Intracerebroventricular administration of lipopolysaccharide induces indoleamine-2,3-dioxygenase-dependent depression-like behaviors

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Lawson, Marcus A ^a   Parrott, Jennifer M ^b,c   McCusker, Robert H ^a   Dantzer, Robert ^d   Kelley, Keith W ^a   O'Connor, Jason C ^b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLTRYPTOPHAN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; KYNURENINE; LIPOPOLYSACCHARIDE; MESSENGER RNA; SUCROSE; TRYPTOPHAN DERIVATIVE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 1-METHYLTRYPTOPHAN; ANTIDEPRESSANT AGENT; IDO1 PROTEIN, MOUSE; TRYPTOPHAN;

AMINO ACID BRAIN LEVEL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE; GENE DELETION; IDO1 GENE; IMMOBILITY; MALE; MOUSE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; BLOOD; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; FOOD PREFERENCE; GENETICS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TIME; UPREGULATION;

ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; DEPRESSION; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FOOD PREFERENCES; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INJECTIONS, INTRAVENTRICULAR; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; SUCROSE; TIME FACTORS; TRYPTOPHAN; UP-REGULATION;

EID: 84880183932     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-87     Document Type: Article

References (38)

1. Miller AH, Maletic V, Raison CL. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 2009, 65(9):732-741. 10.1016/j.biopsych.2008.11.029, 2680424, 19150053.
2. Maes M, Bosmans E, De Jongh R, Kenis G, Vandoolaeghe E, Neels H. Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment resistant depression. Cytokine 1997, 9(11):853-858. 10.1006/cyto.1997.0238, 9367546.
3. Howren MB, Lamkin DM, Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom Med 2009, 71(2):171-186. 10.1097/PSY.0b013e3181907c1b, 19188531.
4. Reichenberg A, Yirmiya R, Schuld A, Kraus T, Haack M, Morag A, Pollmacher T. Cytokine-associated emotional and cognitive disturbances in humans. Arch Gen Psychiatry 2001, 58(5):445-452. 10.1001/archpsyc.58.5.445, 11343523.
5. Krabbe KS, Reichenberg A, Yirmiya R, Smed A, Pedersen BK, Bruunsgaard H. Low-dose endotoxemia and human neuropsychological functions. Brain Behav Immun 2005, 19(5):453-460. 10.1016/j.bbi.2005.04.010, 15963684.
6. Yirmiya R. Endotoxin produces a depressive-like episode in rats. Brain Res 1996, 711(1-2):163-174.
7. O'Connor JC, Lawson MA, Andre 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(5):511-522. 10.1038/sj.mp.4002148, 2683474, 18195714.
8. Feinstein A. Multiple sclerosis and depression. Mult Scler 2011, 17(11):1276-1281. 10.1177/1352458511417835, 22058085.
9. Rosenblatt A. Neuropsychiatry of Huntington's disease. Dialogues Clin Neurosci 2007, 9(2):191-197. 3181855, 17726917.
10. Aarsland D, Pahlhagen S, Ballard CG, Ehrt U, Svenningsson P. Depression in Parkinson disease-epidemiology, mechanisms and management. Nat Rev Neurol 2012, 8(1):35-47.
11. Aznar S, Knudsen GM. Depression and Alzheimer's disease: is stress the initiating factor in a common neuropathological cascade?. J Alzheimers Dis 2011, 23(2):177-193.
12. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008, 9(1):46-56. 10.1038/nrn2297, 2919277, 18073775.
13. Cunningham AJ, Murray CA, O'Neill LA, Lynch MA, O'Connor JJ. Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro. Neurosci Lett 1996, 203(1):17-20. 10.1016/0304-3940(95)12252-4, 8742036.
14. O'Connor JJ, Coogan AN. Actions of the pro-inflammatory cytokine IL-1 beta on central synaptic transmission. Exp Physiol 1999, 84(4):601-614. 10.1017/S0958067099018928, 10481219.
15. Cumiskey D, Butler MP, Moynagh PN, O'Connor J. Evidence for a role for the group I metabotropic glutamate receptor in the inhibitory effect of tumor necrosis factor-alpha on long-term potentiation. Brain Res 2007, 1136(1):13-19.
16. Dantzer R, O'Connor JC, Lawson MA, Kelley KW. Inflammation-associated depression: from serotonin to kynurenine. Psychoneuroendocrinology 2011, 36(3):426-436. 10.1016/j.psyneuen.2010.09.012, 3053088, 21041030.
17. Christmas DM, Potokar J, Davies SJ. A biological pathway linking inflammation and depression: activation of indoleamine 2,3-dioxygenase. Neuropsychiatr Dis Treat 2011, 7:431-439. 3140295, 21792309.
18. Myint AM. Kynurenines: from the perspective of major psychiatric disorders. FEBS J 2012, 279(8):1375-1385. 10.1111/j.1742-4658.2012.08551.x, 22404766.
19. Schwarcz R, Bruno JP, Muchowski PJ, Wu HQ. Kynurenines in the mammalian brain: when physiology meets pathology. Nat Rev Neurosci 2012, 13(7):465-477. 10.1038/nrn3257, 3681811, 22678511.
