Lithium modulates the production of peripheral and cerebral cytokines in an animal model of mania induced by dextroamphetamine

Bipolar Disorders

Volumn 17, Issue 5, 2015, Pages 507-517

  Valvassori, Samira S ^a   Tonin, Paula T ^a   Varela, Roger B ^a   Carvalho, André F ^b   Mariot, Edemilson ^a   Amboni, Rafaela T ^a   Bianchini, Guilherme ^a   Andersen, Monica L ^c   Quevedo, João ^a,d  

^a UNIVERSIDADE DO EXTREMO SUL CATARINENSE   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Amphetamine; Bipolar disorder; Cytokines; Lithium; Mania

Indexed keywords

DEXAMPHETAMINE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; LITHIUM; TUMOR NECROSIS FACTOR ALPHA; CENTRAL STIMULANT AGENT; CYTOKINE; IL1B PROTEIN, RAT; LITHIUM DERIVATIVE; TRANQUILIZER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN LEVEL; CEREBROSPINAL FLUID; CONTROLLED STUDY; CORPUS STRIATUM; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; FRONTAL CORTEX; HIPPOCAMPUS; HYPERACTIVITY; MALE; MANIA; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; REGULATORY MECHANISM; ANIMAL; ANIMAL BEHAVIOR; BIPOLAR DISORDER; BRAIN; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; FRONTAL LOBE; HYPERKINESIS; IMMUNOLOGY; MOTOR ACTIVITY; NEOSTRIATUM; WISTAR RAT;

ANIMALS; ANTIMANIC AGENTS; BEHAVIOR, ANIMAL; BIPOLAR DISORDER; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; CYTOKINES; DEXTROAMPHETAMINE; DISEASE MODELS, ANIMAL; FRONTAL LOBE; HIPPOCAMPUS; HYPERKINESIS; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-4; INTERLEUKIN-6; LITHIUM COMPOUNDS; MALE; MOTOR ACTIVITY; NEOSTRIATUM; RATS; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84938982434     PISSN: 13985647     EISSN: 13995618     Source Type: Journal    
DOI: 10.1111/bdi.12299     Document Type: Article

References (92)

