Skip to main content
Erschienen in: Brain Structure and Function 1/2017

31.03.2016 | Review

Oxidative and nitrosative stress pathways in the brain of socially isolated adult male rats demonstrating depressive- and anxiety-like symptoms

Erschienen in: Brain Structure and Function | Ausgabe 1/2017

Einloggen, um Zugang zu erhalten

Abstract

Various stressors may disrupt the redox homeostasis of an organism by causing oxidative and nitrosative stress that may activate stressor-specific pathways and provoke specific responses. Chronic social isolation (CSIS) represents a mild chronic stress that evokes a variety of neurobehavioral changes in rats similar to those observed in people with psychiatric disorders, including depression. Most rodent studies have focused on the effect of social isolation during weaning or adolescence, while its effect in adult rats has not been extensively examined. In this review, we discuss the current knowledge regarding the involvement of oxidative/nitrosative stress pathways in the prefrontal cortex and hippocampus of adult male rats exposed to CSIS, focusing on hypothalamic-pituitary-adrenocortical (HPA) axis activity, behavior parameters, antioxidative defense systems, stress signaling mediated by nuclear factor-kappa B (NF-κB), and mitochondria-related proapoptotic signaling. Although increased concentrations of corticosterone (CORT) have been shown to induce oxidative and nitrosative stress, we suggest a mechanism underlying the glucocorticoid paradox whereby a state of oxidative/nitrosative stress may exist under basal CORT levels. This review also highlights the differential susceptibility of prefrontal cortex and hippocampus to oxidative stress following CSIS and suggests a possible cellular pathway of stress tolerance that preserves the hippocampus from molecular damage and apoptosis. The differential regulation of the transcriptional factor NF-κB, and the enzymes inducible nitric oxide synthase (iNOS) and cyclooxygenase-2 (COX-2) following CSIS may be one functional difference between the response of the prefrontal cortex and hippocampus, thus identifying potentially relevant targets for antidepressant treatment.
Literatur
Zurück zum Zitat Ahmad A, Rasheed N, Banu N, Palit G (2010) Alterations in monoamine levels and oxidative systems in frontal cortex, striatum, and hippocampus of the rat brain during chronic unpredictable stress. Stress 13:355–364. doi:10.3109/10253891003667862 PubMedCrossRef Ahmad A, Rasheed N, Banu N, Palit G (2010) Alterations in monoamine levels and oxidative systems in frontal cortex, striatum, and hippocampus of the rat brain during chronic unpredictable stress. Stress 13:355–364. doi:10.​3109/​1025389100366786​2 PubMedCrossRef
Zurück zum Zitat Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70:200–214CrossRef Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 70:200–214CrossRef
Zurück zum Zitat Aoyama K, Watabe M, Nakaki T (2008) Regulation of neuronal glutathione synthesis. J Pharmacol Sci 108:227–238PubMedCrossRef Aoyama K, Watabe M, Nakaki T (2008) Regulation of neuronal glutathione synthesis. J Pharmacol Sci 108:227–238PubMedCrossRef
Zurück zum Zitat Arieli Y, Eynan M, Gancz H et al (2003) Heat acclimation prolongs the time to central nervous system oxygen toxicity in the rat. Possible involvement of HSP72. Brain Res 962:15–20PubMedCrossRef Arieli Y, Eynan M, Gancz H et al (2003) Heat acclimation prolongs the time to central nervous system oxygen toxicity in the rat. Possible involvement of HSP72. Brain Res 962:15–20PubMedCrossRef
Zurück zum Zitat Arimoto T, Bing G (2003) Up-regulation of inducible nitric oxide synthase in the substantia nigra by lipopolysaccharide causes microglial activation and neurodegeneration. Neurobiol Dis 12:35–45PubMedCrossRef Arimoto T, Bing G (2003) Up-regulation of inducible nitric oxide synthase in the substantia nigra by lipopolysaccharide causes microglial activation and neurodegeneration. Neurobiol Dis 12:35–45PubMedCrossRef
Zurück zum Zitat Beere HM, Wolf BB, Cain K et al (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2:469–475. doi:10.1038/35019501 PubMedCrossRef Beere HM, Wolf BB, Cain K et al (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2:469–475. doi:10.​1038/​35019501 PubMedCrossRef
Zurück zum Zitat Belay HT, Brown IR (2003) Spatial analysis of cell death and Hsp70 induction in brain, thymus, and bone marrow of the hyperthermic rat. Cell Stress Chaperones 8:395–404PubMedPubMedCentralCrossRef Belay HT, Brown IR (2003) Spatial analysis of cell death and Hsp70 induction in brain, thymus, and bone marrow of the hyperthermic rat. Cell Stress Chaperones 8:395–404PubMedPubMedCentralCrossRef
Zurück zum Zitat Blanchard DC, Cholvanich P, Blanchard RJ et al (1991) Serotonin, but not dopamine, metabolites are increased in selected brain regions of subordinate male rats in a colony environment. Brain Res 568:61–66PubMedCrossRef Blanchard DC, Cholvanich P, Blanchard RJ et al (1991) Serotonin, but not dopamine, metabolites are increased in selected brain regions of subordinate male rats in a colony environment. Brain Res 568:61–66PubMedCrossRef
Zurück zum Zitat Bowie A, O’Neill LA (2000) Oxidative stress and nuclear factor-kappaB activation: a reassessment of the evidence in the light of recent discoveries. Biochem Pharmacol 59:13–23PubMedCrossRef Bowie A, O’Neill LA (2000) Oxidative stress and nuclear factor-kappaB activation: a reassessment of the evidence in the light of recent discoveries. Biochem Pharmacol 59:13–23PubMedCrossRef
