N-acetyl cysteine reverses social isolation rearing induced changes in cortico-striatal monoamines in rats

Metabolic Brain Disease

Volumn 28, Issue 4, 2013, Pages 687-696

  Möller, Marisa ^a   Du Preez, Jan L ^a   Viljoen, Francois P ^a   Berk, Michael ^b   Harvey, Brian H ^a  

^a NORTH WEST UNIVERSITY   (South Africa)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Frontal cortex; Monoamines; N acetyl cysteine; Schizophrenia; Social isolation rearing; Striatum

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; ACETYLCYSTEINE; BRAIN MONOAMINE; DOPAMINE; HOMOVANILLIC ACID; NORADRENALIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN METABOLISM; BRAIN TISSUE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; FEMALE; FRONTAL CORTEX; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; REARING; SCHIZOPHRENIA; SOCIAL ISOLATION;

ANIMALIA; RATTUS;

3,4-DIHYDROXYPHENYLACETIC ACID; ACETYLCYSTEINE; ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; HOMOVANILLIC ACID; HYDROXYINDOLEACETIC ACID; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SOCIAL ISOLATION;

EID: 84887256413     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-013-9433-z     Document Type: Article

References (79)

1. Aghajanian GK, Marek GJ (2000) Serotonin model of schizophrenia: emerging role of glutamate mechanisms. Brain Res Rev 31:302-312
2. Arent CO, Réus GZ, Abelaira HM, Ribeiro KF, Steckert AV, Mina F et al (2012) Synergist effects of n-acetylcysteine and deferoxamine treatment on behavioral and oxidative parameters induced by chronic mild stress in rats. Neurochem Int 61:1072-80
3. Avshalumov MV, Rice ME (2003) Activation ofATP-sensitive K + (K(ATP)) channels by H2O2 underlies glutamate-dependent inhibition of striatal dopamine release. Proc. Natl Acad Sci USA 100:11729-11734
4. Berk M, Copolov DL, Dean O, Lu K, Jeavons S, Schapkaitz I, Anderson-Hunt M, Bush AI (2008a) N-Acetyl cysteine for depressive symptoms in bipolar disorder - a double-blind randomized placebo-controlled trial. Biol Psychiatry 64:468-475
5. Berk M, Copolov DL, Dean O, Lu K, Jeavons S, Schapkaitz I, Anderson-Hunt M, Judd F, Katz F, Katz P et al (2008b) N-Acetyl cysteine as a glutathione precursor for schizophrenia - a double-blind, randomized, placebo-controlled trial. Biol Psychiatry 64:361-368
6. Berk M, Dean O, Cotton SM, Gama CS, Kapczinski F, Fernandes BS, Kohlmann K, Jeavons S, Hewitt K, Allwang C, Cobb H, Bush AI, Dodd S, Malhi GS (2011) The efficacy of n-acetylcysteine as an adjunctive treatment in bipolar depression: an open label trial. J Affect Disord 135:389-394
7. Berk M, Malhi GS, Gray LJ, Dean OM (2013) The promise of N-acetylcysteine in neuropsychiatry. Trends Pharmacol Sci 34:167-177
8. Bernstein HG, Keilhoff G, Steiner J, Dobrowolny H, Bogerts B (2011) Nitric oxide and schizophrenia: present knowledge and emerging concepts of therapy. CNS Neurol Disord Drug Targets 10:792-807
9. Blier P, El Mansari M (2007) The importance of serotonin and noradrenaline in anxiety. Int J Psychiatry Clin Pract 11:16-23
10. 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
11. Cabungcal JH, Steullet P, Kraftsik R, Cuenod M, Do KQ (2012) Early-life insults impair parvalbumin interneurons via oxidative stress: Reversal by N-acetylcysteine. Biol Psychiatry 73:574-82
12. Carlsson A, Waters N, Holm-Waters S, Tedroff J, Nilsson M, Carlsson ML (2001) Interactions between monoamines, glutomate, and GABA in schizophrenia: New evidence. Ann Rev Pharmacol Toxicol 41:237-260
13. Chorpita BF, Barlow DH (1998) The development of anxiety: the role of control in the early environment. Psychol Bull 124:3-21
14. Dantzer R, O'Connor JC, Lawson MA, Kelley KW (2011) Inflammation- associated depression: from serotonin to kynurenine. Psychoneuroendocrinology 36:426-436
15. Dean OM, van den Buuse M, Bush AI (2009) A role for glutathione in the pathophysiology of bipolar disorder and schizophrenia? Animal models and relevance to clinical practice. Curr Med Chem 16:2965-76