1. Gardner A, Boles RG. Beyond the serotonin hypothesis: mitochondria, inflammation and neurodegeneration in major depression and affective spectrum disorders. Prog Neuropsychopharmacol Biol Psychiatry 2011; 35: 730-743.
2. Grande I, Magalhães PV, Kunz M, Vieta E, Kapczinski F. Mediators of allostasis and systemic toxicity in bipolar disorder. Physiol Behav 2012; 106: 46-50.
3. Bauer MS, Altshuler L, Evans DR, Beresford T, Williford WO, Hauger R. Prevalence and distinct correlates of anxiety, substance, and combined comorbidity in a multi-site public sector sample with bipolar disorder. J Affect Disord 2005; 85: 301-315.
4. Leboyer M, Soreca I, Scott J et al. Can bipolar disorder be viewed as a multi-system inflammatory disease? J Affect Disord 2012; 141: 1-10.
5. Drexhage RC, Knijff EM, Padmos RC et al. The mononuclear phagocyte system and its cytokine inflammatory networks in schizophrenia and bipolar disorder. Expert Rev Neurother 2010; 10: 59-76.
6. Haroon E, Raison CL, Miller AH. Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 2012; 37: 137-162.
7. Brietzke E, Stertz L, Fernandes BS et al. Comparison of cytokine levels in depressed, manic and euthymic patients with bipolar disorder. J Affect Disord 2009; 116: 214-217.
8. Goldstein BI, Kemp DE, Soczynska JK, McIntyre RS. Inflammation and the phenomenology, pathophysiology, comorbidity, and treatment of bipolar disorder: a systematic review of the literature. J Clin Psychiatry 2009; 70: 1078-1090.
9. Munkholm K, Vinberg M, Kessing LV. Cytokines in bipolar disorder: a systematic review and meta-analysis. J Affect Disord 2013; 144: 16-27.
10. Yatham LN, Kennedy SH, Parikh SV et al. Canadian Network for Mood and Anxiety Treatments (CANMAT) and International Society for Bipolar Disorders (ISBD) collaborative update of CANMAT guidelines for the management of patients with bipolar disorder: update 2013. Bipolar Disord 2013; 15: 1-44.
11. Nassar A, Azab AN. Effects of lithium on inflammation. ACS Chem Neurosci 2014; 5: 451-458.
12. Li H, Li Q, Du X et al. Lithium-mediated long-term neuroprotection in neonatal rat hypoxia-ischemia is associated with anti-inflammatory effects and enhanced proliferation and survival of neural stem/progenitor cells. J Cereb Blood Flow Metab 2011; 31: 2106-2115.
13. Nahman S, Belmaker RH, Azab AN. Effects of lithium on lipopolysaccharide-induced inflammation in rat primary glia cells. Innate Immun 2012; 18: 447-458.
14. Manji HK, Chen G. PKC, MAP quinases e da família Bcl-2 de proteínas como alvos a longo prazo para estabilizadores de humor. Mol Psychiatry 2002; 7: 46-56.
15. Einat H, Yuan P, Gould TD et al. The role of the extracellular signal-regulated kinase signaling pathway in mood modulation. J Neurosci 2003; 23: 7311-7316.
16. Machado-Vieira R, Kapczinski F, Soares JC. Perspectives for the development of animal models of bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2004; 28: 209-224.
17. Valvassori SS, Budni J, Varela RB, Quevedo J. Contributions of animal models to the study of mood disorders. Rev Bras Psiquiatr 2013; 35: 121-131.
18. Kara NZ, Einat H. Rodent models for mania: practical approaches. Cell Tissue Res 2013; 354: 191-201.
19. Strakowski SM, Sax KW. Progressive behavioral response to repeated d-amphetamine challenge: further evidence for sensitization in humans. Biol Psychiatry 1998; 44: 1171-1177.
20. Anand A, Verhoeff P, Seneca N et al. Brain SPECT imaging of amphetamine-induced dopamine release in euthymic bipolar disorder patients. Am J Psychiatry 2000; 157: 1108-1114.
21. Joyce PR, Fergusson DM, Woollard G, Abbott RM, Horwood LJ, Upton J. Urinary catecholamines and plasma hormones predict mood state in rapid cycling bipolar affective disorder. J Affect Disord 1995; 33: 233-243.
22. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 5th edn. Arlington: American Psychiatric Publishing, 2013.
23. Post RM, Weiss SR. Sensitization, kindling, and anticonvulsants in mania. J Clin Psychiatry 1989; 50 (Suppl.): 23-30.
24. Kessing LV, Andersen PK, Mortensen PB, Bolwig TG. Recurrence in affective disorder. I. Case register study. Br J Psychiatry 1998; 172: 23-28.
