Expression of the kynurenine pathway in human peripheral blood mononuclear cells: Implications for inflammatory and neurodegenerative disease

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Jones, Simon P ^a,b   Franco, Nunzio F ^a   Varney, Bianca ^a   Sundaram, Gayathri ^a   Brown, David A ^a,b   De Bie, Josien ^c   Lim, Chai K ^c   Guillemin, Gilles J ^a,c   Brew, Bruce J ^a,b,d  

^a St Vincent's Centre for Applied Medical Research   (Australia)

^b ST VINCENT'S CLINIC   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

^d ST VINCENT S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; KYNURENINE 3 MONOOXYGENASE; NEOPTERIN; PHOSPHORIBOSYLTRANSFERASE; QUINOLINATE PHOSPHORIBOSYLTRANSFERASE; QUINOLINIC ACID; TRYPTOPHAN; UNCLASSIFIED DRUG; INDOLEAMINE 2,3-DIOXYGENASE 1, HUMAN;

ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFLAMMATORY DISEASE; LYMPHOCYTE; MASS FRAGMENTOGRAPHY; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; UPREGULATION; BIOSYNTHESIS; FEMALE; GENE EXPRESSION REGULATION; MALE; METABOLISM; MONONUCLEAR CELL; PATHOLOGY;

FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; KYNURENINE 3-MONOOXYGENASE; LEUKOCYTES, MONONUCLEAR; MALE; NEURODEGENERATIVE DISEASES; UP-REGULATION;

EID: 84938635816     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131389     Document Type: Article

References (78)

