Phthalate Ester-induced Thymic Stromal Lymphopoietin Mediates Allergic Dermatitis in Mice

Overview

Journal Immunology

Specialty Allergy & Immunology

Date 2009 Sep 11

PMID 19740346

Citations 13

Authors

Tomomi Shigeno

Mayako Katakuse

Tomoyuki Fujita

Yohei Mukoyama

Hideki Watanabe

Affiliations

Soon will be listed here.

Abstract

Recently air pollutants and irritants have been labelled as possible exogenous risk factors for allergic disorders. Although the underlying causes of allergic disorders such as atopic dermatitis and asthma remain unclear, the T helper type 2 (Th2) cell-mediated allergic inflammatory cascade may contribute to their pathogenesis. In the last decade, it has been documented that one of the candidates for triggering Th2 commitment is thymic stromal lymphopoietin (TSLP), the expression of which is up-regulated in the lesions of allergic patients. Here, we describe TSLP function in a fluorescein isothiocyanate (FITC) -induced contact hypersensitivity (CHS) model. A cytokine profile indicated that the model was dominantly mediated by the Th2 milieu. Interestingly, TSLP was increased in the skin during the sensitization phase when stimulated by a solvent, dibutyl phthalate (DBP), but not by FITC hapten or another solvent, acetone. Ear swelling in FITC-induced CHS was totally abrogated by removing DBP from the sensitization or elicitation phase, and was restored by complementary injection of TSLP. Inversely, the ear swelling was suppressed by injection of small interfering RNA against TSLP during the sensitization phase, which was concomitant with decreasing expression of interleukin-4 at the swollen skin site. Taken together, DBP-induced TSLP during the sensitization phase plays a role in establishing FITC-induced CHS and may be one of the causes of Th2 commitment in the model, suggesting that certain environmental toxins, such as DBP, may endow pro-allergic and atopic predisposition in humans or animals.

Citing Articles

Expression of Thymic Stromal Lymphopoietin in Immune-Related Dermatoses.

Li S, Jin X, Shan Y, Jin H, Zuo Y Mediators Inflamm. 2022; 2022:9242383.

PMID: 36046760 PMC: 9420647. DOI: 10.1155/2022/9242383.

The Gastrointestinal Helminth Suppresses Inflammation in a Model of Contact Hypersensitivity.

Filbey K, Mehta P, Meijlink K, Pellefigues C, Schmidt A, Le Gros G Front Immunol. 2020; 11:950.

PMID: 32508831 PMC: 7249854. DOI: 10.3389/fimmu.2020.00950.

Associations between prenatal maternal urinary concentrations of personal care product chemical biomarkers and childhood respiratory and allergic outcomes in the CHAMACOS study.

Berger K, Eskenazi B, Balmes J, Holland N, Calafat A, Harley K Environ Int. 2018; 121(Pt 1):538-549.

PMID: 30293015 PMC: 6239199. DOI: 10.1016/j.envint.2018.09.027.

A multistrain probiotic formulation attenuates skin symptoms of atopic dermatitis in a mouse model through the generation of CD4Foxp3 T cells.

Shin J, Chung M, Seo J Food Nutr Res. 2016; 60:32550.

PMID: 27802847 PMC: 5090133. DOI: 10.3402/fnr.v60.32550.

The Impact of Bisphenol A and Phthalates on Allergy, Asthma, and Immune Function: a Review of Latest Findings.

Robinson L, Miller R Curr Environ Health Rep. 2015; 2(4):379-87.

PMID: 26337065 PMC: 4626318. DOI: 10.1007/s40572-015-0066-8.

References

Sinke J, Rutten V, Willemse T . Immune dysregulation in atopic dermatitis. Vet Immunol Immunopathol. 2002; 87(3-4):351-6. DOI: 10.1016/s0165-2427(02)00066-1. View

Nielsen G, Larsen S, Olsen O, Lovik M, Poulsen L, Glue C . Do indoor chemicals promote development of airway allergy?. Indoor Air. 2007; 17(3):236-55. DOI: 10.1111/j.1600-0668.2006.00468.x. View

Maruyama T, Shiba T, Iizuka H, Matsuda T, Kurohane K, Imai Y . Effects of phthalate esters on dendritic cell subsets and interleukin-4 production in fluorescein isothiocyanate-induced contact hypersensitivity. Microbiol Immunol. 2007; 51(3):321-6. DOI: 10.1111/j.1348-0421.2007.tb03914.x. View

Kitagaki H, Fujisawa S, Watanabe K, Hayakawa K, Shiohara T . Immediate-type hypersensitivity response followed by a late reaction is induced by repeated epicutaneous application of contact sensitizing agents in mice. J Invest Dermatol. 1995; 105(6):749-55. DOI: 10.1111/1523-1747.ep12325538. View