25. Kessing LV, Hansen MG, Andersen PK, Angst J. The predictive effect of episodes on the risk of recurrence in depressive and bipolar disorders-a life-long perspective. Acta Psychiatr Scand 2004; 109: 339-344.
26. Post RM. Mechanisms of illness progression in the recurrent affective disorders. Neurotox Res 2010; 18: 256-271.
27. Post RM. Kindling and sensitization as models for affective episode recurrence, cyclicity, and tolerance phenomena. Neurosci Biobehav Rev 2007; 31: 858-873.
28. Strakowski SM, Delbello MP, Adler CM. The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 2005; 10: 105-116.
29. Bearden CE, Glahn DC, Monkul ES et al. Sources of declarative memory impairment in bipolar disorder: mnemonic processes and clinical features. J Psychiatr Res 2006; 40: 47-58.
30. Bearden CE, Glahn DC, Monkul ES et al. Patterns of memory impairment in bipolar disorder and unipolar major depression. J Psychiatr Res 2006; 142: 139-150.
31. Nugent AC, Milham MP, Bain EE et al. Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry. NeuroImage 2005; 30: 485-497.
32. Frey BN, Valvassori SS, Réus GZ et al. Effects of lithium and valproate on amphetamine-induced oxidative stress generation in an animal model of mania. J Psychiatry Neurosci 2006; 31: 326-332.
33. Frey BN, Andreazza AC, Ceresér KM et al. Effects of mood stabilizers on hippocampus BDNF levels in an animal model of mania. Life Sci 2006; 13: 281-286.
34. Frey BN, Martins MR, Petronilho FC, Dal-Pizzol F, Quevedo J, Kapczinski F. Increased oxidative stress after repeated amphetamine exposure: possible relevance as a model of mania. Bipolar Disord 2006; 8: 275-280.
35. Valvassori SS, Rezin GT, Ferreira CL et al. Effects of mood stabilizers on mitochondrial respiratory chain activity in brain of rats treated with d-amphetamine. J Psychiatr Res 2010; 44: 903-909.
36. Schaeffer JC, Cho AK, Fischer JF. Inhibition of synaptosomal accumulation of l-norepinephrine II: N-aryloxyalkylphentermines, quaternary d-amphetamines, and 3-aryloxypropylamines. J Pharm Sci 1976; 65: 122-126.
37. Hoffman BB, Lefkowitz RJ. Catecholamines, sympathomimetic drugs, and adrenergic receptor antagonists. In: Hardman JG, Limbird LE, Molinoff PB, Ruddon RW, Gilman AG eds. Goodman & Gilman's the Pharmacological Basis of Therapeutics, 9th edn. New York, NY: McGraw-Hill, 1996: 199-248.
38. Feier G, Valvassori SS, Lopes-Borges J et al. Behavioral changes and brain energy metabolism dysfunction in rats treated with methamphetamine or dextroamphetamine. Neurosci Lett 2012; 530: 75-79.
39. Feier G, Valvassori SS, Varela RB et al. Lithium and valproate modulate energy metabolism in an animal model of mania induced by methamphetamine. Pharmacol Biochem Behav 2013; 103: 89-96.
40. Pinsonneault JK, Han DD, Burdick KE et al. Dopamine transporter gene variant affecting expression in human brain is associated with bipolar disorder. Neuropsychopharmacology 2011; 36: 1644-1655.
41. Holder MK, Hadjimarkou MM, Zup SL et al. Methamphetamine facilitates female sexual behavior and enhances neuronal activation in the medial amygdala and ventromedial nucleus of the hypothalamus. Psychoneuroendocrinology 2010; 35: 197-208.
42. Frohmader KS, Bateman KL, Lehman MN, Coolen LM. Effects of methamphetamine on sexual performance and compulsive sex behavior in male rats. Psychopharmacology 2010; 212: 93-104.
43. Frohmader KS, Lehman MN, Laviolette SR, Coolen LM. Concurrent exposure to methamphetamine and sexual behavior enhances subsequent drug reward and causes compulsive sexual behavior in male rats. J Neurosci 2011; 31: 16473-16482.
44. Steckert AV, Valvassori SS, Mina F et al. Protein kinase C and oxidative stress in an animal model of mania. Curr Neurovasc Res 2012; 9: 47-57.
45. Beaulieu JM, Sotnikova TD, Yao WD et al. Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc Natl Acad Sci USA 2004; 101: 5099-5104.
46. Kapczinski F, Dias VV, Kauer-Sant'Anna M et al. The potential use of biomarkers as an adjunctive tool for staging bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2009; 33: 1366-1371.
47. Berk M, Kapczinski F, Andreazza AC et al. Pathways underlying neuroprogression in bipolar disorder: focus on inflammation, oxidative stress and neurotrophic factors. Neurosci Biobehav Rev 2011; 35: 804-817.
