Repeated LPS Injection Induces Distinct Changes in the Kynurenine Pathway in Mice

Neurochemical Research

Volumn 41, Issue 9, 2016, Pages 2243-2255

  Larsson, M K ^a   Faka, A ^a   Bhat, M ^b   Imbeault, S ^a   Goiny, M ^a   Orhan, F ^a   Oliveros, A ^c   Stahl S ^d   Liu, X C ^a   Choi, D S ^c,e   Sandberg, K ^a,c,f   Engberg, G ^a   Schwieler, L ^a   Erhardt, S ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b ASTRAZENECA R AND D   (Sweden)

^c MAYO GRADUATE SCHOOL   (United States)

^d SCIENCE FOR LIFE LABORATORY   (Sweden)

^e Mayo Clinic College of Medicine   (United States)

^f KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Kynurenic acid; Kynurenine pathway; Lipopolysaccharide; Neuroinflammation; Psychiatric disorders; Quinolinic acid

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; DOPAMINE; KYNURENIC ACID; KYNURENINE; LIPOPOLYSACCHARIDE; QUINOLINIC ACID; SEROTONIN; TRYPTOPHAN;

ADULT; AMINO ACID BLOOD LEVEL; AMINO ACID BRAIN LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CLINICAL EVALUATION; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ILLNESS BEHAVIOR; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNTHESIS; TRYPTOPHAN BRAIN LEVEL; WEIGHT REDUCTION; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECT; IMMUNE SYSTEM; INFLAMMATION; METABOLISM;

ANIMALS; BRAIN; IMMUNE SYSTEM; INFLAMMATION; KYNURENIC ACID; KYNURENINE; LIPOPOLYSACCHARIDES; MALE; MICE, INBRED C57BL; QUINOLINIC ACID;

EID: 84966539133     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-016-1939-4     Document Type: Article

References (72)