Zurück zum Zitat Brenes JC, Fornaguera J (2009) The effect of chronic fluoxetine on social isolation-induced changes on sucrose consumption, immobility behavior, and on serotonin and dopamine function in hippocampus and ventral striatum. Behav Brain Res 198:199–205. doi:10.1016/j.bbr.2008.10.036 PubMedCrossRef Brenes JC, Fornaguera J (2009) The effect of chronic fluoxetine on social isolation-induced changes on sucrose consumption, immobility behavior, and on serotonin and dopamine function in hippocampus and ventral striatum. Behav Brain Res 198:199–205. doi:10.​1016/​j.​bbr.​2008.​10.​036 PubMedCrossRef
Zurück zum Zitat Brown GW, Prudo R (1981) Psychiatric disorder in a rural and an urban population: 1. Aetiology of depression. Psychol Med 11:581–599PubMedCrossRef Brown GW, Prudo R (1981) Psychiatric disorder in a rural and an urban population: 1. Aetiology of depression. Psychol Med 11:581–599PubMedCrossRef
Zurück zum Zitat Cai J, Jones DP (1998) Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273:11401–11404PubMedCrossRef Cai J, Jones DP (1998) Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273:11401–11404PubMedCrossRef
Zurück zum Zitat Calabrese V, Copani A, Testa D et al (2000) Nitric oxide synthase induction in astroglial cell cultures: effect on heat shock protein 70 synthesis and oxidant/antioxidant balance. J Neurosci Res 60:613–622PubMedCrossRef Calabrese V, Copani A, Testa D et al (2000) Nitric oxide synthase induction in astroglial cell cultures: effect on heat shock protein 70 synthesis and oxidant/antioxidant balance. J Neurosci Res 60:613–622PubMedCrossRef
Zurück zum Zitat Cao G, Minami M, Pei W et al (2001) Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J Cereb Blood Flow Metab 21:321–333. doi:10.1097/00004647-200104000-00001 PubMedCrossRef Cao G, Minami M, Pei W et al (2001) Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J Cereb Blood Flow Metab 21:321–333. doi:10.​1097/​00004647-200104000-00001 PubMedCrossRef
Zurück zum Zitat Cassina P, Peluffo H, Pehar M et al (2002) Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis. J Neurosci Res 67:21–29PubMedCrossRef Cassina P, Peluffo H, Pehar M et al (2002) Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis. J Neurosci Res 67:21–29PubMedCrossRef
Zurück zum Zitat Chang LY, Slot JW, Geuze HJ, Crapo JD (1988) Molecular immunocytochemistry of the CuZn superoxide dismutase in rat hepatocytes. J Cell Biol 107:2169–2179PubMedCrossRef Chang LY, Slot JW, Geuze HJ, Crapo JD (1988) Molecular immunocytochemistry of the CuZn superoxide dismutase in rat hepatocytes. J Cell Biol 107:2169–2179PubMedCrossRef
Zurück zum Zitat Chen F, Demers LM, Vallyathan V et al (1999) Involvement of 5′-flanking kappaB-like sites within bcl-x gene in silica-induced Bcl-x expression. J Biol Chem 274:35591–35595PubMedCrossRef Chen F, Demers LM, Vallyathan V et al (1999) Involvement of 5′-flanking kappaB-like sites within bcl-x gene in silica-induced Bcl-x expression. J Biol Chem 274:35591–35595PubMedCrossRef
Zurück zum Zitat Connelly L, Palacios-Callender M, Ameixa C et al (2001) Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 166:3873–3881PubMedCrossRef Connelly L, Palacios-Callender M, Ameixa C et al (2001) Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 166:3873–3881PubMedCrossRef
Zurück zum Zitat Couto N, Malys N, Gaskell SJ, Barber J (2013) Partition and turnover of glutathione reductase from Saccharomyces cerevisiae: a proteomic approach. J Proteome Res 12:2885–2894. doi:10.1021/pr4001948 PubMedCrossRef Couto N, Malys N, Gaskell SJ, Barber J (2013) Partition and turnover of glutathione reductase from Saccharomyces cerevisiae: a proteomic approach. J Proteome Res 12:2885–2894. doi:10.​1021/​pr4001948 PubMedCrossRef
Zurück zum Zitat Cruthirds DL, Novak L, Akhi KM et al (2003) Mitochondrial targets of oxidative stress during renal ischemia/reperfusion. Arch Biochem Biophys 412:27–33PubMedCrossRef Cruthirds DL, Novak L, Akhi KM et al (2003) Mitochondrial targets of oxidative stress during renal ischemia/reperfusion. Arch Biochem Biophys 412:27–33PubMedCrossRef
Zurück zum Zitat Datta SR, Dudek H, Tao X et al (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231–241PubMedCrossRef Datta SR, Dudek H, Tao X et al (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231–241PubMedCrossRef
Zurück zum Zitat Desagher S, Martinou JC (2000) Mitochondria as the central control point of apoptosis. Trends Cell Biol 10:369–377PubMedCrossRef Desagher S, Martinou JC (2000) Mitochondria as the central control point of apoptosis. Trends Cell Biol 10:369–377PubMedCrossRef
Zurück zum Zitat Didelot C, Schmitt E, Brunet M et al (2006) Heat shock proteins: endogenous modulators of apoptotic cell death. Handb Exp Pharmacol 172:171–198CrossRef Didelot C, Schmitt E, Brunet M et al (2006) Heat shock proteins: endogenous modulators of apoptotic cell death. Handb Exp Pharmacol 172:171–198CrossRef
Zurück zum Zitat Dringen R (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62:649–671PubMedCrossRef Dringen R (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62:649–671PubMedCrossRef
Zurück zum Zitat Dronjak S, Gavrilović L, Filipović D, Radojcić MB (2004) Immobilization and cold stress affect sympatho-adrenomedullary system and pituitary-adrenocortical axis of rats exposed to long-term isolation and crowding. Physiol Behav 81:409–415. doi:10.1016/j.physbeh.2004.01.011 PubMedCrossRef Dronjak S, Gavrilović L, Filipović D, Radojcić MB (2004) Immobilization and cold stress affect sympatho-adrenomedullary system and pituitary-adrenocortical axis of rats exposed to long-term isolation and crowding. Physiol Behav 81:409–415. doi:10.​1016/​j.​physbeh.​2004.​01.​011 PubMedCrossRef
Zurück zum Zitat Filipović D, Gavrilović L, Dronjak S, Radojcić MB (2005) Brain glucocorticoid receptor and heat shock protein 70 levels in rats exposed to acute, chronic or combined stress. Neuropsychobiology 51:107–114. doi:10.1159/000084168 PubMedCrossRef Filipović D, Gavrilović L, Dronjak S, Radojcić MB (2005) Brain glucocorticoid receptor and heat shock protein 70 levels in rats exposed to acute, chronic or combined stress. Neuropsychobiology 51:107–114. doi:10.​1159/​000084168 PubMedCrossRef