48. Kauer-Sant'Anna M, Kapczinski F, Andreazza AC et al. Brain-derived neurotrophic factor and inflammatory markers in patients with early- vs. late-stage bipolar disorder. Int J Neuropsychopharmacol 2009; 12: 447-458.
49. Modabbernia A, Taslimi S, Brietzke E, Ashrafi M. Cytokine alterations in bipolar disorder: a meta-analysis of 30 studies. Biol Psychiatry 2013; 74: 15-25.
50. Yamamoto BK, Moszczynska A, Gudelsky GA. Amphetamine toxicities: classical and emerging mechanisms. Ann N Y Acad Sci 2010; 1187: 101-121.
51. Thomas DM, Kuhn DM. Cyclooxygenase-2 is an obligatory factor in methamphetamine-induced neurotoxicity. J Pharmacol Exp Ther 2005; 313: 870-876.
52. Andreazza AC, Kauer-Sant'Anna M, Frey BN et al. Effects of mood stabilizers on DNA damage in an animal model of mania. J Psychiatry Neurosci 2008; 33: 516-524.
53. Cechinel-Recco K, Valvassori SS, Varela RB et al. Lithium and tamoxifen modulate cellular plasticity cascades in animal model of mania. J Psychopharmacol 2012; 26: 1594-1604.
54. Northrop NA, Yamamoto BK. Persistent neuroinflammatory effects of serial exposure to stress and methamphetamine on the blood-brain barrier. J Neuroimmune Pharmacol 2012; 7: 951-968.
55. Mura A, Jackson D, Manley MS, Young SJ, Groves PM. Aromatic L-amino acid decarboxylase immunoreactive cells in the rat striatum: a possible site for the conversion of exogenous L-DOPA to dopamine. Brain Res 1995; 704: 51-60.
56. Ikemoto K, Kitahama K, Jouvet A et al. Demonstration of L-dopa decarboxylating neurons specific to human striatum. Neurosci Lett 1997; 232: 111-114.
57. Porritt MJ, Batchelor PE, Hughes AJ, Kalnins R, Donnan GA, Howells DW. New dopaminergic neurons in Parkinson's disease striatum. Lancet 2000; 356: 44-45.
58. Gudelsky GA, Yamamoto BK. Actions of 3, 4-methylenedioxymethamphetamine (MDMA) on cerebral dopaminergic, serotonergic and cholinergic neurons. Pharmacol Biochem Behav 2008; 90: 198-207.
59. Scatton B, Simon H, Le Moal M, Bischoff S. Origin of dopaminergic innervation of the rat hippocampal formation. Neurosci Lett 1980; 18: 125-131.
60. Hiramatasu MT, Cho K. Enantiomeric differences in the effects of 3, 4-methylenedioxymethamphetamine on extracellular monoamines and metabolites in the striatum of freely-moving rats: an in vivo microdialysis study. Neuropharmacology 1990; 29: 269-275.
61. Bonaccorso S, Meltzer HY, Li Z, Dai J, Alboszta AR, Ichikawa J. SR46349-B, a 5-HT(2A/2C) receptor antagonist, potentiates haloperidol-induced dopamine release in rat medial prefrontal cortex and nucleus accumbens. Neuropsychopharmacology 2002; 27: 430-441.
62. Tonin PT, Valvassori SS, Lopes-Borges J et al. Effects of ouabain on cytokine/chemokine levels in an animal model of mania. J Neuroimmunol 2014; 276: 236-239.
63. Abbott NJ. Inflammatory mediators and modulation of bloodbrain barrier permeability. Cell Mol Neurobiol 2000; 20: 131-147.
64. Ramirez SH, Potula R, Fan S et al. Methamphetamine disrupts blood-brain barrier function by induction of oxidative stress in brain endothelial cells. J Cereb Blood Flow Metab 2009; 29: 1933-1945.
65. Kita T, Shimada K, Mastunari Y, Wagner GC, Kubo K, Nakashima T. Methamphetamine-induced striatal dopamine neurotoxicity and cyclooxygenase-2 protein expression in BALB/c mice. Neuropharmacology 2000; 39: 399-406.
66. Remlinger-Molenda A, Wójciak P, Michalak M, Rybakowski J. Activity of selected cytokines in bipolar patients during manic and depressive episodes. Psychiatr Pol 2012; 46: 599-611.
67. Rapaport MH, Guylai L, Whybrow P. Immune parameters in rapid cycling bipolar patients before and after lithium treatment. J Psychiatr Res 1999; 33: 335-340.
68. Nardacci R, Falciatori I, Moreno S, Stefanini S. Immunohistochemical localization of peroxisomal enzymes during rat embryonic development. J Histochem Cytochem 2004; 52: 423-436.
69. Ghersi-Egea JF, Strazielle N, Murat A, Jouvet A, Buenerd A, Belin MF. Brain protection at the blood-cerebrospinal fluid interface involves a glutathione-dependent metabolic barrier mechanism. J Cereb Blood Flow Metab 2006; 26: 1165-1175.