1. Söderlund J, Schröder J, Nordin C, Samuelsson M, Walther-Jallow L, Karlsson H et al (2009) Activation of brain interleukin-1beta in schizophrenia. Mol Psychiatry 14:1069–1071. doi:10.1038/mp.2009.52
2. Söderlund J, Olsson SK, Samuelsson M, Walther-Jallow L, Johansson C, Erhardt S et al (2011) Elevation of cerebrospinal fluid interleukin-1ß in bipolar disorder. J Psychiatry Neurosci 36:114–118. doi:10.1503/jpn.100080
3. Schwieler L, Larsson MK, Skogh E, Orhan F, Bhat M, Samuelsson M et al (2015) Increased levels of IL-6 in the cerebrospinal fluid of patients with chronic schizophrenia—significance for activation of the kynurenine pathway. J Psychiatry Neurosci 40:126–133. doi:10.1503/jpn.140126
4. Lindqvist D, Janelidze S, Hagell P, Erhardt S, Samuelsson M, Minthon L et al (2009) Interleukin-6 is elevated in the cerebrospinal fluid of suicide attempters and related to symptom severity. Biol Psychiatry 66:287–292. doi:10.1016/j.biopsych.2009.01.030
5. Beumer W, Gibney SM, Drexhage RC, Pont-Lezica L, Doorduin J, Klein HC et al (2012) The immune theory of psychiatric diseases: a key role for activated microglia and circulating monocytes. J Leukoc Biol 92:959–975. doi:10.1189/jlb.0212100
6. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK et al (2010) A meta-analysis of cytokines in major depression. Biol Psychiatry 67:446–457. doi:10.1016/j.biopsych.2009.09.033
7. Valkanova V, Ebmeier KP, Allan CL (2013) CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. J Affect Disord 150:736–744. doi:10.1016/j.jad.2013.06.004
8. Yirmiya R (1996) Endotoxin produces a depressive-like episode in rats. Brain Res 711:163–174. doi:10.1016/0006-8993(95)01415-2
9. Walker AK, Budac DP, Bisulco S, Lee AW, Smith RA, Beenders B et al (2013) NMDA receptor blockade by ketamine abrogates lipopolysaccharide-induced depressive-like behavior in C57BL/6J mice. Neuropsychopharmacology 38:1609–1616. doi:10.1038/npp.2013.71
10. Borrell J, Vela JM, Arevalo-Martin A, Molina-Holgado E, Guaza C (2002) Prenatal immune challenge disrupts sensorimotor gating in adult rats: implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology 26:204–215
11. Sellgren C, Kegel ME, Bergen SE, Ekman CJ, Olsson SK, Larsson MK et al (2015) A genome-wide association study of kynurenic acid in cerebrospinal fluid: implications for psychosis and cognitive impairment in bipolar disorder. Mol Psychiatry. doi:10.1038/mp.2015.186
12. Urata Y, Koga K, Hirota Y, Akiyama I, Izumi G, Takamura M et al (2014) IL-1β increases expression of tryptophan 2,3-dioxygenase and stimulates tryptophan catabolism in endometrioma stromal cells. Am J Reprod Immunol 72:496–503. doi:10.1111/aji.12282
13. Campbell BM, Charych E, Lee AW, Möller T (2014) Kynurenines in CNS disease: regulation by inflammatory cytokines. Front Neurosci 8:12. doi:10.3389/fnins.2014.00012
14. Guillemin GJ (2012) Quinolinic acid: neurotoxicity. FEBS J 279:1355. doi:10.1111/j.1742-4658.2012.08493.x
15. Guillemin GJ (2012) Quinolinic acid, the inescapable neurotoxin. FEBS J 279:1356–1365. doi:10.1111/j.1742-4658.2012.08485.x
16. Schwarcz R, Bruno JP, Muchowski PJ, Wu H-Q (2012) Kynurenines in the mammalian brain: when physiology meets pathology. Nat Rev Neurosci 13:465–477. doi:10.1038/nrn3257
17. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46–56. doi:10.1038/nrn2297
18. Shepard PD, Joy B, Clerkin L, Schwarcz R (2003) Micromolar brain levels of kynurenic acid are associated with a disruption of auditory sensory gating in the rat. Neuropsychopharmacology 28:1454–1462. doi:10.1038/sj.npp.1300188
19. Erhardt S, Schwieler L, Emanuelsson C, Geyer M (2004) Endogenous kynurenic acid disrupts prepulse inhibition. Biol Psychiatry 56:255–260. doi:10.1016/j.biopsych.2004.06.006
20. Chess AC, Bucci DJ (2006) Increased concentration of cerebral kynurenic acid alters stimulus processing and conditioned responding. Behav Brain Res. 170:326–332. doi:10.1016/j.bbr.2006.03.006
