Advertisement

Psychopharmacology

, Volume 232, Issue 16, pp 2921–2938 | Cite as

Ozone exposure of Flinders Sensitive Line rats is a rodent translational model of neurobiological oxidative stress with relevance for depression and antidepressant response

  • Mmalebuso L. Mokoena
  • Brian H. Harvey
  • Francois Viljoen
  • Susanna M. Ellis
  • Christiaan B. Brink
Original Investigation

Abstract

Rationale

Major depression has been associated with higher levels of air pollution that in turn leads to neurodegeneration via increased oxidative stress. There is a need for suitable translational animal models to study the role of oxidative stress in depression and antidepressant action.

Objective

Considering the gene X environment hypothesis of depression, the present study investigated the effect of chronic ozone inhalation on depression and anxiety-related behavior, cognition, and brain markers of oxidative stress in the Flinders Sensitive Line (FSL) rat. In addition, response to the antioxidant melatonin, and the antidepressants desipramine or escitalopram, was assessed.

Methods

Rats were exposed to ozone (0.0 or 0.3 parts per million (ppm)) per inhalation for 4 h daily for a period of 15 days, while simultaneously receiving saline or the above-mentioned drugs.

Results

The data indicate that chronic ozone inhalation induced memory impairment, anxiety and depression-like effects, reduced cortical and hippocampal superoxide dismutase and catalase activity, and compromised central monoamine levels similar to that noted in depression. Moreover, the behavioral and neurochemical effects of melatonin, desipramine, and escitalopram were mostly attenuated in the presence of ozone.

Conclusion

Thus, genetically susceptible individuals exposed to high levels of oxidative stress are at higher risk of developing mood and/or an anxiety disorders, showing greater redox imbalance and altered behavior. These animals are also more resistant to contemporary antidepressant treatment. The presented model provides robust face, construct, and predictive validity, suitable for studying neuronal oxidative stress in depression, antidepressant action and mechanisms to prevent neuronal oxidative stress.

Keywords

Ozone Oxidative stress Flinders Sensitive Line Rats Depression Melatonin Desipramine Escitalopram Animal model 

Notes

Acknowledgments

The South African National Research Foundation (NRF) (Grant no. IFR2011033000023) is acknowledged for financial support. This article is dedicated to the first author and PhD student, Lilly Mokoena, who died tragically and prematurely after submission of the manuscript. She distinguished herself early in her career at both national and international level in pharmacology circles, being a brilliant upcoming young scientist and compassionate colleague and friend.

Conflict of interest

There is no actual or potential conflict of interest in relation to this article.

