Tryptophan 2,3-dioxygenase and indoleamine 2,3-dioxygenase 1 make separate, tissue-specific contributions to basal and inflammation-induced kynurenine pathway metabolism in mice

Biochimica et Biophysica Acta - General Subjects

Volumn 1860, Issue 11, 2016, Pages 2345-2354

  Larkin, Paul B ^a,b   Sathyasaikumar, Korrapati V ^c   Notarangelo, Francesca M ^c   Funakoshi, Hiroshi ^d   Nakamura, Toshikazu ^e   Schwarcz, Robert ^c   Muchowski, Paul J ^a,b,f,g  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d ASAHIKAWA MEDICAL COLLEGE   (Japan)

^e Neurogen Inc   (Japan)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g Taube Koret Center for Huntington's Disease Research   (United States)

Author keywords

Cancer; Inflammation; Neurodegeneration; Schizophrenia; Tryptophan

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; TRYPTOPHAN 2,3 DIOXYGENASE; LIPOPOLYSACCHARIDE;

3 HAO GENE; ADULT; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; GENE DELETION; IDO1 GENE; IMMUNE SYSTEM; IMMUNOREACTIVITY; IMMUNOSTIMULATION; IN VIVO STUDY; KAT I GENE; KAT II GENE; KYNA GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUIN GENE; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; ANTIBODY SPECIFICITY; BLOOD; BRAIN; C57BL MOUSE; GENETICS; INFLAMMATION; LIVER; METABOLISM;

ANIMALS; BRAIN; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INFLAMMATION; KYNURENINE; LIPOPOLYSACCHARIDES; LIVER; MICE; MICE, INBRED C57BL; ORGAN SPECIFICITY; TRYPTOPHAN OXYGENASE;

EID: 84984653817     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2016.07.002     Document Type: Article

References (91)

1. [1] Schwarcz, R., Bruno, J.P., Muchowski, P.J., Wu, H.Q., Kynurenines in the mammalian brain: when physiology meets pathology. Nat. Rev. Neurosci. 13 (2012), 465–477.
2. [2] Rafice, S.A., Chauhan, N., Efimov, I., Basran, J., Raven, E.L., Oxidation of L-tryptophan in biology: a comparison between tryptophan 2,3-dioxygenase and indoleamine 2,3-dioxygenase. Biochem. Soc. Trans. 37 (2009), 408–412.
3. [3] Knox, W.E., Mehler, A.H., The conversion of tryptophan to kynurenine in liver. I. The coupled tryptophan peroxidase-oxidase system forming formylkynurenine. J. Biol. Chem. 187 (1950), 419–430.
4. [4] Gál, E.M., Cerebral tryptophan-2,3-dioxygenase (pyrrolase) and its induction in rat brain. J. Neurochem. 22 (1974), 861–863.
5. [5] Haber, R., Bessette, D., Hulihan-Giblin, B., Durcan, M.J., Goldman, D., Identification of tryptophan 2,3-dioxygenase RNA in rodent brain. J. Neurochem. 60 (1993), 1159–1162.
6. [6] Kanai, M., Nakamura, T., Funakoshi, H., Identification and characterization of novel variants of the tryptophan 2,3-dioxygenase gene: differential regulation in the mouse nervous system during development. Neurosci. Res. 64 (2009), 111–117.
7. [7] Miller, C.L., Llenos, I.C., Dulay, J.R., Barillo, M.M., Yolken, R.H., Weis, S., Expression of the kynurenine pathway enzyme tryptophan 2,3-dioxygenase is increased in the frontal cortex of individuals with schizophrenia. Neurobiol. Dis. 15 (2004), 618–629.
8. [8] Tatsumi, K., Higuchi, T., Fujiwara, H., Nakayama, T., Egawa, H., Itoh, K., Fujii, S., Fujita, J., Induction of tryptophan 2,3-dioxygenase in the mouse endometrium during implantation. Biochem. Biophys. Res. Commun. 274 (2000), 166–170.