Zurück zum Zitat Filipović D, Zlatković J, Pajović SB (2009) The effect of acute or/and chronic stress on the MnSOD protein expression in rat prefrontal cortex and hippocampus. Gen Physiol Biophys 28 Spec No:53–61PubMed Filipović D, Zlatković J, Pajović SB (2009) The effect of acute or/and chronic stress on the MnSOD protein expression in rat prefrontal cortex and hippocampus. Gen Physiol Biophys 28 Spec No:53–61PubMed
Zurück zum Zitat Filipović D, Zlatković J, Inta D et al (2011) Chronic isolation stress predisposes the frontal cortex but not the hippocampus to the potentially detrimental release of cytochrome c from mitochondria and the activation of caspase-3. J Neurosci Res 89:1461–1470. doi:10.1002/jnr.22687 PubMedCrossRef Filipović D, Zlatković J, Inta D et al (2011) Chronic isolation stress predisposes the frontal cortex but not the hippocampus to the potentially detrimental release of cytochrome c from mitochondria and the activation of caspase-3. J Neurosci Res 89:1461–1470. doi:10.​1002/​jnr.​22687 PubMedCrossRef
Zurück zum Zitat Fuchs E (2005) Social stress in tree shrews as an animal model of depression: an example of a behavioral model of a CNS disorder. CNS Spectr 10:182–190PubMedCrossRef Fuchs E (2005) Social stress in tree shrews as an animal model of depression: an example of a behavioral model of a CNS disorder. CNS Spectr 10:182–190PubMedCrossRef
Zurück zum Zitat Garrido C, Bruey JM, Fromentin A et al (1999) HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J 13:2061–2070PubMed Garrido C, Bruey JM, Fromentin A et al (1999) HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J 13:2061–2070PubMed
Zurück zum Zitat Garzón J, Del Río J (1981) Hyperactivity induced in rats by long-term isolation: further studies on a new animal model for the detection of antidepressants. Eur J Pharmacol 74:287–294PubMedCrossRef Garzón J, Del Río J (1981) Hyperactivity induced in rats by long-term isolation: further studies on a new animal model for the detection of antidepressants. Eur J Pharmacol 74:287–294PubMedCrossRef
Zurück zum Zitat Gass P, Reichardt HM, Strekalova T et al (2001) Mice with targeted mutations of glucocorticoid and mineralocorticoid receptors: models for depression and anxiety? Physiol Behav 73:811–825PubMedCrossRef Gass P, Reichardt HM, Strekalova T et al (2001) Mice with targeted mutations of glucocorticoid and mineralocorticoid receptors: models for depression and anxiety? Physiol Behav 73:811–825PubMedCrossRef
Zurück zum Zitat Gawryluk JW, Wang J-F, Andreazza AC et al (2011) Decreased levels of glutathione, the major brain antioxidant, in post-mortem prefrontal cortex from patients with psychiatric disorders. Int J Neuropsychopharmacol 14:123–130. doi:10.1017/S1461145710000805 PubMedCrossRef Gawryluk JW, Wang J-F, Andreazza AC et al (2011) Decreased levels of glutathione, the major brain antioxidant, in post-mortem prefrontal cortex from patients with psychiatric disorders. Int J Neuropsychopharmacol 14:123–130. doi:10.​1017/​S146114571000080​5 PubMedCrossRef
Zurück zum Zitat Ghatan S, Larner S, Kinoshita Y et al (2000) p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J Cell Biol 150:335–347PubMedPubMedCentralCrossRef Ghatan S, Larner S, Kinoshita Y et al (2000) p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J Cell Biol 150:335–347PubMedPubMedCentralCrossRef
Zurück zum Zitat Gutierrez-Correa J, Stoppani AO (1997) Inactivation of yeast glutathione reductase by Fenton systems: effect of metal chelators, catecholamines and thiol compounds. Free Radic Res 27:543–555PubMedCrossRef Gutierrez-Correa J, Stoppani AO (1997) Inactivation of yeast glutathione reductase by Fenton systems: effect of metal chelators, catecholamines and thiol compounds. Free Radic Res 27:543–555PubMedCrossRef
Zurück zum Zitat Hall FS (1998) Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 12:129–162PubMedCrossRef Hall FS (1998) Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 12:129–162PubMedCrossRef
Zurück zum Zitat Hall AV, Antoniou H, Wang Y et al (1994) Structural organization of the human neuronal nitric oxide synthase gene (NOS1). J Biol Chem 269:33082–33090PubMed Hall AV, Antoniou H, Wang Y et al (1994) Structural organization of the human neuronal nitric oxide synthase gene (NOS1). J Biol Chem 269:33082–33090PubMed
Zurück zum Zitat Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Oxford University Press, Oxford Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Oxford University Press, Oxford
Zurück zum Zitat Hao W, Myhre AP, Palmer JP (1999) Nitric oxide mediates IL-1beta stimulation of heat shock protein but not IL-1beta inhibition of glutamic acid decarboxylase. Autoimmunity 29:93–101PubMedCrossRef Hao W, Myhre AP, Palmer JP (1999) Nitric oxide mediates IL-1beta stimulation of heat shock protein but not IL-1beta inhibition of glutamic acid decarboxylase. Autoimmunity 29:93–101PubMedCrossRef
Zurück zum Zitat Haroon E, Raison CL, Miller AH (2012) Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 37:137–162. doi:10.1038/npp.2011.205 PubMedCrossRef Haroon E, Raison CL, Miller AH (2012) Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 37:137–162. doi:10.​1038/​npp.​2011.​205 PubMedCrossRef
Zurück zum Zitat Hatch AM, Wiberg GS, Zawidzka Z et al (1965) Isolation syndrome in the rat. Toxicol Appl Pharmacol 7:737–745PubMedCrossRef Hatch AM, Wiberg GS, Zawidzka Z et al (1965) Isolation syndrome in the rat. Toxicol Appl Pharmacol 7:737–745PubMedCrossRef
Zurück zum Zitat Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49:1023–1039PubMedCrossRef Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49:1023–1039PubMedCrossRef
