A role for inflammatory metabolites as modulators of the glutamate N-methyl-d-aspartate receptor in depression and suicidality

Brain, Behavior, and Immunity

Volumn 43, Issue , 2015, Pages 110-117

  Bay Richter, Cecilie ^a   Linderholm, Klas R ^b   Lim, Chai K ^c   Samuelsson, Martin ^d   Träskman Bendz, Lil ^e   Guillemin, Gilles J ^c   Erhardt, Sophie ^b   Brundin, Lena ^f,g  

^a AARHUS UNIVERSITY   (Denmark)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MACQUARIE UNIVERSITY   (Australia)

^d LINKÖPING UNIVERSITY   (Sweden)

^e LUND UNIVERSITY   (Sweden)

^f MICHIGAN STATE UNIVERSITY   (United States)

^g VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

Cerebrospinal fluid; Glutamate; Interleukin 6; Kynurenic acid; Quinolinic acid; Suicide

Indexed keywords

INTERLEUKIN 6; KYNURENIC ACID; KYNURENINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; QUINOLINIC ACID; CYTOKINE;

ADULT; ARTICLE; CEREBROSPINAL FLUID LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; DEPRESSION; DISEASE SEVERITY; FEMALE; FOLLOW UP; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; METABOLITE; MONTGOMERY ASBERG DEPRESSION RATING SCALE; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; PROTEIN BLOOD LEVEL; SUICIDAL BEHAVIOR; SUICIDE ASSESSMENT SCALE; SUICIDE ATTEMPT; CEREBROSPINAL FLUID; METABOLISM; MIDDLE AGED; SUICIDAL IDEATION; YOUNG ADULT;

ADULT; CYTOKINES; DEPRESSIVE DISORDER; FEMALE; HUMANS; INFLAMMATION; KYNURENIC ACID; KYNURENINE; MALE; MIDDLE AGED; QUINOLINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; SUICIDAL IDEATION; SUICIDE, ATTEMPTED; YOUNG ADULT;

EID: 84919402536     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.07.012     Document Type: Article

