Indoleamine 2,3-dioxygenase-dependent neurotoxic kynurenine metabolism mediates inflammation-induced deficit in recognition memory

Brain, Behavior, and Immunity

Volumn 50, Issue , 2015, Pages 115-124

  Heisler, Jillian M ^a   O'Connor, Jason C ^a,b  

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

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

Author keywords

Behavior; Indoleamine 2,3 dioxygenase; Kynurenine; Kynurenine monooxygenase; Mouse; Neuroinflammation; Neuropsychiatric symptom; Novel object recognition; Perirhinal cortex; Recognition memory

Indexed keywords

3 HYDROXYANTHRANILATE 3,4 DIOXYGENASE; ALLOGRAFT INFLAMMATORY FACTOR 1; GLIAL FIBRILLARY ACIDIC PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1BETA; KYNURENINE; KYNURENINE 3 MONOOXYGENASE; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; IDO1 PROTEIN, MOUSE; LIPOPOLYSACCHARIDE;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; ENTORHINAL CORTEX; GENE EXPRESSION; INFLAMMATION; MALE; MOUSE; MOUSE MODEL; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PERIRHINAL CORTEX; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DEPRESSION; DRUG EFFECTS; ENCEPHALITIS; KNOCKOUT MOUSE; MEMORY DISORDER; METABOLISM; PARAHIPPOCAMPAL GYRUS; PHYSIOLOGY; RECOGNITION;

ANIMALS; CYTOKINES; DEPRESSION; ENCEPHALITIS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; LIPOPOLYSACCHARIDES; MALE; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PARAHIPPOCAMPAL GYRUS; RECOGNITION (PSYCHOLOGY); RNA, MESSENGER;

EID: 84933556000     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.06.022     Document Type: Article

References (44)