References

  1. Aguiar CC, Almeida AB, Araújo PV, Vasconcelos GS, Chaves EM, do Vale OC, Macêdo DS, Leal LK, de Barros Viana GS, Vasconcelos SM (2013) Effects of agomelatine on oxidative stress in the brain of mice after chemically induced seizures. Cell Mol Neurobiol 33:825–835PubMedCrossRefGoogle Scholar
  2. Avila-Costa MR, Colín-Barenque L, Fortoul TI, Machado-Salas JP, Espinosa-Villanueva J, Rugerio-Vargas C, Rivas-Arancibia S (1999) Memory deterioration in an oxidative stress model and its correlation with cytological changes on rat hippocampus CA1. Neurosci Lett 270:107–109PubMedCrossRefGoogle Scholar
  3. Avila-Costa MR, Colín-Barenque L, Fortoul TI, Machado-Salas JP, Espinosa-Villanueva J, Rugerio-Vargas C, Borgonio C, Dorado C, Rivas-arancibia S (2001) Motor impairments in an oxidative stress model and its correlation with cytological changes on rat striatum and prefrontal cortex. Int J Neurosci 108:193–200PubMedCrossRefGoogle Scholar
  4. Baldessarini RJ (2006) Drug therapy of depression and anxiety disorders. Goodman and Gilman’s the pharmacological basis of therapeutics. Edited by Brunton LL, Lazo JS, Parker KL. New York, McGraw-Hill:429–460.Google Scholar
  5. Beck CH, Fibiger HC (1995) Chronic desipramine alters stress-induced behaviors and regional expression of the immediate early gene,< i > c-fos. Pharmacol Biochem Behav 51:331–338PubMedCrossRefGoogle Scholar
  6. Beckman KB, Ames BN (1999) Endogenous oxidative damage of mtDNA. Mutat Res/Fundam Mol Mech Mutagen 424:51–58CrossRefGoogle Scholar
  7. Berk M, Copolov DL, Dean O, Lu K, Jeavons S, Schapkaitz I, Anderson-Hunt M, Bush AI (2008) N-acetyl cysteine for depressive symptoms in bipolar disorder—a double-blind randomized placebo-controlled trial. Biol Psychiatry 64:468–475PubMedCrossRefGoogle Scholar
  8. Berk M, Dean OM, Cotton SM, Jeavons S, Tanious M, Kohlmann K, Hewitt K, Moss K, Allwang C, Schapkaitz I, Robbins J, Cobb H, Ng F, Dodd S, Bush AI, Malhi GS (2014) The efficacy of adjunctive N-acetylcysteine in major depressive disorder: a double-blind, randomized, placebo-controlled trial. J Clin Psychiatry 75:628–636PubMedCrossRefGoogle Scholar
  9. Bertaina-Anglade V, Drieu-La-Rochelle C, Mocaër E, Seguin L (2011) Memory facilitating effects of agomelatine in the novel object recognition memory paradigm in the rat. Pharmacol Biochem Behav 98:511–517PubMedCrossRefGoogle Scholar
  10. 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 64:43–51PubMedCrossRefGoogle Scholar
  11. Block ML, Elder A, Auten RL, Bilbo SD, Chen H, Chen J, Cory-Slechta DA, Costa D, Diaz-Sanchez D, Dorman DC (2012) The outdoor air pollution and brain health workshop. Neurotoxicology 33:972–984PubMedCentralPubMedCrossRefGoogle Scholar
  12. Blokland A, ten Oever S, van Gorp D, van Draanen M, Schmidt T, Nguyen E, Krugliak A, Napoletano A, Keuter S, Klinkenberg I (2012) The use of a test battery assessing affective behavior in rats: order effects. Behav Brain Res 228:16–21PubMedCrossRefGoogle Scholar
  13. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  14. Brand A, Jolles J, Gispen-de Wied C (1992) Recall and recognition memory deficits in depression. J Affect Disord 25:77–86PubMedCrossRefGoogle Scholar
  15. Bravo JA, Diaz-Veliz G, Mora S, Ulloa JL, Berthoud VM, Morales P, Arancibia S, Fiedler JL (2009) Desipramine prevents stress-induced changes in depressive-like behavior and hippocampal markers of neuroprotection. Behav Pharmacol 20:273–285. doi: 10.1097/FBP.0b013e32832c70d9 PubMedCrossRefGoogle Scholar
  16. Bremner JD, Randall P, Vermetten E, Staib L, Bronen RA, Mazure C, Capelli S, McCarthy G, Innis RB, Charney DS (1997) Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse—a preliminary report. Biol Psychiatry 41:23–32PubMedCentralPubMedCrossRefGoogle Scholar