9. [9] Civen, M., Knox, W.E., The independence of hydrocortisone and tryptophan inductions of tryptophan pyrrolase. J. Biol. Chem. 234 (1959), 1787–1790.
10. [10] Greengard, O., Feigelson, P., A difference between the modes of action of substrate and hormonal inducers of rat liver tryptophan pyrrolase. Nature 190 (1961), 446–447.
11. [11] Schutz, G., Chow, E., Feigelson, P., Regulatory properties of hepatic tryptophan oxygenase. J. Biol. Chem. 247 (1972), 5333–5337.
12. [12] Hirata, F., Hayaishi, O., Studies on indoleamine 2,3-dioxygenase. I. Superoxide anion as substrate. J. Biol. Chem. 250 (1975), 5960–5966.
13. [13] Takikawa, O., Yoshida, R., Kido, R., Hayaishi, O., Tryptophan degradation in mice initiated by indoleamine 2,3-dioxygenase. J. Biol. Chem. 261 (1986), 3648–3653.
14. [14] Ruddick, J.P., Evans, A.K., Nutt, D.J., Lightman, S.L., Rook, G.A., Lowry, C.A., Tryptophan metabolism in the central nervous system: medical implications. Expert Rev. Mol. Med. 8 (2006), 1–27.
15. [15] Yuasa, H.J., Takubo, M., Takahashi, A., Hasegawa, T., Noma, H., Suzuki, T., Evolution of vertebrate indoleamine 2,3-dioxygenases. J. Mol. Evol. 65 (2007), 705–714.
16. [16] Mellor, A.L., Munn, D.H., IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4 (2004), 762–774.
17. [17] Yoshida, R., Hayaishi, O., Induction of pulmonary indoleamine 2,3-dioxygenase by intraperitoneal injection of bacterial lipopolysaccharide. Proc. Natl. Acad. Sci. U. S. A. 75 (1978), 3998–4000.
18. [18] Yoshida, R., Imanishi, J., Oku, T., Kishida, T., Hayaishi, O., Induction of pulmonary indoleamine 2,3-dioxygenase by interferon. Proc. Natl. Acad. Sci. U. S. A. 78 (1981), 129–132.
19. [19] Ball, H.J., Sanchez-Perez, A., Weiser, S., Austin, C.J., Astelbauer, F., Miu, J., McQuillan, J.A., Stocker, R., Jermiin, L.S., Hunt, N.H., Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene 396 (2007), 203–213.
20. [20] Metz, R., Duhadaway, J.B., Kamasani, U., Laury-Kleintop, L., Muller, A.J., Prendergast, G.C., Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2,3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer Res. 67 (2007), 7082–7087.
21. [21] Austin, C.J., Mailu, B.M., Maghzal, G.J., Sanchez-Perez, A., Rahlfs, S., Zocher, K., Yuasa, H.J., Arthur, J.W., Becker, K., Stocker, R., Hunt, N.H., Ball, H.J., Biochemical characteristics and inhibitor selectivity of mouse indoleamine 2,3-dioxygenase-2. Amino Acids 39 (2010), 565–578.
22. [22] Pantouris, G., Serys, M., Yuasa, H.J., Ball, H.J., Mowat, C.G., Human indoleamine 2,3-dioxygenase-2 has substrate specificity and inhibition characteristics distinct from those of indoleamine 2,3-dioxygenase-1. Amino Acids 46 (2014), 2155–2163.
23. [23] 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. 41 (2009), 467–471.
24. [24] Heyes, M.P., Rubinow, D., Lane, C., Markey, S.P., Cerebrospinal fluid quinolinic acid concentrations are increased in acquired immune deficiency syndrome. Ann. Neurol. 26 (1989), 275–277.
25. [25] Beal, M.F., Matson, W.R., Storey, E., Milbury, P., Ryan, E.A., Ogawa, T., Bird, E.D., Kynurenic acid concentrations are reduced in Huntington's disease cerebral cortex. J. Neurol. Sci. 108 (1992), 80–87.
26. [26] Oxenkrug, G.F., Genetic and hormonal regulation of tryptophan kynurenine metabolism: implications for vascular cognitive impairment, major depressive disorder, and aging. Ann. N. Y. Acad. Sci. 1122 (2007), 35–49.
