Food allergy in mice is modulated through the thymic stromal lymphopoietin pathway

Clinical and Translational Allergy

Volumn 6, Issue 1, 2016, Pages

  Frossard, Christophe P ^a   Zimmerli, Simone C ^a,b   Rincon Garriz, José M ^a,c   Eigenmann, Philippe A ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b EMD Serono   (United States)

^c FASTERIS SA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTOGLOBULIN; CHOLERA TOXIN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; THYMIC STROMAL LYMPHOPOIETIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIGEN SPECIFICITY; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENTERITIS; FEMALE; FOOD ALLERGY; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; INTESTINE EPITHELIUM; LAMINA PROPRIA; LYMPHOCYTE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; SENSITIZATION; TH2 CELL; WILD TYPE;

EID: 85006237004     PISSN: None     EISSN: 20457022     Source Type: Journal    
DOI: 10.1186/s13601-016-0090-2     Document Type: Article

References (43)

1. Vickery BP, Scurlock AM, Jones SM, Burks AW. Mechanisms of immune tolerance relevant to food allergy. J Allergy Clin Immunol. 2011;127:576-84.
2. Li XM, Serebrisky D, Lee SY, Huang CK, Bardina L, Schofield BH, Stanley JS, Burks AW, Bannon GA, Sampson HA. A murine model of peanut anaphylaxis: T- and B-cell responses to a major peanut allergen mimic human responses. J Allergy Clin Immunol. 2000;106(1 Pt 1):150-8.
3. Frossard CP, Tropia L, Hauser C, Eigenmann PA. Lymphocytes in Peyer's patches regulate clinical tolerance in a murine model of food allergy. J Allergy Clin Immunol. 2004;113:958-64.
4. Strait RT, Morris SC, Finkelman FD. IgG-blocking antibodies inhibit IgE-mediated anaphylaxis in vivo through both antigen interception and Fc gamma RIIb cross-linking. J Clin Invest. 2006;116:833-41.
5. Khodoun M, Strait R, Orekov T, Hogan S, Karasuyama H, Herbert DR, Köhl J, Finkelman FD. Peanuts can contribute to anaphylactic shock by activating complement. J Allergy Clin Immunol. 2009;123:342-51.
6. Noti M, Kim BS, Siracusa MC, Rak GD, Kubo M, Moghaddam AE, Sattentau QA, Comeau MR, Spergel JM, Artis D. Exposure to food allergens through inflamed skin promotes intestinal food allergy through the thymic stromal lymphopoietin-basophil axis. J Allergy Clin Immunol. 2014;133:1390-9 (1399.e1-6).
7. Blázquez AB, Mayer L, Berin MC. Thymic stromal lymphopoietin is required for gastrointestinal allergy but not oral tolerance. Gastroenterology. 2010;139:1301-9.
8. Bogiatzi SI, Fernandez I, Bichet J-C, Marloie-Provost M-A, Volpe E, Sastre X, Soumelis V. Cutting edge: proinflammatory and Th2 cytokines synergize to induce thymic stromal lymphopoietin production by human skin keratinocytes. J Immunol. 2007;178:3373-7.
9. Kato A, Favoreto S Jr, Avila PC, Schleimer RP. TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. J Immunol. 2007;179:1080-7.
10. Lee H-C, Ziegler SF. Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkappaB. Proc Natl Acad Sci USA. 2007;104:914-9.
11. Zhang K, Shan L, Rahman MS, Unruh H, Halayko AJ, Gounni AS. Constitutive and inducible thymic stromal lymphopoietin expression in human airway smooth muscle cells: role in chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol. 2007;293:L375-82.
12. Miyata M, Nakamura Y, Shimokawa N, Ohnuma Y, Katoh R, Matsuoka S, Okumura K, Ogawa H, Masuyama K, Nakao A. Thymic stromal lymphopoietin is a critical mediator of IL-13-driven allergic inflammation. Eur J Immunol. 2009;39:3078-83.
13. Tanaka J, Saga K, Kido M, Nishiura H, Akamatsu T, Chiba T, Watanabe N. Proinflammatory Th2 cytokines induce production of thymic stromal lymphopoietin in human colonic epithelial cells. Dig Dis Sci. 2010;55:1896-904.
14. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, Gilliet M, Ho S, Antonenko S, Lauerma A, Smith K, Gorman D, Zurawski S, Abrams J, Menon S, McClanahan T, de Waal-Malefyt Rd R, Bazan F, Kastelein RA, Liu Y-J. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol. 2002;3:673-80.
15. Al-Shami A, Spolski R, Kelly J, Keane-Myers A, Leonard WJ. A role for TSLP in the development of inflammation in an asthma model. J Exp Med. 2005;202:829-39.
16. Zhou B, Comeau MR, De Smedt T, Liggitt HD, Dahl ME, Lewis DB, Gyarmati D, Aye T, Campbell DJ, Ziegler SF. Thymic stromal lymphopoietin as a key initiator of allergic airway inflammation in mice. Nat Immunol. 2005;6:1047-53.
17. Larson RP, Zimmerli SC, Comeau MR, Itano A, Omori M, Iseki M, Hauser C, Ziegler SF. Dibutyl phthalate-induced thymic stromal lymphopoietin is required for Th2 contact hypersensitivity responses. J Immunol. 2010;184:2974-84.
18. Zaph C, Troy AE, Taylor BC, Berman-Booty LD, Guild KJ, Du Y, Yost EA, Gruber AD, May MJ, Greten FR, Eckmann L, Karin M, Artis D. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature. 2007;446:552-6.
19. Taylor BC, Zaph C, Troy AE, Du Y, Guild KJ, Comeau MR, Artis D. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J Exp Med. 2009;206:655-67.
20. Li XM, Schofield BH, Huang CK, Kleiner GI, Sampson HA. A murine model of IgE-mediated cow's milk hypersensitivity. JAllergy ClinImmunol. 1999;103(2 Pt 1):206-14.
21. Frossard CP, Hauser C, Eigenmann PA. Oral carrageenan induces antigen-dependent oral tolerance: prevention of anaphylaxis and induction of lymphocyte anergy in a murine model of food allergy. Pediatr Res. 2001;49:417-22.
22. Carpino N, Thierfelder WE, Chang M, Saris C, Turner SJ, Ziegler SF, Ihle JN. Absence of an essential role for thymic stromal lymphopoietin receptor in murine B-cell development. Mol Cell Biol. 2004;24:2584-92.
23. Adel-Patient K, Créminon C, Bernard H, Clément G, Négroni L, Frobert Y, Grassi J, Wal JM, Chatel JM. Evaluation of a high IgE-responder mouse model of allergy to bovine beta-lactoglobulin (BLG): development of sandwich immunoassays for total and allergen-specific IgE, IgG1 and IgG2a in BLG-sensitized mice. J Immunol Methods. 2000;235:21-32.
24. Frossard CP, Steidler L, Eigenmann PA. Oral administration of an IL-10-secreting Lactococcus lactis strain prevents food-induced IgE sensitization. J Allergy Clin Immunol. 2007;119:952-9.
25. Lefrancois L. Carbohydrate differentiation antigens of murine T cells: expression on intestinal lymphocytes and intestinal epithelium. J Immunol. 1987;138:3375-84.
26. Asigbetse KE, Eigenmann PA, Frossard CP. Intestinal lamina propria TcRgammadelta + lymphocytes selectively express IL-10 and IL-17. J Investig Allergol Clin Immunol. 2010;20:391-401.
27. Miyajima I, Dombrowicz D, Martin TR, Ravetch JV, Kinet JP, Galli SJ. Systemic anaphylaxis in the mouse can be mediated largely through IgG1 and Fc gammaRIII. Assessment of the cardiopulmonary changes, mast cell degranulation, and death associated with active or IgE- or IgG1-dependent passive anaphylaxis. J Clin Invest. 1997;99:901-14.
28. Muraro A, Werfel T, Hoffmann-Sommergruber K, Roberts G, Beyer K, Bindslev-Jensen C, Cardona V, Dubois A, duToit G, Eigenmann P, Fernandez Rivas M, Halken S, Hickstein L, Høst A, Knol E, Lack G, Marchisotto MJ, Niggemann B, Nwaru BI, Papadopoulos NG, Poulsen LK, Santos AF, Skypala I, Schoepfer A, Van Ree R, Venter C, Worm M, Vlieg-Boerstra B, Panesar S, de Silva D, et al. EAACI food allergy and anaphylaxis guidelines: diagnosis and management of food allergy. Allergy. 2014;69:1008-25.
