Isolation Stress During the Prepubertal Period in Rats Induces Long-Lasting Neurochemical Changes in the Prefrontal Cortex

Kvetnansky R, Pacak K, Fukuhara K et al (1995) Sympathoadrenal system in stress. Interaction with the hypothalamic–pituitary–adrenocortical system. Ann N Y Acad Sci 771:131–158 Weiss IC, Pryce CR, Jongen-Relo AL et al (2004) Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Bran Res 152:279–295 Gogtay N, Giedd JN, Lusk L et al (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101:8174–8179 Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009) Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 97:484–494 Serra M, Pisu MG, Littera M, Papi G, Sanna E, Tuveri F, Usala L, Purdy RH, Biggio G (2000) Social isolation-induced decreases in both the abundance of neuroactive steroids and GABA(A) receptor function in rat brain. J Neurochem 75:732–740 Serra M, Pisu MG, Floris I, Biggio G (2005) Social isolation-induced changes in the hypothalamic–pituitary–adrenal axis in the rat. Stress 8:259–264 Weiss IC, Pryce CR, Jongen-Rêlo AL, Nanz-Bahr NI, Feldon J (2004) Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 152:279–295 Ferdman N, Murmu RP, Bock J et al (2007) Weaning age, social isolation, and gender, interact to determine adult explorative and social behavior, and dendritic and spine morphology in prefrontal cortex of rats. Behav Brain Res 180:174–182 Mc Cormick CM, Mathews IZ (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 86:220–233 Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947–957 Pecoraro N, Gomez F, Dallman MF (2005) Glucocorticoids dose-dependently remodel energy stores and amplify incentive relativity effects. Psychoneuroendocrinology 30:815–825 Epel E, Lapidus R, McEwen B, Brownell K (2001) Stress may add bite to appetite in women: a laboratory study of stress-induced cortisol and eating behavior. Psychoneuroendocrinology 26:37–49 Zellner DA, Loaiza S, Gonzalez Z et al (2006) Food selection changes under stress. Physiol Behav 87:789–793 Adam TC, Epel ES (2007) Stress, eating and the reward system. Physiol Behav 91:449–458 Pecoraro N, Reyes F, Gomez F (2004) Chronic stress promotes palatable feeding, which reduces signs of stress. Feedforward and feedback effects of chronic stress. Endocrinology 145:3754–3762 Manoli I, Alesci S, Blackman MR et al (2007) Mitochondria as key components of the stress response. Trends Endocrinol Metabol 18:190–198 Halliwell B, Gutteridge JM (2000) Free radicals and antioxidants in the year 2000. A historical look to the future. Ann N Y Acad Sci 899:136–147 Kovacheva-Ivanova S, Bakalova R, Ribavov SR (1994) Immobilization stress enhances lipid peroxidation in the rat lungs. Materials and methods. Gen Physiol Biophys 13:469–482 Oishi K, Yokoi M, Maekawa S et al (1999) Oxidative stress and haematological changes in immobilized rats. Acta Physiol Scand 165:65–69 Radak Z, Sasvari M, Nyakas C et al (2001) Single bout of exercise eliminates the immobilization-induced oxidative stress in rat brain. Neurochem Int 39:33–38 Mitra R, Vyas A, Chatterjee G et al (2005) Chronic stress induced modulation of different states of anxiety like behaviour in female rats. Neurosci Lett 383:278–283 Papadopoulos MC, Koumenis IL, Dugan LL, Giffard RG (1997) Vulnerability to glucose deprivation injury correlates with glutathione levels in astrocytes. Brain Res 748:151–156 Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3:614–620 Lees GJ (1993) Contributory mechanisms in the causation of neurodegenerative disorders. Neuroscience 54:287–322 Tagliari B, Noschang CG, Ferreira AG et al (2010) Chronic variable stress impairs energy metabolism in prefrontal cortex and hippocampus of rats: prevention by