Kynurenine metabolic balance is disrupted in the hippocampus following peripheral lipopolysaccharide challenge

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Parrott, Jennifer M ^a   Redus, Laney ^a   O'Connor, Jason C ^a,b  

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

^b SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

Author keywords

Brain regions; Hippocampus; Indoleamine 2,3 dioxygenase; Kynurenine; Kynurenine 3 monooxygenase; Microglia; Neuroinflammation; Pro inflammatory cytokines

Indexed keywords

CELL MARKER; CYTOKINE; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; LIPOPOLYSACCHARIDE; MESSENGER RNA; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL ACTIVATION; CIRCULATION; CONTROLLED STUDY; GLIA CELL; HIPPOCAMPUS; METABOLIC BALANCE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UPREGULATION; ANIMAL; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; GENETICS; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; METABOLISM; NEUROGENIC INFLAMMATION; PATHOLOGY; SIGNAL TRANSDUCTION; TIME FACTOR;

ANIMALS; BRAIN; CALCIUM-BINDING PROTEINS; CHROMATOGRAPHY, LIQUID; CYTOKINES; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; LIPOPOLYSACCHARIDES; MALE; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; NEUROGENIC INFLAMMATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84970028218     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0590-y     Document Type: Article

References (72)

1. Moussavi S, Chatterji S, Verdes E, Tandon A, Patel V, Ustun B. Depression, chronic diseases, and decrements in health: results from the World Health Surveys. Lancet. 2007;370:851-8.
2. Capuron L, Miller AH. Cytokines and psychopathology: lessons from interferon-alpha. Biol Psychiatry. 2004;56:819-24.
3. Brydon L, Harrison NA, Walker C, Steptoe A, Critchley HD. Peripheral inflammation is associated with altered substantia nigra activity and psychomotor slowing in humans. Biol Psychiatry. 2008;63:1022-9.
4. Harrison NA, Brydon L, Walker C, Gray MA, Steptoe A, Critchley HD. Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biol Psychiatry. 2009;66:407-14.
5. Eisenberger NI, Berkman ET, Inagaki TK, Rameson LT, Mashal NM, Irwin MR. Inflammation-induced anhedonia: endotoxin reduces ventral striatum responses to reward. Biol Psychiatry. 2010;68:748-54.
6. Grigoleit JS, Kullmann JS, Wolf OT, Hammes F, Wegner A, Jablonowski S, Engler H, Gizewski E, Oberbeck R, Schedlowski M. Dose-dependent effects of endotoxin on neurobehavioral functions in humans. PLoS One. 2011;6:e28330.
7. Felger JC, Alagbe O, Hu F, Mook D, Freeman AA, Sanchez MM, Kalin NH, Ratti E, Nemeroff CB, Miller AH. Effects of interferon-alpha on rhesus monkeys: a nonhuman primate model of cytokine-induced depression. Biol Psychiatry. 2007;62:1324-33.
8. Felger JC, Mun J, Kimmel HL, Nye JA, Drake DF, Hernandez CR, Freeman AA, Rye DB, Goodman MM, Howell LL, Miller AH. Chronic interferon-alpha decreases dopamine 2 receptor binding and striatal dopamine release in association with anhedonia-like behavior in nonhuman primates. Neuropsychopharmacology. 2013;38:2179-87.
9. Orsal AS, Blois SM, Bermpohl D, Schaefer M, Coquery N. Administration of interferon-alpha in mice provokes peripheral and central modulation of immune cells, accompanied by behavioral effects. Neuropsychobiology. 2008;58:211-22.
10. Hayley S, Scharf J, Anisman H. Central administration of murine interferon-alpha induces depressive-like behavioral, brain cytokine and neurochemical alterations in mice: a mini-review and original experiments. Brain Behav Immun. 2013;31:115-27.
