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Different susceptibility of prefrontal cortex and hippocampus to oxidative stress following chronic social isolation stress

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Abstract

Chronic oxidative stress plays an important role in depression. The aim of present study was to examine the stress-induced changes in serum corticosterone (CORT) levels, cytosolic protein carbonyl groups, malondialdehyde (MDA), reduced glutathione (GSH), nitric oxide (NO) and total superoxide dismutase (SOD) activity in the prefrontal cortex versus hippocampus of male Wistar rats exposed to acute (2 h of immobilization or cold), chronic (21d of social isolation) stress, and their combination (chronic + acute stress). The subcellular distribution of nuclear factor-κB (NF-κB) and cytosolic cyclooxygenase 2 (COX-2) protein expressions were also examined. Depressive- and anxiety-like behaviors were assessed via the forced swim, sucrose preference, and marble burying tests in chronically isolated rats. Although both acute stressors resulted in elevated CORT, increased MDA in the prefrontal cortex and NF-κB activation accompanied by increased NO in the hippocampus were detected only following acute cold stress. Chronic isolation resulted in no change in CORT levels, but disabled appropriate response to novel acute stress and led to depressive- and anxiety-like behaviors. Increased oxidative/nitrosative stress markers, likely by NF-κB nuclear translocation and concomitant COX-2 upregulation, associated with decreased SOD activity and GSH levels, suggested the existence of oxidative stress in the prefrontal cortex. In contrast, hippocampus was less susceptible to oxidative damage showing only increase in protein carbonyl groups and depleted GSH. Taken together, the prefrontal cortex seems to be more sensitive to oxidative stress than the hippocampus following chronic isolation stress, which may be relevant for further research related to stress-induced depressive-like behavior.

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References

  1. Pacák K, Palkovits M (2001) Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22(4):502–548. doi:10.1210/er.22.4.502

    Article  PubMed  Google Scholar 

  2. de Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475. doi:10.1038/nrn1683

    Article  PubMed  Google Scholar 

  3. McEwen BS (2008) Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583(2–3):174–185. doi:10.1016/j.ejphar.2007.11.071

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Friedman J (2011) Why is the nervous system vulnerable to oxidative stress? In: Gadoth N, Göbel HH (eds.) Oxidative stress and free radical damage in neurology. Humana Press, Clifton, p 19–27. doi: 10.1007/978-1-60327-514-9_2

  5. Şahin E, Gümüşlü S (2004) Cold-stress-induced modulation of antioxidant defence: role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidation. Int J Biometeorol 48(4):165–171. doi:10.1007/s00484-004-0205-7

    Article  PubMed  Google Scholar 

  6. Lei XG (2002) In vivo antioxidant role of glutathione peroxidase: evidence from knockout mice. Methods Enzymol 347:213–225. doi:10.1016/S0076-6879(02)47021-8

    Article  CAS  PubMed  Google Scholar 

  7. Madrigal JL, Hurtado O, Moro MA, Lizasoain I, Lorenzo P, Castrillo A, et al. (2002) The increase in TNF-alpha levels is implicated in NFkappaB activation and inducible nitric oxide synthase expression in brain cortex after immobilization stress. Neuropsychopharmacology 26(2):155-163. doi: 155-163.10.1038/S0893-133X(01)00292-5

    Google Scholar 

  8. Sahin E, Gumuslu S (2004) Alterations in brain antioxidant status, protein oxidation and lipid peroxidation in response to different stress models. Behav Brain Res 155(2):241–248. doi:10.1016/j.bbr.2004.04.022

    Article  CAS  PubMed  Google Scholar 

  9. André M, Felley-Bosco E (2003) Heme oxygenase-1 induction by endogenous nitric oxide: influence of intracellular glutathione. FEBS Lett 546(2–3):223–227. doi:10.1016/S0014-5793(03)00576-3

    Article  PubMed  Google Scholar 

  10. Moncada S, Bolaños JP (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97(6):1676–1689. doi:10.1111/j.1471-4159.2006.03988.x

    Article  CAS  PubMed  Google Scholar 

  11. Zhang XY, da Chen C, Xiu MH, Wang F, Qi LY, Sun HQ, Chen S, He SC, Wu GY, Haile CN, Kosten TA, Lu L, Kosten TR (2009) The novel oxidative stress marker thioredoxin is increased in first-episode schizophrenic patients. Schizophr Res 113:151–157. doi:10.1016/j.schres.2009.05.016