chronic antioxidant treatment. Metab Brain Dis 2:169–176 Souza CG, Moreira JD, Siqueira IR et al (2007) Highly palatable diet consumption increases protein oxidation in rat frontal cortex and anxiety-like behavior. Life Sci 81:198–203 Douglas L, Varlinskaya E, Spear L (2004) Rewarding properties of social interactions in adolescent and adult male and female rates: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45:153–162 Delmas-Beauvieux MC, Peuchant E, Dumon MF et al (1995) Relationship between red blood cell antioxidant enzymatic system status and lipoperoxidation during the acute phase of malaria. Clin Biochem 28:163–169 Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126 Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–333 Sriram K, Pai KS, Boyd MR, Ravindranath V (1997) Evidence for generation of oxidative stress in brain by MPTP: in vitro and in vivo studies in mice. Brain Res 21:44–52 Aksenov MY, Markesbery WR (2001) Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer’s disease. Neurosci Lett 302:141–145 Wyse ATS, Streck EL, Worm P et al (2000) Preconditioning prevents the inhibition of Na + , K + -ATPase activity after brain ischemia. Neurochem Res 25:971–975 Chan K, Delfert D, Junger K (1986) A direct colorimetric assay for Ca2+-stimulated ATPase activity. Anal Biochem 157:375–380 Fischer JC, Ruitenbeek W, Berden JA et al (1985) Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 153:23–36 Rustin P, Chretien D, Bourgeron T et al (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 28:35–51 Schapira AH, Mann VM, Cooper JM (1990) Anatomic and disease specificity of NADH CoQ1 reductase (complex I) deficiency in Parkinson’s disease. J Neurochem 55:2142–2145 Pendergrass W, Wolf N, Poot M (2004) Efficacy of MitoTracker Green and CMX rosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry 61:162–169 Khanal G, Chung K, Solis-Wever X et al (2011) Ischemia/reperfusion injury of primary porcine cardiomyocytes in a low-shear microfluidic culture and analysis device. Analyst 36:19–26 Rodriguez-Enriquez S, Kai Y, Maldonado E et al (2009) Roles of mitophagy and the mitochondrial permeability transition in remodeling of cultured rat hepatocytes. Autophagy 5:1099–1106 Keij JF, Bell-Prince C, Steinkamp JA (2000) Staining of mitochondrial membranes with 10-nonyl acridine orange, MitoFluor Green, and MitoTracker Green is affected by mitochondrial membrane potential al-tering drugs. Cytometry 39:203–210 Leira F, Vieites JM, Vieytes MR, Botana LM (2001) Apoptotic events induced by the phosphatase inhibitor okadaic acid in normal human lung fibroblasts. Toxicol In Vitro 15:99–208 Kalbacova M, Vrbacky M, Drahota Z, Melkova Z (2003) Comparison of the effect of mitochondrial inhibitors on mitochondrial membrane potential in two different cell lines using flow cytometry and spectrofluorometry. Cytom A 52:110–116 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275 Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254 De Oliveira MR, Silvestrin RB, Souza TM, Moreira JCF (2007) Oxidative stress in the hippocampus, anxiety-like behavior and decreased locomotory and exploratory activity of adult rats. Effects of sub acute vitamin A supplementation at therapeutic doses. Neurotoxicology 28:1191–1199 Pinho RA, Andrades ME, Oliveira MR et al (2006) Imbalance in SOD/CAT activities in rat skeletal muscles submitted to treadmill training exercise. Cell Biol Int 30:848–858 Halliwell B (2006) Oxidative stress and neurodegeneration. Where are we now? J Neurochem 97:1634–1658 Ward PA, Till GO (1990) Pathophysiologic events related to thermal injury of skin. J Trauma 30:S75–S79 Kovacheva-Ivanova S, Bakalova R, Ribavov SR (1994) Immobilization stress enhances