Tryptophan depletion in depressed patients occurs independent of kynurenine pathway activation

Brain, Behavior, and Immunity

Volumn 26, Issue 6, 2012, Pages 979-987

  Hughes, Martina M ^a   Carballedo, Angela ^b   McLoughlin, Declan M ^a   Amico, Francesco ^b   Harkin, Andrew ^a   Frodl, Thomas ^b   Connor, Thomas J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ADELAIDE AND MEATH HOSPITAL   (Ireland)

Author keywords

Cytokine; Depression; IDO; IFN ; IL 1; IL 6; Inflammation; Kynurenine; SERT; TNF

Indexed keywords

3 HYDROXYANTHRANILIC ACID; C REACTIVE PROTEIN; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; KYNURENIC ACID; KYNURENINASE; KYNURENINE; KYNURENINE 3 MONOOXYGENASE; KYNURENINE AMINOTRANSFERASE; MESSENGER RNA; SEROTONIN TRANSPORTER; TRYPTOPHAN; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; BLOOD CELL; CLINICAL ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; DEPLETION; FEMALE; HUMAN; INFLAMMATION; MAJOR DEPRESSION; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOKINES; DEPRESSIVE DISORDER, MAJOR; FEMALE; HUMANS; KYNURENINE; MALE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SIGNAL TRANSDUCTION; TRYPTOPHAN;

EID: 84863858002     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.05.010     Document Type: Article

References (53)

