The tryptophan metabolism enzyme L-kynureninase is a novel inflammatory factor in psoriasis and other inflammatory diseases

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 6, 2016, Pages 1830-1840

  Harden, Jamie L ^a   Lewis, Steven M ^a   Lish, Samantha R ^a   Suárez Fariñas, Mayte ^a,c   Gareau, Daniel ^a   Lentini, Tim ^a   Johnson Huang, Leanne M ^a   Krueger, James G ^a   Lowes, Michelle A ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

inflammation; L kynureninase; Psoriasis vulgaris; tryptophan metabolism

Indexed keywords

CXCL1 CHEMOKINE; CYTOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; ETANERCEPT; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 23P40; INTERLEUKIN 8; KYNURENINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TRYPTOPHAN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; USTEKINUMAB; VASCULAR CELL ADHESION MOLECULE 1; AUTACOID; HYDROLASE;

ARTICLE; ATOPIC DERMATITIS; BIOLOGICAL THERAPY; BONE MARROW CELL; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; DATA MINING; DERMATITIS; DISEASE SEVERITY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOLOGY; INFLAMMATION; META ANALYSIS (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS; SIGNAL TRANSDUCTION; SKIN BIOPSY; TRYPTOPHAN METABOLISM; UPREGULATION; BIOPSY; CELL CULTURE; FEMALE; GENE EXPRESSION PROFILING; GENETICS; MALE; METABOLISM; PATHOLOGY; SKIN;

BIOPSY; CELLS, CULTURED; DERMATITIS, ATOPIC; FEMALE; GENE EXPRESSION PROFILING; HUMANS; HYDROLASES; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; METABOLIC NETWORKS AND PATHWAYS; MYELOID CELLS; PSORIASIS; SKIN; TRYPTOPHAN;

EID: 84950987524     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.09.055     Document Type: Article

References (50)

