Activation of brain indoleamine 2,3-dioxygenase contributes to epilepsy-associated depressive-like behavior in rats with chronic temporal lobe epilepsy

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Xie, Wei ^a   Cai, Lun ^a,b   Yu, Yunhong ^c   Gao, Liang ^a   Xiao, Limin ^a   He, Qianchao ^b   Ren, Zhijun ^a   Liu, Yuanzheng ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF GUANGXI UNIVERSITY OF CHINESE MEDICINE   (China)

^c GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

Author keywords

1 methyltryptophan; Depression; Epilepsy; Forced swim test; Interleukin 1 ; Interleukin 6; Kynurenine; Minocycline; Serotonin; Taste preference test; Tryptophan

Indexed keywords

1 METHYLTRYPTOPHAN; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; KYNURENINE; MESSENGER RNA; MINOCYCLINE; N METHYLTRYPTOPHAN; PILOCARPINE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; ENZYME ACTIVATION; EPILEPTIC STATE; FORCED SWIM TEST; HIPPOCAMPUS; IL 1BETA GENE; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROTONIN BRAIN LEVEL; TASTE PREFERENCE; TEMPORAL LOBE EPILEPSY; TRYPTOPHAN BRAIN LEVEL;

ANIMALS; CHROMATOGRAPHY, LIQUID; CYTOKINES; DEPRESSION; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; FOOD PREFERENCES; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LITHIUM CHLORIDE; MALE; MASS SPECTROMETRY; MINOCYCLINE; RATS; RATS, WISTAR; STATISTICS, NONPARAMETRIC; TIME FACTORS; TRYPTOPHAN;

EID: 84897959130     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-41     Document Type: Article

References (40)