1. Tan L, Yu JT, Tan L. The kynurenine pathway in neurodegenerative diseases: mechanistic and therapeutic considerations. Journal of the neurological sciences. 2012; 323(1-2):1-8. doi: 10.1016/j.jns.2012.08.005 PMID: 22939820
2. Ball HJ, Sanchez-Perez A, Weiser S, Austin CJ, Astelbauer F, Miu J, et al. Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene. 2007; 396(1):203-13. PMID: 17499941
3. Shimizu T, Nomiyama S, Hirata F, Hayaishi O. Indoleamine 2,3-dioxygenase: purification and some properties. J Biol Chem. 1978; 253(13):4700-6. PMID: 26687
4. Salter M, Pogson CI. The role of tryptophan 2,3-dioxygenase in the hormonal control of tryptophan metabolism in isolated rat liver cells. Effects of glucocorticoids and experimental diabetes. The Biochemical journal. 1985; 229(2):499-504. PMID: 3899109
5. Miller CL, Llenos IC, Dulay JR, Barillo MM, Yolken RH, Weis S. Expression of the kynurenine pathway enzyme tryptophan 2,3-dioxygenase is increased in the frontal cortex of individuals with schizophrenia. Neurobiology of disease. 2004; 15(3):618-29. PMID: 15056470
6. Guillemin GJ, Kerr SJ, Smythe GA, Smith DG, Kapoor V, Armati PJ, et al. Kynurenine pathway metabolism in human astrocytes: a paradox for neuronal protection. J Neurochem. 2001; 78:1-13.
7. Guillemin GJ, Smythe G, Takikawa O, Brew BJ. Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia. 2005; 49(1):15-23. PMID: 15390107
8. Lim CK, Smythe GA, Stocker R, Brew BJ, Guillemin GJ. Characterization of the kynurenine pathway in human oligodendrocytes. International Congress Series. 2007; 1304(213-217).
9. Fujigaki S, Saito K, Takemura M, Fujii H, Wada H, Noma A, et al. Species differences in L-tryptophankynurenine pathway metabolism: quantification of anthranilic acid and its related enzymes. Arch Biochem Biophys. 1998; 358(2):329-35. PMID: 9784247
10. Guillemin GJ, Smythe GA, Veas LA, Takikawa O, Brew BJ. A beta 1-42 induces production of quinolinic acid by human macrophages and microglia. Neuroreport. 2003; 14(18):2311-5. PMID: 14663182
11. Takikawa O. Biochemical and medical aspects of the indoleamine 2,3-dioxygenase-initiated L-tryptophan metabolism. Biochemical and biophysical research communications. 2005; 338(1):12-9. PMID: 16176799
12. Werner-Felmayer G, Werner ER, Fuchs D, Hausen A, Reibnegger G, Wachter H. Characteristics of interferon induced tryptophan metabolism in human cells in vitro. Biochim Biophys Acta. 1989; 1012 (2):140-7. PMID: 2500976
13. Yasui H, Takai K, Yoshida R, Hayaishi O. Interferon enhances tryptophan metabolism by inducing pulmonary indoleamine 2,3-dioxygenase: its possible occurrence in cancer patients. Proceedings of the National Academy of Sciences of the United States of America. 1986; 83(17):6622-6. PMID: 2428037
14. Dai W, Gupta SL. Regulation of indoleamine 2,3-dioxygenase gene expression in human fibroblasts by interferon-g. 1990.
15. Metz R, Duhadaway JB, Kamasani U, Laury-Kleintop L, Muller AJ, Prendergast GC. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2,3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer research. 2007; 67(15):7082-7. PMID: 17671174
16. Goldstein LE, Leopold MC, Huang X, Atwood CS, Saunders AJ, Hartshorn M, et al. 3-Hydroxykynurenine and 3-hydroxyanthranilic acid generate hydrogen peroxide and promote alpha-crystallin crosslinking by metal ion reduction. Biochemistry. 2000; 39(24):7266-75. PMID: 10852726
17. Stone TW. Neuropharmacology of quinolinic and kynurenic acids. Pharmacological reviews. 1993; 45(3):309-79. PMID: 8248282
18. Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, Ferrara GB. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. The Journal of experimental medicine. 2002; 196(4):459-68. PMID: 12186838
19. Stone TW, Perkins MN. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur J Pharmacol. 1981; 72(4):411-2. PMID: 6268428
20. Jhamandas K, Boegman RJ, Beninger RJ, Bialik M. Quinolinate-induced cortical cholinergic damage: modulation by tryptophan metabolites. Brain Res. 1990; 529(1-2):185-91. PMID: 2149296