    Article  PubMed  Google Scholar 

  12. García-Bueno B, Caso JR, Leza JC (2008) Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 32:1136–1151. doi:10.1016/j.neubiorev.2008.04.001

    Article  PubMed  Google Scholar 

  13. Buchanan MM, Hutchinson M, Watkins LR, Yin H (2010) Toll-like receptor 4 in CNS pathologies. J Neurochem 114(1):13–27. doi:10.1111/j.1471-4159.2010.06736.x

    CAS  PubMed Central  PubMed  Google Scholar 

  14. O’Neill LA, Kaltschmidt C (1997) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20(6):252–258. doi:10.1016/S0166-2236(96)01035-1

    Article  PubMed  Google Scholar 

  15. Li N, Karin M (1999) Is NF-kappaB the sensor of oxidative stress? FASEB J 13(10):1137–1143

    CAS  PubMed  Google Scholar 

  16. Guerrini L, Blasi F, Denis-Donini S (1995) Synaptic activation of NF-kappa B by glutamate in cerebellar granule neurons in vitro. Proc Natl Acad Sci 92(20):9077–9081

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Rojo AI, Salinas M, Martín D, Perona R, Cuadrado A (2004) Regulation of Cu/Zn-superoxide dismutase expression via the phosphatidylinositol 3 kinase/Akt pathway and nuclear factor-kappaB. J Neurosci 24(33):7324–7334. doi:10.1523/JNEUROSCI.2111-04.2004

    Article  CAS  PubMed  Google Scholar 

  18. 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 39(4):247–254. doi:10.1111/j.1745-7270.2007.00280.x

    Article  CAS  PubMed  Google Scholar 

  19. Madrigal JL, García-Bueno B, Caso JR, Pérez-Nievas BG, Leza JC (2006) Stress-induced oxidative changes in brain. CNS Neurol Disord: Drug Targets 5:561–568. doi:10.2174/187152706778559327

    Article  Google Scholar 

  20. Minghetti L (2004) Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. J Neuropathol Exp Neurol 63(9):901–910

    CAS  PubMed  Google Scholar 

  21. Phillis JW, Horrocks LA, Farooqui AA (2006) Cyclooxygenases, lipoxygenases, and epoxygenases in CNS: their role and involvement in neurological disorders. Brain Res Rev 52:201–243. doi:10.1016/j.brainresrev.2006.02.002

    Article  CAS  PubMed  Google Scholar 

  22. Guo JY, Li CY, Ruan YP, Sun M, Qi XL, Zhao BS, Luo F (2009) Chronic treatment with celecoxib reverses chronic unpredictable stress-induced depressive-like behavior via reducing cyclooxygenase-2 expression in rat brain. Eur J Pharmacol 612(1–3):54–60. doi:10.1016/j.ejphar.2009.03.076

    Article  CAS  PubMed  Google Scholar 

  23. Müller N, Schwarz MJ (2008) COX-2 inhibition in schizophrenia and major depression. Curr Pharm Des 14(14):1452–1465. doi:10.2174/138161208784480243

    Article  PubMed  Google Scholar 

  24. Bremner JD (2006) Traumatic stress: effects on the brain. Dialogues Clin Neurosci 8(4):445–461

    PubMed Central  PubMed  Google Scholar 

  25. Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic–pituitary–adrenal responses to stress. J Neurosci 13(9):3839–3847

    CAS  PubMed  Google Scholar 

  26. Arnsten AFT (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10(6):410–422. doi:10.1038/nrn2648

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105–122. doi:10.1146/annurev.neuro.22.1.105

    Article  CAS  PubMed  Google Scholar 

  28. Müller HK, Wegener G, Popoli M, Elfving B (2011) Differential expression of synaptic proteins after chronic restraint stress in rat prefrontal cortex and hippocampus. Brain Res 1385:26–37. doi:10.1016/j.brainres.2011.02.048

    Article  PubMed  Google Scholar 

  29. Filipović D, Zlatković J, Inta D, Bjelobaba I, Stojiljkovic M, Gass P (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(9):1461–1470. doi:10.1002/jnr.22687

    Article  PubMed  Google Scholar 

  30. Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007) The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 27(11):2781–2787. doi:10.1523/JNEUROSCI.4372-06.2007