21. Chess AC, Simoni MK, Alling TE, Bucci DJ (2007) Elevations of endogenous kynurenic acid produce spatial working memory deficits. Schizophr Bull 33:797–804. doi:10.1093/schbul/sbl033
22. Chess AC, Landers AM, Bucci DJ (2009) L-kynurenine treatment alters contextual fear conditioning and context discrimination but not cue-specific fear conditioning. Behav Brain Res 201:325–331. doi:10.1016/j.bbr.2009.03.013
23. Olsson SK, Larsson MK, Erhardt S (2012) Subchronic elevation of brain kynurenic acid augments amphetamine-induced locomotor response in mice. J Neural Transm 119:155–163. doi:10.1007/s00702-011-0706-6
24. Pocivavsek A, Wu HQ, Elmer GI, Bruno JP, Schwarcz R (2012) Pre- and postnatal exposure to kynurenine causes cognitive deficits in adulthood. Eur J Neurosci 35:1605–1612. doi:10.1111/j.1460-9568.2012.08064.x
25. Alexander KS, Pocivavsek A, Wu HQ, Pershing ML, Schwarcz R, Bruno JP (2013) Early developmental elevations of brain kynurenic acid impair cognitive flexibility in adults: reversal with galantamine. Neuroscience 238:19–28. doi:10.1016/j.neuroscience.2013.01.063
26. Trecartin KV, Bucci DJ (2011) Administration of kynurenine during adolescence, but not during adulthood, impairs social behavior in rats. Schizophr Res 133:156–158. doi:10.1016/j.schres.2011.08.014
27. Iaccarino HF, Suckow RF, Xie S, Bucci DJ (2013) The effect of transient increases in kynurenic acid and quinolinic acid levels early in life on behavior in adulthood: implications for schizophrenia. Schizophr Res 150:392–397. doi:10.1016/j.schres.2013.09.004
28. DeAngeli NE, Todd TP, Chang SE, Yeh HH, Yeh PW, Bucci DJ (2015) Exposure to kynurenic acid during adolescence increases sign-tracking and impairs long-term potentiation in adulthood. Front Behav Neurosci 8:451. doi:10.3389/fnbeh.2014.00451
29. Forrest CM, McNair K, Pisar M, Khalil OS, Darlington LG, Stone TW (2015) Altered hippocampal plasticity by prenatal kynurenine administration, kynurenine-3-monoxygenase (KMO) deletion or galantamine. Neuroscience 310:91–105. doi:10.1016/j.neuroscience.2015.09.022
30. O’Connor JC, André C, Wang Y, Lawson MA, Szegedi SS, Lestage J, Castanon N, Kelley KW, Dantzer R (2009) Interferon-γ and tumor necrosis factor-α 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 29:4200–4209. doi:10.1523/JNEUROSCI.5032-08.2009
31. Connor JC, Lawson MA, André C, Briley EM, Szegedi SS, Lestage J, Castanon N, Herkenham M, Dantzer R, Kelley KW (2009) Induction of IDO by Bacille Calmette-Guérin is responsible for development of murine depressive-like behavior. J Immunol 182:3202–3212. doi:10.4049/jimmunol.0802722
32. O’Connor JC, Lawson MA, André C, Moreau M, Lestage J, Castanon N, Kelley KW, Dantzer R (2009) Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatry 14:511–522. doi:10.1038/sj.mp.4002148
33. Kegel ME, Bhat M, Skogh E, Samuelsson M, Lundberg K, Dahl M-L et al (2014) Imbalanced kynurenine pathway in schizophrenia. Int J Tryptophan Res 7:15–22. doi:10.4137/IJTR.S16800
34. Schwarcz R, Tamminga CA, Kurlan R, Shoulson I (1988) Cerebrospinal fluid levels of quinolinic acid in Huntington’s disease and schizophrenia. Ann Neurol 24:580–582. doi:10.1002/ana.410240417
35. Schwarcz R, Rassoulpour A, Wu HQ, Medoff D, Tamminga CA, Roberts RC (2001) Increased cortical kynurenate content in schizophrenia. Biol Psychiatry 50:521–530. doi:10.1016/S0006-3223(01)01078-2
36. Erhardt S, Blennow K, Nordin C, Skogh E, Lindström LH, Engberg G (2001) Kynurenic acid levels are elevated in the cerebrospinal fluid of patients with schizophrenia. Neurosci Lett 313:96–98. doi:10.1016/S0304-3940(01)02242-X
37. Linderholm KR, Skogh E, Olsson SK, Dahl M-L, Holtze M, Engberg G et al (2012) Increased levels of kynurenine and kynurenic acid in the CSF of patients with schizophrenia. Schizophr Bull 38:426–432. doi:10.1093/schbul/sbq086
38. Nilsson LK, Linderholm KR, Engberg G, Paulson L, Blennow K, Lindström LH et al (2005) Elevated levels of kynurenic acid in the cerebrospinal fluid of male patients with schizophrenia. Schizophr Res 80:315–322. doi:10.1016/j.schres.2005.07.013