References (82)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 1987, American Psychiatric Press, Washington, DC.
2. Atlas A., Gisslen M., Nordin C., Lindstrom L., Schwieler L. Acute psychotic symptoms in HIV-1 infected patients are associated with increased levels of kynurenic acid in cerebrospinal fluid. Brain Behav. Immun. 2007, 21:86-91.
3. Atlas A., Franzen-Röhl E., Söderlund J., Jönsson E.G., Samuelsson M., Schwieler L., Sköldenberg B., Engberg G. Sustained elevation of kynurenic acid in the cerebrospinal fluid of patients with herpes simplex virus type 1 encephalitis. Int. J. Tryptophan Res. 2013, 6:89-96.
4. Berk M., Wadee A.A., Kuschke R.H., O'Neill-Kerr A. Acute phase proteins in major depression. J. Psychosom. Res. 1997, 43:529-534.
5. Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. Am. J. Psychiatry 2000, 157:115-118.
6. Chaudhury D., Walsh J.J., Friedman A.K., Juarez B., Ku S.M., Koo J.W., et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 2013, 493:532-536.
7. Chen Y., Stankovic R., Cullen K.M., Meininger V., Garner B., Coggan S., Grant R., Brew B.J., Guillemin G.J. The kynurenine pathway and inflammation in amyotrophic lateral sclerosis. Neurotox. Res. 2010, 18:132-142.
8. Claes S., Myint A.M., Domschke K., Del-Favero J., Entrich K., Engelborghs S., De Deyn P., Mueller N., Baune B., Rothermundt M. The kynurenine pathway in major depression: haplotype analysis of three related functional candidate genes. Psychiatry Res. 2011, 188:355-360.
9. Dahl J., Ormstad H., Aass H.C., Malt U.F., Bendz L.T., Sandvik L., Brundin L., Andreassen O.A. The plasma levels of various cytokines are increased during ongoing depression and are reduced to normal levels after recovery. Psychoneuroendocrinology 2014, 45:77-86.
10. de Carvalho L.P., Bochet P., Rossier J. The endogenous agonist quinolinic acid and the non endogenous homoquinolinic acid discriminate between NMDAR2 receptor subunits. Neurochem. Int. 1996, 28:445-452.
11. DiazGranados N., Ibrahim L.A., Brutsche N.E., Ameli R., Henter I.D., Luckenbaugh D.A., Machado-Vieira R., Zarate C.A. Rapid resolution of suicidal ideation after a single infusion of an N-methyl-d-aspartate antagonist in patients with treatment-resistant major depressive disorder. J. Clin. Psychiatry 2010, 71:1605-1611.
12. Dieperink E., Ho S.B., Tetrick L., Thuras P., Dua K., Willenbring M.L. Suicidal ideation during interferon-alpha2b and ribavirin treatment of patients with chronic hepatitis C. Gen. Hosp. Psychiatry 2004, 26:237-240.
13. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., LanctÔt K.L. A meta-analysis of cytokines in major depression. Biol. Psychiatry 2010, 67:446-457.
14. Erhardt S., Lim C.K., Linderholm K.R., Janelidze S., Lindqvist D., Samuelsson M., Lundberg K., Postolache T.T., Traskman-Bendz L., Guillemin G.J., Brundin L. Connecting inflammation with glutamate agonism in suicidality. Neuropsychopharmacology 2013, 38:743-752.
15. Foster A.C., Vezzani A., French E.D., Schwarcz R. Kynurenic acid blocks neurotoxicity and seizures induced in rats by the related brain metabolite quinolinic acid. Neurosci. Lett. 1984, 48:273-278.
16. Fragoso Y.D., Frota E.R., Lopes J.S., Noal J.S., Giocomo M.C., Gomes S., Goncalves M.V., da Gama P.D., Finkelsztejn A. Severe depression, suicide attempts, and ideation during the use of interferon beta by patients with multiple sclerosis. Clin. Neuropharmacol. 2010, 33:312-316.
17. Galarraga E., Surmeier D.J., Kitai S.T. Quinolinate and kainate neurotoxicity in neostriatal cultures is potentiated by co-culturing with neocortical neurons. Brain Res. 1990, 512:269-276.
18. Guillemin G.J. Quinolinic acid, the inescapable neurotoxin. FEBS J. 2012, 279:1356-1365.
19. Guillemin G.J. Quinolinic acid: neurotoxicity. FEBS J. 2012, 279:1355.
20. Guillemin G.J., Wang L., Brew B.J. Quinolinic acid selectively induces apoptosis of human astrocytes: potential role in AIDS dementia complex. J. Neuroinflamm. 2005, 2:16.