11. Konsman JP, Veeneman J, Combe C, Poole S, Luheshi GN, Dantzer R. Central nervous action of interleukin-1 mediates activation of limbic structures and behavioural depression in response to peripheral administration of bacterial lipopolysaccharide. Eur J Neurosci. 2008;28:2499-510.
12. 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;29:4200-9.
13. Raison CL, Capuron L, Miller AH. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 2006;27:24-31.
14. Polazzi E, Contestabile A. Reciprocal interactions between microglia and neurons: from survival to neuropathology. Rev Neurosci. 2002;13:221-42.
15. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8:57-69.
16. Dantzer R, O'Connor JC, Lawson MA, Kelley KW. Inflammation-associated depression: from serotonin to kynurenine. Psychoneuroendocrinology. 2011;36:426-36.
17. Andre C, O'Connor JC, Kelley KW, Lestage J, Dantzer R, Castanon N. Spatio-temporal differences in the profile of murine brain expression of proinflammatory cytokines and indoleamine 2,3-dioxygenase in response to peripheral lipopolysaccharide administration. J Neuroimmunol. 2008;200:90-9.
18. 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;182:3202-12.
19. 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;14:511-22.
20. Ganong AH, Cotman CW. Kynurenic acid and quinolinic acid act at N-methyl-D-aspartate receptors in the rat hippocampus. J Pharmacol Exp Ther. 1986;236:293-9.
21. Hilmas C, Pereira EF, Alkondon M, Rassoulpour A, Schwarcz R, Albuquerque EX. The brain metabolite kynurenic acid inhibits alpha7 nicotinic receptor activity and increases non-alpha7 nicotinic receptor expression: physiopathological implications. J Neurosci. 2001;21:7463-73.
22. Stone TW, Perkins MN. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur J Pharmacol. 1981;72:411-2.
23. Walker AK, Budac DP, Bisulco S, Lee AW, Smith RA, Beenders B, Kelley KW, Dantzer R. NMDA receptor blockade by ketamine abrogates lipopolysaccharide-induced depressive-like behavior in C57BL/6 J mice. Neuropsychopharmacology. 2013;38:1609-16.
24. Parrott JM, O'Connor JC. Kynurenine 3-monooxygenase: an influential mediator of neuropathology. Front Psychiatry. 2015;6:116.
25. 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;62:202-9.
26. Heisler JM, O'Connor JC. Indoleamine 2,3-dioxygenase-dependent neurotoxic kynurenine metabolism mediates inflammation-induced deficit in recognition memory. Brain Behav Immun. 2015;50:115-24.
27. Wichers MC, Koek GH, Robaeys G, Verkerk R, Scharpe S, Maes M. IDO and interferon-alpha-induced depressive symptoms: a shift in hypothesis from tryptophan depletion to neurotoxicity. Mol Psychiatry. 2005;10:538-44.
28. Raison CL, Dantzer R, Kelley KW, Lawson MA, Woolwine BJ, Vogt G, Spivey JR, Saito K, Miller AH. CSF concentrations of brain tryptophan and kynurenines during immune stimulation with IFN-alpha: relationship to CNS immune responses and depression. Mol Psychiatry. 2010;15:393-403.
29. Insel T, Cuthbert B, Garvey M, Heinssen R, Pine DS, Quinn K, Sanislow C, Wang P. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry. 2010;167:748-51.
30. Insel TR. The NIMH Research Domain Criteria (RDoC) Project: precision medicine for psychiatry. Am J Psychiatry. 2014;171:395-7.
31. 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;58:445-52.
32. Krabbe KS, Reichenberg A, Yirmiya R, Smed A, Pedersen BK, Bruunsgaard H. Low-dose endotoxemia and human neuropsychological functions. Brain Behav Immun. 2005;19:453-60.