39. Sathyasaikumar KV, Stachowski EK, Wonodi I, Roberts RC, Rassoulpour A, McMahon RP et al (2011) Impaired kynurenine pathway metabolism in the prefrontal cortex of individuals with schizophrenia. Schizophr Bull 37:1147–1156. doi:10.1093/schbul/sbq112
40. Olsson SK, Sellgren C, Engberg G, Landén M, Erhardt S (2012) Cerebrospinal fluid kynurenic acid is associated with manic and psychotic features in patients with bipolar I disorder. Bipolar Disord 14:719–726. doi:10.1111/bdi.12009
41. Lavebratt C, Olsson SK, Backlund L, Frisén L, Sellgren C, Priebe L et al (2014) The KMO allele encoding Arg452 is associated with psychotic features in bipolar disorder type 1, and with increased CSF KYNA level and reduced KMO expression. Mol Psychiatry 19:334–341. doi:10.1038/mp.2013.11
42. Erhardt S, Lim CK, Linderholm KR, Janelidze S, Lindqvist D, Samuelsson M et al (2013) Connecting inflammation with glutamate agonism in suicidality. Neuropsychopharmacology 38:743–752. doi:10.1038/npp.2012.248
43. Bay-Richter C, Linderholm KR, Lim CK, Samuelsson M, Träskman-Bendz L, Guillemin GJ et al (2015) A role for inflammatory metabolites as modulators of the glutamate N-methyl-d-aspartate receptor in depression and suicidality. Brain Behav Immun 43:110–117. doi:10.1016/j.bbi.2014.07.012
44. Gyoneva S, Davalos D, Biswas D, Swanger SA, Garnier-Amblard E, Loth F et al (2014) Systemic inflammation regulates microglial responses to tissue damage in vivo. Glia 62:1345–1360. doi:10.1002/glia.22686
45. Rhee SH, Hwang D (2000) Murine TOLL-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J Biol Chem 275:34035–34040. doi:10.1074/jbc.M007386200
46. Dunn A, Swiergiel A (2005) Effects of interleukin-1 and endotoxin in the forced swim and tail suspension tests in mice. Pharmacol Biochem Behav 81:688–693. doi:10.1016/j.pbb.2005.04.019
47. Salazar A, Gonzalez-Rivera BL, Redus L, Parrott JM, O’Connor JC (2012) Indoleamine 2,3-dioxygenase mediates anhedonia and anxiety-like behaviors caused by peripheral lipopolysaccharide immune challenge. Horm Behav 62:202–209. doi:10.1016/j.yhbeh.2012.03.010
48. Czerniawski J, Miyashita T, Lewandowski G, Guzowski JF (2015) Systemic lipopolysaccharide administration impairs retrieval of context-object discrimination, but not spatial, memory: evidence for selective disruption of specific hippocampus-dependent memory functions during acute neuroinflammation. Brain Behav Immun 44:159–166. doi:10.1016/j.bbi.2014.09.014
49. Haba R, Shintani N, Onaka Y, Wang H, Takenaga R, Hayata A et al (2012) 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 228:423–431. doi:10.1016/j.bbr.2011.12.027
50. Ming Z, Sawicki G, Bekar LK (2015) Acute systemic LPS-mediated inflammation induces lasting changes in mouse cortical neuromodulation and behavior. Neurosci Lett 590:96–100. doi:10.1016/j.neulet.2015.01.081
51. Camara ML, Corrigan F, Jaehne EJ, Jawahar MC, Anscomb H, Baune BT (2015) Effects of centrally administered etanercept on behavior, microglia, and astrocytes in mice following a peripheral immune challenge. Neuropsychopharmacology 40:502–512. doi:10.1038/npp.2014.199
52. Banks WA, Erickson MA (2010) The blood-brain barrier and immune function and dysfunction. Neurobiol Dis 37:26–32. doi:10.1016/j.nbd.2009.07.031
53. Erickson MA, Banks WA (2011) Cytokine and chemokine responses in serum and brain after single and repeated injections of lipopolysaccharide: multiplex quantification with path analysis. Brain Behav Immun 25:1637–1648. doi:10.1016/j.bbi.2011.06.006
54. Tarr AJ, Chen Q, Wang Y, Sheridan JF, Quan N (2012) Neural and behavioral responses to low-grade inflammation. Behav Brain Res 235:334–341. doi:10.1016/j.bbr.2012.07.038
55. Stalder AK, Pagenstecher A, Yu NC, Kincaid C, Chiang CS, Hobbs MV, Bloom FE, Campbell IL (1997) Lipopolysaccharide-induced IL-12 expression in the central nervous system and cultured astrocytes and microglia. J Immunol. 159:1344–1351
