Indoleamine 2,3-dioxygenase expression in patients with allergic rhinitis: a case-control study

Clinical and Translational Allergy

Sanna Toppila-Salmi²  Timo Paavonen⁵  Mikko Lehtonen³  Teemu Honkanen¹  Jussi Karjalainen⁶  Annika Luukkainen⁴ 

[1] Department of Pathology, University of Tampere, Tampere, Finland;Transplantation laboratory, Haartman Institute, University of Helsinki, Helsinki, Finland;Department of Otorhinolaryngology, Kanta-Hame Central Hospital, Hameenlinna, Finland;Department of Otorhinolaryngology, University of Tampere, Tampere, Finland;Department of Pathology, Centre for Laboratory Medicine, Tampere University Hospital, Tampere, Finland;Allergy Centre, Tampere University Hospital, Tampere, Finland

关键词: eosinophil;    leukocyte;    interferon gamma;    kynurenine;    tryptophan;    dendritic cell;    birch pollen;    allergic rhinitis;    Indoleamine 2,3-dioxygenase;   

Others  :  794724
DOI  :  10.1186/2045-7022-1-17

 received in 2011-11-14, accepted in 2011-12-12,  发布年份 2011

【 摘 要 】

Background

Indoleamine 2,3-dioxygenase (IDO) is a tryptophan catalyzing enzyme. It has been suggested that it has a role in lower airway allergic inflammations, but its role in allergic rhinitis has not been investigated.

Objective

Our aim was to evaluate the expression of IDO in the nasal mucosa of allergic rhinitis patients allergic to birch pollen during peak exposure to birch pollen allergen and compare it to non-atopic patients.

Methods

IDO expression was immunohistochemically evaluated from nasal specimens obtained in- and off-season from otherwise healthy non-smoking volunteers both allergic to birch pollen (having mild or moderate allergic rhinoconjunctivitis) and non-allergic controls. Results: The IDO expression levels were low in healthy controls and remained low also in patients allergic to birch pollen. There were no differences in the expression of IDO in- and off-season in either healthy or allergic subjects.

Conclusions

There is a controversy in the role of IDO in upper and lower airways during allergic airway disease. It seems that IDO is associated to allergic inflammations of the lower airways, but does not have a local role in the nasal cavity at least in mild or moderate forms of allergic rhinitis.