Zurück zum Zitat Heneka MT, Sharp A, Klockgether T et al (2000) The heat shock response inhibits NF-kappaB activation, nitric oxide synthase type 2 expression, and macrophage/microglial activation in brain. J Cereb Blood Flow Metab 20:800–811. doi:10.1097/00004647-200005000-00006 PubMedCrossRef Heneka MT, Sharp A, Klockgether T et al (2000) The heat shock response inhibits NF-kappaB activation, nitric oxide synthase type 2 expression, and macrophage/microglial activation in brain. J Cereb Blood Flow Metab 20:800–811. doi:10.​1097/​00004647-200005000-00006 PubMedCrossRef
Zurück zum Zitat Hinwood M, Morandini J, Day TA, Walker FR (2012) Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb Cortex 22:1442–1454. doi:10.1093/cercor/bhr229 PubMedCrossRef Hinwood M, Morandini J, Day TA, Walker FR (2012) Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb Cortex 22:1442–1454. doi:10.​1093/​cercor/​bhr229 PubMedCrossRef
Zurück zum Zitat Holson RR, Scallet AC, Ali SF, Turner BB (1991) “Isolation stress” revisited: isolation-rearing effects depend on animal care methods. Physiol Behav 49:1107–1118PubMedCrossRef Holson RR, Scallet AC, Ali SF, Turner BB (1991) “Isolation stress” revisited: isolation-rearing effects depend on animal care methods. Physiol Behav 49:1107–1118PubMedCrossRef
Zurück zum Zitat Hsu YT, Wolter KG, Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 94:3668–3672PubMedPubMedCentralCrossRef Hsu YT, Wolter KG, Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 94:3668–3672PubMedPubMedCentralCrossRef
Zurück zum Zitat Ishida H, Mitsui K, Nukaya H et al (2003) Study of active substances involved in skin dysfunction induced by crowding stress. I. Effect of crowding and isolation on some physiological variables, skin function and skin blood perfusion in hairless mice. Biol Pharm Bull 26:170–181PubMedCrossRef Ishida H, Mitsui K, Nukaya H et al (2003) Study of active substances involved in skin dysfunction induced by crowding stress. I. Effect of crowding and isolation on some physiological variables, skin function and skin blood perfusion in hairless mice. Biol Pharm Bull 26:170–181PubMedCrossRef
Zurück zum Zitat Janáky R, Ogita K, Pasqualotto BA et al (1999) Glutathione and signal transduction in the mammalian CNS. J Neurochem 73:889–902PubMedCrossRef Janáky R, Ogita K, Pasqualotto BA et al (1999) Glutathione and signal transduction in the mammalian CNS. J Neurochem 73:889–902PubMedCrossRef
Zurück zum Zitat Janáky R, Shaw CA, Varga V et al (2000) Specific glutathione binding sites in pig cerebral cortical synaptic membranes. Neuroscience 95:617–624PubMedCrossRef Janáky R, Shaw CA, Varga V et al (2000) Specific glutathione binding sites in pig cerebral cortical synaptic membranes. Neuroscience 95:617–624PubMedCrossRef
Zurück zum Zitat Jiang B, Wang K, Liang P et al (2009) ATP-binding domain of heat shock protein 70 is essential for its effects on the inhibition of the release of the second mitochondria-derived activator of caspase and apoptosis in C2C12 cells. FEBS J 276:2615–2624. doi:10.1111/j.1742-4658.2009.06989.x PubMedCrossRef Jiang B, Wang K, Liang P et al (2009) ATP-binding domain of heat shock protein 70 is essential for its effects on the inhibition of the release of the second mitochondria-derived activator of caspase and apoptosis in C2C12 cells. FEBS J 276:2615–2624. doi:10.​1111/​j.​1742-4658.​2009.​06989.​x PubMedCrossRef
Zurück zum Zitat Jin W, Wang H, Yan W et al (2008) Disruption of Nrf2 enhances upregulation of nuclear factor-kappaB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediat Inflamm 2008:725174. doi:10.1155/2008/725174 CrossRef Jin W, Wang H, Yan W et al (2008) Disruption of Nrf2 enhances upregulation of nuclear factor-kappaB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediat Inflamm 2008:725174. doi:10.​1155/​2008/​725174 CrossRef
Zurück zum Zitat Kim HT, Kim YH, Nam JW et al (1994) Study of 5′-flanking region of human Cu/Zn superoxide dismutase. Biochem Biophys Res Commun 201:1526–1533PubMedCrossRef Kim HT, Kim YH, Nam JW et al (1994) Study of 5′-flanking region of human Cu/Zn superoxide dismutase. Biochem Biophys Res Commun 201:1526–1533PubMedCrossRef
Zurück zum Zitat Lapiz MDS, Fulford A, Muchimapura S et al (2003) Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci Behav Physiol 33:13–29PubMedCrossRef Lapiz MDS, Fulford A, Muchimapura S et al (2003) Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci Behav Physiol 33:13–29PubMedCrossRef
Zurück zum Zitat Leza JC, Salas E, Sawicki G et al (1998) The effects of stress on homeostasis in JCR-LA-cp rats: the role of nitric oxide. J Pharmacol Exp Ther 286:1397–1403PubMed Leza JC, Salas E, Sawicki G et al (1998) The effects of stress on homeostasis in JCR-LA-cp rats: the role of nitric oxide. J Pharmacol Exp Ther 286:1397–1403PubMed
Zurück zum Zitat Li N, Karin M (1999) Is NF-kappaB the sensor of oxidative stress? FASEB J 13:1137–1143PubMed Li N, Karin M (1999) Is NF-kappaB the sensor of oxidative stress? FASEB J 13:1137–1143PubMed
Zurück zum Zitat Li Y, Li G, Li C, Zhao Y (2007) Identification of nuclear factor-kappaB responsive element within the neuronal nitric oxide synthase exon 1f-specific promoter. Acta Biochim Biophys Sin (Shanghai) 39:247–254CrossRef Li Y, Li G, Li C, Zhao Y (2007) Identification of nuclear factor-kappaB responsive element within the neuronal nitric oxide synthase exon 1f-specific promoter. Acta Biochim Biophys Sin (Shanghai) 39:247–254CrossRef