1. Anisman H. Inflaming depression. J. Psychiatry Neurosci. 2011, 36:291-295.
2. Ball H.J., Yuasa H.J., Austin C.J., Weiser S., Hunt N.H. Indoleamine 2,3-dioxygenase-2; a new enzyme in the kynurenine pathway. Int. J. Biochem. Cell Biol. 2009, 41:467-471.
3. Benmansour S., Cecchi M., Morilak D.A., Gerhardt G.A., Javors M.A., Gould G.G., Frazer A. Effects of chronic antidepressant treatments on serotonin transporter function, density, and mRNA level. J. Neurosci. 1999, 19:10494-10501.
4. Brown R.R., Lee C.M., Kohler P.C., Hank J.A., Storer B.E., Sondel P.M. Altered tryptophan and neopterin metabolism in cancer patients treated with recombinant interleukin 2. Cancer Res. 1989, 49:4941-4944.
5. Capuron L., Fornwalt F.B., Knight B.T., Harvey P.D., Ninan P.T., Miller A.H. Does cytokine-induced depression differ from idiopathic major depression in medically healthy individuals? J Affect. Disord. 2009, 119:181-185.
6. Capuron L., Raison C.L., Musselman D.L., Lawson D.H., Nemeroff C.B., Miller A.H. Association of exaggerated HPA axis response to the initial injection of interferon-alpha with development of depression during interferon-alpha therapy. Am. J. Psychiatry 2003, 160:1342-1345.
7. Capuron L., Ravaud A., Dantzer R. Early depressive symptoms in cancer patients receiving interleukin 2 and/or interferon alfa-2b therapy. J. Clin. Oncol. 2000, 18:2143-2151.
8. Capuron L., Ravaud A., Gualde N., Bosmans E., Dantzer R., Maes M., Neveu P.J. Association between immune activation and early depressive symptoms in cancer patients treated with interleukin-2-based therapy. Psychoneuroendocrinology 2001, 26:797-808.
9. 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, 7:468-473.
10. Carlin J.M., Borden E.C., Sondel P.M., Byrne G.I. Interferon-induced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. J. Leukoc. Biol. 1989, 45:29-34.
11. Chai V., Vassilakos A., Lee Y., Wright J.A., Young A.H. Optimization of the PAXgene blood RNA extraction system for gene expression analysis of clinical samples. J. Clin. Lab. Anal. 2005, 19:182-188.
12. 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.
13. Cizza G., Marques A.H., Eskandari F., Christie I.C., Torvik S., Silverman M.N., Phillips T.M., Sternberg E.M. Elevated neuroimmune biomarkers in sweat patches and plasma of premenopausal women with major depressive disorder in remission: the POWER study. Biol. Psychiatry. 2008, 64:907-911. POWER Study Group.
14. Connor T.J., Starr N., O'Sullivan J.B., 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.
15. Coppen A.J., Doogan D.P. Serotonin and its place in the pathogenesis of depression. J. Clin. Psychiatry 1988, 49(Suppl):4-11.
16. Cryan J.F., Leonard B.E. 5-HT1A and beyond: the role of serotonin and its receptors in depression and the antidepressant response. Hum. Psychopharmacol. 2000, 15:113-135.
17. 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, 9:46-56.
18. Diniz B.S., Teixeira A.L., Talib L.L., Mendonça V.A., Gattaz W.F., Forlenza O.V. Increased soluble TNF receptor 2 in antidepressant-free patients with late-life depression. J. Psychiatr. Res. 2010, 44:917-920.
19. 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.
20. Frodl T., Carballedo A., Hughes M.M., Saleh K., Fagan A., Skokauskas N., McLoughlin D.M., Meaney J., O'Keane V., Connor T.J. Reduced expression of glucocorticoid-inducible genes GILZ and SGK-1: high IL-6 levels are associated with reduced hippocampal volumes in major depressive disorder. Translational Psychiat. 2012, 2:e88.
21. Fujigaki H., Saito K., Fujigaki S., Takemura M., Sudo K., Ishiguro H., Seishima M. The signal transducer and activator of transcription 1alpha and interferon regulatory factor 1 are not essential for the induction of indoleamine 2,3-dioxygenase by lipopolysaccharide: involvement of p38 mitogen-activated protein kinase and nuclear factor-kappaB pathways, and synergistic effect of several proinflammatory cytokines. J. Biochem. (Tokyo) 2006, 139:655-662.
22. Gimeno D., Kivimäki M., Brunner E.J., Elovainio M., De Vogli R., Steptoe A., Kumari M., Lowe G.D., Rumley A., Marmot M.G., Ferrie J.E. Associations of C-reactive protein and interleukin-6 with cognitive symptoms of depression: 12-year follow-up of the Whitehall II study. Psychol. Med. 2009, 39:413-423.
23. Grassi-Oliveira R., Brietzke E., Pezzi J.C., Lopes R.P., Teixeira A.L., Bauer M.E. Increased soluble tumor necrosis factor-alpha receptors in patients with major depressive disorder. Psychiatry Clin. Neurosci. 2009, 63:202-208.
24. Hamilton M. Standardised assessment and recording of depressive symptoms. Psychiatry Neurol. Neurochir. 1969, 72:201-205.
25. 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.
26. Hughes M.M., McLoughlin D.M., Harkin A., Connor T.J. Comparison of kynurenine pathway activation and tryptophan depletion induced by activation of human T-cells and innate immune cells. Brain Behav. Immun. 2011, 25(Suppl 2):208-209.