lipid peroxidation in the rat lungs. Materials and methods. Gen Physiol Biophys 13:469–482 Madrigal JL, Olivenza R, Moro MA et al (2001) Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 24:420–429 Zhang X, Dong F, Ren J et al (2005) High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp Neurol 191:318–325 Krolow R, Noschang CG, Arcego D et al (2010) Consumption of a palatable diet by chronically stressed rats prevents effects on anxiety-like behavior but increases oxidative stress in a sex-specific manner. Appetite 55:108–116 de Vasconcellos AP, Zugno AI, dos Santos AH et al (2005) Na + , K + -ATPase activity is educed 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 Crema L, Schlabitz M, Tagliari B et al (2010) Na+,K+-ATPase activity is reduced in amygdala of rats with chronic stress-induced anxiety-like behavior. Neurochem Res 35:1787–1795 Kaplan JH (2002) Biochemistry of Na +,K +-ATPase. Annu Rev Biochem 71:511–535 Dobrota D, Matejovicova M, Kurrela EG, Boldyrev AA (1999) Na +/K +-ATPase under oxidative stress: molecular mechanisms of injury. Cell Mol Neurobiol 19:141–149 Streck EL, Zugno AI, Tagliari B et al (2001) Inhibition of rat brain Na+,K+-ATPase activity induced by homocysteine is probably mediated by oxidative stress. Neurochem Res 26:1195–1200 da S Benetti C, Silveira PP, Matté C et al (2010) Effects of a chronic exposure to a highly palatable diet and its withdrawal, in adulthood, on cerebral Na + , K + -ATPase and plasma S100B in neonatally handled rats. Int J Dev Neurosci 28:153–159 Lenroot RK, Giedd JN (2006) Brain development in children and adolescents: 857insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev 30:718–729 Paus T (2005) Mapping brain maturation and cognitive development during ado- 891 lescence. Trends Cogn Sci 9:60–68 Gassner B, Wuthrich A, Scholtysik G, Solioz M (1997) The pyrethroids permethrin and cyhalothrin are potent inhibitors of the mitochondrial complex I. J Pharmacol Exp Ther 281:855–860 Gruno M, Peet N, Tein A et al (2008) Atrophic gastritis: deficient complex I of the respiratory chain in the mitochondria of corpusmucosal cells. J Gastroenterol 43:780–788 Madrigal JL, Garcia-Bueno B, Caso JR et al (2006) Stress-induced oxidative changes in brain. CNS Neurolog Disord Drugs Targets 5:561–568 Boekema EJ, Braun HP (2007) Supramolecular structure of the mitochondrial oxidative phosphorylation system. J Biol Chem 282:1–4 Serviddio G, Bellanti F, Giudetti AM, et al. (2011) Mitochondrial oxidative stress and respiratory chain dysfunction account for liver toxicity during amiodarone but not dronedarone administration. Free Radic Biol Med [Epub ahead of print] Rezin GT, Jeremias IC, Ferreira GK et al (2008) Brain energy metabolism is activated after acute and chronic administration of fenproporex in young rats. Int J Dev Neurosci 53:395–400 Tsiriyotis C, Spandidos DA, Sekeris CE (1997) The mitochondrion as a primary site of action of glucocorticoids: mitochondrial nucleotide sequences, showing similarity to hormone response elements, confer dexamethasone inducibility to chimaeric genes transfected in LATK-cells. Biochem Biophys Res Commun 235:349–354 Adzic M, Djordjevic A, Demonacos C et al (2009) The role of phosphorylated glucocorticoid receptor in mitochondrial functions and apoptotic signalling in brain tissue of stressed Wistar rats. Int J Biochem Cell Biol 41:2181–2188 Liang HL, Ongwijitwat S, Wong-Riley MTT (2006) Bigenomic functional regulation of all 13 cytochrome c oxidase subunit transcripts in rat neurons in vitro and in vivo. Neuroscience 140:177–190 Demonacos CV, Karayanni N, Hatzoglou E et al (1996) Mitochondrial genes as sites of primary action of steroid hormones. Steroids 61:226–232