1. M.A. Lowes, M. Suarez-Farinas, and J.G. Krueger Immunology of psoriasis Annu Rev Immunol 32 2014 227
2. G.K. Perera, P. Di Meglio, and F.O. Nestle Psoriasis Annu Rev Pathol 7 2012 385
3. M.A. Lowes, A.M. Bowcock, and J.G. Krueger Pathogenesis and therapy of psoriasis Nature 445 2007 866
4. B.B. Davidovici, N. Sattar, J. Prinz, L. Puig, P. Emery, J.N. Barker, and et al. Psoriasis and systemic inflammatory diseases: potential mechanistic links between skin disease and co-morbid conditions J Invest Dermatol 130 2010 1785 1796
5. J.E. Gudjonsson, J. Ding, A. Johnston, T. Tejasvi, A.M. Guzman, R.P. Nair, and et al. Assessment of the psoriatic transcriptome in a large sample: additional regulated genes and comparisons with in vitro models J Invest Dermatol 130 2010 1829 1840
6. S. Tian, J.G. Krueger, K. Li, A. Jabbari, C. Brodmerkel, M.A. Lowes, and et al. Meta-analysis derived (MAD) transcriptome of psoriasis defines the "core" pathogenesis of disease PLoS One 7 2012 e44274
7. H. Mitsui, M. Suárez-Fariñas, D.A. Belkin, N. Levenkova, J. Fuentes-Duculan, I. Coats, and et al. Combined use of laser capture microdissection and cDNA microarray analysis identifies locally expressed disease-related genes in focal regions of psoriasis vulgaris skin lesions J Invest Dermatol 132 2012 1615 1626
8. M. Ito, K. Ogawa, K. Takeuchi, A. Nakada, M. Heishi, H. Suto, and et al. Gene expression of enzymes for tryptophan degradation pathway is upregulated in the skin lesions of patients with atopic dermatitis or psoriasis J Dermatol Sci 36 2004 157 164
9. E.D. Roberson, Y. Liu, C. Ryan, C.E. Joyce, S. Duan, L. Cao, and et al. A subset of methylated CpG sites differentiate psoriatic from normal skin J Invest Dermatol 132 2012 583 592
10. M. Suarez-Farinas, J. Fuentes-Duculan, M.A. Lowes, and J.G. Krueger Resolved psoriasis lesions retain expression of a subset of disease-related genes J Invest Dermatol 131 2011 391 400
11. A. Chiricozzi, E. Guttman-Yassky, M. Suárez-Fariñas, K.E. Nograles, S. Tian, I. Cardinale, and et al. Integrative responses to IL-17 and TNF-alpha in human keratinocytes account for key inflammatory pathogenic circuits in psoriasis J Invest Dermatol 131 2011 677 687
12. M. Suarez-Farinas, M.A. Lowes, L.C. Zaba, and J.G. Krueger Evaluation of the psoriasis transcriptome across different studies by gene set enrichment analysis (GSEA) PLoS One 5 2010 e10247
13. J.L. Harden, and N.K. Egilmez Indoleamine 2,3-dioxygenase and dendritic cell tolerogenicity Immunol Invest 41 2012 738 764
14. D.H. Munn, M. Zhou, J.T. Attwood, I. Bondarev, S.J. Conway, B. Marshall, and et al. Prevention of allogeneic fetal rejection by tryptophan catabolism Science 281 1998 1191 1193
15. F. Fallarino, U. Grohmann, S. You, B.C. McGrath, D.R. Cavener, C. Vacca, and 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 J Immunol 176 2006 6752 6761
16. G.C. Prendergast, C. Smith, S. Thomas, L. Mandik-Nayak, L. Laury-Kleintop, R. Metz, and et al. Indoleamine 2,3-dioxygenase pathways of pathogenic inflammation and immune escape in cancer Cancer Immunol Immunother 63 2014 721 735
17. A.L. Mellor, and D.H. Munn Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol Today 20 1999 469 473
18. J.D. Mezrich, J.H. Fechner, X. Zhang, B.P. Johnson, W.J. Burlingham, and C.A. Bradfield An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells J Immunol 185 2010 3190 3198
19. W. Julliard, J.H. Fechner, and J.D. Mezrich The aryl hydrocarbon receptor meets immunology: friend or foe? A little of both Front Immunol 5 2014 458
20. C.J. Darcy, J.S. Davis, T. Woodberry, Y.R. McNeil, D.P. Stephens, T.W. Yeo, and et al. An observational cohort study of the kynurenine to tryptophan ratio in sepsis: association with impaired immune and microvascular function PLoS One 6 2011 e21185
21. N. Gulati, M. Suárez-Fariñas, J. Fuentes-Duculan, P. Gilleaudeau, M. Sullivan-Whalen, J. Correa da Rosa, and et al. Molecular characterization of human skin response to diphencyprone at peak and resolution phases: therapeutic insights J Invest Dermatol 134 2014 2531 2540
22. J.L. Harden, T. Gu, M.O. Kilinc, R.B. Rowswell-Turner, L.P. Virtuoso, and N.K. Egilmez Dichotomous effects of IFN-γ on dendritic cell function determine the extent of IL-12-driven antitumor T cell immunity J Immunol 187 2011 126 132
23. T. Gu, R.B. Rowswell-Turner, M.O. Kilinc, and N.K. Egilmez Central role of IFNgamma-indoleamine 2,3-dioxygenase axis in regulation of interleukin-12-mediated antitumor immunity Cancer Res 70 2010 129 138
24. J. Fuentes-Duculan, M. Suárez-Fariñas, L.C. Zaba, K.E. Nograles, K.C. Pierson, H. Mitsui, and et al. A subpopulation of CD163-positive macrophages is classically activated in psoriasis J Invest Dermatol 130 2010 2412 2422