    Article  CAS  PubMed  Google Scholar 

  31. Colaianna M, Schiavone S, Zotti M, Tucci P, Morgese MG, Ba L, Holmdahl R, Krause KH, Cuomo V, Trabace L (2013) Neuroendocrine profile in a rat model of psychosocial stress: relation to oxidative stress. Antioxid Redox Signal 18:1385–1399. doi:10.1089/ars.2012.4569

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiat 49:1023–1039. doi:10.1016/S0006-3223(01)01157-X

    Article  CAS  PubMed  Google Scholar 

  33. Heinrich LM, Gullone E (2006) The clinical significance of loneliness: a literature review. Clin Psychol Rev 26:695–718. doi:10.1016/j.cpr.2006.04.002

    Article  PubMed  Google Scholar 

  34. Hall FS (1998) Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 12:129–162. doi:10.1615/CritRevNeurobiol.v12.i1-2.50

    Article  CAS  PubMed  Google Scholar 

  35. Liu YH, Liu AH, Xu Y, Tie L, Yu HM, Li XJ (2005) Effect of chronic unpredictable mild stress on brain-pancreas relative protein in rat brain and pancreas. Behav Brain Res 165(1):63–71. doi:10.1016/j.bbr.2005.06.034

    Article  PubMed  Google Scholar 

  36. Dronjak S, Spasojevic N, Gavrilovic L, Varagic V (2007) Behavioural and endocrine responses of socially isolated rats to long-term diazepam treatment. Acta Vet 57(4):291–302. doi:10.2298/AVB0704291D

    Article  Google Scholar 

  37. Serra M, Sanna E, Mostallino MC, Biggio G (2007) Social isolation stress and neuroactive steroids. Eur Neuropsychopharmacol 17(1):1–11. doi:10.1016/j.euroneuro.2006.03.004

    Article  CAS  PubMed  Google Scholar 

  38. Carnevali L, Mastorci F, Graiani G, Razzoli M, Trombini M, Pico-Alfonso MA, Arban R, Grippo AJ, Quaini F, Sgoifo A (2012) Social defeat and isolation induce clear signs of a depression-like state, but modest cardiac alterations in wild-type rats. Physiol Behav 106(2):142–150. doi:10.1016/j.physbeh.2012.01.022

    Article  CAS  PubMed  Google Scholar 

  39. Djordjevic J, Djordjevic A, Adzic M, Radojcic MB (2012) Effects of chronic social isolation on Wistar rat behavior and brain plasticity markers. Neuropsychobiology 66(2):112–119. doi:10.1159/000338605

    Article  PubMed  Google Scholar 

  40. Holsboer F (2000) The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23(5):477–501. doi:10.1016/S0893-133X(00)00159-7

    Article  CAS  PubMed  Google Scholar 

  41. Gold PW, Chrousos GP (2002) Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol Psychiat 7:254–275. doi:10.1038/sj/mp/400103

    Article  CAS  Google Scholar 

  42. Westenbroek C, Den Boer JA, Veenhuis M, Ter Horst GJ (2004) Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res Bull 64:303–308. doi:10.1016/j.brainresbull.2004.08.006

    Article  PubMed  Google Scholar 

  43. Wainwright SR, Galea LAM (2013) The neural plasticity theory of depression: assessing the roles of adult neurogenesis and PSA-NCAM within the hippocampus. Neural Plast. doi:10.1155/2013/805497

  44. Schiepers OJ, Wichers MC, Maes M (2005) Cytokines and major depression. Prog Neuropsychopharmacol Biol Psychiat 29(2):201–217. doi:10.1016/j.pnpbp.2004.11.003

    Article  CAS  Google Scholar 

  45. Ben Menachem-Zidon O, Goshen I, Kreisel T, Ben Menahem Y, Reinhartz E, Ben Hur T, Yirmiya R (2008) Intrahippocampal transplantation of transgenic neural precursor cells overexpressing interleukin-1 receptor antagonist blocks chronic isolation-induced impairment in memory and neurogenesis. Neuropsychopharmacology 33(9):2251–2262. doi:10.1038/sj.npp.1301606

    Article  CAS  PubMed  Google Scholar 

  46. Shao L, Martin MV, Watson SJ, Schatzberg A, Akil H, Myers RM, Jones EG, Bunney WE, Vawter MP (2008) Mitochondrial involvement in psychiatricdisorders. Ann Med 40:281–295. doi:10.1080/07853890801923753