21. Guillemin GJ. Quinolinic acid, the inescapable neurotoxin. FEBS J. 2012.
22. Liu H, Woznica K, Catton G, Crawford A, Botting N, Naismith JH. Structural and kinetic characterization of quinolinate phosphoribosyltransferase (hQPRTase) from homo sapiens. Journal of molecular biology. 2007; 373(3):755-63. PMID: 17868694
23. Mándi Y, Vécsei L. The kynurenine system and immunoregulation. Journal of neural transmission (Vienna, Austria: 1996). 2012; 119(2):197-209.
24. Munn DH. Prevention of Allogeneic Fetal Rejection by Tryptophan Catabolism. Science. 1998; 281.
25. Kwidzinski E, Bunse J, Aktas O, Richter D, Mutlu L, Zipp F, et al. Indolamine 2,3-dioxygenase is expressed in the CNS and down-regulates autoimmune inflammation. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2005; 19(10):1347-9.
26. Sakurai K, Zou JPP, Tschetter JR, Ward JM, Shearer GM. Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. Journal of neuroimmunology. 2002; 129(1-2):186-96. PMID: 12161035
27. Catherine U, Luc P, Ivan T, Vincent S, Didier C, Nicolas P, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nature Medicine. 2003.
28. Munn DH, Shafizadeh E, Attwood JT, Bondarev I, Pashine A, Mellor AL. Inhibition of T cell proliferation by macrophage tryptophan catabolism. Journal of Experimental Medicine. 1999; 189(9):1363-72. PMID: 10224276
29. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 1998; 281(5380):1191-3. PMID: 9712583
30. Terness P, Bauer TM, Rose L, Dufter C, Watzlik A, Simon H, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med. 2002; 196(4):447-57. PMID: 12186837
31. Pilotte L, Larrieu P, Stroobant V, Colau D, Dolusic E, Frederick R, et al. Reversal of tumoral immune resistance by inhibition of tryptophan 2,3-dioxygenase. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(7):2497-502. doi: 10.1073/pnas.1113873109 PMID: 22308364
32. Grohmann U, Fallarino F, Puccetti P. Tolerance, DCs and tryptophan: much ado about IDO. Trends in immunology. 2003; 24(5):242-8. PMID: 12738417
33. McIlroy D, Tanguy-Royer S, Le Meur N, Guisle I, Royer P-JJ, Léger J, et al. Profiling dendritic cell maturation with dedicated microarrays. Journal of leukocyte biology. 2005; 78(3):794-803. PMID: 15961579
34. Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, Ferrara GB. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. The Journal of experimental medicine. 2002; 196(4):459-68. PMID: 12186838
35. Fallarino F, Grohmann U, Hwang KW, Orabona C, Vacca C, Bianchi R, et al. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol. 2003; 4(12):1206-12. PMID: 14578884
36. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, et al. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature. 2011.
37. Terness P, Bauer TM, Rose L, Dufter C, Watzlik A, Simon H, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. The Journal of experimental medicine. 2002; 196(4):447-57. PMID: 12186837
38. Moffett JR, Els T, Espey MG, Walter SA, Streit WJ, Namboodiri MA. Quinolinate immunoreactivity in experimental rat brain tumors is present in macrophages but not in astrocytes. Exp Neurol. 1997; 144(2):287-301. PMID: 9168830
39. Guillemin GJ, Brew BJ, Noonan CE, Takikawa O, Cullen KM. Indoleamine 2,3 dioxygenase and quinolinic acid immunoreactivity in Alzheimer's disease hippocampus. Neuropathology and applied neurobiology. 2005; 31(4):395-404. PMID: 16008823
40. Guillemin GJ, Wang L, Brew BJ. Quinolinic acid selectively induces apoptosis of human astrocytes: potential role in AIDS dementia complex. Journal of neuroinflammation. 2005; 2:16. PMID: 16042813
41. Trevor WS, Darlington LG. The kynurenine pathway as a therapeutic target in cognitive and neurodegenerative disorders. British Journal of Pharmacology. 2013; 169(6):1211-27. doi: 10.1111/bph.12230 PMID: 23647169
42. Vécsei L, Szalárdy L, Fülöp F, Toldi J. Kynurenines in the CNS: recent advances and new questions. Nature reviews Drug discovery. 2013; 12(1):64-82. doi: 10.1038/nrd3793 PMID: 23237916