21. Harris E.C., Barraclough B. Suicide as an outcome for mental disorders. A meta-analysis. Br J. Psychiatry 1997, 170:205-228.
22. Hashimoto K. Emerging role of glutamate in the pathophysiology of major depressive disorder. Brain Res. Rev. 2009, 61:105-123.
23. Heresco-Levy U., Javitt D.C. The role of N-methyl-d-aspartate (NMDA) receptor-mediated neurotransmission in the pathophysiology and therapeutics of psychiatric syndromes. Eur. Neuropsychopharmacol. 1998, 8:141-152.
24. Heron M. Deaths: leading causes for 2008. National vital statistics reports: from the centers for disease control and prevention, national center for health statistics. Natl. Vital Stat. Syst. 2012, 60:1-94.
25. Hestad K.A., Tonseth S., Stoen C.D., Ueland T., Aukrust P. Raised plasma levels of tumor necrosis factor alpha in patients with depression: normalization during electroconvulsive therapy. J ECT 2003, 19:183-188.
26. Heyes M.P., Saito K., Crowley J.S., Davis L.E., Demitrack M.A., Der M., Dilling L.A., Elia J., Kruesi M.J., Lackner A., et al. Quinolinic acid and kynurenine pathway metabolism in inflammatory and non-inflammatory neurological disease. Brain 1992, 115:1249-1273.
27. Janelidze S., Mattei D., Westrin A., Traskman-Bendz L., Brundin L. Cytokine levels in the blood may distinguish suicide attempters from depressed patients. Brain Behav. Immun. 2011, 25:335-339.
28. Kerr S.J., Armati P.J., Guillemin G.J., Brew B.J. Chronic exposure of human neurons to quinolinic acid results in neuronal changes consistent with AIDS dementia complex. AIDS 1998, 12:355-363.
29. Khaspekov L., Kida E., Victorov I., Mossakowski M.J. Neurotoxic effect induced by quinolinic acid in dissociated cell culture of mouse hippocampus. J. Neurosci. Res. 1989, 22:150-157.
30. Kim H., Chen L., Lim G., Sung B., Wang S., McCabe M.F., et al. Brain indoleamine 2,3-dioxygenase contributes to the comorbidity of pain and depression. J. Clin. Investig. 2012, 122:2940-2954.
31. King N.J., Thomas S.R. Molecules in focus: indoleamine 2,3-dioxygenase. Int. J. Biochem. Cell Biol. 2007, 39:2167-2172.
32. Kita T., Morrison P.F., Heyes M.P., Markey S.P. Effects of systemic and central nervous system localized inflammation on the contributions of metabolic precursors to the L-kynurenine and quinolinic acid pools in brain. J. Neurochem. 2002, 82(2):258-268.
33. Larkin G.L., Beautrais A.L. A preliminary naturalistic study of low-dose ketamine for depression and suicide ideation in the emergency department. Int. J. Neuropsychopharmacol. 2011, 14:1127-1131.
34. Lehrmann E., Molinari A., Speciale C., Schwarcz R. Immunohistochemical visualization of newly formed quinolinate in the normal and excitotoxically lesioned rat striatum. Exp. Brain Res. 2001, 141(3):389-397.
35. Linderholm K.R., Skogh E., Olsson S.K., Dahl M.L., Holtze M., Engberg G., Samuelsson M., Erhardt S. Increased levels of kynurenine and kynurenic acid in the CSF of patients with schizophrenia. Schizophr. Bull. 2012, 38:426-432.
36. Lindqvist D., Janelidze S., Hagell P., Erhardt S., Samuelsson M., Minthon L., Hansson O., Bjorkqvist M., Traskman-Bendz L., Brundin L. Interleukin-6 is elevated in the cerebrospinal fluid of suicide attempters and related to symptom severity. Biol. Psychiatry 2009, 66:287-292.
37. Lodge D.J., Grace A.A. The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:5167-5172.
38. Machado-Vieira R., Salvadore G., Diazgranados N., Zarate C.A. Ketamine and the next generation of antidepressants with a rapid onset of action. Pharmacol. Ther. 2009, 123:143-150.
39. McKinnon M.C., Yucel K., Nazarov A., MacQueen G.M. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J. Psychiatry Neurosci. 2009, 34:41-54.
40. Mikova O., Yakimova R., Bosmans E., Kenis G., Maes M. Increased serum tumor necrosis factor alpha concentrations in major depression and multiple sclerosis. Eur. Neuropsychopharmacol. 2001, 11:203-208.
41. Montgomery S.A., Asberg M. A new depression scale designed to be sensitive to change. Br. J. Psychiatry 1979, 134:382-389.