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Sapolsky RM (1999) Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol 34(6):721–732. doi:10.1016/S0531-5565(99)00047-9

    Article  CAS  PubMed  Google Scholar 

  48. Kvetnansky R, Mikulaj L (1970) Adrenal and urinary catecholamines in rat during adaptation to repeated immobilization stress. Endocrinology 87:738–743. doi:10.1210/endo-87-4-738

    Article  CAS  PubMed  Google Scholar 

  49. Garzón J, del Rio J (1981) Hyperactivity induced in rats by longterm isolation: further studies on a new animal model for the detection of antidepressants. Eur J Pharmacol 74:287–294. doi:10.1016/0014-2999(81)90047-9

    Article  PubMed  Google Scholar 

  50. Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730–732. doi:10.1038/266730a0

    Article  CAS  PubMed  Google Scholar 

  51. Porsolt RD, Brossard G, Hautbois C, Roux S (2001) Rodent models of depression: forced swimming and tail suspension behavioral despair tests in rats and mice. Curr Protoc Neurosci. doi: 10.1002/0471142301.ns0810as14

  52. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R (1987) Reduction of sucrose preference by chronic unpredictable mild stress and its restoration by a tricyclic antidepressant. Psychopharmacology 93:358–364. doi:10.1007/BF00187257

    Article  CAS  PubMed  Google Scholar 

  53. Ho YJ, Eichendorff J, Schwarting RK (2002) Individual response profiles of male Wistar rats in animal models for anxiety and depression. Behav Brain Res 136:1–12. doi:10.1016/s0166-4328(02)00089-x

    Article  PubMed  Google Scholar 

  54. Lowry OH, Rosebrough NJ, Farr AJ, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  PubMed  Google Scholar 

  55. Zlatković J, Filipović D (2013) Chronic social isolation induces NF-κB activation and upregulation of iNOS protein expression in rat prefrontal cortex. Neurochem Int 63(3):172–179. doi:10.1016/j.neuint.2013.06.002

    Article  PubMed  Google Scholar 

  56. Zlatković J, Bernardi RE, Filipović D (2014) Protective effect of Hsp70i against chronic social isolation stress in the rat hippocampus. J Neural Transm 121(1):3–14. doi:10.1007/s00702-013-1066-1

    Article  PubMed  Google Scholar 

  57. Albro PW, Corbett JT, Schroeder JL (1986) Application of the thiobarbiturate assay to the measurement of lipid peroxidation products in microsomes. J Biochem Biophys Methods 13(3):185–194. doi:10.1016/0165-022X(86)90092-8

    Article  CAS  PubMed  Google Scholar 

  58. Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  PubMed  Google Scholar 

  59. Hissin PJ, Hilf R (1973) A fluorometric method for the determination of oxidized and reduced glutathione in tissue. Anal Biochem 74:214–226. doi:10.1016/0003-2697(76)90326-2

    Article  Google Scholar 

  60. Cortas NK, Wakid NW (1990) Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction method. Clin Chem 36(8):1440–1443

    CAS  PubMed  Google Scholar 

  61. Navarro-Gonzálvez JA, García-Benayas C, Arenas J (1998) Semiautomated measurement of nitrate in biological fluids. Clin Chem 44(3):679–681

    PubMed  Google Scholar 

  62. Blagojevic DP, Grubor-Lajsic GN, Spasic MB (2011) Cold defence responses: the role of oxidative stress. Front Biosci 3:416–427. doi:10.2741/s161

    Article  Google Scholar 

  63. Selman C, McLaren JS, Himanka MJ, Speakman JR (2000) Effect of long-term cold exposure on antioxidant enzyme activities in a small mammal. Free Radic Biol Med 28(8):1279–1285. doi:10.1016/S0891-5849(00)00263-X

    Article  CAS  PubMed  Google Scholar 

  64. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM (2007) Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 8(10):766–775. doi:10.1038/nrn2214

    Article  CAS  PubMed  Google Scholar 

  65. Contestabile A, Ciani E (2004) Role of nitric oxide in the regulation of neuronal proliferation, survival and differentiation. Neurochem Int 45(6):903–914. doi:10.1016/j.neuint.2004.03.021