  17. Calderón-Garcidueñas L, D’Angiulli A, Kulesza RJ, Torres-Jardón R, Osnaya N, Romero L, Keefe S, Herritt L, Brooks DM, Avila-Ramirez J (2011) Air pollution is associated with brainstem auditory nuclei pathology and delayed brainstem auditory evoked potentials. Int J Dev Neurosci 29:365–375PubMedCentralPubMedCrossRefGoogle Scholar
  18. Calderón-Garcidueñas L, Serrano-Sierra A, Torres-Jardón R, Zhu H, Yuan Y, Smith D, Delgado-Chávez R, Cross JV, Medina-Cortina H, Kavanaugh M (2013) The impact of environmental metals in young urbanites’ brains. Exp Toxicol Pathol 65:503–511PubMedCentralPubMedCrossRefGoogle Scholar
  19. Carman JS, Post RM, Buswell R, Goodwin FK (1976) Negative effects of melatonin on depression. Am J Psychiatry 133:1181–1186PubMedCrossRefGoogle Scholar
  20. Chelikani P, Fita I, Loewen P (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci CMLS 61:192–208PubMedCrossRefGoogle Scholar
  21. Chen F, Wegener G, Madsen TM, Nyengaard JR (2013) Mitochondrial plasticity of the hippocampus in a genetic rat model of depression after antidepressant treatment. Synapse 67:127–134PubMedCrossRefGoogle Scholar
  22. Clinton S, Sucharski I, Finlay J (2006) Desipramine attenuates working memory impairments induced by partial loss of catecholamines in the rat medial prefrontal cortex. Psychopharmacol (Berl) 183:404–412CrossRefGoogle Scholar
  23. Cottet-Emard J, Dalmaz Y, Pequignot J, Peyrin L, Pequignot J (1997) Long-term exposure to ozone alters peripheral and central catecholamine activity in rats. Pflugers Arch 433:744–749PubMedCrossRefGoogle Scholar
  24. Couto FS, Batalha VL, Valadas JS, Data-Franca J, Ribeiro JA, Lopes LV (2012) Escitalopram improves memory deficits induced by maternal separation in the rat. Eur J Pharmacol 695:71–75PubMedCrossRefGoogle Scholar
  25. Cryan JF, Holmes A (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4:775–790PubMedCrossRefGoogle Scholar
  26. Duman R (2002) Pathophysiology of depression: the concept of synaptic plasticity. Eur Psychiatr 17:306–310CrossRefGoogle Scholar
  27. Espejo E, Minano F (1999) Prefrontocortical dopamine depletion induces antidepressant-like effects in rats and alters the profile of desipramine during Porsolt’s test. Neuroscience 88:609–615PubMedCrossRefGoogle Scholar
  28. Ferreira FR, Biojone C, Joca SR, Guimaraes FS (2008) Antidepressant-like effects of N-acetyl-l-cysteine in rats. Behav Pharmacol 19:747–750. doi: 10.1097/FBP.0b013e3283123c98 PubMedCrossRefGoogle Scholar
  29. File SE, Seth P (2003) A review of 25 years of the social interaction test. Eur J Pharmacol 463:35–53PubMedCrossRefGoogle Scholar
  30. Fischer CW, Liebenberg N, Elfving B, Lund S, Wegener G (2012) Isolation-induced behavioural changes in a genetic animal model of depression. Behav Brain Res 230:85–91PubMedCrossRefGoogle Scholar
  31. Flandreau EI, Bourke CH, Ressler KJ, Vale WW, Nemeroff CB, Owens MJ (2013) Escitalopram alters gene expression and HPA axis reactivity in rats following chronic overexpression of corticotropin-releasing factor from the central amygdala. Psychoneuroendocrinology 38:1349–1361PubMedCentralPubMedCrossRefGoogle Scholar
  32. Fonken L, Xu X, Weil Z, Chen G, Sun Q, Rajagopalan S, Nelson R (2011) Air pollution impairs cognition, provokes depressive-like behaviors and alters hippocampal cytokine expression and morphology. Mol Psychiatry 16:987–995PubMedCentralPubMedCrossRefGoogle Scholar
  33. Fukui K, Onodera K, Shinkai T, Suzuki S, Urano S (2001) Impairment of learning and memory in rats caused by oxidative stress and aging, and changes in antioxidative defense systems. Ann N Y Acad Sci 928:168–175PubMedCrossRefGoogle Scholar
  34. Galano A, Tan DX, Reiter RJ (2011) Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 51:1–16PubMedCrossRefGoogle Scholar
  35. Galecki P, Kedziora J, Florkowski A, Galecka E (2007) Lipid peroxidation and copper-zinc superoxide dismutase activity in patients treated with fluoxetine during the first episode of depression. Psychiatr Pol 41:615–624PubMedGoogle Scholar