27. [27] Chen, Y., Guillemin, G.J., Kynurenine pathway metabolites in humans: disease and healthy states. Int. J. Tryptophan Res. 2 (2009), 1–19.
28. [28] Sato, N., Saga, Y., Mizukami, H., Wang, D., Takahashi, S., Nonaka, H., Fujiwara, H., Takei, Y., Machida, S., Takikawa, O., Ozawa, K., Suzuki, M., Downregulation of indoleamine-2,3-dioxygenase in cervical cancer cells suppresses tumor growth by promoting natural killer cell accumulation. Oncol. Rep. 28 (2012), 1574–1578.
29. [29] Cole, J.E., Astola, N., Cribbs, A.P., Goddard, M.E., Park, I., Green, P., Davies, A.H., Williams, R.O., Feldmann, M., Monaco, C., Indoleamine 2,3-dioxygenase-1 is protective in atherosclerosis and its metabolites provide new opportunities for drug development. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 13033–13038.
30. [30] Favennec, M., Hennart, B., Caiazzo, R., Leloire, A., Yengo, L., Verbanck, M., Arredouani, A., Marre, M., Pigeyre, M., Bessede, A., Guillemin, G.J., Chinetti, G., Staels, B., Pattou, F., Balkau, B., Allorge, D., Froguel, P., Poulain-Godefroy, O., The kynurenine pathway is activated in human obesity and shifted toward kynurenine monooxygenase activation. Obesity (Silver Spring) 23 (2015), 2066–2074.
31. [31] Masaki, A., Ishida, T., Maeda, Y., Suzuki, S., Ito, A., Takino, H., Ogura, H., Totani, H., Yoshida, T., Kinoshita, S., Narita, T., Ri, M., Kusumoto, S., Inagaki, A., Komatsu, H., Niimi, A., Ueda, R., Utsunomiya, A., Inagaki, H., Iida, S., Prognostic significance of tryptophan catabolism in adult t-cell leukemia/lymphoma. Clin. Cancer Res. 21 (2015), 2830–2839.
32. [32] Schwarcz, R., Okuno, E., White, R.J., Bird, E.D., Whetsell, W.O. Jr., 3-Hydroxyanthranilic acid oxygenase activity is increased in the brains of Huntington disease victims. Proc. Natl. Acad. Sci. U. S. A. 85 (1988), 4079–4081.
33. [33] Bosnyak, E., Kamson, D.O., Guastella, A.R., Varadarajan, K., Robinette, N.L., Kupsky, W.J., Muzik, O., Michelhaugh, S.K., Mittal, S., Juhász, C., Molecular imaging correlates of tryptophan metabolism via the kynurenine pathway in human meningiomas. Neuro-Oncol. 17 (2015), 1284–1292.
34. [34] Murakami, Y., Hoshi, M., Imamura, Y., Arioka, Y., Yamamoto, Y., Saito, K., Remarkable role of indoleamine 2,3-dioxygenase and tryptophan metabolites in infectious diseases: potential role in macrophage-mediated inflammatory diseases. Mediat. Inflamm., 2013, 2013, 391984.
35. [35] Pilotte, L., Larrieu, P., Stroobant, V., Colau, D., Dolusic, E., Frederick, R., De Plaen, E., Uyttenhove, C., Wouters, J., Masereel, B., Van den Eynde, B.J., Reversal of tumoral immune resistance by inhibition of tryptophan 2,3-dioxygenase. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 2497–2502.
36. [36] Dolusic, E., Frederick, R., Indoleamine 2,3-dioxygenase inhibitors: a patent review (2008–2012). Expert Opin. Ther. Pat. 23 (2013), 1367–1381.
37. [37] Kanai, M., Funakoshi, H., Takahashi, H., Hayakawa, T., Mizuno, S., Matsumoto, K., Nakamura, T., Tryptophan 2,3-dioxygenase is a key modulator of physiological neurogenesis and anxiety-related behavior in mice. Mol. Brain, 2, 2009, 8.