16. Dean OM, Giorlando F, Berk M (2011) N-acetylcysteine in psychiatry: current therapeutic evidence and potential mechanisms of action. J Psychiatry Neurosci 36:78-86
17. Dodd S, Dean O, Copolov DL, Malhi GS, Berk M (2008) N-acetylcysteine for antioxidant therapy: Pharmacology and clinical utility. Expert Opin Biol Ther 8:1955-1962
18. Galynker II, Cai J, Ongseng F, Finestone H, Dutta E, Serseni D (1998) Hypofrontality and negative symptoms in major depressive disorder. J Nucl Med 39:608-612
19. Garcia-Cazorla A, Duarte S, Serrano M, Nascimento A, Ormazabal A, Carrilho I et al (2008) Mitochondrial diseases mimicking neurotransmitter defects. Mitochondrion 8:273-278
20. Garvey MJ, Tuason VB (1996) Low levels of MHPG in depressive spectrum patients. J Affect Disord 37:103-108
21. Gawryluk JW, Wang J, Andreazza AC, Shao L, Yatham LM, Young LT (2011) Prefrontal cortex glutathione S-transferase levels in patients with bipolar disorder, major depression and schizophrenia. Int J Neuropsychopharmacol 14:1069-1074
22. Grant JE, Odlaug BL, Kim SW (2009) N-acetylcysteine, a glutamate modulator, in the treatment of trichotillomania: a double-blind, placebo-controlled study. Arch Gen Psychiatry 66:756-763
23. Guillin O, Abi-Dargham A, Laruelle M (2007) Neurobiology of dopamine in schizophrenia. Int Rev Neurobiol 78:1-39
24. Haroutunian V, Dracheva S, Davis KL (2003) Neurobiology of glutamatergic abnormalities in schizophrenia. Clin Neurosci Res 3:67-76
25. Harsing LG, Prauda I, Barkoczy J, Matyus P, Juranyi Z (2004) A 5-HT7 heteroreceptor-mediated inhibition of [3H]serotonin release in raphe nuclei slices of the rat: evidence for a serotonergic-glutamatergic interaction. Neurochem Res 29:1487-1497
26. Harvey BH, Stein DJ, Emsley RA (1999) The new generation antipsychotics: integrating the neuropathology and pharmacology of schizophrenia. S Afr Med J 89:661-672
27. 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 87:881-90
28. Heresco-Levy U, Ermilov M, Shimoni J, Shapira B, Silipo G, Javitt DC (2002) Placebo-controlled trial of D-cycloserine added to conventional neuroleptics, olanzapine, or risperidone in schizophrenia. Am J Psychiatry 159:480-482
29. Hovattaa J, Juhila J, Donner J (2010) Oxidative stress in anxiety and comorbid disorders. Neurosci Res 68:261-275
30. Howes OD, Kapur S (2009) The Dopamine Hypothesis of Schizophrenia: Version III - The Final Common Pathway. Schizophr Bull 35:549-562
31. Jaffe E, De Frias V, Ibarra C (1991) Changes in basal and stimulated release of endogenous serotonin from different nuclei of rats subjected to two models of depression. Neurosci Lett 62:157-160
32. Joyce JN, Shane A, Lexow N, Winokur A, Casanova MF, Kleinman JE (1993) Serotonin uptake sites and serotonin receptors are altered in the limbic system of schizophrenics. Neuropsychopharmacology 8:315-36
33. Kerksick C, Willoughby D (2005) The Antioxidant Role of Glutathione and N-Acetyl-Cysteine Supplements and Exercise-Induced Oxidative Stress. J Int Soc Sports Nutr 2:38-44
34. Krivoy A, Fischel T, Weizman A (2008) The possible involvement of metabotropic glutamate receptors in schizophrenia. Euro Neuropsychopharmacol 18:395-405
35. Krügel U, Kittner H, Illes P (2001) Mechanisms of adenosine 50-triphosphate-induced dopamine release in the rat nucleus accumbens in vivo. Synapse 39:222-232
36. Kuloglu M, Ustundag B, Atmaca M, Canatan H, Tezcan AE, Cinkilinc N (2002) Lipid peroxidation and antioxidant enzyme levels in patients with schizophrenia and bipolar disorder. Cell Biochem Func 20:171-175
37. Kunz M, Gama CS, Andreazza AC, Salvador M, Ceresér KM, Gomes FA, Belmonte-de-Abreu PS, Berk M, Kapczinski F (2008) Elevated serum superoxide dismutase and thiobarbituric acid reactive substances in different phases of bipolar disorder and in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 32:1677-1681