33. Inagaki TK, Muscatell KA, Irwin MR, Cole SW, Eisenberger NI. Inflammation selectively enhances amygdala activity to socially threatening images. Neuroimage. 2012;59:3222-6.
34. Muscatell KA, Dedovic K, Slavich GM, Jarcho MR, Breen EC, Bower JE, Irwin MR, Eisenberger NI. Greater amygdala activity and dorsomedial prefrontal-amygdala coupling are associated with enhanced inflammatory responses to stress. Brain Behav Immun. 2015;43:46-53.
35. Konsman JP, Kelley K, Dantzer R. Temporal and spatial relationships between lipopolysaccharide-induced expression of Fos, interleukin-1beta and inducible nitric oxide synthase in rat brain. Neuroscience. 1999;89:535-48.
36. Drevets WC, Price JL, Furey ML. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct. 2008;213:93-118.
37. Gal EM, Sherman AD. L-kynurenine: its synthesis and possible regulatory function in brain. Neurochem Res. 1980;5:223-39.
38. Franklin KBJ, Paxinos G. The mouse brain in sterotaxic coordinates. 3rd ed. New York, NY: Academic Press; 2007.
39. Lawson LJ, Perry VH, Dri P, Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 1990;39:151-70.
40. Buttini M, Limonta S, Boddeke HW. Peripheral administration of lipopolysaccharide induces activation of microglial cells in rat brain. Neurochem Int. 1996;29:25-35.
41. Okuno E, Nakamura M, Schwarcz R. Two kynurenine aminotransferases in human brain. Brain Res. 1991;542:307-12.
42. 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 (CX(3)CR1)-deficient mice. Brain Behav Immun. 2013;31:134-42.
43. Dinel AL, Andre C, Aubert A, Ferreira G, Laye S, Castanon N. Lipopolysaccharide-induced brain activation of the indoleamine 2,3-dioxygenase and depressive-like behavior are impaired in a mouse model of metabolic syndrome. Psychoneuroendocrinology. 2014;40:48-59.
44. Connor TJ, Starr N, O'Sullivan JB, Harkin A. Induction of indolamine 2,3-dioxygenase and kynurenine 3-monooxygenase in rat brain following a systemic inflammatory challenge: a role for IFN-gamma? Neurosci Lett. 2008;441:29-34.
45. Bluthe RM, Pawlowski M, Suarez S, Parnet P, Pittman Q, Kelley KW, Dantzer R. Synergy between tumor necrosis factor alpha and interleukin-1 in the induction of sickness behavior in mice. Psychoneuroendocrinology. 1994;19:197-207.
46. Kozak W, Conn CA, Kluger MJ. Lipopolysaccharide induces fever and depresses locomotor activity in unrestrained mice. Am J Physiol. 1994;266:R125-35.
47. 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;9:46-56.
48. Lenczowski MJ, Bluthe RM, Roth J, Rees GS, Rushforth DA, van Dam AM, Tilders FJ, Dantzer R, Rothwell NJ, Luheshi GN. Central administration of rat IL-6 induces HPA activation and fever but not sickness behavior in rats. Am J Physiol. 1999;276:R652-8.
49. Quan N, Banks WA. Brain-immune communication pathways. Brain Behav Immun. 2007;21:727-35.
50. Banks WA, Kastin AJ, Broadwell RD. Passage of cytokines across the blood-brain barrier. Neuroimmunomodulation. 1995;2:241-8.
51. Sugaya K, Chou S, Xu SJ, McKinney M. Indicators of glial activation and brain oxidative stress after intraventricular infusion of endotoxin. Brain Res Mol Brain Res. 1998;58:1-9.
52. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res. 1998;57:1-9.
53. Schwarcz R, Bruno JP, Muchowski PJ, Wu HQ. Kynurenines in the mammalian brain: when physiology meets pathology. Nat Rev Neurosci. 2012;13:465-77.
54. Brahmachari S, Fung YK, Pahan K. Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci. 2006;26:4930-9.