38. [38] Baban, B., Chandler, P., McCool, D., Marshall, B., Munn, D.H., Mellor, A.L., Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J. Reprod. Immunol. 61 (2004), 67–77.
39. [39] Too, L.K., McQuillan, J.A., Ball, H.J., Kanai, M., Nakamura, T., Funakoshi, H., McGregor, I.S., Hunt, N.H., The kynurenine pathway contributes to long-term neuropsychological changes in experimental pneumococcal meningitis. Behav. Brain Res. 270 (2014), 179–195.
40. [40] Salazar, A., Gonzalez-Rivera, B.L., Redus, L., Parrott, J.M., O'Connor, J.C., Indoleamine 2,3-dioxygenase mediates anhedonia and anxiety-like behaviors caused by peripheral lipopolysaccharide immune challenge. Horm. Behav. 62 (2012), 202–209.
41. [41] Mazarei, G., Budac, D.P., Lu, G., Lee, H., Moller, T., Leavitt, B.R., The absence of indoleamine 2,3-dioxygenase expression protects against NMDA receptor-mediated excitotoxicity in mouse brain. Exp. Neurol. 249 (2013), 144–148.
42. [42] Heyes, M.P., Quearry, B.J., Quantification of 3-hydroxykynurenine in brain by high-performance liquid chromatography and electrochemical detection. J. Chromatogr. 428 (1988), 340–344.
43. [43] Giorgini, F., Huang, S.Y., Sathyasaikumar, K.V., Notarangelo, F.M., Thomas, M.A., Tararina, M., Wu, H.Q., Schwarcz, R., Muchowski, P.J., Targeted deletion of kynurenine 3-monooxygenase in mice: a new tool for studying kynurenine pathway metabolism in periphery and brain. J. Biol. Chem. 288 (2013), 36554–36566.
44. [44] Foster, A.C., White, R.J., Schwarcz, R., Synthesis of quinolinic acid by 3-hydroxyanthranilic acid oxygenase in rat brain tissue in vitro. J. Neurochem. 47 (1986), 23–30.
45. [45] Okuno, E., Schmidt, W., Parks, D.A., Nakamura, M., Schwarcz, R., Measurement of rat brain kynurenine aminotransferase at physiological kynurenine concentrations. J. Neurochem. 57 (1991), 533–540.
46. [46] Notarangelo, F.M., Wu, H.Q., Macherone, A., Graham, D.R., Schwarcz, R., Gas chromatography/tandem mass spectrometry detection of extracellular kynurenine and related metabolites in normal and lesioned rat brain. Anal. Biochem. 421 (2012), 573–581.
47. [48] Shibata, K., Fluorimetric micro-determination of kynurenic acid, an endogenous blocker of neurotoxicity, by high-performance liquid chromatography. J. Chromatogr. 430 (1988), 376–380.
48. [49] Pabinger, S., Thallinger, G.G., Snajder, R., Eichhorn, H., Rader, R., Trajanoski, Z., QPCR: application for real-time PCR data management and analysis. BMC Bioinf., 10, 2009, 268.
49. [50] Leklem, J.E., Quantitative aspects of tryptophan metabolism in humans and other species: a review. Am. J. Clin. Nutr. 24 (1971), 659–672.
50. [51] Németh, H., Toldi, J., Vécsei, L., Role of kynurenines in the central and peripheral nervous systems. Curr. Neurovasc. Res. 2 (2005), 249–260.
51. [52] Moroni, F., Cozzi, A., Sili, M., Mannaioni, G., Kynurenic acid: a metabolite with multiple actions and multiple targets in brain and periphery. J. Neural Transm. 119 (2012), 133–139.
52. [53] Badawy, A.A., Tryptophan metabolism, disposition and utilization in pregnancy. Biosci. Rep., 35, 2015.
53. [54] Vyboh, K., Jenabian, M.A., Mehraj, V., Routy, J.P., HIV and the gut microbiota, partners in crime: breaking the vicious cycle to unearth new therapeutic targets. J. Immunol. Res., 2015, 2015, 614127.