38. Lewis D, González-Burgos G (2008) Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacology 33:141-165
39. Lieberman JA (1993) Understanding the mechanism of action of atypical antipsychotic drugs: a review of compounds in use and development. Brit J Psychiatry 163:7-18
40. Lysaker PH, Salyers MP (2007) Anxiety symptoms in schizophrenia spectrum disorders: associations with social function, positive and negative symptoms, hope and trauma history. Acta Psychiatr Scand 116:290-298
41. Magalhaes PV, Dean O, Bush AI, Copolov DL, Malhi GS, Kohlmann K, Jeavons S, Schapkaitz I, Anderson-Hunt M, Berk M (2011) N-acetylcysteine for major depressive episodes in bipolar disorder. Rev Bras Psiquiatr 33:374-378
42. Matheson SL, Shepherd AM, Laurens KR, Carr VJ (2011) A systematic metareview grading the evidence for non-genetic risk factors and putative antecedents of schizophrenia. Schizophr Res 133:133-142
43. McNamee EN, Griffin EW, Ryan KM, Ryan KJ, Heffernan S, Harkin A, Connor TJ (2010) Noradrenaline acting at beta-adrenoceptors induces expression of IL-1beta and its negative regulators IL-1ra and IL-1RII, and drives an overall anti-inflammatory phenotype in rat cortex. Neuropharmacology 59:37-48
44. Meltzer HY, Li Z, Kaneda Y, Ichikawa J (2003) Serotonin receptors: their key role in drugs to treat schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 27:1159-1172
45. Meyer U, Feldon J (2009) Prenatal exposure to infection: a primary mechanism for abnormal dopaminergic development in schizophrenia. Psychopharmacol 206:587-60
46. Meyer-Lindenberg A, Miletich RS, Kohn PD, Esposito G, Carson RE, Quarantelli M, Weinberger DR, Berman KF (2002) Reduced prefrontal activity predicts exaggerated striatal dopaminergic function in schizophrenia. Nat Neurosci 5:267-71
47. Milusheva E, Sperlágh B, Shikova L, Baranyi M, Tretter L, Adám-Vizi V, Vizi ES (2003) Non-synaptic release of [3H]noradrenaline in response to oxidative stress combined with mitochondrial dysfunction in rat hippocampal slices. Neurosci 120:771-781
48. Miyamoto S, Duncan GE, Marx CE, Lieberman JA (2005) Treatments for schizophrenia: a critical review of pharmacology and mechanisms of action of antipsychotic drugs. Mol Psychiatry 10:79-104
49. 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
50. Möller M, Du Preez JL, Emsley R, Harvey BH (2012) Social isolation rearing in rats alters plasma tryptophan metabolism and is reversed by sub-chronic clozapine treatment. Neuropharmacology 62:2499-2506
51. Möller M, Du Preez JL, Viljoen FP, Berk M, Emsley R, Harvey BH (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 30:156-67
52. Mukherjee S, Mahadik SP, Scheffer R, Correntie E, Kelkar H (1996) Impaired antioxidant defence at the onset of psychosis. Schizophr Res 19:19-26
53. Musazzi L, Racagni G, Popoli M (2011) Stress, glucocorticoids and glutamate release: effects of antidepressant drugs. Neurochem Int 59:138-49
54. Ng F, Berk M, Dean O, Bush AI (2008) Oxidative stress in psychiatric disorders: evidence base and therapeutic implications. Int J Neuropsychopharmacol 11:851-876
55. Okuno A, Fukuwatari T, Shibata K (2011) High tryptophan diet reduces extracellular dopamine release via kynurenic acid production in rat striatum. J Neurochem 118:796-805
56. O'Sullivan JB, Ryan KM, Curtin NM, Harkin A, Connor TJ (2009) Noradrenaline reuptake inhibitors limit neuroinflammation in rat cortex following a systemic inflammatory challenge: implications for depression and neurodegeneration. Int J Neuropsychopharmacol 12:687-99
57. Pervanidou P (2008) Biology of post-traumatic stress disorder in childhood and adolescence. J Neuroendocrinol 20:632-638
58. Powell SB, Geyer MA, Preece MA, Pitcher LK, Reynolds GP, Swerdlow NR (2003) Dopamine depletion of the nucleus accumbens reverses isolation-induced deficits in prepulse inhibition in rats. Neurosci 119:233-40
59. Prabakaran S, Swatton J, Ryan MM, Huffaker SJ, Huang JT, Griffin JL et al (2004) Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9:684-697