Zurück zum Zitat Liu J, Mori A (1994) Involvement of reactive oxygen species in emotional stress: a hypothesis based on the immobilization stress-induced oxidative damage and antioxidant defense changes in rat brain, and the effect of antioxidant treatment with reduced glutathione. Int J Stress Manag 1:249–263. doi:10.1007/BF01857992 CrossRef Liu J, Mori A (1994) Involvement of reactive oxygen species in emotional stress: a hypothesis based on the immobilization stress-induced oxidative damage and antioxidant defense changes in rat brain, and the effect of antioxidant treatment with reduced glutathione. Int J Stress Manag 1:249–263. doi:10.​1007/​BF01857992 CrossRef
Zurück zum Zitat Lucassen PJ, Vollmann-Honsdorf GK, Gleisberg M et al (2001) Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur J Neurosci 14:161–166PubMedCrossRef Lucassen PJ, Vollmann-Honsdorf GK, Gleisberg M et al (2001) Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur J Neurosci 14:161–166PubMedCrossRef
Zurück zum Zitat Madan AP, DeFranco DB (1993) Bidirectional transport of glucocorticoid receptors across the nuclear envelope. Proc Natl Acad Sci USA 90:3588–3592PubMedPubMedCentralCrossRef Madan AP, DeFranco DB (1993) Bidirectional transport of glucocorticoid receptors across the nuclear envelope. Proc Natl Acad Sci USA 90:3588–3592PubMedPubMedCentralCrossRef
Zurück zum Zitat Madrigal JL, Moro MA, Lizasoain I et al (2001a) Inducible nitric oxide synthase expression in brain cortex after acute restraint stress is regulated by nuclear factor kappaB-mediated mechanisms. J Neurochem 76:532–538PubMedCrossRef Madrigal JL, Moro MA, Lizasoain I et al (2001a) Inducible nitric oxide synthase expression in brain cortex after acute restraint stress is regulated by nuclear factor kappaB-mediated mechanisms. J Neurochem 76:532–538PubMedCrossRef
Zurück zum Zitat Madrigal JLM, García-Bueno B, Moro MA et al (2003) Relationship between cyclooxygenase-2 and nitric oxide synthase-2 in rat cortex after stress. Eur J Neurosci 18:1701–1705PubMedCrossRef Madrigal JLM, García-Bueno B, Moro MA et al (2003) Relationship between cyclooxygenase-2 and nitric oxide synthase-2 in rat cortex after stress. Eur J Neurosci 18:1701–1705PubMedCrossRef
Zurück zum Zitat Madrigal JLM, García-Bueno B, Caso JR et al (2006) Stress-induced oxidative changes in brain. CNS Neurol Disord Drug Targets 5:561–568PubMedCrossRef Madrigal JLM, García-Bueno B, Caso JR et al (2006) Stress-induced oxidative changes in brain. CNS Neurol Disord Drug Targets 5:561–568PubMedCrossRef
Zurück zum Zitat Maes M, Mihaylova I, Bosmans E (2007a) Not in the mind of neurasthenic lazybones but in the cell nucleus: patients with chronic fatigue syndrome have increased production of nuclear factor kappa beta. Neuro Endocrinol Lett 28:456–462PubMed Maes M, Mihaylova I, Bosmans E (2007a) Not in the mind of neurasthenic lazybones but in the cell nucleus: patients with chronic fatigue syndrome have increased production of nuclear factor kappa beta. Neuro Endocrinol Lett 28:456–462PubMed
Zurück zum Zitat Maes M, Mihaylova I, Kubera M, Bosmans E (2007b) Not in the mind but in the cell: increased production of cyclo-oxygenase-2 and inducible NO synthase in chronic fatigue syndrome. Neuro Endocrinol Lett 28:463–469PubMed Maes M, Mihaylova I, Kubera M, Bosmans E (2007b) Not in the mind but in the cell: increased production of cyclo-oxygenase-2 and inducible NO synthase in chronic fatigue syndrome. Neuro Endocrinol Lett 28:463–469PubMed
Zurück zum Zitat Maes M, Galecki P, Chang YS, Berk M (2011) A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry 35:676–692. doi:10.1016/j.pnpbp.2010.05.004 PubMedCrossRef Maes M, Galecki P, Chang YS, Berk M (2011) A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry 35:676–692. doi:10.​1016/​j.​pnpbp.​2010.​05.​004 PubMedCrossRef
Zurück zum Zitat Maines MD, Eke BC, Zhao X (1996) Corticosterone promotes increased heme oxygenase-2 protein and transcript expression in the newborn rat brain. Brain Res 722:83–94PubMedCrossRef Maines MD, Eke BC, Zhao X (1996) Corticosterone promotes increased heme oxygenase-2 protein and transcript expression in the newborn rat brain. Brain Res 722:83–94PubMedCrossRef
Zurück zum Zitat Makino Y, Okamoto K, Yoshikawa N et al (1996) Thioredoxin: a redox-regulating cellular cofactor for glucocorticoid hormone action. Cross talk between endocrine control of stress response and cellular antioxidant defense system. J Clin Invest 98:2469–2477. doi:10.1172/JCI119065 PubMedPubMedCentralCrossRef Makino Y, Okamoto K, Yoshikawa N et al (1996) Thioredoxin: a redox-regulating cellular cofactor for glucocorticoid hormone action. Cross talk between endocrine control of stress response and cellular antioxidant defense system. J Clin Invest 98:2469–2477. doi:10.​1172/​JCI119065 PubMedPubMedCentralCrossRef
Zurück zum Zitat Malhotra V, Wong HR (2002) Interactions between the heat shock response and the nuclear factor-kappaB signaling pathway. Crit Care Med 30:S89–S95CrossRef Malhotra V, Wong HR (2002) Interactions between the heat shock response and the nuclear factor-kappaB signaling pathway. Crit Care Med 30:S89–S95CrossRef
Zurück zum Zitat McCoubrey WK, Huang TJ, Maines MD (1997) Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem 272:12568–12574PubMedCrossRef McCoubrey WK, Huang TJ, Maines MD (1997) Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J Biol Chem 272:12568–12574PubMedCrossRef
Zurück zum Zitat McIntosh LJ, Cortopassi KM, Sapolsky RM (1998a) Glucocorticoids may alter antioxidant enzyme capacity in the brain: kainic acid studies. Brain Res 791:215–222PubMedCrossRef McIntosh LJ, Cortopassi KM, Sapolsky RM (1998a) Glucocorticoids may alter antioxidant enzyme capacity in the brain: kainic acid studies. Brain Res 791:215–222PubMedCrossRef
Zurück zum Zitat McIntosh LJ, Hong KE, Sapolsky RM (1998b) Glucocorticoids may alter antioxidant enzyme capacity in the brain: baseline studies. Brain Res 791:209–214PubMedCrossRef McIntosh LJ, Hong KE, Sapolsky RM (1998b) Glucocorticoids may alter antioxidant enzyme capacity in the brain: baseline studies. Brain Res 791:209–214PubMedCrossRef
