Does tryptophan degradation along the kynurenine pathway mediate the association between pro-inflammatory immune activity and depressive symptoms?

Psychoneuroendocrinology

Volumn 45, Issue , 2014, Pages 202-210

  Quak, Jacqueline ^a   Doornbos, Bennard ^a   Roest, Annelieke M ^a   Duivis, Hester E ^b   Vogelzangs, Nicole ^c   Nolen, Willem A ^a   Penninx, Brenda W J H ^c   Kema, Ido P ^a   De Jonge, Peter ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b TILBURG UNIVERSITY   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Depression; Depressive symptoms; Indoleamine 2,3 dioxygenase; Inflammation; Kynurenine; Tryptophan

Indexed keywords

C REACTIVE PROTEIN; INTERLEUKIN 6; KYNURENINE; TRYPTOPHAN; TUMOR NECROSIS FACTOR ALPHA; AUTACOID;

ADULT; AGED; AMINO ACID METABOLISM; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE MARKER; FEMALE; HUMAN; INFLAMMATION; INVENTORY OF DEPRESSIVE SYMPTOMATOLOGY; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; ADOLESCENT; CASE CONTROL STUDY; DEPRESSION; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM; MIDDLE AGED; NETHERLANDS; PROTEIN DEGRADATION; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; CASE-CONTROL STUDIES; DEPRESSION; DEPRESSIVE DISORDER, MAJOR; FEMALE; HUMANS; IMMUNE SYSTEM; INFLAMMATION; INFLAMMATION MEDIATORS; KYNURENINE; MALE; METABOLIC NETWORKS AND PATHWAYS; MIDDLE AGED; NETHERLANDS; PROTEOLYSIS; TRYPTOPHAN; YOUNG ADULT;

EID: 84901228336     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.03.013     Document Type: Article

References (45)