  36. Garcia-Cazorla A, Duarte S, Serrano M, Nascimento A, Ormazabal A, Carrilho I, Briones P, Montoya J, Garesse R, Sala-Castellvi P (2008) Mitochondrial diseases mimicking neurotransmitter defects. Mitochondrion 8:273–278PubMedCrossRefGoogle Scholar
  37. Gaur V, Kumar A (2010) Protective effect of desipramine, venlafaxine and trazodone against experimental animal model of transient global ischemia: possible involvement of NO–cGMP pathway. Brain Res 1353:204–212PubMedCrossRefGoogle Scholar
  38. Golombek DA, Martini M, Cardinali DP (1993) Melatonin as an anxiolytic in rats: time dependence and interaction with the central GABAergic system. Eur J Pharmacol 237:231–236PubMedCrossRefGoogle Scholar
  39. Gonenc S, Uysal N, Acikgoz O, Kayatekin B, Sonmez A, Kiray M, Aksu I, Gulecer B, Topcu A, Semin I (2005) Effects of melatonin on oxidative stress and spatial memory impairment induced by acute ethanol treatment in rats. Physiol Res 54:341–348PubMedGoogle Scholar
  40. Hansson AC, Rimondini R, Heilig M, Mathe AA, Sommer WH (2011) Dissociation of antidepressant-like activity of escitalopram and nortriptyline on behaviour and hippocampal BDNF expression in female rats. J Psychopharmacol 25:1378–1387. doi: 10.1177/0269881110393049 PubMedCrossRefGoogle Scholar
  41. Haridas S, Kumar M, Manda K (2013) Melatonin ameliorates chronic mild stress induced behavioral dysfunctions in mice. Physiol Behav 119:201–207PubMedCrossRefGoogle Scholar
  42. Harvey BH, McEwen BS, Stein DJ (2003) Neurobiology of antidepressant withdrawal: implications for the longitudinal outcome of depression. Biol Psychiatry 54:1105–1117PubMedCrossRefGoogle Scholar
  43. Harvey BH, Brand L, Jeeva Z, Stein DJ (2006) Cortical/hippocampal monoamines, HPA-axis changes and aversive behavior following stress and restress in an animal model of post-traumatic stress disorder. Physiol Behav 87:881–890PubMedCrossRefGoogle Scholar
  44. Harvey BH, Joubert C, du Preez JL, Berk M (2008) Effect of chronic N-acetyl cysteine administration on oxidative status in the presence and absence of induced oxidative stress in rat striatum. Neurochem Res 33:508–517PubMedCrossRefGoogle Scholar
  45. Harvey BH, Hamer M, Louw R, van der Westhuizen FH, Malan L (2013) Metabolic and glutathione redox markers associated with brain-derived neurotrophic factor in depressed African men and women: evidence for counterregulation? Neuropsychobiology 67:33–40. doi: 10.1159/000343501 PubMedCrossRefGoogle Scholar
  46. Husum H, Aznar S, Høyer-Hansen S, Hald Larsen M, Mikkelsen JD, Møller A, Mathé AA, Wörtwein G (2006) Exacerbated loss of cell survival, neuropeptide Y-immunoreactive (IR) cells, and serotonin-IR fiber lengths in the dorsal hippocampus of the aged flinders sensitive line “depressed” rat: implications for the pathophysiology of depression? J Neurosci Res 84:1292–1302PubMedCrossRefGoogle Scholar
  47. Ilsley J, Moffoot AP, O’Carroll R (1995) An analysis of memory dysfunction in major depression. J Affect Disord 35:1–9PubMedCrossRefGoogle Scholar
  48. Kumar A, Garg R (2009) Protective effects of antidepressants against chronic fatigue syndrome-induced behavioral changes and biochemical alterations. Fundam Clin Pharmacol 23:89–95PubMedCrossRefGoogle Scholar
  49. Leonard B, Maes M (2012) Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci Biobehav Rev 36:764–785PubMedCrossRefGoogle Scholar
  50. Lesch KP (2004) Gene-environment interaction and the genetics of depression. J Psychiatry Neurosci 29:174–184PubMedCentralPubMedGoogle Scholar
  51. Levkovitz Y, Caftori R, Avital A, Richter-Levin G (2002) The SSRIs drug fluoxetine, but not the noradrenergic tricyclic drug desipramine, improves memory performance during acute major depression. Brain Res Bull 58:345–350PubMedCrossRefGoogle Scholar