54. [55] Baran, H., Schwarcz, R., Presence of 3-hydroxyanthranilic acid in rat tissues and evidence for its production from anthranilic acid in the brain. J. Neurochem. 55 (1990), 738–744.
55. [56] Clark, C.J., Mackay, G.M., Smythe, G.A., Bustamante, S., Stone, T.W., Phillips, R.S., Prolonged survival of a murine model of cerebral malaria by kynurenine pathway inhibition. Infect. Immun. 73 (2005), 5249–5251.
56. [57] Terakata, M., Fukuwatari, T., Kadota, E., Sano, M., Kanai, M., Nakamura, T., Funakoshi, H., Shibata, K., The niacin required for optimum growth can be synthesized from L-tryptophan in growing mice lacking tryptophan-2,3-dioxygenase. J. Nutr. 143 (2013), 1046–1051.
57. [58] Saito, K., Markey, S.P., Heyes, M.P., Effects of immune activation on quinolinic acid and neuroactive kynurenines in the mouse. Neuroscience 51 (1992), 25–39.
58. [59] 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. Psychiatry 14 (2009), 511–522.
59. [60] Walker, A.K., Budac, D.P., Bisulco, S., Lee, A.W., Smith, R.A., Beenders, B., Kelley, K.W., Dantzer, R., NMDA receptor blockade by ketamine abrogates lipopolysaccharide-induced depressive-like behavior in C57BL/6J mice. Neuropsychopharmacology 38 (2013), 1609–1616.
60. [61] Campesan, S., Green, E.W., Breda, C., Sathyasaikumar, K.V., Muchowski, P.J., Schwarcz, R., Kyriacou, C.P., Giorgini, F., The kynurenine pathway modulates neurodegeneration in a Drosophila model of Huntington's disease. Curr. Biol. 21 (2011), 961–966.
61. [62] Stephens, G.L., Wang, Q., Swerdlow, B., Bhat, G., Kolbeck, R., Fung, M., Kynurenine 3-monooxygenase mediates inhibition of Th17 differentiation via catabolism of endogenous aryl hydrocarbon receptor ligands. Eur. J. Immunol. 43 (2013), 1727–1734.
62. [63] Forrest, C.M., McNair, K., Pisar, M., Khalil, O.S., Darlington, L.G., Stone, T.W., Altered hippocampal plasticity by prenatal kynurenine administration, kynurenine-3-monoxygenase (KMO) deletion or galantamine. Neuroscience 310 (2015), 91–105.
63. [64] Parrott, J.M., O'Connor, J.C., Kynurenine 3-monooxygenase: an influential mediator of neuropathology. Front Psychiatry, 6, 2015, 116.
64. [65] Heyes, M.P., Achim, C.L., Wiley, C.A., Major, E.O., Saito, K., Markey, S.P., Human microglia convert L-tryptophan into the neurotoxin quinolinic acid. Biochem. J. 320 (1996), 595–597.
65. [66] Guillemin, G.J., Kerr, S.J., Smythe, G.A., Smith, D.G., Kapoor, V., Armati, P.J., Croitoru, J., Brew, B.J., Kynurenine pathway metabolism in human astrocytes: a paradox for neuronal protection. J. Neurochem. 78 (2001), 842–853.
66. [67] van der Goot, A.T., Zhu, W., Vazquez-Manrique, R.P., Seinstra, R.I., Dettmer, K., Michels, H., Farina, F., Krijnen, J., Melki, R., Buijsman, R.C., Ruiz Silva, M., Thijssen, K.L., Kema, I.P., Neri, C., Oefner, P.J., Nollen, E.A., Delaying aging and the aging-associated decline in protein homeostasis by inhibition of tryptophan degradation. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 14912–14917.
67. [68] Okuda, S., Nishiyama, N., Saito, H., Katsuki, H., Hydrogen peroxide-mediated neuronal cell death induced by an endogenous neurotoxin, 3-hydroxykynurenine. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 12553–12558.
68. [69] Forrest, C.M., Mackay, G.M., Stoy, N., Egerton, M., Christofides, J., Stone, T.W., Darlington, L.G., Tryptophan loading induces oxidative stress. Free Radic. Res. 38 (2004), 1167–1171.
