PubMed  Google Scholar 

  • Steptoe A, Kunz-Ebrecht SR, Owen N (2003) Lack of association between depressive symptoms and markers of immune and vascular inflammation in middle-aged men and women. Psychol Med 33:667–674

    Article  CAS  PubMed  Google Scholar 

  • Swaab DF, Bao AM, Lucassen PJ (2005) The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 4:141–194

    Article  CAS  PubMed  Google Scholar 

  • Tagliari B, Noschang CG, Ferreira AGK, Ferrari OA, Feksa LR, Wannmacher CMD, Dalmaz C, Wyse ATS (2010) Chronic variable stress impairs energy metabolism in brain of rats. Metab Brain Dis 25(2):169–176

    Article  CAS  PubMed  Google Scholar 

  • Tolmunen T, Hintikka J, Voutilainen S, Ruusunen A, Alfthan G, Nyyssönen K, Viinamäki H, Kaplan GA, Salonen JT (2004) Association between depressive symptoms and serum concentrations of homocysteine in men: a population study. Am J Clin Nutr 80:1574–1578

    CAS  PubMed  Google Scholar 

  • Tracey KJ (2002) The inflammatory reflex. Nature 420:853–859

    Article  CAS  PubMed  Google Scholar 

  • Triantafyllou N, Evangelopoulos ME, Kimiskidis VK, Kararizou E, Boufidou F, Fountoulakis KN, Siamouli M, Konstantinos N, Nikolaou C, Sfagos C, Vlaikidis N, Vassilopoulos D (2008) Increased plasma homocysteine levels in patients with multiple sclerosis and depression. Ann Gen Psychiatry 7:17–21

    Article  PubMed  Google Scholar 

  • Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–332

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm J, Muller E, de Zwaan M, Fischer J, Hillemacher T, Komhuber J, Bleich S, Frieling H (2010) Elevation of homocysteine levels is only partially reversed after therapy in females with eating disorders. J Neural Transm 117:521–527

    Article  CAS  PubMed  Google Scholar 

  • Wilner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52:90–110

    Article  Google Scholar 

  • Wilson DO, Johnson P (2000) Exercise modulates antioxidant enzyme gene expression in rat myocardium and liver. J Appl Physiol 88:1791–1796

    CAS  PubMed  Google Scholar 

  • Wyse ATS, Zugno AI, Streck EL, Matté C, Calcagnotto T, Wannmacher CM, Wajner M (2002) Inhibition of Na(+),K(+)-ATPase activity in hippocampus of rats subjected to acute administration of homocysteine is prevented by vitamins E and C treatment. Neurochem Res 27(12):1685–1689

    Article  CAS  PubMed  Google Scholar 

  • You JM, Yun SJ, Nam KN, Kang C, Won R, Lee EH (2009) Mechanism of glucocorticoid-induced oxidative stress in rat hippocampal slice cultures. Can J Physiol Pharmacol 87(6):440–447

    Article  CAS  PubMed  Google Scholar 

  • Zafir A, Banu N (2009) Modulation of in vivo oxidative status by exogenous corticosterone and restraint stress in rats. Stress 12(2):167–177

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Lucas P. Mocelin for his technical assistance. This work was supported in part by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and by the FINEP Research Grant “Rede Instituto Brasileiro de Neurociência (IBN-Net), # 01.06.0842-00”.

Author information

Authors and Affiliations

  1. Laboratório de Neuroproteção e Doenças Metabólicas, Departamento de Bioquímica, ICBS, Universidade Federal do Rio Grande do Sul, UFRGS, Rua Ramiro Barcelos, 2600-Anexo, Porto Alegre, RS, CEP 90035-003, Brazil

    Bárbara Tagliari, Tiago M. dos Santos, Aline A. Cunha & Angela T. S. Wyse

  2. Laboratório de Erros Inatos do Metabolismo, Departamento de Bioquímica, ICBS, Universidade Federal do Rio Grande do Sul, UFRGS, Rua Ramiro Barcelos, 2600-Anexo, Porto Alegre, RS, CEP 90035-003, Brazil

    Bárbara Tagliari, Tiago M. dos Santos, Aline A. Cunha & Angela T. S. Wyse

  3. Laboratório de Neurobiologia do Estresse, Departamento de Bioquímica, ICBS, Universidade Federal do Rio Grande do Sul, UFRGS, Rua Ramiro Barcelos, 2600-Anexo, Porto Alegre, RS, CEP 90035-003, Brazil

    Carla Dalmaz

  4. Serviço de Genética Médica, HCPA, Rua Ramiro Barcelos 2350, Porto Alegre, RS, CEP 90035-003, Brazil

    Angela Sitta & Carmem R. Vargas

  5. Centro de Ciências da Saúde, Universidade Comunitária da Região de Chapecó, Avenida Senador Attílio Fontana, 591-E, Chapecó, SC, CEP 89809-000, Brazil

    Daniela D. Lima

  6. Departamento de Ciências Naturais, Centro de Ciências Exatas e Naturais, Universidade Regional de Blumenau, Rua Antônio da Veiga, 140, Blumenau, SC, CEP 89012-900, Brazil

    Débora Delwing

Authors
  1. Bárbara Tagliari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tiago M. dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aline A. Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniela D. Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Débora Delwing
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Angela Sitta
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carmem R. Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Carla Dalmaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Angela T. S. Wyse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela T. S. Wyse.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tagliari, B., dos Santos, T.M., Cunha, A.A. et al. Chronic variable stress induces oxidative stress and decreases butyrylcholinesterase activity in blood of rats. J Neural Transm 117, 1067–1076 (2010). https://doi.org/10.1007/s00702-010-0445-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-010-0445-0

Keywords

Search

Navigation