1. Ara I., Bano S. Citalopram decreases tryptophan 2,3-dioxygenase activity and brain 5-HT turnover in swim stressed rats. Pharmacol. Rep. 2012, 64:558-566.
2. Badawy A.A., Morgan C.J. Effects of acute paroxetine administration on tryptophan metabolism and disposition in the rat. Br. J. Pharmacol. 1991, 102:429-433.
3. Bannink M., Fekkes D., Van Gool A.R., Kruit W.H.J., Sleijfer S., van d.H., Eggermont A.M.M., Stoter G., Hengeveld M.W. Interferon-α influences tryptophan metabolism without inducing psychiatric side effects. Neuropsychobiology 2007, 55:225-231.
4. Capuron L., Neurauter G., Musselman D.L., Lawson D.H., Nemeroff C.B., Fuchs D., Miller A.H. Interferon-alpha-induced changes in tryptophan metabolism. Relationship to depression and paroxetine treatment. Biol. Psychiatr. 2003, 54:906-914.
5. Chopra K., Kumar B., Kuhad A. Pathobiological targets of depression. Expert Opin. Ther. Targets 2011, 15:379-400.
6. Christmas D.M., Potokar J., Davies S.J. A biological pathway linking inflammation and depression: activation of indoleamine 2,3-dioxygenase. Neuropsychiatr. Dis. Treat. 2011, 7:431-439.
7. Comai S., Cavalletto L., Chemello L., Bernardinello E., Ragazzi E., Costa C.V.L., Bertazzo A. Effects of PEG-interferon alpha plus ribavirin on tryptophan metabolism in patients with chronic hepatitis C. Pharmacol. Res. 2011, 63:85-92.
8. Cozzi A., Zignego A.L., Carpendo R., Biagiotti T., Aldinucci A., Monti M., Giannini C., Rosselli M., Laffi G., Moroni F. Low serum tryptophan levels, reduced macrophage IDO activity and high frequency of psychopathology in HCV patients. J. Viral Hepat. 2006, 13:402-408.
9. Dantzer R., O'Connor J.C., Lawson M.A., Kelley K.W. Inflammation-associated depression: from serotonin to kynurenine. Psychoneuroendocrinology 2011, 36:426-436.
10. de Jong W.H., Smit R., Bakker S.J., de Vries E.G., Kema I.P. Plasma tryptophan, kynurenine and 3-hydroxykynurenine measurement using automated on-line solid-phase extraction HPLC-tandem mass spectrometry. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2009, 877:603-609.
11. Dobos N., de Vries E.F., Kema I.P., Patas K., Prins M., Nijholt I.M., Dierckx R.A., Korf J., den Boer J.A., Luiten P.G., Eisel U.L. The role of indoleamine 2,3-dioxygenase in a mouse model of neuroinflammation-induced depression. J. Alzheimers Dis. 2012, 28:905-915.
12. 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. Psychiatr. 2010, 67:446-457.
13. Duivis H.E., Vogelzangs N., Kupper N., de Jonge P., Penninx B.W. Differential association of somatic and cognitive symptoms of depression and anxiety with inflammation: findings from the Netherlands Study of Depression and Anxiety (NESDA). Psychoneuroendocrinology 2013, 38(9):1573-1585.
14. Elovainio M., Hurme M., Jokela M., Pulkki-Raback L., Kivimaki M., Hintsanen M., Hintsa T., Lehtimaki T., Viikari J., Raitakari O.T., Keltikangas-Jarvinen L. Moderating effect of indoleamine 2,3-dioxygenase (IDO) activation in the association between depressive symptoms and carotid atherosclerosis: evidence from the Young Finns study. J. Affect. Disord. 2011, 133(3):611-614.
15. Elovainio M., Hurme M., Jokela M., Pulkki-Raback L., Kivimaki M., Hintsanen M., Hintsa T., Lehtimaki T., Viikari J., Raitakari O.T., Keltikangas-Jarvinen L. Indoleamine 2,3-dioxygenase activation and depressive symptoms: results from the young Finns study. Psychosom. Med. 2012, 74:675-681.
16. Fitzgerald P., Cassidy Eugene M., Clarke G., Scully P., Barry S., Quigley Eamonn M.M., Shanahan F., Cryan J., Dinan Timothy G. Tryptophan catabolism in females with irritable bowel syndrome: relationship to interferon-gamma, severity of symptoms and psychiatric co-morbidity. Neurogastroenterol. Motil. 2008, 20:1291-1297.
17. Gabbay V., Klein R.G., Katz Y., Mendoza S., Guttman L.E., Alonso C.M., Babb J.S., Hirsch G.S., Liebes L. The possible role of the kynurenine pathway in adolescent depression with melancholic features. J. Child Psychol. Psychiatr. 2010, 51:935-943.
18. Howren M.B., Lamkin D.M., Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 2009, 71:171-186.
19. Hughes M.M., Carballedo A., McLoughlin D.M., Amico F., Harkin A., Frodl T., Connor T.J. Tryptophan depletion in depressed patients occurs independent of kynurenine pathway activation. Brain Behav. Immun. 2012, 26:979-987.
20. Lapin I.P., Oxenkrug G.F. Intensification of the central serotoninergic processes as a possible determinant of the thymoleptic effect. Lancet 1969, 1:132-136.
21. Leonard B.E. The concept of depression as a dysfunction of the immune system. Curr. Immunol. Rev. 2010, 6:205-212.
22. Maes M., Leonard B.E., Myint A.M., Kubera M., Verkerk R. The new '5-HT' hypothesis of depression: cell-mediated immune activation induces indoleamine 2,3-dioxygenase, which leads to lower plasma tryptophan and an increased synthesis of detrimental tryptophan catabolites (TRYCATs), both of which contribute to the onset of depression. Prog. Neuro-Psychopharmacol. Biol. Psychiatr. 2011, 35:702-721.