69. [70] Lugo-Huitron, R., Blanco-Ayala, T., Ugalde-Muniz, P., Carrillo-Mora, P., Pedraza-Chaverri, J., Silva-Adaya, D., Maldonado, P.D., Torres, I., Pinzon, E., Ortiz-Islas, E., Lopez, T., Garcia, E., Pineda, B., Torres-Ramos, M., Santamaria, A., Perez-De La Cruz, V.P., On the antioxidant properties of kynurenic acid: free radical scavenging activity and inhibition of oxidative stress. Neurotoxicol. Teratol. 33 (2011), 538–547.
70. [71] Perez-De La Cruz, V., Carrillo-Mora, P., Santamaria, A., Quinolinic acid, an endogenous molecule combining excitotoxicity, oxidative stress and other toxic mechanisms. Int. J. Tryptophan Res. 5 (2012), 1–8.
71. [72] Heath-Pagliuso, S., Rogers, W.J., Tullis, K., Seidel, S.D., Cenijn, P.H., Brouwer, A., Denison, M.S., Activation of the Ah receptor by tryptophan and tryptophan metabolites. Biochemistry (Mosc) 37 (1998), 11508–11515.
72. [73] Mezrich, J.D., Fechner, J.H., Zhang, X., Johnson, B.P., Burlingham, W.J., Bradfield, C.A., An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J. Immunol. 185 (2010), 3190–3198.
73. [74] Opitz, C.A., Litzenburger, U.M., Sahm, F., Ott, M., Tritschler, I., Trump, S., Schumacher, T., Jestaedt, L., Schrenk, D., Weller, M., Jugold, M., Guillemin, G.J., Miller, C.L., Lutz, C., Radlwimmer, B., Lehmann, I., von Deimling, A., Wick, W., Platten, M., An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 478 (2011), 197–203.
74. [75] Stone, T.W., Stoy, N., Darlington, L.G., An expanding range of targets for kynurenine metabolites of tryptophan. Trends Pharmacol. Sci. 34 (2013), 136–143.
75. [76] Fazio, F., Lionetto, L., Molinaro, G., Bertrand, H.O., Acher, F., Ngomba, R.T., Notartomaso, S., Curini, M., Rosati, O., Scarselli, P., Di Marco, R., Battaglia, G., Bruno, V., Simmaco, M., Pin, J.P., Nicoletti, F., Goudet, C., Cinnabarinic acid, an endogenous metabolite of the kynurenine pathway, activates type 4 metabotropic glutamate receptors. Mol. Pharmacol. 81 (2012), 643–656.
76. [77] Copeland, C.S., Neale, S.A., Salt, T.E., Actions of xanthurenic acid, a putative endogenous group II metabotropic glutamate receptor agonist, on sensory transmission in the thalamus. Neuropharmacology 66 (2013), 133–142.
77. [78] Taleb, O., Maammar, M., Brumaru, D., Bourguignon, J.J., Schmitt, M., Klein, C., Kemmel, V., Maitre, M., Mensah-Nyagan, A.G., Xanthurenic acid binds to neuronal G-protein-coupled receptors that secondarily activate cationic channels in the cell line NCB-20. PLoS One, 7, 2012, e48553.
78. [79] Ohira, K., Hagihara, H., Toyama, K., Takao, K., Kanai, M., Funakoshi, H., Nakamura, T., Miyakawa, T., Expression of tryptophan 2,3-dioxygenase in mature granule cells of the adult mouse dentate gyrus. Mol. Brain, 3, 2010, 26.
79. [80] Maeta, A., Fukuwatari, T., Funakoshi, H., Nakamura, T., Shibata, K., Tryptophan-restriction diets help to maintain L-tryptophan homeostasis in tryptophan 2,3-dioxygenase knockout mice. Int. J. Tryptophan Res. 6 (2013), 55–65.