1. Andre C., O'Connor J.C., Kelley K.W., 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(1-2):90-99.
2. Capuron L., Miller A.H. Cytokines and psychopathology: lessons from interferon-alpha. Biol. Psychiatry 2004, 56(11):819-824.
3. Capuron L., Ravaud A., Neveu P.J., Miller A.H., Maes M., Dantzer R. Association between decreased serum tryptophan concentrations and depressive symptoms in cancer patients undergoing cytokine therapy. Mol. Psychiatry 2002, 7(5):468-473.
4. Chiarugi A., Carpenedo R., Moroni F. Kynurenine disposition in blood and brain of mice: effects of selective inhibitors of kynurenine hydroxylase and of kynureninase. J. Neurochem. 1996, 67(2):692-698.
5. Collingridge G.L., Volianskis A., Bannister N., France G., Hanna L., Mercier M., Tidball P., Fang G., Irvine M.W., Costa B.M., Monaghan D.T., Bortolotto Z.A., Molnar E., Lodge D., Jane D.E. The NMDA receptor as a target for cognitive enhancement. Neuropharmacology 2013, 64:13-26.
6. Conradi H.J., Ormel J., de Jonge P. Presence of individual (residual) symptoms during depressive episodes and periods of remission: a 3-year prospective study. Psychol. Med. 2011, 41(6):1165-1174.
7. Corona A.W., Huang Y., O'Connor J.C., Dantzer R., Kelley K.W., Popovich P.G., Godbout J.P. Fractalkine receptor (CX3CR1) deficiency sensitizes mice to the behavioral changes induced by lipopolysaccharide. J. Neuroinflammation 2010, 7:93.
8. Cross L., Brown M.W., Aggleton J.P., Warburton E.C. The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative recognition and recency but not item recognition. Learn. Mem. 2012, 20(1):41-50.
9. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9(1):46-56.
10. Dantzer R., O'Connor J.C., Lawson M.A., Kelley K.W. Inflammation-associated depression: from serotonin to kynurenine. Psychoneuroendocrinology 2011, 36(3):426-436.
11. de Lima M.N., Laranja D.C., Bromberg E., Roesler R., Schroder N. Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behav. Brain Res. 2005, 156(1):139-143.
12. Dere E., Huston J.P., De Souza Silva M.A. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci. Biobehav. Rev. 2007, 31(5):673-704.
13. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., Lanctot K.L. A meta-analysis of cytokines in major depression. Biol. Psychiatry 2010, 67(5):446-457.
14. Ennaceur A., Aggleton J.P. The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat. Behav. Brain Res. 1997, 88(2):181-193.
15. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav. Brain Res. 1988, 31(1):47-59.
16. Evans D.L., Charney D.S., Lewis L., Golden R.N., Gorman J.M., Krishnan K.R., Nemeroff C.B., Bremner J.D., Carney R.M., Coyne J.C., Delong M.R., Frasure-Smith N., Glassman A.H., Gold P.W., Grant I., Gwyther L., Ironson G., Johnson R.L., Kanner A.M., Katon W.J., Kaufmann P.G., Keefe F.J., Ketter T., Laughren T.P., Leserman J., Lyketsos C.G., McDonald W.M., McEwen B.S., Miller A.H., Musselman D., O'Connor C., Petitto J.M., Pollock B.G., Robinson R.G., Roose S.P., Rowland J., Sheline Y., Sheps D.S., Simon G., Spiegel D., Stunkard A., Sunderland T., Tibbits P., Valvo W.J. Mood disorders in the medically ill: scientific review and recommendations. Biol. Psychiatry 2005, 58(3):175-189.
17. Frenois F., Moreau M., O'Connor J., Lawson M., Micon C., Lestage J., Kelley K.W., Dantzer R., Castanon N. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 2007, 32(5):516-531.
18. Haba R., Shintani N., Onaka Y., Wang H., Takenaga R., Hayata A., Baba A., Hashimoto H. Lipopolysaccharide affects exploratory behaviors toward novel objects by impairing cognition and/or motivation in mice: possible role of activation of the central amygdala. Behav. Brain Res. 2012, 228(2):423-431.
19. Hammond R.S., Tull L.E., Stackman R.W. On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol. Learn. Mem. 2004, 82(1):26-34.
20. Hasselbalch B.J., Knorr U., Kessing L.V. Cognitive impairment in the remitted state of unipolar depressive disorder: a systematic review. J. Affect. Disord. 2011, 134(1-3):20-31.
21. Jaeger J., Berns S., Uzelac S., Davis-Conway S. Neurocognitive deficits and disability in major depressive disorder. Psychiatry Res. 2006, 145(1):39-48.
22. Jo Y.S., Choi J.S. Memory retrieval in response to partial cues requires NMDA receptor-dependent neurotransmission in the medial prefrontal cortex. Neurobiol. Learn. Mem. 2014, 109:20-26.
23. Keller M.B., Lavori P.W., Kane J.M., Gelenberg A.J., Rosenbaum J.F., Walzer E.A., Baker L.A. Subsyndromal symptoms in bipolar disorder. A comparison of standard and low serum levels of lithium. Arch. Gen. Psychiatry 1992, 49(5):371-376.
24. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 2005, 62(6):593-602.
25. Morriss R. Clinical importance of inter-episode symptoms in patients with bipolar affective disorder. J. Affect. Disord. 2002, 72(Suppl. 1):S3-13.
26. Mumby D.G., Glenn M.J., Nesbitt C., Kyriazis D.A. Dissociation in retrograde memory for object discriminations and object recognition in rats with perirhinal cortex damage. Behav. Brain Res. 2002, 132(2):215-226.
27. Nierenberg A.A., Keefe B.R., Leslie V.C., Alpert J.E., Pava J.A., Worthington J.J., Rosenbaum J.F., Fava M. Residual symptoms in depressed patients who respond acutely to fluoxetine. J. Clin. Psychiatry 1999, 60(4):221-225.
28. Norman G., Eacott M.J. Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions. Behav. Brain Res. 2004, 148(1-2):79-91.
29. O'Connor J.C., Lawson M.A., Andre C., Briley E.M., Szegedi S.S., Lestage J., Castanon N., Herkenham M., Dantzer R., Kelley K.W. Induction of IDO by bacille Calmette-Guerin is responsible for development of murine depressive-like behavior. J. Immunol. 2009, 182(5):3202-3212.
30. O'Connor J.C., Lawson M.A., Andre C., Moreau M., Lestage J., Castanon N., Kelley K.W., Dantzer R. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol. Psychiatry 2009, 14(5):511-522.
31. O'Connor J.C., Satpathy A., Hartman M.E., Horvath E.M., Kelley K.W., Dantzer R., Johnson R.W., Freund G.G. IL-1beta-mediated innate immunity is amplified in the db/db mouse model of type 2 diabetes. J. Immunol. 2005, 174(8):4991-4997.
32. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2004, Elsevier Academic Press, Amsterdam, Boston.
33. Paykel E.S. Partial remission, residual symptoms, and relapse in depression. Dialogues Clin. Neurosci. 2008, 10(4):431-437.
34. Pocivavsek A., Wu H.Q., Elmer G.I., Bruno J.P., Schwarcz R. Pre- and postnatal exposure to kynurenine causes cognitive deficits in adulthood. Eur. J. Neurosci. 2012, 35(10):1605-1612.
35. Raison C.L., Borisov A.S., Woolwine B.J., Massung B., Vogt G., Miller A.H. Interferon-alpha effects on diurnal hypothalamic-pituitary-adrenal axis activity: relationship with proinflammatory cytokines and behavior. Mol. Psychiatry 2010, 15(5):535-547.
36. Raison C.L., Dantzer R., Kelley K.W., Lawson M.A., Woolwine B.J., Vogt G., Spivey J.R., Saito K., Miller A.H. CSF concentrations of brain tryptophan and kynurenines during immune stimulation with IFN-alpha: relationship to CNS immune responses and depression. Mol. Psychiatry 2010, 15(4):393-403.
37. 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.
38. Salazar A., Gonzalez-Rivera B.L., Redus L., Parrott J.M., O'Connor J.C. Indoleamine 2,3-dioxygenase mediates anhedonia and anxiety-like behaviors caused by peripheral lipopolysaccharide immune challenge. Horm. Behav. 2012, 62(3):202-209.
39. Schwarcz R., Bruno J.P., Muchowski P.J., Wu H.Q. Kynurenines in the mammalian brain: when physiology meets pathology. Nat. Rev. Neurosci. 2012, 13(7):465-477.
40. Taylor J.R. An Introduction to Error Analysis: The Study of Uncertainties in Physical Measurements 1997, University Science Books, Sausalito, Calif.
41. Trivedi M.H., Hollander E., Nutt D., Blier P. Clinical evidence and potential neurobiological underpinnings of unresolved symptoms of depression. J. Clin. Psychiatry 2008, 69(2):246-258.
42. Walker A.K., Budac D.P., Bisulco S., Lee A.W., Smith R.A., Beenders B., Kelley K.W., Dantzer R. NMDA receptor blockade by ketamine abrogates lipopolysaccharide-induced depressive-like behavior in C57BL/6J mice. Neuropsychopharmacology 2013.
43. Winters B.D., Bussey T.J. Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. J. Neurosci. 2005, 25(17):4243-4251.
44. Zarrindast M.R., Ownegh V., Rezayof A., Ownegh F. The involvement of dorsal hippocampus in dextromethorphan-induced state-dependent learning in mice. Pharmacol. Biochem. Behav. 2014, 116:90-95.