1. Mazarati AM, Pineda E, Shin D, Tio D, Taylor AN, Sankar R. Comorbidity between epilepsy and depression: role of hippocampal interleukin-1β. Neurobiol Dis 2010, 37:461-478. 10.1016/j.nbd.2009.11.001, 2818460, 19900553.
2. Minami M, Kuraishi Y, Satoh M. Effects of kainic acid on messenger RNA levels of IL-1 beta, IL-6, TNF alpha and LIF in the rat brain. Biochem Biophys Res Commun 1991, 176:593-598. 10.1016/S0006-291X(05)80225-6, 1709015.
3. Lehtimäki KA, Peltola J, Koskikallio E, Keränen T, Honkaniemi J. Expression of cytokines and cytokine receptors in the rat brain after kainic acid-induced seizures. Mol Brain Res 2003, 110:253-260. 10.1016/S0169-328X(02)00654-X, 12591161.
4. De Simoni MG, Perego C, Ravizza T, Moneta D, Conti M, Marchesi F, De Luigi A, Garattini S, Vezzani A. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur J Neurosci 2000, 12:2623-2633. 10.1046/j.1460-9568.2000.00140.x, 10947836.
5. Minami M, Kuraishi Y, Yamaguchi T, Nakai S, Hirai Y, Satoh M. Convulsants induce interleukin-1 beta messenger RNA in rat brain. Biochem Biophys Res Commun 1990, 171:832-837. 10.1016/0006-291X(90)91221-D, 1698365.
6. Omran A, Peng J, Zhang C, Xiang QL, Xue J, Gan N, Kong H, Yin F. Interleukin-1β and microRNA-146a in an immature rat model. Epilepsia 2012, 53:1215-1224. 10.1111/j.1528-1167.2012.03540.x, 22708826.
7. Schwarcz R, Bruno JP, Muchowski PJ, Wu HQ. Kynurenines in the mammalian brain: when physiology meets pathology. Nat rev Neurosci 2012, 13:465-477. 10.1038/nrn3257, 3681811, 22678511.
8. O'Connor JC, Lawson MA, André C, Moreau M, Lestage J, Castanon N, Kelley KW, Dantzer R. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatry 2009, 14:511-522. 10.1038/sj.mp.4002148, 2683474, 18195714.
9. Kim H, Chen L, Lim G, Sung B, Wang S, McCabe MF, Rusanescu G, Yang L, Tian Y, Mao J. Brain indoleamine 2,3-dioxygenase contributes to the comorbidity of pain and depression. J Clin Invest 2012, 122:2940-2954. 10.1172/JCI61884, 3408737, 22751107.
10. Sublette ME, Postolache TT. Neuroinflammation and depression: the role of indoleamine 2,3-dioxygenase (IDO) as a molecular pathway. Psychosom Med 2012, 74:668-672. 10.1097/PSY.0b013e318268de9f, 22923699.
11. Myint AM. Kynurenines: from the perspective of major psychiatric disorders. FEBS J 2012, 279:1375-1385. 10.1111/j.1742-4658.2012.08551.x, 22404766.
12. Mazarati AM, Siddarth P, Baldwin RA, Shin D, Caplan R, Sankar R. Depression after status epilepticus: behavioural and biochemical deficits and effects of fluoxetine. Brain 2008, 131:2071-2083. 10.1093/brain/awn117, 2587254,2587254, 18559371.
13. Mazarati AM, Shin D, Kwon YS, Bragin A, Pineda E, Tio D, Taylor AN, Sankar R. Elevated plasma corticosterone level and depressive behavior in experimental temporal lobe epilepsy. Neurobiol Dis 2009, 34:457-461. 10.1016/j.nbd.2009.02.018, 2683188, 19285131.
14. Racine RJ. Modification of seizure activity by electrical stimulation: II. Motor seizures. Electroencephalogr Clin Neurophysiol 1972, 32:281-294. 10.1016/0013-4694(72)90177-0, 4110397.
15. Pucilowski O, Overstreet DH. Effect of chronic antidepressant treatment on responses to apomorphine in selectively bred rat strains. Brain Res Bull 1993, 32:471-475. 10.1016/0361-9230(93)90293-K, 8221139.
16. Pucilowski O, Overstreet DH, Rezvani AH, Janowsky DS. Chronic mild stress-induced anhedonia: greater effect in a genetic rat model of depression. Physiol Behav 1993, 54:1215-1220. 10.1016/0031-9384(93)90351-F, 8295967.
17. Overstreet DH, Pucilowski O, Rezvani AH, Janowsky DS. Administration of antidepressants, diazepam and psychomotor stimulants further confirms the utility of Flinders Sensitive Line rats as an animal model of depression. Psychopharmacology (Berl) 1995, 121:27-37. 10.1007/BF02245589, 8539339.
18. Zhao F, Cai TJ, Liu MC, Zheng G, Luo W, Chen J. Manganese induces dopaminergic neurodegeneration via microglial activation in a rat model of manganism. Toxicol Sci 2009, 107:156-164.
19. Möller M, Du Preez JL, Harvey BH. Development and validation of a single analytical method for the determination of tryptophan, and its kynurenine metabolites in rat plasma. J Chromatogr B Analyt Technol Biomed Life Sci 2012, 898:121-129.
20. Gonzalez RR, Fernandez RF, Vidal JL, Frenich AG, Perez ML. Development and validation of an ultra-high performance liquid chromatography-tandem mass-spectrometry (UHPLC-MS/MS) method for the simultaneous determination of neurotransmitters in rat brain samples. J Neurosci Methods 2011, 198:187-194. 10.1016/j.jneumeth.2011.03.023, 21459108.
21. Fiest KM, Dykeman J, Patten SB, Wiebe S, Kaplan GG, Maxwell CG, Bulloch AG, Jette N. Depression in epilepsy: a systematic review and meta-analysis. Neurology 2013, 80:590-599. 10.1212/WNL.0b013e31827b1ae0, 3589287, 23175727.