80. [81] Bessede, A., Gargaro, M., Pallotta, M.T., Matino, D., Servillo, G., Brunacci, C., Bicciato, S., Mazza, E.M., Macchiarulo, A., Vacca, C., Iannitti, R., Tissi, L., Volpi, C., Belladonna, M.L., Orabona, C., Bianchi, R., Lanz, T.V., Platten, M., Della Fazia, M.A., Piobbico, D., Zelante, T., Funakoshi, H., Nakamura, T., Gilot, D., Denison, M.S., Guillemin, G.J., DuHadaway, J.B., Prendergast, G.C., Metz, R., Geffard, M., Boon, L., Pirro, M., Iorio, A., Veyret, B., Romani, L., Grohmann, U., Fallarino, F., Puccetti, P., Aryl hydrocarbon receptor control of a disease tolerance defence pathway. Nature 511 (2014), 184–190.
81. [82] Potula, R., Poluektova, L., Knipe, B., Chrastil, J., Heilman, D., Dou, H., Takikawa, O., Munn, D.H., Gendelman, H.E., Persidsky, Y., Inhibition of indoleamine 2,3-dioxygenase (IDO) enhances elimination of virus-infected macrophages in an animal model of HIV-1 encephalitis. Blood 106 (2005), 2382–2390.
82. [83] Fox, J.M., Sage, L.K., Huang, L., Barber, J., Klonowski, K.D., Mellor, A.L., Tompkins, S.M., Tripp, R.A., Inhibition of indoleamine 2,3-dioxygenase enhances the T-cell response to influenza virus infection. J. Gen. Virol. 94 (2013), 1451–1461.
83. [84] Prendergast, G.C., Smith, C., Thomas, S., Mandik-Nayak, L., Laury-Kleintop, L., Metz, R., Muller, A.J., Indoleamine 2,3-dioxygenase pathways of pathogenic inflammation and immune escape in cancer. Cancer Immunol. Immunother. 63 (2014), 721–735.
84. [85] Chang, M.Y., Smith, C., DuHadaway, J.B., Pyle, J.R., Boulden, J., Soler, A.P., Muller, A.J., Laury-Kleintop, L.D., Prendergast, G.C., Cardiac and gastrointestinal liabilities caused by deficiency in the immune modulatory enzyme indoleamine 2,3-dioxygenase. Cancer Biol. Ther. 12 (2011), 1050–1058.
85. [86] Murakami, Y., Hoshi, M., Hara, A., Takemura, M., Arioka, Y., Yamamoto, Y., Matsunami, H., Funato, T., Seishima, M., Saito, K., Inhibition of increased indoleamine 2,3-dioxygenase activity attenuates toxoplasma gondii replication in the lung during acute infection. Cytokine 59 (2012), 245–251.
86. [87] Nagano, J., Shimizu, M., Hara, T., Shirakami, Y., Kochi, T., Nakamura, N., Ohtaki, H., Ito, H., Tanaka, T., Tsurumi, H., Saito, K., Seishima, M., Moriwaki, H., Effects of indoleamine 2,3-dioxygenase deficiency on high-fat diet-induced hepatic inflammation. PLoS One, 8, 2013, e73404.
87. [88] 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. 441 (2008), 29–34.
88. [89] Corona, A.W., Huang, Y., O'Connor, J.C., Dantzer, R., Kelley, K.W., Popovich, P.G., Godbout, J.P., Fractalkine receptor (CX3CR1) deficiency sensitizes mice to the behavioral changes induced by lipopolysaccharide. J. Neuroinflammation, 7, 2010, 93.
89. [90] Andre, C., O'Connor, J.C., Kelley, K.W., Lestage, J., Dantzer, R., Castanon, N., Spatio-temporal differences in the profile of murine brain expression of proinflammatory cytokines and indoleamine 2,3-dioxygenase in response to peripheral lipopolysaccharide administration. J. Neuroimmunol. 200 (2008), 90–99.
90. [91] 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. 82 (2002), 258–268.
91. [92] Glass, C.K., Saijo, K., Winner, B., Marchetto, M.C., Gage, F.H., Mechanisms underlying inflammation in neurodegeneration. Cell 140 (2010), 918–934.