29. DeLong JH, Simpson KH, Wambre E, James EA, Robinson D, Kwok WW. Ara h 1-reactive T cells in individuals with peanut allergy. J Allergy Clin Immunol. 2011;127(1211-1218):e3.
30. Dhuban KB, d'Hennezel E, Ben-Shoshan M, McCusker C, Clarke A, Fiset P, Mazer B, Piccirillo CA. Altered T helper 17 responses in children with food allergy. Int Arch Allergy Immunol. 2013;162:318-22.
31. Souwer Y, Szegedi K, Kapsenberg ML, de Jong EC. IL-17 and IL-22 in atopic allergic disease. Curr Opin Immunol. 2010;22:821-6.
32. Yoo J, Omori M, Gyarmati D, Zhou B, Aye T, Brewer A, Comeau MR, Campbell DJ, Ziegler SF. Spontaneous atopic dermatitis in mice expressing an inducible thymic stromal lymphopoietin transgene specifically in the skin. J Exp Med. 2005;202:541-9.
33. Ashrin MN, Arakaki R, Yamada A, Kondo T, Kurosawa M, Kudo Y, Watanabe M, Ichikawa T, Hayashi Y, Ishimaru N. A critical role for thymic stromal lymphopoietin in nickel-induced allergy in mice. J Immunol. 2014;192:4025-31.
34. Ying S, O'Connor B, Ratoff J, Meng Q, Mallett K, Cousins D, Robinson D, Zhang G, Zhao J, Lee TH, Corrigan C. Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity. J Immunol. 2005;174:8183-90.
35. Hong X, Wang G, Liu X, Kumar R, Tsai H-J, Arguelles L, Hao K, Pearson C, Ortiz K, Bonzagni A, Apollon S, Fu L, Caruso D, Pongracic JA, Schleimer R, Holt PG, Bauchner H, Wang X. Gene polymorphisms, breast-feeding, and development of food sensitization in early childhood. J Allergy Clin Immunol. 2011;128(374-381):e2.
36. Noti M, Wojno EDT, Kim BS, Siracusa MC, Giacomin PR, Nair MG, Benitez AJ, Ruymann KR, Muir AB, Hill DA, Chikwava KR, Moghaddam AE, Sattentau QJ, Alex A, Zhou C, Yearley JH, Menard-Katcher P, Kubo M, Obata-Ninomiya K, Karasuyama H, Comeau MR, Brown-Whitehorn T, de Waal Malefyt R, Sleiman PM, Hakonarson H, Cianferoni A, Falk GW, Wang M-L, Spergel JM, Artis D. Thymic stromal lymphopoietin-elicited basophil responses promote eosinophilic esophagitis. Nat Med. 2013;19:1005-13.
37. Han H, Thelen TD, Comeau MR, Ziegler SF. Thymic stromal lymphopoietin-mediated epicutaneous inflammation promotes acute diarrhea and anaphylaxis. J Clin Invest. 2014;124:5442-52.
38. Spadoni I, Iliev ID, Rossi G, Rescigno M. Dendritic cells produce TSLP that limits the differentiation of Th17 cells, fosters Treg development, and protects against colitis. Mucosal Immunol. 2012;5:184.
39. Chu DK, Llop-Guevara A, Walker TD, Flader K, Goncharova S, Boudreau JE, Moore CL, In TS, Waserman S, Coyle AJ, Kolbeck R, Humbles AA, Jordana M. IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol. 2013;131(187-200):e8.
40. Lee SY, Huang CK, Zhang TF, Schofield BH, Burks AW, Bannon GA, Sampson HA, Li XM. Oral administration of IL-12 suppresses anaphylactic reactions in a murine model of peanut hypersensitivity. Clin Immunol. 2001;101:220-8.
41. Zhu F-G, Kandimalla ER, Yu D, Agrawal S. Oral administration of a synthetic agonist of Toll-like receptor 9 potently modulates peanut-induced allergy in mice. J Allergy Clin Immunol. 2007;120:631-7.
42. Arias K, Baig M, Colangelo M, Chu D, Walker T, Goncharova S, Coyle A, Vadas P, Waserman S, Jordana M. Concurrent blockade of platelet-activating factor and histamine prevents life-threatening peanut-induced anaphylactic reactions. J Allergy Clin Immunol. 2009;124:307-14 (314.e1-2).
43. Gauvreau GM, O'Byrne PM, Boulet L-P, Wang Y, Cockcroft D, Bigler J, FitzGerald JM, Boedigheimer M, Davis BE, Dias C, Gorski KS, Smith L, Bautista E, Comeau MR, Leigh R, Parnes JR. Effects of an anti-TSLP antibody on allergen-induced asthmatic responses. N Engl J Med. 2014;370:2102-10.