25. J.L. Harden, S.M. Lewis, K.C. Pierson, M. Suárez-Fariñas, T. Lentini, F.S. Ortenzio, and et al. CARD14 expression in dermal endothelial cells in psoriasis PLoS One 9 2014 e111255
26. L.M. Johnson-Huang, M. Suárez-Fariñas, M. Sullivan-Whalen, P. Gilleaudeau, J.G. Krueger, and M.A. Lowes Effective narrow-band UVB radiation therapy suppresses the IL-23/IL-17 axis in normalized psoriasis plaques J Invest Dermatol 130 2010 2654 2663
27. M. Kennedy-Crispin, E. Billick, H. Mitsui, N. Gulati, H. Fujita, P. Gilleaudeau, and et al. Human keratinocytes' response to injury upregulates CCL20 and other genes linking innate and adaptive immunity J Invest Dermatol 132 2012 105 113
28. W. Daubener, S.K. Schmidt, K. Heseler, K.H. Spekker, and C.R. MacKenzie Antimicrobial and immunoregulatory effector mechanisms in human endothelial cells. Indoleamine 2,3-dioxygenase versus inducible nitric oxide synthase Thromb Haemost 102 2009 1110 1116
29. Y. Wang, H. Liu, G. McKenzie, P.K. Witting, J.P. Stasch, M. Hahn, and et al. Kynurenine is an endothelium-derived relaxing factor produced during inflammation Nat Med 16 2010 279 285 [published erratum in: 2010;16:607]
30. L. Asp, A.S. Johansson, A. Mann, B. Owe-Larsson, E.M. Urbanska, T. Kocki, and et al. Effects of pro-inflammatory cytokines on expression of kynurenine pathway enzymes in human dermal fibroblasts J Inflamm (Lond) 8 2011 25
31. M.A. Lowes, F. Chamian, M.V. Abello, J. Fuentes-Duculan, S.L. Lin, R. Nussbaum, and et al. Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a) Proc Natl Acad Sci U S A 102 2005 19057 19062
32. L.C. Zaba, J.G. Krueger, and M.A. Lowes Resident and "inflammatory" dendritic cells in human skin J Invest Dermatol 129 2009 302 308
33. L.C. Zaba, M. Suárez-Fariñas, J. Fuentes-Duculan, K.E. Nograles, E. Guttman-Yassky, I. Cardinale, and et al. Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes J Allergy Clin Immunol 124 2009 1022
34. T.W. Stone, and L.G. Darlington Endogenous kynurenines as targets for drug discovery and development Nat Rev Drug Discov 1 2002 609 620
35. J.D. Hamilton, M. Suárez-Fariñas, N. Dhingra, I. Cardinale, X. Li, A. Kostic, and et al. Dupilumab improves the molecular signature in skin of patients with moderate-to-severe atopic dermatitis J Allergy Clin Immunol 134 2014 1293 1300
36. J.M. Jensen, A. Scherer, C. Wanke, M. Bräutigam, S. Bongiovanni, M. Letzkus, and et al. Gene expression is differently affected by pimecrolimus and betamethasone in lesional skin of atopic dermatitis Allergy 67 2012 413 423
37. E. Kwidzinski, and I. Bechmann IDO expression in the brain: a double-edged sword J Mol Med (Berl) 85 2007 1351 1359
38. Y. Chen, R. Stankovic, K.M. Cullen, V. Meininger, B. Garner, S. Coggan, and et al. The kynurenine pathway and inflammation in amyotrophic lateral sclerosis Neurotox Res 18 2010 132 142
39. L. Vecsei, L. Szalardy, F. Fulop, and J. Toldi Kynurenines in the CNS: recent advances and new questions Nat Rev Drug Discov 12 2013 64 82
40. R. Carruthers Low tryptophan diet in the treatment of psoriasis Med J Aust 1 1968 493 495
41. H. Spiera, and A.M. Lefkovits Remission of psoriasis with low dietary tryptophan Lancet 2 1967 137 139
42. J.E. Gudjonsson, J. Ding, X. Li, R.P. Nair, T. Tejasvi, Z.S. Qin, and et al. Global gene expression analysis reveals evidence for decreased lipid biosynthesis and increased innate immunity in uninvolved psoriatic skin J Invest Dermatol 129 2009 2795 2804
43. R. Dantzer, J.C. O'Connor, G.G. Freund, R.W. Johnson, and K.W. Kelley From inflammation to sickness and depression: when the immune system subjugates the brain Nat Rev Neurosci 9 2008 46 56
44. E.A. Dowlatshahi, M. Wakkee, L.R. Arends, and T. Nijsten The prevalence and odds of depressive symptoms and clinical depression in psoriasis patients: a systematic review and meta-analysis J Invest Dermatol 134 2014 1542 1551
45. L. Riol-Blanco, J. Ordovas-Montanes, M. Perro, E. Naval, A. Thiriot, D. Alvarez, and et al. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation Nature 510 2014 157 161
46. M. Colonna AHR: making the keratinocytes thick skinned Immunity 40 2014 863 864
47. J.S. Lee, M. Cella, K.G. McDonald, C. Garlanda, G.D. Kennedy, M. Nukaya, and et al. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch Nat Immunol 13 2012 144 151
48. C.A. Opitz, U.M. Litzenburger, F. Sahm, M. Ott, I. Tritschler, S. Trump, and et al. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor Nature 478 2011 197 203
49. F.J. Quintana, A.S. Basso, A.H. Iglesias, T. Korn, M.F. Farez, E. Bettelli, and et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor Nature 453 2008 65 71
50. P. Di Meglio, J.H. Duarte, H. Ahlfors, N.D. Owens, Y. Li, F. Villanova, and et al. Activation of the aryl hydrocarbon receptor dampens the severity of inflammatory skin conditions Immunity 40 2014 989 1001