    Article  CAS  PubMed  Google Scholar 

  66. Mühl H, Pfeilschifter J (1995) Amplification of nitric oxide synthase expression by nitric oxide in interleukin 1b-stimulated rat mesangial cells. J Clin Invest 95:1941–1946. doi:10.1172/JCI117876

    Article  PubMed Central  PubMed  Google Scholar 

  67. Filipović D, Pajović SB (2009) Differential regulation of CuZnSOD expression in rat brain by acute and/or chronic stress. Cell Mol Neurobiol 29(5):673–681. doi:10.1007/s10571-009-9375-5

    Article  PubMed  Google Scholar 

  68. Borsini F, Podhorna J, Marazziti D (2002) Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology 163(2):121–141. doi:10.1007/s00213-002-1155-6

    Article  CAS  PubMed  Google Scholar 

  69. Farley S, Apazoglou K, Witkin JM, Giros B, Tzavara ET (2010) Antidepressant- like effects of an AMPA receptor potentiator under a chronic mild stress paradigm. Int J Neuropsychopharmacol 13:1207–1218. doi:10.1017/S1461145709991076

    Article  CAS  PubMed  Google Scholar 

  70. Sandi C, Richter-Levin G (2009) From high anxiety trait to depression: a neurocognitive hypothesis. Trends Neurosci 32(6):312–320. doi:10.1016/j.tins.2009.02.004

    Article  CAS  PubMed  Google Scholar 

  71. Pal SN, Dandiya PC (1994) Glutathione as a cerebral substrate in depressive behavior. Pharmacol Biochem Behav 48(4):845–851. doi:10.1016/0091-3057(94)90191-0

    Article  CAS  PubMed  Google Scholar 

  72. Eren I, Naziroglu M, Demirdas A, Celik O, Uguz AC, Altunbasak A, Ozmen I, Uz E (2007) Venlafaxine modulates depression-induced oxidative stress in brain and medulla of rat. Neurochem Res 32(3):497–505. doi:10.1007/s11064-006-9258-9

    Article  CAS  PubMed  Google Scholar 

  73. 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(5–6):358–362. doi:10.1016/j.neuint.2009.01.001

    Article  CAS  PubMed  Google Scholar 

  74. Ljubuncic PS, Bar-shai M, Reznik AZ (2008) The role of reactive nitrogen species (RNS) in the activation of nuclear factor kappa B (NFkB) and its implications for biological systems: the question of balance. In: Valacchi G, Davis P (eds) Oxidants in biology: a question of balance. Springer, New York, 67-111. doi: 10.1007/978-1-4020-8399-0_4

  75. Hu F, Wang X, Pace TWW, Wu H, Miller AH (2005) Inhibition of COX-2 by celecoxib enhances glucocorticoid receptor function. Mol Psychiat 10(5):426–428. doi:10.1038/sj.mp.4001644

    Article  CAS  Google Scholar 

  76. 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 12:35–45. doi:10.1016/S0969-9961(02)00017-7

    Article  CAS  PubMed  Google Scholar 

  77. Brown GC (2010) Nitric oxide and neuronal death. Nitric Oxide 23:153–165. doi:10.1016/j.niox.2010.06.001

    Article  CAS  PubMed  Google Scholar 

  78. Olivenza R, Moro MA, Lizasoain I, Lorenzo P, Fernández 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(2):785–791. doi:10.1046/j.1471-4159.2000.740785.x

    Article  CAS  PubMed  Google Scholar 

  79. Madrigal JLM, Garcia-Bueno B, Moro A, Lizasoanin I, Lorenzo P, Leza JC (2003) Relationship between cyclooxygenase-2 and nitric oxide synthase-2 in rat cortex after stress. Eur J Neurosci 18:1701–1705. doi:10.1046/j.1460-9568.2003.02888.x

    Article  PubMed  Google Scholar 

  80. Zlatković J, Filipović D (2012) Bax and Bcl-2 mediate proapoptotic signaling following chronic isolation stress in rat brain. Neuroscience 223:238–245. doi:10.1016/j.neuroscience.2012.08.005

    Article  PubMed  Google Scholar 

  81. Macmillan Crow LA, Crow JP, Thompson JA (1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37:1613–1622. doi:10.1021/bi971894b