  52. Liu Y, Ni C, Tang Y, Tian X, Zhou Y, Qian M, Li Z, Chui D, Guo X (2013) Melatonin attenuates isoflurane‐induced acute memory impairments in aged rats. Basic Clin Pharmacol Toxicol 113:215–220PubMedCrossRefGoogle Scholar
  53. Maes M, Mihaylova I, Kubera M, Uytterhoeven M, Vrydags N, Bosmans E (2009) Lower plasma Coenzyme Q 10 in depression: a marker for treatment resistance and chronic fatigue in depression and a risk factor to cardiovascular disorder in that illness. Neuroendocrinol Lett 30:462–469PubMedGoogle Scholar
  54. Mantovani M, Pértile R, Calixto JB, Santos AR, Rodrigues ALS (2003) Melatonin exerts an antidepressant-like effect in the tail suspension test in mice: evidence for involvement of < i > N-methyl-d-aspartate receptors and the l-arginine-nitric oxide pathway. Neurosci Lett 343:1–4PubMedCrossRefGoogle Scholar
  55. McCord JM, Edeas MA (2005) SOD, oxidative stress and human pathologies: a brief history and a future vision. Biomed Pharmacother 59:139–142PubMedCrossRefGoogle Scholar
  56. McIlwain KL, Merriweather MY, Yuva-Paylor LA, Paylor R (2001) The use of behavioral test batteries: effects of training history. Physiol Behav 73:705–717PubMedCrossRefGoogle Scholar
  57. Mikrouli E, Wörtwein G, Soylu R, Mathé AA, Petersén Å (2011) Increased numbers of orexin/hypocretin neurons in a genetic rat depression model. Neuropeptides 45:401–406PubMedCrossRefGoogle Scholar
  58. Mokoena ML, Harvey BH, Oliver DW, Brink CB (2010) Ozone modulates the effects of imipramine on immobility in the forced swim test, and nonspecific parameters of hippocampal oxidative stress in the rat. Metab Brain Dis 25:125–133PubMedCrossRefGoogle Scholar
  59. Mokoena ML, Brink CB, Harvey BH, Oliver DW (2011) Appraisal of ozone as biologically active molecule and experimental tool in biomedical sciences. Med Chem Res 20:1687–1695CrossRefGoogle Scholar
  60. 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 21:471–483PubMedCrossRefGoogle Scholar
  61. Möller M, Du Preez JL, Viljoen FP, Berk M, Emsley R, Harvey BH (2013a) Social isolation rearing induces mitochondrial, immunological, neurochemical and behavioural deficits in rats, and is reversed by clozapine or N-acetyl cysteine. Brain Behav Immun 30:156–167PubMedCrossRefGoogle Scholar
  62. Möller M, Du Preez JL, Viljoen FP, Berk M, Harvey BH (2013b) N-acetyl cysteine reverses social isolation rearing induced changes in cortico-striatal monoamines in rats. Metab Brain Dis 28:687–696PubMedCrossRefGoogle Scholar
  63. Montgomery K (1955) The relation between fear induced by novel stimulation and exploratory drive. J Comp Physiol Psychol 48:254PubMedCrossRefGoogle Scholar
  64. Ng F, Berk M, Dean O, Bush AI (2008) Oxidative stress in psychiatric disorders: evidence base and therapeutic implications. Int J Neuropsychopharmacol 11:851–876PubMedCrossRefGoogle Scholar
  65. Overstreet DH, Griebel G (2004) Antidepressant-like effects of CRF < sub > 1 receptor antagonist SSR125543 in an animal model of depression. Eur J Pharmacol 497:49–53PubMedCrossRefGoogle Scholar
  66. Overstreet DH, Wegener G (2013) The flinders sensitive line rat model of depression—25 years and still producing. Pharmacol Rev 65:143–155. doi: 10.1124/pr.111.005397 PubMedCrossRefGoogle Scholar
  67. Overstreet DH, Keeney A, Hogg S (2004) Antidepressant effects of citalopram and CRF receptor antagonist CP-154,526 in a rat model of depression. Eur J Pharmacol 492:195–201PubMedCrossRefGoogle Scholar
  68. Overstreet DH, Friedman E, Mathé AA, Yadid G (2005) The flinders sensitive line rat: a selectively bred putative animal model of depression. Neurosci Biobehav Rev 29:739–759PubMedCrossRefGoogle Scholar
  69. Ozdemir D, Tugyan K, Uysal N, Sonmez U, Sonmez A, Acikgoz O, Ozdemir N, Duman M, Ozkan H (2005) Protective effect of melatonin against head trauma-induced hippocampal damage and spatial memory deficits in immature rats. Neurosci Lett 385:234–239PubMedCrossRefGoogle Scholar