【 授权许可】

   
2011 Luukkainen et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Moffett JR, Namboodiri MA: Tryptophan and the immune response. Immunol Cell Biol 2003, 81:247-65.
• [2]Xu H, Oriss TB, Fei M, et al.: Indoleamine 2,3-dioxygenase in lung dendritic cells promotes Th2 responses and allergic inflammation. Proc Natl Acad Sci USA 2008, 105:6690-5.
• [3]Yoshida R, Urade Y, Tokuda M, Hayaishi O: Induction of indoleamine 2,3-dioxygenase in mouse lung during virus infection. Proc Natl Acad Sci USA 1979, 76:4084-6.
• [4]Daubener W, MacKenzie CR: IFN-gamma activated indoleamine 2,3-dioxygenase activity in human cells is an antiparasitic and an antibacterial effector mechanism. Adv Exp Med Biol 1999, 467:517-24.
• [5]von Bubnoff D, Hanau D, Wenzel J, Takikawa O, Hall B, Koch S, Bieber T: Indoleamine 2,3-dioxygenase-expressing antigen-presenting cells and peripheral T-cell tolerance: another piece to the atopic puzzle? J Allergy Clin Immunol 2003, 112:854-60.
• [6]van der Marel AP, Samsom JN, Greuter M, van Berkel LA, O'Toole T, Kraal G, Mebius RE: Blockade of IDO inhibits nasal tolerance induction. J Immunol 2007, 179:894-900.
• [7]Chen W, Liang X, Peterson AJ, Munn DH, Blazar BR: The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol 2008, 181:5396-404.
• [8]Taher YA, Piavaux BJ, Gras R, et al.: Indoleamine 2,3-dioxygenase-dependent tryptophan metabolites contribute to tolerance induction during allergen immunotherapy in a mouse model. J Allergy Clin Immunol 2008, 121:983. 91.e2
• [9]Brenk M, Scheler M, Koch S, et al.: Tryptophan deprivation induces inhibitory receptors ILT3 and ILT4 on dendritic cells favoring the induction of human CD4+CD25+ Foxp3+ T regulatory cells. J Immunol 2009, 183:145-54.
• [10]Onodera T, Jang MH, Guo Z, et al.: Constitutive expression of IDO by dendritic cells of mesenteric lymph nodes: functional involvement of the CTLA-4/B7 and CCL22/CCR4 interactions. J Immunol 2009, 183:5608-14.
• [11]Xu H, Zhang GX, Ciric B, Rostami A: IDO: a double-edged sword for T(H)1/T(H)2 regulation. Immunol Lett 2008, 121:1-6.
• [12]Grohmann U, Volpi C, Fallarino F, et al.: Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat Med 2007, 13:579-86.
• [13]Hayashi T, Beck L, Rossetto C, et al.: Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J Clin Invest 2004, 114:270-9.
• [14]Gordon JR, Li F, Nayyar A, Xiang J, Zhang X: CD8 alpha+, but not CD8 alpha-, dendritic cells tolerize Th2 responses via contact-dependent and -independent mechanisms, and reverse airway hyperresponsiveness, Th2, and eosinophil responses in a mouse model of asthma. J Immunol 2005, 175:1516-22.
• [15]Maneechotesuwan K, Wamanuttajinda V, Kasetsinsombat K, Huabprasert S, Yaikwawong M, Barnes PJ, Wongkajornsilp A: Der p 1 suppresses indoleamine 2, 3-dioxygenase in dendritic cells from house dust mite-sensitive patients with asthma. J Allergy Clin Immunol 2009, 123:239-48.
• [16]Forsythe P, Inman MD, Bienenstock J: Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med 2007, 175:561-9.
• [17]Wolf AM, Wolf D, Rumpold H, et al.: Overexpression of indoleamine 2,3-dioxygenase in human inflammatory bowel disease. Clin Immunol 2004, 113:47-55.
• [18]Torres MI, Lopez-Casado MA, Lorite P, Rios A: Tryptophan metabolism and indoleamine 2,3-dioxygenase expression in coeliac disease. Clin Exp Immunol 2007, 148:419-24.
• [19]Joenvaara S, Mattila P, Renkonen J, et al.: Caveolar transport through nasal epithelium of birch pollen allergen Bet v 1 in allergic patients. J Allergy Clin Immunol 2009, 124:135. 142.e1-21
• [20]Paveglio SA, Allard J, Foster Hodgkins SR, et al.: Airway epithelial indoleamine 2,3-dioxygenase inhibits CD4+ T cells during Aspergillus fumigatus antigen exposure. Am J Respir Cell Mol Biol 2011, 44:11-23.
• [21]von Bubnoff D, Fimmers R, Bogdanow M, Matz H, Koch S, Bieber T: Asymptomatic atopy is associated with increased indoleamine 2,3-dioxygenase activity and interleukin-10 production during seasonal allergen exposure. Clin Exp Allergy 2004, 34:1056-63.
• [22]Maneechotesuwan K, Supawita S, Kasetsinsombat K, Wongkajornsilp A, Barnes PJ: Sputum indoleamine-2, 3-dioxygenase activity is increased in asthmatic airways by using inhaled corticosteroids. J Allergy Clin Immunol 2008, 121:43-50.
• [23]Araujo E, Palombini BC, Cantarelli V, Pereira A, Mariante A: Microbiology of middle meatus in chronic rhinosinusitis. Am J Rhinol 2003, 17:9-15.
• [24]Dai X, Zhu BT: Indoleamine 2,3-dioxygenase tissue distribution and cellular localization in mice: implications for its biological functions. J Histochem Cytochem 2010, 58:17-28.
• [25]Ball HJ, Sanchez-Perez A, Weiser S, et al.: Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene 2007, 396:203-13.
• [26]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 Res 2007, 67:7082-7.
• [27]Lob S, Konigsrainer A, Zieker D, Brucher BL, Rammensee HG, Opelz G, Terness P: IDO1 and IDO2 are expressed in human tumors: levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol Immunother 2009, 58:153-7.
• [28]Busse WW: The role of allergy in disease. Immunol Rev 2011, 242:5-9.
• [29]An XJ, Bai CX, Xia JB, Dang T, Qian P, Qian GS, Liao W: Immature dendritic cells expressing indoleamine 2, 3-dioxygenase suppress ovalbumin-induced allergic airway inflammation in mice. J Investig Allergol Clin Immunol 2011, 21:185-92.