55. Roy A, Fung YK, Liu X, Pahan K. Up-regulation of microglial CD11b expression by nitric oxide. J Biol Chem. 2006;281:14971-80.
56. Rios C, Santamaria A. Quinolinic acid is a potent lipid peroxidant in rat brain homogenates. Neurochem Res. 1991;16:1139-43.
57. Santamaria A, Santamaria D, Diaz-Munoz M, Espinoza-Gonzalez V, Rios C. Effects of N omega-nitro-L-arginine and L-arginine on quinolinic acid-induced lipid peroxidation. Toxicol Lett. 1997;93:117-24.
58. Perez-Severiano F, Escalante B, Rios C. Nitric oxide synthase inhibition prevents acute quinolinate-induced striatal neurotoxicity. Neurochem Res. 1998;23:1297-302.
59. Fatokun AA, Hunt NH, Ball HJ. Indoleamine 2,3-dioxygenase 2 (IDO2) and the kynurenine pathway: characteristics and potential roles in health and disease. Amino Acids. 2013;45:1319-29.
60. Ball HJ, Sanchez-Perez A, Weiser S, Austin CJ, Astelbauer F, Miu J, McQuillan JA, Stocker R, Jermiin LS, Hunt NH. Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene. 2007;396:203-13.
61. Divanovic S, Sawtell NM, Trompette A, Warning JI, Dias A, Cooper AM, Yap GS, Arditi M, Shimada K, Duhadaway JB, et al. Opposing biological functions of tryptophan catabolizing enzymes during intracellular infection. J Infect Dis. 2012;205:152-61.
62. Danesch U, Hashimoto S, Renkawitz R, Schutz G. Transcriptional regulation of the tryptophan oxygenase gene in rat liver by glucocorticoids. J Biol Chem. 1983;258:4750-3.
63. Kiss C, Ceresoli-Borroni G, Guidetti P, Zielke CL, Zielke HR, Schwarcz R. Kynurenate production by cultured human astrocytes. J Neural Transm. 2003;110:1-14.
64. Guidetti P, Hoffman GE, Melendez-Ferro M, Albuquerque EX, Schwarcz R. Astrocytic localization of kynurenine aminotransferase II in the rat brain visualized by immunocytochemistry. Glia. 2007;55:78-92.
65. Heyes MP, Achim CL, Wiley CA, Major EO, Saito K, Markey SP. Human microglia convert l-tryptophan into the neurotoxin quinolinic acid. Biochem J. 1996;320(Pt 2):595-7.
66. Guillemin GJ, Smythe G, Takikawa O, Brew BJ. Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia. 2005;49:15-23.
67. Lawson MA, Parrott JM, McCusker RH, Dantzer R, Kelley KW, O'Connor JC. Intracerebroventricular administration of lipopolysaccharide induces indoleamine-2,3-dioxygenase-dependent depression-like behaviors. J Neuroinflammation. 2013;10:87.
68. Zeisel A, Munoz-Manchado AB, Codeluppi S, Lonnerberg P, La Manno G, Jureus A, Marques S, Munguba H, He L, Betsholtz C, et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science. 2015;347:1138-42.
69. Fuertig R, Azzinnari D, Bergamini G, Cathomas F, Sigrist H, Seifritz E, Vavassori S, Luippold A, Hengerer B, Ceci A, Pryce CR. Mouse chronic social stress increases blood and brain kynurenine pathway activity and fear behaviour: both effects are reversed by inhibition of indoleamine 2,3-dioxygenase. Brain Behav Immun. 2016;54:59-72.
70. Cathomas F, Fuertig R, Sigrist H, Newman GN, Hoop V, Bizzozzero M, Mueller A, Luippold A, Ceci A, Hengerer B, et al. CD40-TNF activation in mice induces extended sickness behavior syndrome co-incident with but not dependent on activation of the kynurenine pathway. Brain Behav Immun. 2015;50:125-40.
71. Saito K, Markey SP, Heyes MP. Effects of immune activation on quinolinic acid and neuroactive kynurenines in the mouse. Neuroscience. 1992;51:25-39.
72. Pettitt SJ, Liang Q, Rairdan XY, Moran JL, Prosser HM, Beier DR, Lloyd KC, Bradley A, Skarnes WC. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat Methods. 2009;6:493-5.