56. Lestage J, Verrier D, Palin K, Dantzer R (2002) The enzyme indoleamine 2,3-dioxygenase is induced in the mouse brain in response to peripheral administration of lipopolysaccharide and superantigen. Brain Behav Immun 16:596–601. doi:10.1016/S0889-1591(02)00014-4
57. Tang Y-M, Chen T, Zhang X-J (2009) Determination and clinical significance of serum kynurenine and kynurenic acid levels in schizophrenia. Chin J Behav Med Brain Sci. doi:10.3760/cma.j.issn.1674-6554.2009.02.003
58. Goehler LE, Gaykema RPA, Nguyen KT, Lee JE, Tilders FJH, Maier SF et al (1999) Interleukin-1β in Immune cells of the abdominal vagus nerve: a link between the immune and nervous systems? J Neurosci 19:2799–2806
59. Romeo HE, Tio DL, Rahman SU, Chiappelli F, Taylor AN (2001) The glossopharyngeal nerve as a novel pathway in immune-to-brain communication: relevance to neuroimmune surveillance of the oral cavity. J Neuroimmunol 115:91–100. doi:10.1016/S0165-5728(01)00270-3
60. Xaio HP, Banks WA, Niehoff ML, Morley JE (2001) Effect of LPS on the permeability of the blood-brain barrier to insulin. Brain Res 896:36–42. doi:10.1016/S0006-8993(00)03247-9
61. Blatteis CM, Bealer SL, Hunter WS, Llanos-Q J, Ahokas RA, Mashburn TA (1983) Suppression of fever after lesions of the anteroventral third ventricle in guinea pigs. Brain Res Bull 11:519–526. doi:10.1016/0361-9230(83)90124-7
62. Mormède C, Palin K, Kelley KW, Castanon N, Dantzer R (2004) Conditioned taste aversion with lipopolysaccharide and peptidoglycan does not activate cytokine gene expression in the spleen and hypothalamus of mice. Brain Behav Immun 18:186–200. doi:10.1016/S0889-1591(03)00133-8
63. Facci L, Barbierato M, Marinelli C, Argentini C, Skaper SD, Giusti P (2014) Toll-like receptors 2, -3 and -4 prime microglia but not astrocytes across central nervous system regions for ATP-dependent interleukin-1β release. Sci Rep 4:6824. doi:10.1038/srep06824
64. Burnstock G, Boeynaems J-M (2014) Purinergic signalling and immune cells. Purinergic Signal 10:529–564. doi:10.1007/s11302-014-9427-2
65. Kahlenberg JM, Dubyak GR (2004) Mechanisms of caspase-1 activation by P2X7 receptor-mediated K + release. Am J Physiol Cell Physiol 286:C1100–C1108. doi:10.1152/ajpcell.00494.2003
66. André C, Dinel A-L, Ferreira G, Layé S, Castanon N (2014) Diet-induced obesity progressively alters cognition, anxiety-like behavior and lipopolysaccharide-induced depressive-like behavior: focus on brain indoleamine 2,3-dioxygenase activation. Brain Behav Immun 41:10–21. doi:10.1016/j.bbi.2014.03.012
67. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH (2005) Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 25:9275–9284. doi:10.1523/JNEUROSCI.2614-05.2005
68. Murray CL, Skelly DT, Cunningham C (2011) Exacerbation of CNS inflammation and neurodegeneration by systemic LPS treatment is independent of circulating IL-1β and IL-6. J Neuroinflammation 8:50. doi:10.1186/1742-2094-8-50
69. Miura H, Ozaki N, Sawada M, Isobe K, Ohta T, Nagatsu T (2008) A link between stress and depression: shifts in the balance between the kynurenine and serotonin pathways of tryptophan metabolism and the etiology and pathophysiology of depression. Stress 11:198–209. doi:10.1080/10253890701754068
70. Miura H, Shirokawa T, Ozaki N, Isobe K (2010) Shifts in the balance of brain tryptophan metabolism due to age and systemic administration of lipopolysaccharide. Health 02:225–233. doi:10.1080/10253890802252442
71. van Heesch F, Prins J, Konsman JP, Korte-Bouws GAH, Westphal KGC, Rybka J et al (2014) Lipopolysaccharide increases degradation of central monoamines: an in vivo microdialysis study in the nucleus accumbens and medial prefrontal cortex of mice. Eur J Pharmacol 725:55–63. doi:10.1016/j.ejphar.2014.01.014
72. Helkamaa T, Reenilä I, Tuominen RK, Soinila S, Väänänen A, Tilgmann C, Rauhala P (2007) Increased catechol-O-methyltransferase activity and protein expression in OX-42-positive cells in the substantia nigra after lipopolysaccharide microinfusion. Neurochem Int 51:412–423. doi:10.1016/j.neuint.2007.04.020