Zurück zum Zitat McKay LI, Cidlowski JA (2000) CBP (CREB binding protein) integrates NF-kappaB (nuclear factor-kappaB) and glucocorticoid receptor physical interactions and antagonism. Mol Endocrinol 14:1222–1234. doi:10.1210/mend.14.8.0506 PubMed McKay LI, Cidlowski JA (2000) CBP (CREB binding protein) integrates NF-kappaB (nuclear factor-kappaB) and glucocorticoid receptor physical interactions and antagonism. Mol Endocrinol 14:1222–1234. doi:10.​1210/​mend.​14.​8.​0506 PubMed
Zurück zum Zitat McLeod TM, López-Figueroa AL, López-Figueroa MO (2001) Nitric oxide, stress, and depression. Psychopharmacol Bull 35:24–41PubMed McLeod TM, López-Figueroa AL, López-Figueroa MO (2001) Nitric oxide, stress, and depression. Psychopharmacol Bull 35:24–41PubMed
Zurück zum Zitat Meyer M, Schreck R, Baeuerle PA (1993) H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 12:2005–2015PubMedPubMedCentral Meyer M, Schreck R, Baeuerle PA (1993) H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 12:2005–2015PubMedPubMedCentral
Zurück zum Zitat Miachon S, Rochet T, Mathian B et al (1993) Long-term isolation of Wistar rats alters brain monoamine turnover, blood corticosterone, and ACTH. Brain Res Bull 32:611–614PubMedCrossRef Miachon S, Rochet T, Mathian B et al (1993) Long-term isolation of Wistar rats alters brain monoamine turnover, blood corticosterone, and ACTH. Brain Res Bull 32:611–614PubMedCrossRef
Zurück zum Zitat Mihara M, Erster S, Zaika A et al (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11:577–590PubMedCrossRef Mihara M, Erster S, Zaika A et al (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11:577–590PubMedCrossRef
Zurück zum Zitat Mihm S, Galter D, Dröge W (1995) Modulation of transcription factor NF kappa B activity by intracellular glutathione levels and by variations of the extracellular cysteine supply. FASEB J 9:246–252PubMed Mihm S, Galter D, Dröge W (1995) Modulation of transcription factor NF kappa B activity by intracellular glutathione levels and by variations of the extracellular cysteine supply. FASEB J 9:246–252PubMed
Zurück zum Zitat Mizoguchi K, Ishige A, Aburada M, Tabira T (2003) Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus. Neuroscience 119:887–897PubMedCrossRef Mizoguchi K, Ishige A, Aburada M, Tabira T (2003) Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus. Neuroscience 119:887–897PubMedCrossRef
Zurück zum Zitat Möller M, Du Preez JL, Emsley R, Harvey BH (2011) Isolation rearing-induced deficits in sensorimotor gating and social interaction in rats are related to cortico-striatal oxidative stress, and reversed by sub-chronic clozapine administration. Eur Neuropsychopharmacol 21:471–483. doi:10.1016/j.euroneuro.2010.09.006 PubMedCrossRef Möller M, Du Preez JL, Emsley R, Harvey BH (2011) Isolation rearing-induced deficits in sensorimotor gating and social interaction in rats are related to cortico-striatal oxidative stress, and reversed by sub-chronic clozapine administration. Eur Neuropsychopharmacol 21:471–483. doi:10.​1016/​j.​euroneuro.​2010.​09.​006 PubMedCrossRef
Zurück zum Zitat Möller M, Du Preez JL, Viljoen FP et al (2013) Social isolation rearing induces mitochondrial, immunological, neurochemical and behavioural deficits in rats, and is reversed by clozapine or N-acetyl cysteine. Brain Behav Immun 30:156–167. doi:10.1016/j.bbi.2012.12.011 PubMedCrossRef Möller M, Du Preez JL, Viljoen FP et al (2013) Social isolation rearing induces mitochondrial, immunological, neurochemical and behavioural deficits in rats, and is reversed by clozapine or N-acetyl cysteine. Brain Behav Immun 30:156–167. doi:10.​1016/​j.​bbi.​2012.​12.​011 PubMedCrossRef
Zurück zum Zitat Morimoto RI, Tissieres AGC (1994) Molecular chaperone functions of hsp70 and hsp60 in protein folding. In: Frydman JHF (ed) The biology of the heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, New York, pp 251–283 Morimoto RI, Tissieres AGC (1994) Molecular chaperone functions of hsp70 and hsp60 in protein folding. In: Frydman JHF (ed) The biology of the heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, New York, pp 251–283
Zurück zum Zitat Nithipongvanitch R, Ittarat W, Cole MP et al (2007) Mitochondrial and nuclear p53 localization in cardiomyocytes: redox modulation by doxorubicin (Adriamycin)? Antioxid Redox Signal 9:1001–1008. doi:10.1089/ars.2007.1632 PubMedCrossRef Nithipongvanitch R, Ittarat W, Cole MP et al (2007) Mitochondrial and nuclear p53 localization in cardiomyocytes: redox modulation by doxorubicin (Adriamycin)? Antioxid Redox Signal 9:1001–1008. doi:10.​1089/​ars.​2007.​1632 PubMedCrossRef
Zurück zum Zitat Okamoto K, Tanaka H, Ogawa H et al (1999) Redox-dependent regulation of nuclear import of the glucocorticoid receptor. J Biol Chem 274:10363–10371PubMedCrossRef Okamoto K, Tanaka H, Ogawa H et al (1999) Redox-dependent regulation of nuclear import of the glucocorticoid receptor. J Biol Chem 274:10363–10371PubMedCrossRef
Zurück zum Zitat Olivenza R, Moro MA, Lizasoain I et al (2000) Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex. J Neurochem 74:785–791PubMedCrossRef Olivenza R, Moro MA, Lizasoain I et al (2000) Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex. J Neurochem 74:785–791PubMedCrossRef
Zurück zum Zitat Ozden O, Park S-H, Kim H-S et al (2011) Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Aging (Albany NY) 3:102–107CrossRef Ozden O, Park S-H, Kim H-S et al (2011) Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Aging (Albany NY) 3:102–107CrossRef
Zurück zum Zitat Pacak K, Palkovits M, Yadid G et al (1998) Heterogeneous neurochemical responses to different stressors: a test of Selye’s doctrine of nonspecificity. Am J Physiol 275:R1247–R1255PubMed Pacak K, Palkovits M, Yadid G et al (1998) Heterogeneous neurochemical responses to different stressors: a test of Selye’s doctrine of nonspecificity. Am J Physiol 275:R1247–R1255PubMed