42. Myint A.M., Kim Y.K., Verkerk R., Scharpe S., Steinbusch H., Leonard B. Kynurenine pathway in major depression: evidence of impaired neuroprotection. J. Affect. Disord. 2007, 98:143-151.
43. Nilsson L.K., Nordin C., Jonsson E.G., Engberg G., Linderholm K.R., Erhardt S. Cerebrospinal fluid kynurenic acid in male and female controls - correlation with monoamine metabolites and influences of confounding factors. J. Psychiatr. Res. 2007, 41:144-151.
44. Nilsson-Todd L.K., Nordin C., Jönsson E.G., Skogh E., Erhardt S. Cerebrospinal fluid kynurenic acid in male patients with schizophrenia - correlation with monoamine metabolites. Acta Neuropsychiatrica 2007, 19:45-52.
45. Nimeus A., Alsen M., Traskman-Bendz L. The Suicide Assessment Scale: an instrument assessing suicide risk of suicide attempters. Eur. Psychiatry 2000, 15:416-423.
46. Nowak G., Ordway G.A., Paul I.A. Alterations in the N-methyl-d-aspartate (NMDA) receptor complex in the frontal cortex of suicide victims. Brain Res. 1995, 675:157-164.
47. Nowak G., Szewczyk B., Sadlik K., Piekoszewski W., Trela F., Florek E., Pilc A. Reduced potency of zinc to interact with NMDA receptors in hippocampal tissue of suicide victims. Pol. J. Pharmacol. 2003, 55:455-459.
48. Obrenovitch T.P., Urenjak J. In vivo assessment of kynurenate neuroprotective potency and quinolinate excitotoxicity. Amino Acids 2000, 19:299-309.
49. Obrenovitch T.P., Urenjak J. Accumulation of quinolinic acid with neuroinflammation: does it mean excitotoxicity?. Adv. Exp. Med. Biol. 2003, 527:147-154.
50. Olfson M., Marcus S.C., Bridge J.A. Focusing suicide prevention on periods of high risk. JAMA 2014, 311:1107-1108.
51. Olsson S.K., Samuelsson M., Saetre P., Lindström L., Jönsson E.G., Nordin C., Engberg G., Erhardt S., Landén M. Elevated levels of kynurenic acid in the cerebrospinal fluid of patients with bipolar disorder. J. Psychiatry Neurosci. 2010, 35:195-199.
52. Pandey G.N., Rizavi H.S., Ren X., Fareed J., Hoppensteadt D.A., Roberts R.C., Conley R.R., Dwivedi Y. Proinflammatory cytokines in the prefrontal cortex of teenage suicide victims. J. Psychiatr. Res. 2012, 46:57-63.
53. Pizzagalli D.A., Iosifescu D., Hallett L.A., Ratner K.G., Fava M. Reduced hedonic capacity in major depressive disorder: evidence from a probabilistic reward task. J. Psychiatr. Res. 2008, 43:76-87.
54. Price R.B., Nock M.K., Charney D.S., Mathew S.J. Effects of intravenous ketamine on explicit and implicit measures of suicidality in treatment-resistant depression. Biol. Psychiatry 2009, 66:522-526.
55. 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, 15:393-403.
56. Sanacora G., Zarate C.A., Krystal J.H., Manji H.K. Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat. Rev. Drug Discov. 2008, 7:426-437.
57. Sapko M.T., Guidetti P., Yu P., Tagle D.A., Pellicciari R., Schwarcz R. Endogenous kynurenate controls the vulnerability of striatal neurons to quinolinate: implications for Huntington's disease. Exp. Neurol. 2006, 197:31-40.
58. Savitz J., Hodgkinson C.A., Martin-Soelch C., Shen P.H., Szczepanik J., Nugent A., et al. DRD2/ANKK1 Taq1A polymorphism (rs1800497) has opposing effects on D2/3 receptor binding in healthy controls and patients with major depressive disorder. Int. J. Neuropsychopharmacol. 2013, 16:2095-2101.
59. Schultz W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 1998, 80:1-27.
60. Schwarcz R., Pellicciari R. Manipulation of brain kynurenines: glial targets, neuronal effects, and clinical opportunities. J. Pharmacol. Exp. Ther. 2002, 303:1-10.
61. Schwarcz R., Guidetti P., Sathyasaikumar K.V., Muchowski P.J. Of mice, rats and men: revisiting the quinolinic acid hypothesis of Huntington's disease. Prog. Neurobiol. 2010, 90:230-245.
62. Schwarcz R., Bruno J.P., Muchowski P.J., Wu H.Q. Kynurenines in the mammalian brain: when physiology meets pathology. Nat. Rev. Neurosci. 2012, 13:465-477.
63. Schwieler L., Erhardt S., Nilsson L., Linderholm K., Engberg G. Effects of COX-1 and COX-2 inhibitors on the firing of rat midbrain dopaminergic neurons - possible involvement of endogenous kynurenic acid. Synapse 2006, 59:290-298.