22. Pineda E, Shin D, Sankar R, Mazarati AM. Comorbidity between epilepsy and depression: experimental evidence for the involvement of serotonergic, glucocorticoid, and neuroinflammatory mechanisms. Epilepsia 2010, 51(Suppl 3):110-114. 2909020, 20618414.
23. Kanner AM, Schachter SC, Barry JJ, Hersdorffer DC, Mula M, Trimble M, Hermann B, Ettinger AE, Dunn D, Caplan R, Ryvlin P, Gilliam F. Depression and epilepsy: epidemiologic and neurobiologic perspectives that may explain their high comorbid occurrence. Epilepsy Behav 2012, 24:156-168. 10.1016/j.yebeh.2012.01.007, 22632406.
24. Järvelä JT, Lopez-Picon FR, Plysjuk A, Ruohonen S, Holopainen IE. Temporal profiles of age-dependent changes in cytokine mRNA expression and glial cell activation after status epilepticus in postnatal rat hippocampus. J Neuroinflammation 2011, 8:29. 10.1186/1742-2094-8-29, 3084156, 21477276.
25. Pernot F, Heinrich C, Barbier L, Peinnequin A, Carpentier P, Dhote F, Baille V, Beaup C, Depaulis A, Dorandeu F. Inflammatory changes during epileptogenesis and spontaneous seizures in a mouse model of mesiotemporal lobe epilepsy. Epilepsia 2011, 52:2315-2325. 10.1111/j.1528-1167.2011.03273.x, 21955106.
26. Ashhab MU, Omran A, Kong H, Gan N, He F, Peng J, Yin F. Expressions of tumor necrosis factor alpha and microRNA-155 in immature rat model of status epilepticus and children with mesial temporal lobe epilepsy. J Mol Neurosci 2013, 51:950-958. 10.1007/s12031-013-0013-9, 23636891.
27. Teocchi MA, Ferreira A, da Luz de Oliveira EP, Tedeschi H, D'Souza-Li L. Hippocampal gene expression dysregulation of Klotho, nuclear factor kappa B and tumor necrosis factor in temporal lobe epilepsy patients. J Neuroinflammation 2013, 10:53. 10.1186/1742-2094-10-53, 3651326, 23634661.
28. Valente KD, Busatto FG. Depression and temporal lobe epilepsy represent an epiphenomenon sharing similar neural networks: clinical and brain structural evidences. Arq Neuropsiquiatr 2013, 71:183-190. 10.1590/S0004-282X2013000300011, 23563720.
29. Martinez A, Finegersh A, Cannon DM, Dustin I, Nugent A, Herscovitch P, Theodore WH. The 5-HT 1A receptor and 5-HT transporter in temporal lobe epilepsy. Neurology 2013, 80:1465-1471. 10.1212/WNL.0b013e31828cf809, 3662359, 23516322.
30. Maes M, Leonard BE, Myint AM, Kubera M, Verkerk R. The new '5-HT' hypothesis of depression: cell-mediated immune activation induces indoleamine 2,3-dioxygenase, which leads to lower plasma tryptophan and an increased synthesis of detrimental tryptophan catabolites (TRYCATs), both of which contribute to the onset of depression. Prog Neuro-Psychopharmacol Biol Psychiatry 2011, 35:702-721. 10.1016/j.pnpbp.2010.12.017, 21185346.
31. Christmas DM, Potokar JP, Davies SJ. A biological pathway linking inflammation and depression: activation of indoleamine 2,3-dioxygenase. Neuropsychiatr Dis Treat 2011, 7:431-439. 3140295, 21792309.
32. Riazi K, Galic MA, Kuzmiski BJ, Ho W, Sharkey KA, Pittman QJ. Microglial activation and TNF-α production mediate altered CNS excitability following peripheral inflammation. Proc Natl Acad Sci U S A 2008, 105:17151-17156. 10.1073/pnas.0806682105, 2579393, 18955701.
33. Andrzejczak D. Epilepsy and pro-inflammatory cytokines. Immunomodulating properties of antiepileptic drugs. Neurol Neurochir Pol 2011, 45:275-285.
34. Vezzani A. The role of inflammation in epilepsy. Nat Rev Neurol 2011, 7:31-40. 10.1038/nrneurol.2010.178, 3378051, 21135885.
35. Leonard B, Maes M. 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 2012, 36:764-785. 10.1016/j.neubiorev.2011.12.005, 22197082.
36. Abraham J, Fox PD, Condello C, Bartolini A, Koh S. Minocycline attenuates microglia activation and blocks the long-term epileptogenic effects of early-life seizures. Neurobiol Dis 2012, 46:425-430. 10.1016/j.nbd.2012.02.006, 3323726, 22366182.
37. Pae CU, Marks DM, Han C, Patkar AA. Does minocycline have antidepressant effect?. Biomed Pharmacother 2008, 62:308-311. 10.1016/j.biopha.2007.12.005, 18267354.
38. Soczynska JK, Mansur RB, Brietzke E, Swardfager W, Kennedy SH, Woldeyohannes HO, Powell AM. Novel therapeutic targets in depression: minocycline as a candidate treatment. Behav Brain Res 2012, 235:302-317. 10.1016/j.bbr.2012.07.026, 22963995.
39. Russi MA, Vandresen-Filho S, Rieger DK, Costa AP, Lopes MW, Cunha RM, Teixeira EH, Nascimento KS, Cavada BS, Tasca CI, Leal RB. ConBr, a lectin from Canavalia brasiliensis seeds, protects against quinolinic acid-induced seizures in mice. Neurochem Res 2012, 37:288-297. 10.1007/s11064-011-0608-x, 21948344.
40. Ganzella M, Faraco RB, Almeida RF, Fernandes VF, Souza DO. Intracerebroventricular administration of inosine is anticonvulsant against quinolinic acid-induced seizures in mice: an effect independent of benzodiazepine and adenosine receptors. Pharmacol Biochem Behav 2011, 100:271-274. 10.1016/j.pbb.2011.09.001, 21945561.