Zurück zum Zitat Panahian N, Yoshiura M, Maines MD (1999) Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 72:1187–1203PubMedCrossRef Panahian N, Yoshiura M, Maines MD (1999) Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem 72:1187–1203PubMedCrossRef
Zurück zum Zitat Papadopoulos MC, Koumenis IL, Dugan LL, Giffard RG (1997) Vulnerability to glucose deprivation injury correlates with glutathione levels in astrocytes. Brain Res 748:151–156PubMedCrossRef Papadopoulos MC, Koumenis IL, Dugan LL, Giffard RG (1997) Vulnerability to glucose deprivation injury correlates with glutathione levels in astrocytes. Brain Res 748:151–156PubMedCrossRef
Zurück zum Zitat Patel RP, Darley-Usmar VM (1996) Using peroxynitrite as oxidant with low-density lipoprotein. Methods Enzymol 269:375–384PubMedCrossRef Patel RP, Darley-Usmar VM (1996) Using peroxynitrite as oxidant with low-density lipoprotein. Methods Enzymol 269:375–384PubMedCrossRef
Zurück zum Zitat Petrosillo G, Ruggiero FM, Pistolese M, Paradies G (2001) Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation. Possible role in the apoptosis. FEBS Lett 509:435–438PubMedCrossRef Petrosillo G, Ruggiero FM, Pistolese M, Paradies G (2001) Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation. Possible role in the apoptosis. FEBS Lett 509:435–438PubMedCrossRef
Zurück zum Zitat Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391PubMedCrossRef Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391PubMedCrossRef
Zurück zum Zitat Pizzi M, Sarnico I, Boroni F et al (2005) Inhibition of IkappaBalpha phosphorylation prevents glutamate-induced NF-kappaB activation and neuronal cell death. Acta Neurochir Suppl 93:59–63PubMedCrossRef Pizzi M, Sarnico I, Boroni F et al (2005) Inhibition of IkappaBalpha phosphorylation prevents glutamate-induced NF-kappaB activation and neuronal cell death. Acta Neurochir Suppl 93:59–63PubMedCrossRef
Zurück zum Zitat Plummer SM, Holloway KA, Manson MM et al (1999) Inhibition of cyclo-oxygenase 2 expression in colon cells by the chemopreventive agent curcumin involves inhibition of NF-kappaB activation via the NIK/IKK signalling complex. Oncogene 18:6013–6020. doi:10.1038/sj.onc.1202980 PubMedCrossRef Plummer SM, Holloway KA, Manson MM et al (1999) Inhibition of cyclo-oxygenase 2 expression in colon cells by the chemopreventive agent curcumin involves inhibition of NF-kappaB activation via the NIK/IKK signalling complex. Oncogene 18:6013–6020. doi:10.​1038/​sj.​onc.​1202980 PubMedCrossRef
Zurück zum Zitat Prabakaran S, Swatton JE, Ryan MM et al (2004) Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9(684–97):643. doi:10.1038/sj.mp.4001511 CrossRef Prabakaran S, Swatton JE, Ryan MM et al (2004) Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9(684–97):643. doi:10.​1038/​sj.​mp.​4001511 CrossRef
Zurück zum Zitat Radi R, Cassina A, Hodara R et al (2002) Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33:1451–1464PubMedCrossRef Radi R, Cassina A, Hodara R et al (2002) Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33:1451–1464PubMedCrossRef
Zurück zum Zitat Raju VS, McCoubrey WK, Maines MD (1997) Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain: characterization of a functional glucocorticoid response element. Biochim Biophys Acta 1351:89–104PubMedCrossRef Raju VS, McCoubrey WK, Maines MD (1997) Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain: characterization of a functional glucocorticoid response element. Biochim Biophys Acta 1351:89–104PubMedCrossRef
Zurück zum Zitat Reed JC, Jurgensmeier JM, Matsuyama S (1998) Bcl-2 family proteins and mitochondria. Biochim Biophys Acta 1366:127–137PubMedCrossRef Reed JC, Jurgensmeier JM, Matsuyama S (1998) Bcl-2 family proteins and mitochondria. Biochim Biophys Acta 1366:127–137PubMedCrossRef
Zurück zum Zitat Ren Q-G, Gong W-G, Wang Y-J et al (2015) Citalopram attenuates tau hyperphosphorylation and spatial memory deficit induced by social isolation rearing in middle-aged rats. J Mol Neurosci 56:145–153. doi:10.1007/s12031-014-0475-4 PubMedCrossRef Ren Q-G, Gong W-G, Wang Y-J et al (2015) Citalopram attenuates tau hyperphosphorylation and spatial memory deficit induced by social isolation rearing in middle-aged rats. J Mol Neurosci 56:145–153. doi:10.​1007/​s12031-014-0475-4 PubMedCrossRef
Zurück zum Zitat Ridnour LA, Thomas DD, Mancardi D et al (2004) The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations. Biol Chem 385:1–10. doi:10.1515/BC.2004.001 PubMedCrossRef Ridnour LA, Thomas DD, Mancardi D et al (2004) The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations. Biol Chem 385:1–10. doi:10.​1515/​BC.​2004.​001 PubMedCrossRef
Zurück zum Zitat Sánchez MM, Aguado F, Sánchez-Toscano F, Saphier D (1998) Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139:579–587. doi:10.1210/endo.139.2.5720 PubMed Sánchez MM, Aguado F, Sánchez-Toscano F, Saphier D (1998) Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139:579–587. doi:10.​1210/​endo.​139.​2.​5720 PubMed
Zurück zum Zitat Scapagnini G, D’Agata V, Calabrese V et al (2002) Gene expression profiles of heme oxygenase isoforms in the rat brain. Brain Res 954:51–59PubMedCrossRef Scapagnini G, D’Agata V, Calabrese V et al (2002) Gene expression profiles of heme oxygenase isoforms in the rat brain. Brain Res 954:51–59PubMedCrossRef
Zurück zum Zitat Schiller L, Jähkel M, Kretzschmar M et al (2003) Autoradiographic analyses of 5-HT1A and 5-HT2A receptors after social isolation in mice. Brain Res 980:169–178PubMedCrossRef Schiller L, Jähkel M, Kretzschmar M et al (2003) Autoradiographic analyses of 5-HT1A and 5-HT2A receptors after social isolation in mice. Brain Res 980:169–178PubMedCrossRef