20. O'Connor JC, Andre C, Wang Y, Lawson MA, Szegedi SS, Lestage J, Castanon N, Kelley KW, Dantzer R. Interferon-gamma and tumor necrosis factor-alpha mediate the upregulation of indoleamine 2,3-dioxygenase and the induction of depressive-like behavior in mice in response to bacillus Calmette-Guerin. J Neurosci 2009, 29(13):4200-4209. 10.1523/JNEUROSCI.5032-08.2009, 2835569, 19339614.
21. O'Connor JC, Lawson MA, Andre C, Briley EM, Szegedi SS, Lestage J, Castanon N, Herkenham M, Dantzer R, Kelley KW. Induction of IDO by bacille Calmette-Guerin is responsible for development of murine depressive-like behavior. J Immunol 2009, 182(5):3202-3212. 10.4049/jimmunol.0802722, 2664258, 19234218.
22. Salazar A, Gonzalez-Rivera BL, Redus L, Parrott JM, O'Connor JC. Indoleamine 2,3-dioxygenase mediates anhedonia and anxiety-like behaviors caused by peripheral lipopolysaccharide immune challenge. Horm Behav 2012, 62(3):202-209. 10.1016/j.yhbeh.2012.03.010, 3425718, 22504306.
23. Dobos N, de Vries EF, Kema IP, Patas K, Prins M, Nijholt IM, Dierckx RA, Korf J, den Boer JA, Luiten PG, Eisel UL. The role of indoleamine 2,3-dioxygenase in a mouse model of neuroinflammation-induced depression. J Alzheimers Dis 2012, 28(4):905-915.
24. Kaster MP, Gadotti VM, Calixto JB, Santos AR, Rodrigues AL. Depressive-like behavior induced by tumor necrosis factor-alpha in mice. Neuropharmacology 2012, 62(1):419-426. 10.1016/j.neuropharm.2011.08.018, 21867719.
25. Lawson MA, Kelley KW, Dantzer R. Intracerebroventricular administration of HIV-1 Tat induces brain cytokine and indoleamine 2,3-dioxygenase expression: a possible mechanism for AIDS comorbid depression. Brain Behav Immun 2011, 25(8):1569-1575. 10.1016/j.bbi.2011.05.006, 3191256, 21620953.
26. Fu X, Zunich SM, O'Connor JC, Kavelaars A, Dantzer R, Kelley KW. Central administration of lipopolysaccharide induces depressive-like behavior in vivo and activates brain indoleamine 2,3 dioxygenase in murine organotypic hippocampal slice cultures. J Neuroinflammation 2010, 7:43. 10.1186/1742-2094-7-43, 2921406, 20678226.
27. Godbout JP, Berg BM, Kelley KW, Johnson RW. alpha-Tocopherol reduces lipopolysaccharide-induced peroxide radical formation and interleukin-6 secretion in primary murine microglia and in brain. J Neuroimmunol 2004, 149(1-2):101-109.
28. Lawson MA, McCusker RH, Kelley KW. Interleukin-1 beta converting enzyme is necessary for development of depression-like behavior following intracerebroventricular administration of lipopolysaccharide to mice. J Neuroinflammation 2013, 10:54. 10.1186/1742-2094-10-54, 3663735, 23634700.
29. Park SE, Dantzer R, Kelley KW, McCusker RH. Central administration of insulin-like growth factor-I decreases depressive-like behavior and brain cytokine expression in mice. J Neuroinflammation 2011, 8:12. 10.1186/1742-2094-8-12, 3045937, 21306618.
30. Nestler EJ, Hyman SE. Animal models of neuropsychiatric disorders. Nat Neurosci 2010, 13(10):1161-1169. 10.1038/nn.2647, 20877280.
31. Park SE, Lawson M, Dantzer R, Kelley KW, McCusker RH. Insulin-like growth factor-I peptides act centrally to decrease depression-like behavior of mice treated intraperitoneally with lipopolysaccharide. J Neuroinflammation 2011, 8:179. 10.1186/1742-2094-8-179, 3264674, 22189158.
32. Kozak W, Conn CA, Kluger MJ. Lipopolysaccharide induces fever and depresses locomotor activity in unrestrained mice. Am J Physiol 1994, 266(1 Pt 2):R125-R135.
33. O'Connor JC, Satpathy A, Hartman ME, Horvath EM, Kelley KW, Dantzer R, Johnson RW, Freund GG. IL-1beta-mediated innate immunity is amplified in the db/db mouse model of type 2 diabetes. J Immunol 2005, 174(8):4991-4997.
34. Corona AW, Norden DM, Skendelas JP, Huang Y, O'Connor JC, Lawson M, Dantzer R, Kelley KW, Godbout JP. Indoleamine 2,3-dioxygenase inhibition attenuates lipopolysaccharide induced persistent microglial activation and depressive-like complications in fractalkine receptor (CX3CR1)-deficient mice. Brain Behav Immun 2013, 31:134-142.
35. Qian F, Liao J, Villella J, Edwards R, Kalinski P, Lele S, Shrikant P, Odunsi K. Effects of 1-methyltryptophan stereoisomers on IDO2 enzyme activity and IDO2-mediated arrest of human T cell proliferation. Cancer Immunol Immunother 2012, 61(11):2013-2020. 10.1007/s00262-012-1265-x, 22527253.
36. Kanai M, Funakoshi H, Takahashi H, Hayakawa T, Mizuno S, Matsumoto K, Nakamura T. Tryptophan 2,3-dioxygenase is a key modulator of physiological neurogenesis and anxiety-related behavior in mice. Mol Brain 2009, 2:8. 10.1186/1756-6606-2-8, 2673217, 19323847.
37. Metz R, Duhadaway JB, Kamasani U, Laury-Kleintop L, Muller AJ, Prendergast GC. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2,3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer Res 2007, 67(15):7082-7087. 10.1158/0008-5472.CAN-07-1872, 17671174.
38. Lob S, Konigsrainer A, Zieker D, Brucher BL, Rammensee HG, Opelz G, Terness P. IDO1 and IDO2 are expressed in human tumors: levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol Immunother 2009, 58(1):153-157. 10.1007/s00262-008-0513-6, 18418598.