Tang A, Judge T, Nickoloff B, Turka L . Suppression of murine allergic contact dermatitis by CTLA4Ig. Tolerance induction of Th2 responses requires additional blockade of CD40-ligand. J Immunol. 1996; 157(1):117-25. View

WEBB E, Tzimas M, Newsholme S, Griswold D . Intralesional cytokines in chronic oxazolone-induced contact sensitivity suggest roles for tumor necrosis factor alpha and interleukin-4. J Invest Dermatol. 1998; 111(1):86-92. DOI: 10.1046/j.1523-1747.1998.00239.x. View

Kitagaki H, Ono N, Hayakawa K, Kitazawa T, Watanabe K, Shiohara T . Repeated elicitation of contact hypersensitivity induces a shift in cutaneous cytokine milieu from a T helper cell type 1 to a T helper cell type 2 profile. J Immunol. 1997; 159(5):2484-91. View

He R, Oyoshi M, Garibyan L, Kumar L, Ziegler S, Geha R . TSLP acts on infiltrating effector T cells to drive allergic skin inflammation. Proc Natl Acad Sci U S A. 2008; 105(33):11875-80. PMC: 2575291. DOI: 10.1073/pnas.0801532105. View

Soumelis V, Reche P, Kanzler H, Yuan W, Edward G, Homey B . Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol. 2002; 3(7):673-80. DOI: 10.1038/ni805. View

10.

Takano H, Yanagisawa R, Inoue K, Ichinose T, Sadakane K, Yoshikawa T . Di-(2-ethylhexyl) phthalate enhances atopic dermatitis-like skin lesions in mice. Environ Health Perspect. 2006; 114(8):1266-9. PMC: 1552025. DOI: 10.1289/ehp.8985. View

11.

Loureiro G, Rabaca M, Blanco B, Andrade S, Chieira C, Pereira C . Urban versus rural environment--any differences in aeroallergens sensitization in an allergic population of Cova da Beira, Portugal?. Eur Ann Allergy Clin Immunol. 2005; 37(5):187-93. View

12.

Oie L, Hersoug L, Madsen J . Residential exposure to plasticizers and its possible role in the pathogenesis of asthma. Environ Health Perspect. 1997; 105(9):972-8. PMC: 1470354. DOI: 10.1289/ehp.97105972. View

13.

Imai Y, Kondo A, Iizuka H, Maruyama T, Kurohane K . Effects of phthalate esters on the sensitization phase of contact hypersensitivity induced by fluorescein isothiocyanate. Clin Exp Allergy. 2006; 36(11):1462-8. DOI: 10.1111/j.1365-2222.2006.02574.x. View

14.

Takeshita K, Yamasaki T, Akira S, Gantner F, Bacon K . Essential role of MHC II-independent CD4+ T cells, IL-4 and STAT6 in contact hypersensitivity induced by fluorescein isothiocyanate in the mouse. Int Immunol. 2004; 16(5):685-95. DOI: 10.1093/intimm/dxh073. View

15.

Seshasayee D, Lee W, Zhou M, Shu J, Suto E, Zhang J . In vivo blockade of OX40 ligand inhibits thymic stromal lymphopoietin driven atopic inflammation. J Clin Invest. 2007; 117(12):3868-78. PMC: 2096422. DOI: 10.1172/JCI33559. View

16.

Morren M, Przybilla B, Bamelis M, Heykants B, Reynaers A, Degreef H . Atopic dermatitis: triggering factors. J Am Acad Dermatol. 1994; 31(3 Pt 1):467-73. DOI: 10.1016/s0190-9622(94)70213-6. View

17.

Thyssen J, Linneberg A, Menne T, Johansen J . The epidemiology of contact allergy in the general population--prevalence and main findings. Contact Dermatitis. 2007; 57(5):287-99. DOI: 10.1111/j.1600-0536.2007.01220.x. View

18.

Ito T, Wang Y, Duramad O, Hori T, Delespesse G, Watanabe N . TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med. 2005; 202(9):1213-23. PMC: 2213234. DOI: 10.1084/jem.20051135. View

19.

Kolarik B, Naydenov K, Larsson M, Bornehag C, Sundell J . The association between phthalates in dust and allergic diseases among Bulgarian children. Environ Health Perspect. 2008; 116(1):98-103. PMC: 2199301. DOI: 10.1289/ehp.10498. View

20.

Holgate S . The epithelium takes centre stage in asthma and atopic dermatitis. Trends Immunol. 2007; 28(6):248-51. DOI: 10.1016/j.it.2007.04.007. View