23. Maes M., Jacobs M.P., Suy E., Minner B., Leclercq C., Christiaens F., Raus J. Suppressant effects of dexamethasone on the availability of plasma l-tryptophan and tyrosine in healthy controls and in depressed patients. Acta Psychiatr. Scand. 1990, 81:19-23.
24. Maes M., Bonaccorso S., Marino V., Puzella A., Pasquini M., Biondi M., Artini M., Almerighi C., Meltzer H. Treatment with interferon-alpha (IFN(alpha)) of hepatitis C patients induces lower serum dipeptidyl peptidase IV activity, which is related to IFN(alpha)-induced depressive and anxiety symptoms and immune activation. Mol. Psychiatr. 2001, 6:475-480.
25. Maes M., Yirmyia R., Noraberg J., Brene S., Hibbeln J., Perini G., Kubera M., Bob P., Lerer B., Maj M. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab. Brain Dis. 2009, 24:27-53.
26. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatr. 2009, 65:732-741.
27. Myint A.-, 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.
28. 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. Psychiatr. 2009, 14:511-522.
29. O'Connor J.C., Andre C., Wang Y., Lawson M.A., Szegedi S.S., Lestage J., Castanon N., Kelley K.W., 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, 29:4200-4209.
30. 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, 182:3202-3212.
31. Penninx B.W., Beekman A.T., Smit J.H., Zitman F.G., Nolen W.A., Spinhoven P., Cuijpers P., De Jong P.J., Van Marwijk H.W., Assendelft W.J., Van Der Meer K., Verhaak P., Wensing M., De Graaf R., Hoogendijk W.J., Ormel J., Van Dyck R. The Netherlands Study of Depression and Anxiety (NESDA): rationale, objectives and methods. Int. J. Methods Psychiatr. Res. 2008, 17:121-140. NESDA Research Consortium.
32. Preacher K.J., Hayes A.F. SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behav. Res. Methods Instrum. Comput. 2004, 36:717-731.
33. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 2006, 27:24-31.
34. 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. Psychiatr. 2010, 15:393-403.
35. Rush A.J., Gullion C.M., Basco M.R., Jarrett R.B., Trivedi M.H. The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychol. Med. 1996, 26:477-486.
36. Russo S., Kema I.P., Haagsma E.B., Boon J.C., Willemse P.H.B., Den Boer J.A., De Vries E.G.E., Korf J. Irritability rather than depression during interferon treatment is linked to increased tryptophan catabolism. Psychosom. Med. 2005, 67:773-777.
37. Schroecksnadel K., Sarcletti M., Winkler C., Mumelter B., Weiss G., Fuchs D., Kemmler G., Zangerle R. Quality of life and immune activation in patients with HIV-infection. Brain Behav. Immun. 2008, 22:881-889.
38. Sublette M.E., Postolache T.T. Neuroinflammation and depression: the role of indoleamine 2,3-dioxygenase (IDO) as a molecular pathway. Psychosom. Med. 2012, 74:668-672.
39. Sublette M.E., Galfalvy H.C., Fuchs D., Lapidus M., Grunebaum M.F., Oquendo M.A., John Mann J., Postolache T.T. Plasma kynurenine levels are elevated in suicide attempters with major depressive disorder. Brain Behav. Immun. 2011, 26(6):1272-1278.
40. Swardfager W., Herrmann N., Dowlati Y., Oh P.I., Kiss A., Walker S.E., Lanctot K.L. Indoleamine 2,3-dioxygenase activation and depressive symptoms in patients with coronary artery disease. Psychoneuroendocrinology 2009, 34:1560-1566.
41. Trivedi M.H., Rush A.J., Ibrahim H.M., Carmody T.J., Biggs M.M., Suppes T., Crismon M.L., Shores-Wilson K., Toprac M.G., Dennehy E.B., Witte B., Kashner T.M. The Inventory of Depressive Symptomatology, Clinician Rating (IDS-C) and Self-Report (IDS-SR), and the Quick Inventory of Depressive Symptomatology, Clinician Rating (QIDS-C) and Self-Report (QIDS-SR) in public sector patients with mood disorders: a psychometric evaluation. Psychol. Med. 2004, 34:73-82.
42. Van Gool A.R., Verkerk R., Fekkes D., Bannink M., Sleijfer S., Kruit W.H.J., Van Der Holt B., Scharpe S., Eggermont A.M.M., Stoter G., Hengeveld M.W. Neurotoxic and neuroprotective metabolites of kynurenine in patients with renal cell carcinoma treated with interferon-(alpha): course and relationship with psychiatric status. Psychiatr. Clin. Neurosci. 2008, 62:597-602.
43. Vogelzangs N., Duivis H.E., Beekman A.T.F., Kluft C., Neuteboom J., Hoogendijk W., Smit J.H., De Jonge P., Penninx B.W.J.H. Association of depressive disorders, depression characteristics and antidepressant medication with inflammation. Transl. Psychiatr. 2012, 2:e79.
44. Wichers M.C., Koek G.H., 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. Psychiatr. 2005, 10:538-544.
45. Wittchen H.U. Reliability and validity studies of the WHO - Composite International Diagnostic Interview (CIDI): a critical review. J. Psychiatr. Res. 1994, 28:57-84.