70. Coisne C, Engelhardt B. Tight junctions in brain barriers during central nervous system inflammation. Antioxid Redox Signal 2011; 15: 1285-1303.
71. Wang HM, Zhang T, Li Q, Huang JK, Chen RF, Sun XJ. Inhibition of glycogen synthase kinase-3β by lithium chloride suppresses 6-hydroxydopamine-induced inflammatory response in primary cultured astrocytes. Neurochem Int 2013; 63: 345-353.
72. Park HJ, Kim HJ, Bae GS et al. Selective GSK-3beta inhibitors attenuate the cisplatin-induced cytotoxicity of auditory cells. Hear Res 2009; 257: 53-62.
73. Tan WF, Cao XZ, Wang JK, Lv HW, Wu BY, Ma H. Protective effects of lithium treatment for spatial memory deficits induced by tau hyperphosphorylation in splenectomized rats. Clin Exp Pharmacol Physiol 2010; 37: 1010-1015.
74. Tay TF, Maheran M, Too SL, Hasidah MS, Ismail G, Embi N. Glycogen synthase kinase-3β inhibition improved survivability of mice infected with burkholderia pseudomallei. Trop Biomed 2012; 29: 551-567.
75. Green HF, Nolan YM. GSK-3 mediates the release of IL-1β, TNF-α and IL-10 from cortical glia. Neurochem Int 2012; 61: 666-671.
76. Kwon YJ, Yoon CH, Lee SW, Park YB, Lee SK, Park MC. Inhibition of glycogen synthase kinase-3β suppresses inflammatory responses in rheumatoid arthritis fibroblast-like synoviocytes and collagen-induced arthritis. Joint Bone Spine 2013; 81: 240-246.
77. Himmerich H, Bartsch S, Hamer H et al. Impact of mood stabilizers and antiepileptic drugs on cytokine production in-vitro. J Psychiatr Res 2013; 47: 1751-1759.
78. Victoratos P, Yiangou M, Avramidis N, Hadjipetrou L. Regulation of cytokine gene expression by adjuvants in vivo. Clin Exp Immunol 1997; 109: 569-578.
79. Kucharz EJ, Sierakowski S, Staite ND, Goodwin JS. Mechanism of lithium-induced augmentation of T-cell proliferation. Int J Immunopharmacol 1998; 10: 253-259.
80. Sztein MB, Simon GL, Parenti DM et al. In vitro effects of thymosin and lithium on lymphoproliferative responses of normal donors and HIV seropositive male homosexuals with AIDS-related complex. Clin Immunol Immunopathol 1987; 44: 51-62.
81. Yuskaitis CJ, Jope RS. Glycogen synthase kinase-3 regulates microglial migration, inflammation, and inflammation-induced neurotoxicity. Cell Signal 2009; 21: 264-273.
82. Arena A, Capozza AB, Orlando ME et al. In vitro effects of lithium chloride on TNF alpha and IL-6 production by monocytes from breast cancer patients. J Chemother 1997; 9: 219-226.
83. Guloksuz S, Cetin EA, Cetin T, Deniz G, Oral ET, Nutt DJ. Cytokine levels in euthymic bipolar patients. J Affect Disord 2010; 126: 458-462.
84. Al-Azemi M, Omu FE, Kehinde EO, Anim JT, Oriowo MA, Omu AE. Lithium protects against toxic effects of cadmium in the rat testes. J Assist Reprod Genet 2010; 27: 469-476.
85. Rapaport MH, Manji HK. The effects of lithium on ex vivo cytokine production. Biol Psychiatry 2001; 50: 217-224.
86. Hashioka S, Klegeris A, Monji A et al. Antidepressants inhibit interferongamma- induced microglial production of IL-6 and nitric oxide. Exp Neurol 2007; 206: 33-42.
87. Merendino RA, Mancuso G, Tomasello F et al. Effects of lithium carbonate on cytokine production in patients affected by breast cancer. J Biol Regul Homeost Agents 1994; 8: 88-91.
88. Maes M, Song C, Lin AH et al. In vitro immunoregulatory effects of lithium in healthy volunteers. Psychopharmacology (Berlin) 1999; 143: 401-407.
89. Liu KJ, Lee YL, Yang YY et al. Modulation of the development of human monocyte-derived dendritic cells by lithium chloride. J Cell Physiol 2011; 226: 424-433.
90. Matsebatlela T, Gallicchio V, Becker R. Lithium modulates cancer cell growth, apoptosis, gene expression and cytokine production in HL-60 promyelocytic leukaemia cells and their drugresistant sub-clones. Biol Trace Elem Res 2012; 149: 323-330.
91. Knijff EM, Breunis MN, Kupka RW et al. An imbalance in the production of IL-1beta and IL-6 by monocytes of bipolar patients: restoration by lithium treatment. Bipolar Disord 2007; 9: 743-753.
92. Carli M, Morissette M, Hébert C, Di Paolo T, Reader TA. Effects of a chronic lithium treatment on central dopamine neurotransporters. Biochem Pharmacol 1997; 54: 391-397.