27. Katafuchi T., Kondo T., Take S., Yoshimura M. Enhanced expression of brain interferon-alpha and serotonin transporter in immunologically induced fatigue in rats. Eur. J. Neurosci. 2005, 22:2817-2826.
28. Lanquillon S., Krieg J.C., Bening-Abu-Shach U., Vedder H. Cytokine production and treatment response in major depressive disorder. Neuropsychopharmacology 2000, 22:370-379.
29. Leonard B., Maes M. Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci. Biobehav. Rev. 2012, 36:764-785.
30. Liu Y., Ho R.C., Mak A. Interleukin (IL)-6, tumour necrosis factor alpha (TNF-α) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: A meta-analysis and meta-regression. J. Affect. Disord. 2012, 139:230-239.
31. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
32. 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. Neuropsychopharmacol. Biol. Psychiatry 2011, 35:702-721.
33. Maes M., Meltzer H.Y., Bosmans E., Bergmans R., Vandoolaeghe E., Ranjan R., Desnyder R. Increased plasma concentrations of interleukin-6, soluble interleukin-6, soluble interleukin-2 and transferrin receptor in major depression. J. Affect. Disord. 1995, 34:301-309.
34. Maes M., Meltzer H.Y., Scharpé S., Bosmans E., Suy E., De Meester I., Calabrese J., Cosyns P. Relationships between lower plasma L-tryptophan levels and immune-inflammatory variables in depression. Psychiatry Res. 1993, 49:151-165.
35. Maes M., Vandewoude M., Schotte C., Martin M., D'Hondt P., Scharpe S., Blockx P. The decreased availability of L-tryptophan in depressed females: clinical and biological correlates. Prog. Neuropsychopharmacol. Biol. Psychiatry 1990, 14:903-919.
36. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65:732-741.
37. Myint A.M., Kim Y.K. Cytokine-serotonin interaction through IDO: neurodegeneration hypothesis of depression. Med. Hypotheses 2003, 61:519-525.
38. 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.
39. O'Connor J.C., Lawson M.A., André 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, 14:511-522.
40. Pasco J.A., Nicholson G.C., Williams L.J., Jacka F.N., Henry M.J., Kotowicz M.A., Schneider H.G., Leonard B.E., Berk M. Association of high-sensitivity C-reactive protein with de novo major depression. Br. J. Psychiatry 2010, 197:372-377.
41. 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.
42. Raison C.L., Borisov A.S., Majer M., Drake D.F., Pagnoni G., Woolwine B.J., Vogt G.J., Massung B., Miller A.H. Activation of central nervous system inflammatory pathways by interferon-alpha: relationship to monoamines and depression. Biol. Psychiatry 2009, 65:296-303.
43. Russo S., Kema I.P., Bosker F., Haavik J., Korf J. Tryptophan as an evolutionarily conserved signal to brain serotonin: molecular evidence and psychiatric implications. World J. Biol. Psychiatry 2009, 10:258-268.
44. Simon N.M., McNamara K., Chow C.W., Maser R.S., Papakostas G.I., Pollack M.H., Nierenberg A.A., Fava M., Wong K.K. A detailed examination of cytokine abnormalities in Major Depressive Disorder. Eur. Neuropsychopharmacol. 2008, 18:230-233.
45. Stone T.W., Darlington L.G. Endogenous kynurenines as targets for drug discovery and development. Nat. Rev. Drug Discov. 2002, 1:609-620.
46. Suzuki Y., Suda T., Furuhashi K., Suzuki M., Fujie M., Hahimoto D., Nakamura Y., Inui N., Nakamura H., Chida K. Increased serum kynurenine/tryptophan ratio correlates with disease progression in lung cancer. Lung Cancer 2010, 67:361-365.
47. Taylor M.W., Feng G.S. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 1991, 5:2516-2522.
48. Tsao C.W., Lin Y.S., Cheng J.T., Lin C.F., Wu H.T., Wu S.R., Tsai W.H. Interferon-alpha-induced serotonin uptake in Jurkat T cells via mitogen-activated protein kinase and transcriptional regulation of the serotonin transporter. J. Psychopharmacol. 2008, 22:753-760.
49. Wichers M.C., Koek G.H., Robaeys G., Verkerk R., Scharpé S., Maes M. IDO and interferon-alpha-induced depressive symptoms: a shift in hypothesis from tryptophan depletion to neurotoxicity. Mol. Psychiatry 2005, 10:538-544.
50. Widner B., Werner E.R., Schennach H., Wachter H., Fuchs D. Simultaneous measurement of serum tryptophan and kynurenine by HPLC. Clin. Chem. 1997, 43:2424-2426.
51. Zhu C.B., Lindler K.M., Owens A.W., Daws L.C., Blakely R.D., Hewlett W.A. Interleukin-1receptor activation by systemic lipopolysaccharide induces behavioral despair linked to MAPK regulation of CNS serotonin transporters. Neuropsychopharmacology 2010, 35:2510-2520.
52. Zhu C.B., Blakely R.D., Hewlett W.A. The proinflammatory cytokines interleukin-1beta and tumor necrosis factor-alpha activate serotonin transporters. Neuropsychopharmacology 2006, 31:2121-2131.
53. Zunszain P.A., Anacker C., Cattaneo A., Choudhury S., Musaelyan K., Myint A.M., Thuret S., Price J., Pariante C.M. Interleukin-1β: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis. Neuropsychopharmacology 2012, 37:939-949.