  70. Öztürk G, Akbulut KG, Güney Ş, Acuna-Castroviejo D (2012) Age-related changes in the rat brain mitochondrial antioxidative enzyme ratios: modulation by melatonin. Exp Gerontol 47:706–711PubMedCrossRefGoogle Scholar
  71. Papp M, Gruca P, Boyer P, Mocaër E (2003) Effect of agomelatine in the chronic mild stress model of depression in the rat. Neuropsychopharmacology 28:694–703PubMedCrossRefGoogle Scholar
  72. Papp M, Litwa E, Gruca P, Mocaër E (2006) Anxiolytic-like activity of agomelatine and melatonin in three animal models of anxiety. Behav Pharmacol 17:9–18PubMedGoogle Scholar
  73. Paylor R, Spencer CM, Yuva-Paylor LA, Pieke-Dahl S (2006) The use of behavioral test batteries, II: Effect of test interval. Physiol Behav 87:95–102PubMedCrossRefGoogle Scholar
  74. Pereyra-Muñoz N, Rugerio-Vargas C, Angoa-Pérez M, Borgonio-Pérez G, Rivas-Arancibia S (2006) Oxidative damage in substantia nigra and striatum of rats chronically exposed to ozone. J Chem Neuroanat 31:114–123PubMedCrossRefGoogle Scholar
  75. Pilar-Cuéllar F, Vidal R, Díaz A, Castro E, dos Anjos S, Pascual-Brazo J, Linge R, Vargas V, Blanco H, Martínez-Villayandre B (2013) Neural plasticity and proliferation in the generation of antidepressant effects: hippocampal implication. Neural Plast 2013:537265. doi: 10.1155/2013/537265
  76. Power MC, Weisskopf MG, Alexeeff SE, Coull BA, Spiro A 3rd, Schwartz J (2011) Traffic-related air pollution and cognitive function in a cohort of older men. Environ Health Perspect 119:682–687. doi: 10.1289/ehp.1002767 PubMedCentralPubMedCrossRefGoogle Scholar
  77. Pryce CR, Klaus F (2013) Translating the evidence for gene association with depression into mouse models of depression-relevant behaviour: current limitations and future potential. Neurosci Biobehav Rev 37:1380–1402PubMedCrossRefGoogle Scholar
  78. Reiter RJ, TAN D, Poeggeler B, Menendez‐Pelaez A, Chen L, Saarela S (1994) Melatonin as a free radical scavenger: implications for aging and age‐related diseasesa. Ann N Y Acad Sci 719:1–12PubMedCrossRefGoogle Scholar
  79. Reiter RJ, Tan D, Osuna C, Gitto E (2000a) Actions of melatonin in the reduction of oxidative stress. J Biomed Sci 7:444–458PubMedCrossRefGoogle Scholar
  80. Reiter RJ, Tan DX, Qi W, Manchester LC, Karbownik M, Calvo JR (2000b) Pharmacology and physiology of melatonin in the reduction of oxidative stress in vivo. Biol Signals Recept 9:160–171PubMedCrossRefGoogle Scholar
  81. Reiter RJ, Acuña‐Castroviejo D, Tan D, Burkhardt S (2001a) Free radical‐mediated molecular damage. Ann N Y Acad Sci 939:200–215PubMedCrossRefGoogle Scholar
  82. Reiter RJ, Tan D, Manchester LC, Qi W (2001b) Biochemical reactivity of melatonin with reactive oxygen and nitrogen species. Cell Biochem Biophys 34:237–256PubMedCrossRefGoogle Scholar
  83. Reiter RJ, Tan D, Terron MP, Flores LJ, Czarnocki Z (2007) Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol-Engl Ed 54:1Google Scholar
  84. Rivas-Arancibia S, Dorado-Martínez C, Colin-Barenque L, Kendrick KM, de la Riva C, Guevara-Guzmán R (2003) Effect of acute ozone exposure on locomotor behavior and striatal function. Pharmacol Biochem Behav 74:891–900PubMedCrossRefGoogle Scholar
  85. Rivas-Arancibia S, Guevara-Guzman R, Lopez-Vidal Y, Rodriguez-Martinez E, Zanardo-Gomes M, Angoa-Perez M, Raisman-Vozari R (2010) Oxidative stress caused by ozone exposure induces loss of brain repair in the hippocampus of adult rats. Toxicol Sci 113:187–197. doi: 10.1093/toxsci/kfp252 PubMedCrossRefGoogle Scholar
  86. Santiago-López D, Bautista-Martinez J, Reyes-Hernandez C, Aguilar-Martinez M, Rivas-Arancibia S (2010) Oxidative stress, progressive damage in the substantia nigra and plasma dopamine oxidation, in rats chronically exposed to ozone. Toxicol Lett 197:193–200PubMedCrossRefGoogle Scholar