Zurück zum Zitat Schliess F, Görg B, Fischer R et al (2002) Ammonia induces MK-801-sensitive nitration and phosphorylation of protein tyrosine residues in rat astrocytes. FASEB J 16:739–741. doi:10.1096/fj.01-0862fje PubMed Schliess F, Görg B, Fischer R et al (2002) Ammonia induces MK-801-sensitive nitration and phosphorylation of protein tyrosine residues in rat astrocytes. FASEB J 16:739–741. doi:10.​1096/​fj.​01-0862fje PubMed
Zurück zum Zitat Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483–487. doi:10.1038/20959 PubMedCrossRef Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483–487. doi:10.​1038/​20959 PubMedCrossRef
Zurück zum Zitat Stojanović S, Stanić D, Nikolić M, Raicević S, Spasić M, Niketić V (2005) Manganese superoxide dismutase (MnSOD) catalyzes NO-dependent tyrosine residue nitration. J Serb Chem Soc 70:601–608CrossRef Stojanović S, Stanić D, Nikolić M, Raicević S, Spasić M, Niketić V (2005) Manganese superoxide dismutase (MnSOD) catalyzes NO-dependent tyrosine residue nitration. J Serb Chem Soc 70:601–608CrossRef
Zurück zum Zitat Spasojevic N, Gavrilovic L, Varagic VV, Dronjak S (2007) Effects of chronic diazepam treatments on behavior on individually housed rats. Arch Biol Sci 59:113–117. doi:10.2298/ABS0702113S CrossRef Spasojevic N, Gavrilovic L, Varagic VV, Dronjak S (2007) Effects of chronic diazepam treatments on behavior on individually housed rats. Arch Biol Sci 59:113–117. doi:10.​2298/​ABS0702113S CrossRef
Zurück zum Zitat Tamatani M, Che YH, Matsuzaki H et al (1999) Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem 274:8531–8538PubMedCrossRef Tamatani M, Che YH, Matsuzaki H et al (1999) Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem 274:8531–8538PubMedCrossRef
Zurück zum Zitat Todorović N, Bošković M, Filipović D (2014) Fluoxetine failed to prevent isolation-induced changes of glutathione-dependent defense in rat hippocampus. Physical Chemistry 2014, 12th International conference on fundamental and applied aspects of Physical Chemistry, vol 3, pp 1121–1124 Todorović N, Bošković M, Filipović D (2014) Fluoxetine failed to prevent isolation-induced changes of glutathione-dependent defense in rat hippocampus. Physical Chemistry 2014, 12th International conference on fundamental and applied aspects of Physical Chemistry, vol 3, pp 1121–1124
Zurück zum Zitat Umegaki H, Yamamoto A, Suzuki Y, Iguchi A (2006) Stimulation of the hippocampal glutamate receptor systems induces stress-like responses. Neuro Endocrinol Lett 27:339–343PubMed Umegaki H, Yamamoto A, Suzuki Y, Iguchi A (2006) Stimulation of the hippocampal glutamate receptor systems induces stress-like responses. Neuro Endocrinol Lett 27:339–343PubMed
Zurück zum Zitat Xie QW, Kashiwabara Y, Nathan C (1994) Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem 269:4705–4708PubMed Xie QW, Kashiwabara Y, Nathan C (1994) Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem 269:4705–4708PubMed
Zurück zum Zitat Xu Y, Kiningham KK, Devalaraja MN et al (1999) An intronic NF-kappaB element is essential for induction of the human manganese superoxide dismutase gene by tumor necrosis factor-alpha and interleukin-1beta. DNA Cell Biol 18:709–722. doi:10.1089/104454999314999 PubMedCrossRef Xu Y, Kiningham KK, Devalaraja MN et al (1999) An intronic NF-kappaB element is essential for induction of the human manganese superoxide dismutase gene by tumor necrosis factor-alpha and interleukin-1beta. DNA Cell Biol 18:709–722. doi:10.​1089/​104454999314999 PubMedCrossRef
Zurück zum Zitat Zafir A, Banu N (2009) Induction of oxidative stress by restraint stress and corticosterone treatments in rats. Indian J Biochem Biophys 46:53–58PubMed Zafir A, Banu N (2009) Induction of oxidative stress by restraint stress and corticosterone treatments in rats. Indian J Biochem Biophys 46:53–58PubMed
Zurück zum Zitat Zhang L, Zhou R, Li X et al (2006) Stress-induced change of mitochondria membrane potential regulated by genomic and non-genomic GR signaling: a possible mechanism for hippocampus atrophy in PTSD. Med Hypotheses 66:1205–1208. doi:10.1016/j.mehy.2005.11.041 PubMedCrossRef Zhang L, Zhou R, Li X et al (2006) Stress-induced change of mitochondria membrane potential regulated by genomic and non-genomic GR signaling: a possible mechanism for hippocampus atrophy in PTSD. Med Hypotheses 66:1205–1208. doi:10.​1016/​j.​mehy.​2005.​11.​041 PubMedCrossRef
Zurück zum Zitat Zhu W, Zhang R, Hu C, Umegaki H (2008) Effect of the entorhinal cortex on diurnal ACTH and corticosterone release in rats. Neuro Endocrinol Lett 29:159–162PubMedCrossRef Zhu W, Zhang R, Hu C, Umegaki H (2008) Effect of the entorhinal cortex on diurnal ACTH and corticosterone release in rats. Neuro Endocrinol Lett 29:159–162PubMedCrossRef
Zurück zum Zitat Zlatković J, Todorović N, Bošković M et al (2014b) Different susceptibility of prefrontal cortex and hippocampus to oxidative stress following chronic social isolation stress. Mol Cell Biochem 393:43–57. doi:10.1007/s11010-014-2045-z PubMedCrossRef Zlatković J, Todorović N, Bošković M et al (2014b) Different susceptibility of prefrontal cortex and hippocampus to oxidative stress following chronic social isolation stress. Mol Cell Biochem 393:43–57. doi:10.​1007/​s11010-014-2045-z PubMedCrossRef
Metadaten
Titel
Oxidative and nitrosative stress pathways in the brain of socially isolated adult male rats demonstrating depressive- and anxiety-like symptoms
Publikationsdatum
31.03.2016
Erschienen in
Brain Structure and Function / Ausgabe 1/2017
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1218-9

Weitere Artikel der Ausgabe 1/2017

Brain Structure and Function 1/2017 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.