60. Radonjić NV, Knezević ID, Vilimanovich U (2010) Decreased glutathione levels and altered antioxidant defense in an animal model of schizophrenia: long-term effects of perinatal phencyclidine administration. Neuropharmacology 58:739-45
61. Rilke O, Will K, Jähkel M, Oehler J (2001) Behavioral and neurochemical effects of anpirtoline and citalopram in isolated and group housed mice. Prog Neuro- Psychopharmacol Biol Psychiatry 25:1125-1144
62. Rollema H, Lu Y, Schmidt AW, Sprouse JS, Zorn SH (2000) 5-HT(1A) receptor activation contributes to ziprasidone-induced dopamine release in the rat prefrontal cortex. Biol Psychiatry 48:229-237
63. Schiavone S, Sorce S, Dubois-Dauphin M, Jaquet V, Colaianna M, Zotti M, Cuomo V, Trabace L, Krause KH (2009) Involvement of Nox2 in the development of behavioral and pathologic alterations in isolated rats. Biol Psychiatry 66:384-392
64. Schiavone S, Jaquet V, Sorce S, Dubois-Dauphin M, Hultqvist M, Bäckdahl L et al (2012) NADPH oxidase elevations in pyramidal neurons drive psychosocial stress-induced neuropathology. Transl Psychiatry 2:e111
65. Schwartz TL, Sachdeva S, Stahl SM (2012) Glutamate neurocircuitry: theoretical underpinnings in Schizophrenia. Front Pharmacol 3:195
66. Singh S, Greene RM, Pisano MM (2010) Arsenate-induced apoptosis in murine embryonic maxillary mesenchymal cells via mitochondrial-mediated oxidative injury. Birth Defects Res A Clin Mol Teratol 88:25-34
67. Smaga I, Pomierny B, Krzyżanowska W, Pomierny-Chamioło L, Miszkiel J, Niedzielska E, Ogórka A, Filip M (2012) N-acetylcysteine possesses antidepressant-like activity through reduction of oxidative stress: Behavioral and biochemical analyses in rats. Prog Neuro-Psychopharmacol Biol Psychiatry 39:280-287
68. Smythies J (1999) Redox mechanisms at the glutamate synapse and their significance: a review. Eur J Pharmacol 370:1-7
69. Sorce S, Schiavone S, Tucci P, Colaianna M, Jaquet V, Cuomo V et al (2010) The NADPH oxidase NOX2 controls glutamate release: a novel mechanism involved in psychosis-like ketamine responses. J Neurosci 30:11317-11325
70. Stahl SM (2007) Beyond the dopamine hypothesis to the NMDA glutamate receptor hypofunction hypothesis of schizophrenia. CNS Spectr 12:265-268
71. Sumiyoshi T, Stockmeier C, Overholser J, Dilley G, Meltzer H (1996) Serotonin-1A receptors are increased in postmortem prefrontal cortex in schizophrenia. Brain Res 708:209-214
72. Swanson LW (2004) Brain maps: structure of the rat brain. Elsevier Academic Press
73. Ting JT, Feng G (2008) Glutamatergic synaptic dysfunction and obsessive-compulsive disorder. Curr Chem Genomics 2:62-75
74. Toua C, Brand L, Möller M, Emsley RA, Harvey BH (2010) The effects of sub-chronic clozapine and haloperidol administration on isolation rearing induced changes in frontal cortical N-methyl-D-aspartate and D1 receptor binding in rats. Neurosci 165:492-499
75. Trabace L, Zotti M, Colaianna M, Mg M, Schiavone S, Tucci P, Harvey BH, Wegener G, Cuomo V (2012) Neurochemical differences in two rat strains exposed to social isolation rearing. Acta Neuropsychiatrica 24:286-295
76. Wang J, Shao L, Sun X, Young LT (2009) Increased oxidative stress in the striatum of subjects with bipolar disorder and schizophrenia. Biopolar Disord 11:523-529
77. Wu G, Fang Y, Yang S, Lupton JR, Turner ND (2004) Glutathione Metabolism and Its Implications for Health. J Nutr 134:489-492
78. Yamamoto K, Hornykiewicz O (2004) Proposal for a noradrenaline hypothesis of schizophrenia. Prog NeuroPsychopharmacol Biol Psychiatry 28:913-922
79. Zumárraga M, Dávila R, Basterreche N, Arrue A, Goienetxea B, Zamalloa MI, Erkoreka L, Bustamante S, Inchausti L, González-Torres MA, Guimón J (2010) Catechol O-methyltransferase and monoamine oxidase A genotypes, and plasma catecholamine metabolites in bipolar and schizophrenic patients. Neurochem Int 56:774-779