  87. Sarandol A, Sarandol E, Eker SS, Erdinc S, Vatansever E, Kirli S (2007) Major depressive disorder is accompanied with oxidative stress: short‐term antidepressant treatment does not alter oxidative–antioxidative systems. Hum Psychopharmacol Clin Exp 22:67–73CrossRefGoogle Scholar
  88. Savitz J, Drevets WC (2009) Bipolar and major depressive disorder: neuroimaging the developmental-degenerative divide. Neurosci Biobehav Rev 33:699–771PubMedCentralPubMedCrossRefGoogle Scholar
  89. Sewerynek E, Melchiorri D, Chen L, Reiter RJ (1995) Melatonin reduces both basal and bacterial lipopolysaccharide-induced lipid peroxidation in vitro. Free Radic Biol Med 19:903–909PubMedCrossRefGoogle Scholar
  90. Shalaby A, Kamal S (2009) Effect of escitalopram on GABA level and anti-oxidant markers in prefrontal cortex and nucleus accumbens of chronic mild stress-exposed albino rats. Int J Physiol Pathophysiol Pharmacol 1:154–161PubMedCentralPubMedGoogle Scholar
  91. Sharma M, Gupta Y (2001) Effect of chronic treatment of melatonin on learning, memory and oxidative deficiencies induced by intracerebroventricular streptozotocin in rats. Pharmacol Biochem Behav 70:325–331PubMedCrossRefGoogle Scholar
  92. Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82:291–295PubMedCrossRefGoogle Scholar
  93. Silva RA, West JJ, Zhang Y, Anenberg SC, Lamarque J, Shindell DT, Collins WJ, Dalsoren S, Faluvegi G, Folberth G (2013) Global premature mortality due to anthropogenic outdoor air pollution and the contribution of past climate change. Environ Res Lett 8:034005CrossRefGoogle Scholar
  94. Soulage C, Perrin D, Cottet-Emard J, Pequignot J, Dalmaz Y, Pequignot J (2004) Central and peripheral changes in catecholamine biosynthesis and turnover in rats after a short period of ozone exposure. Neurochem Int 45:979–986PubMedCrossRefGoogle Scholar
  95. Spijker S (2011) Dissection of rodent brain regions. In: Anonymous neuroproteomics. Springer, pp 13–26Google Scholar
  96. Trams EG, Lauter CJ, Brandenburger Brown EA, Young O (1972) Cerebral cortical metabolism after chronic exposure to ozone. Arch Envir Health: Int J 24:153–159CrossRefGoogle Scholar
  97. von Gall C, Stehle JH, Weaver DR (2002) Mammalian melatonin receptors: molecular biology and signal transduction. Cell Tissue Res 309:151–162CrossRefGoogle Scholar
  98. Wegener G, Volke V, Harvey BH, Rosenberg R (2003) Local, but not systemic, administration of serotonergic antidepressants decreases hippocampal nitric oxide synthase activity. Brain Res 959:128–134PubMedCrossRefGoogle Scholar
  99. Wehr TA, Jacobsen FM, Sack DA, Arendt J, Tamarkin L, Rosenthal NE (1986) Phototherapy of seasonal affective disorder. Time of day and suppression of melatonin are not critical for antidepressant effects. Arch Gen Psychiatry 43:870–875PubMedCrossRefGoogle Scholar
  100. Zhang H, Squadrito GL, Pryor WA (1998) The reaction of melatonin with peroxynitrite: formation of melatonin radical cation and absence of stable nitrated products. Biochem Biophys Res Commun 251:83–87PubMedCrossRefGoogle Scholar
  101. Zhou N, Fu Z, Sun T (2008) Effects of different concentrations of oxygen–ozone on rats’ astrocytes in vitro. Neurosci Lett 441:178–182PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Mmalebuso L. Mokoena
    • 1
  • Brian H. Harvey
    • 2
  • Francois Viljoen
    • 1
  • Susanna M. Ellis
    • 3
  • Christiaan B. Brink
    • 1
  1. 1.Division of Pharmacology, School of PharmacyNorth-West UniversityPotchefstroomSouth Africa
  2. 2.Centre of Excellence for Pharmaceutical Sciences, Faculty of Health SciencesNorth-West UniversityPotchefstroomSouth Africa
  3. 3.Statistical Consultation Services, Centre for Business Mathematics and InformaticsNorth-West UniversityPotchefstroomSouth Africa

Personalised recommendations