43. Carlin JM, Borden EC, Sondel PM, Byrne GI. Biologic-response-modifier-induced indoleamine 2,3-dioxygenase activity in human peripheral blood mononuclear cell cultures. Journal of immunology (Baltimore, Md: 1950). 1987; 139(7):2414-8.
44. Ozaki Y, Edelstein MP, Duch DS. The actions of interferon and antiinflammatory agents of induction of indoleamine 2,3-dioxygenase in human peripheral blood monocytes. Biochemical and biophysical research communications. 1987; 144(3):1147-53. PMID: 3107562
45. Carlin JM, Borden EC, Sondel PM, Byrne GI. Interferon-induced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. Journal of leukocyte biology. 1989; 45(1):29-34. PMID: 2463322
46. Guillemin GJ, Kerr SJ, Pemberton LA, Smith DG, Smythe GA, Armati PJ, et al. IFN-beta1b induces kynurenine pathway metabolism in human macrophages: potential implications for multiple sclerosis treatment. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research. 2001; 21(12):1097-101.
47. Musso T, Gusella GL, Brooks A, Longo DL, Varesio L. Interleukin-4 inhibits indoleamine 2,3-dioxygenase expression in human monocytes. Blood. 1994; 83(5):1408-11. PMID: 8118042
48. Sundaram G, Brew BJ, Jones SP, Adams S, Lim CK, Guillemin GJ. Quinolinic acid toxicity on oligodendroglial cells: relevance for multiple sclerosis and therapeutic strategies. Journal of neuroinflammation. 2014; 11(1):204. doi: 10.1186/s12974-014-0204-5 PMID: 25498310
49. Vidal C, Li W, Santner-Nanan B, Lim CK, Guillemin GJ, Ball HJ, et al. The kynurenine pathway of tryptophan degradation is activated during osteoblastogenesis. Stem cells (Dayton, Ohio). 2015; 33(1):111-21.
50. Chen Y, Stankovic R, Cullen KM, Meininger V, Garner B, Coggan S, et al. The kynurenine pathway and inflammation in amyotrophic lateral sclerosis. Neurotoxicity research. 2010; 18(2):132-42. doi: 10.1007/s12640-009-9129-7 PMID: 19921535
51. Munn DH, Shafizadeh E, Attwood JT, Bondarev I, Pashine A, Mellor AL. Inhibition of T cell proliferation by macrophage tryptophan catabolism. The Journal of experimental medicine. 1999; 189(9):1363-72. PMID: 10224276
52. Lee GK, Park HJ, Macleod M, Chandler P, Munn DH, Mellor AL. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology. 2002; 107(4):452-60. PMID: 12460190
53. Fallarino F, Grohmann U, Vacca C, Bianchi R, Orabona C, Spreca A, et al. T cell apoptosis by tryptophan catabolism. Cell death and differentiation. 2002; 9(10):1069-77. PMID: 12232795
54. Terness P, Bauer TM, Röse L, Dufter C, Watzlik A, Simon H, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. The Journal of experimental medicine. 2002; 196(4):447-57. PMID: 12186837
55. Belladonna ML, Grohmann U, Guidetti P, Volpi C, Bianchi R, Fioretti MC, et al. Kynurenine pathway enzymes in dendritic cells initiate tolerogenesis in the absence of functional IDO. Journal of immunology (Baltimore, Md: 1950). 2006; 177(1):130-7.
56. Mellor AL, Chandler P, Baban B, Hansen AM, Marshall B, Pihkala J, et al. Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase. International immunology. 2004; 16(10):1391-401. PMID: 15351783
57. Fallarino F, Grohmann U, You S, McGrath BC, Cavener DR, Vacca C, et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. Journal of immunology (Baltimore, Md: 1950). 2006; 176(11):6752-61.
58. Noakes R. The Aryl Hydrocarbon Receptor: A Review of Its Role in the Physiology and Pathology of the Integument and Its Relationship to the Tryptophan Metabolism. International Journal of Tryptophan Research. 2015: 7.
59. Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, Bradfield CA. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. Journal of immunology (Baltimore, Md: 1950). 2010; 185(6):3190-8.
60. Madeleine W, Gill W, David OS, Sarrabeth S, Anne Camille La F. Targeting Innate Receptors with MIS416 Reshapes Th Responses and Suppresses CNS Disease in a Mouse Model of Multiple Sclerosis. PLoS ONE. 2014; 9(1).
61. Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, et al. Differential roles of microglia and monocytes in the inflamed central nervous system. J Exp Med. 2014; 211(8):1533-49. doi: 10.1084/jem.20132477 PMID: 25002752
62. Stone TW, Behan WM. Interleukin-1beta but not tumor necrosis factor-alpha potentiates neuronal damage by quinolinic acid: protection by an adenosine A2A receptor antagonist. Journal of neuroscience research. 2007; 85(5):1077-85. PMID: 17304576
63. Guidetti P, Schwarcz R. 3-Hydroxykynurenine potentiates quinolinate but not NMDA toxicity in the rat striatum. The European journal of neuroscience. 1999; 11(11):3857-63. PMID: 10583474
64. Guidetti P, Schwarcz R. 3-Hydroxykynurenine and quinolinate: pathogenic synergism in early grade Huntington's disease? Advances in experimental medicine and biology. 2003; 527:137-45. PMID: 15206726
65. Kerr SJ, Armati PJ, Guillemin GJ, Brew BJ. Chronic exposure of human neurons to quinolinic acid results in neuronal changes consistent with AIDS dementia complex. AIDS (London, England). 1998; 12(4):355-63.
66. Croitoru-Lamoury J, Lamoury FM, Caristo M, Suzuki K, Walker D, Takikawa O, et al. Interferon-γ regulates the proliferation and differentiation of mesenchymal stem cells via activation of indoleamine 2,3 dioxygenase (IDO). PloS one. 2011; 6(2).
67. Zunszain PA, Anacker C, Cattaneo A, Choudhury S, Musaelyan K, Myint AM, et al. Interleukin-1β: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 2012; 37(4):939-49.
68. Connor TJ, Starr N, O'Sullivan JB, 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? Neuroscience letters. 2008; 441(1):29-34. doi: 10.1016/j.neulet.2008.06.007 PMID: 18584961
69. Colín-González AL, Maldonado PD, Santamaría A. 3-Hydroxykynurenine: an intriguing molecule exerting dual actions in the central nervous system. Neurotoxicology. 2013; 34:189-204. doi: 10.1016/j.neuro.2012.11.007 PMID: 23219925
70. Yan Y, Zhang GXX, Gran B, Fallarino F, Yu S, Li H, et al. IDO upregulates regulatory T cells via tryptophan catabolite and suppresses encephalitogenic T cell responses in experimental autoimmune encephalomyelitis. Journal of immunology (Baltimore, Md: 1950). 2010; 185(10):5953-61.
71. Platten M, Ho PP, Youssef S, Fontoura P, Garren H, Hur EM, et al. Treatment of autoimmune neuroinflammation with a synthetic tryptophan metabolite. Science (New York, NY). 2005; 310(5749):850-5.
72. Stone TW. Kynurenic acid blocks nicotinic synaptic transmission to hippocampal interneurons in young rats. The European journal of neuroscience. 2007; 25(9):2656-65. PMID: 17459105
73. Wang J, Simonavicius N, Wu X, Swaminath G, Reagan J, Tian H, et al. Kynurenic acid as a ligand for orphan G protein-coupled receptor GPR35. The Journal of biological chemistry. 2006; 281(31):22021-8. PMID: 16754668
74. Braidy N, Grant R, Brew BJ, Adams S, Jayasena T, Guillemin GJ. Effects of Kynurenine Pathway Metabolites on Intracellular NAD Synthesis and Cell Death in Human Primary Astrocytes and Neurons. International journal of tryptophan research: IJTR. 2009; 2:61-9. PMID: 22084582
75. Chen Y, Guillemin GJ. Kynurenine pathway metabolites in humans: disease and healthy States. International journal of tryptophan research: IJTR. 2009; 2:1-19. PMID: 22084578
76. Chiarugi A, Calvani M, Meli E, Traggiai E, Moroni F. Synthesis and release of neurotoxic kynurenine metabolites by human monocyte-derived macrophages. Journal of neuroimmunology. 2001; 120(1-2):190-8. PMID: 11694334
77. Rahman A, Ting K, Cullen KM, Braidy N, Brew BJ, Guillemin GJ. The excitotoxin quinolinic acid induces tau phosphorylation in human neurons. PloS one. 2009; 4(7).
78. Sahm F, Oezen I, Opitz CA, Radlwimmer B, von Deimling A, Ahrendt T, et al. The endogenous tryptophan metabolite and NAD+ precursor quinolinic acid confers resistance of gliomas to oxidative stress. Cancer research. 2013; 73(11):3225-34. doi: 10.1158/0008-5472.CAN-12-3831 PMID: 23548271