64. Schwieler L., Linderholm K.R., Nilsson-Todd L.K., Erhardt S., Engberg G. Clozapine interacts with the glycine site of the NMDA receptor: electrophysiological studies of dopamine neurons in the rat ventral tegmental area. Life Sci. 2008, 83:170-175.
65. Serafini G., Pompili M., Innamorati M., Dwivedi Y., Brahmachari G., Girardi P. Pharmacological properties of glutamatergic drugs targeting NMDA receptors and their application in major depression. Curr. Pharm. Des. 2013, 19:1898-1922.
66. Smythe G.A., Braga O., Brew B.J., Grant R.S., Guillemin G.J., Kerr S.J., Walker D.W. Concurrent quantification of quinolinic, picolinic, and nicotinic acids using electron-capture negative-ion gas chromatography-mass spectrometry. Anal. Biochem. 2002, 301:21-26.
67. Stanley B., Träskman-Bendz L., Stanley M. The Suicide Assessment Scale: a scale evaluating change in suicidal behavior. Psychopharmacol. Bull. 1986, 22:200-205.
68. Steiner J., Bielau H., Brisch R., Danos P., Ullrich O., Mawrin C., Bernstein H.G., Bogerts B. Immunological aspects in the neurobiology of suicide: elevated microglial density in schizophrenia and depression is associated with suicide. J. Psychiatr. Res. 2008, 42:151-157.
69. Steiner J., Walter M., Gos T., Guillemin G.J., Bernstein H.G., Sarnyai Z., Mawrin C., Brisch R., Bielau H., Meyer Z., Schwabedissen L., Bogerts B., Myint A.M. Severe depression is associated with increased microglial quinolinic acid in subregions of the anterior cingulate gyrus: evidence for an immune-modulated glutamatergic neurotransmission?. J. Neuroinflamm. 2011, 8:94.
70. Stone T.W. Neuropharmacology of quinolinic and kynurenic acids. Pharmacol. Rev. 1993, 45:309-379.
71. Stone T.W., Perkins M.N. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur. J. Pharmacol. 1981, 72:411-412.
72. Stone T.W., Stoy N., Darlington L.G. An expanding range of targets for kynurenine metabolites of tryptophan. Trends Pharmacol. Sci. 2013, 34:136-143.
73. Sublette M.E., Galfalvy H.C., Fuchs D., Lapidus M., Grunebaum M.F., Oquendo M.A., Mann J.J., Postolache T.T. Plasma kynurenine levels are elevated in suicide attempters with major depressive disorder. Brain Behav. Immun. 2011, 25:1272-1278.
74. Suslow T., Junghanns K., Arolt V. Detection of facial expressions of emotions in depression. Percept. Mot. Skills 2001, 92:857-868.
75. Thomas A.J., Davis S., Morris C., Jackson E., Harrison R., O'Brien J.T. Increase in interleukin-1beta in late-life depression. Am. J. Psychiatry 2005, 162:175-177.
76. Tonelli L.H., Stiller J., Rujescu D., Giegling I., Schneider B., Maurer K., Schnabel A., Moller H.J., Chen H.H., Postolache T.T. Elevated cytokine expression in the orbitofrontal cortex of victims of suicide. Acta Psychiatr. Scand. 2008, 117:198-206.
77. Tye K.M., Mirzabekov J.J., Warden M.R., Ferenczi E.A., Tsai H.C., Finkelstein J., et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 2013, 493:537-541.
78. Valkanova V., Ebmeier K.P., Allan C.L. CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. J. Affect. Disord. 2013, 150:736-744.
79. Wang C.E., Brennen T., Holte A. Decreased approach motivation in depression. Scand. J. Psychol. 2006, 47:505-511.
80. Whetsell W.O., Schwarcz R. Prolonged exposure to submicromolar concentrations of quinolinic acid causes excitotoxic damage in organotypic cultures of rat corticostriatal system. Neurosci. Lett. 1989, 97:271-275.
81. Zarate C.A., Singh J.B., Carlson P.J., Brutsche N.E., Ameli R., Luckenbaugh D.A., Charney D.S., Manji H.K. A randomized trial of an N-methyl-d-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiatry 2006, 63:856-864.
82. Zarate C.A., Brutsche N.E., Ibrahim L., Franco-Chaves J., Diazgranados N., Cravchik A., Selter J., Marquardt C.A., Liberty V., Luckenbaugh D.A. Replication of ketamine's antidepressant efficacy in bipolar depression: a randomized controlled add-on trial. Biol. Psychiatry 2012, 71:939-946.