    Article  CAS  PubMed  Google Scholar 

  82. Kamat JP (2006) Peroxynitrite: a potent oxidizing and nitrating agent. Indian J Exp Biol 44(6):436–447

    CAS  PubMed  Google Scholar 

  83. Filipović D, Lj Gavrilović, Dronjak S, Radojčić BM (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

    Article  PubMed  Google Scholar 

  84. 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(3):409–415. doi:10.1016/j.physbeh.2004.01.011

    Article  CAS  PubMed  Google Scholar 

  85. Parihar MS, Pandit MK (2003) Free radical induced increase in protein carbonyl is attenuated by low dose of adenosine in hippocampus and mid brain: implication in neurodegenerative disorders. Gen Physiol Biophys 22(1):29–39

    CAS  PubMed  Google Scholar 

  86. Bizzozero OA, Ziegler JL, De Jesus G, Bolognani F (2006) Acute depletion of reduced glutathione causes extensive carbonylation of rat brain proteins. J Neurosci Res 83(4):656–667. doi:10.1002/jnr.20771

    Article  CAS  PubMed  Google Scholar 

  87. Berendji D, Kolb-Bachofen V, Meyer KL, Kröncke KD (1999) Influence of nitric oxide on the intracellular reduced glutathione pool: different cellular capacities and strategies to encounter nitric oxide-mediated stress. Free Radic Biol Med 27:773–780. doi:10.1016/S0891-5849(99)00123-9

    Article  CAS  PubMed  Google Scholar 

  88. Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329(1–2):23–38. doi:10.1016/S0009-8981(03)00003-2

    Article  CAS  PubMed  Google Scholar 

  89. Bizzozero OA, Reyes S, Ziegler J, Smerjac S (2007) Lipid peroxidation scavengers prevent the carbonylation of cytoskeletal brain proteins induced by glutathione depletion. Neurochem Res 32(12):2114–2122. doi:10.1007/s11064-007-9377-y

    Article  CAS  PubMed  Google Scholar 

  90. Wong GTH, Chang RCC, Law ACK (2013) A breach in the scaffold: the possible role of cytoskeleton dysfunction in the pathogenesis of major depression. Ageing Res Rev 12(1):67–75. doi:10.1016/j.arr.2012.08.004

    Article  CAS  PubMed  Google Scholar 

  91. Lin YC, Koleske AJ (2010) Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu Rev Neurosci 33:349–378. doi:10.1146/annurev-neuro-060909-153204

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  92. Keller JN, Mattson MP (1998) Roles of lipid peroxidation in modulation of cellular signaling pathways, cell dysfunction, and death in the nervous system. Rev Neurosci 9(2):105–116. doi:10.1515/REVNEURO.1998.9.2.105

    Article  CAS  PubMed  Google Scholar 

  93. Zhou QG, Hu Y, Hua Y, Hu M, Luo CX, Han X, Zhu XJ, Wang B, Xu JS, Zhu DY (2007) Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis. J Neurochem 103(5):1843–1854. doi:10.1111/j.1471-4159.2007.04914.x

    Article  CAS  PubMed  Google Scholar 

  94. Ishida H, Mitsui K, Nukaya H, Matsumoto K, Tsuji K (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(2):170–181. doi:10.1248/bpb.26.170

    Article  CAS  PubMed  Google Scholar 

  95. Pacak K, Palkovits M, Yadid G, Kvetnansky R, Kopin IJ, Goldstein DS (1998) Heterogeneous neurochemical responses to different stressors: a test of Selye’s doctrine of nonspecificity. Am J Physiol 275(4 Pt 2):R1247–R1255

    CAS  PubMed  Google Scholar 

  96. Shacter E (2000) Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 32(3–4):307–326. doi:10.1081/DMR-100102336

    Article  CAS  PubMed  Google Scholar 

  97. Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM (2012) 53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 149(7):1536–1548. doi:10.1016/j.cell.2012.05.014

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgment

This work was supported by the Ministry of Sciences of the Republic of Serbia, Grant 173044.

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Correspondence to Dragana Filipović.

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Zlatkovic Jelena and Todorovic Nevena have contributed equally to this work

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Zlatković, J., Todorović, N., Bošković, M. et al. Different susceptibility of prefrontal cortex and hippocampus to oxidative stress following chronic social isolation stress. Mol Cell Biochem 393, 43–57 (2014). https://doi.org/10.1007/s11010-014-2045-z

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  • DOI: https://doi.org/10.1007/s11010-014-2045-z

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