Gastroenterology
Volume 129, Issue 3 , Pages 985-994 , September 2005

Epicutaneous Antigen Exposure Primes for Experimental Eosinophilic Esophagitis in Mice

Received 19 February 2005 ,Accepted 2 June 2005.

References 

  1. Furuta GT , Ackerman SJ , Wershil BK . The role of the eosinophil in gastrointestinal diseases . Curr Opin Gastroenterol . 1995;11:541–547
  2. Rothenberg ME . Eosinophilic gastrointestinal disorders (EGID) . J Allergy Clin Immunol . 2004;113:11–28
  3. Cello JP . Eosinophilic gastroenteritis—a complex disease entity . Am J Med . 1979;67:1097–1104
  4. Orenstein SR, Shalaby TM, Di Lorenzo C, Putnam PE, Sigurdsson L, Mousa H, et al. The spectrum of pediatric eosinophilic esophagitis beyond infancy (a clinical series of 30 children) . Am J Gastroenterol . 2000;95:1422–1430
  5. Teitelbaum JE, Fox VL, Twarog FJ, Nurko S, Antonioli D, Gleich G, et al. Eosinophilic esophagitis in children (immunopathological analysis and response to fluticasone propionate) . Gastroenterology . 2002;122:1216–1225
  6. Fox VL , Nurko S , Furuta GT . Eosinophilic esophagitis (it’s not just kid’s stuff) . Gastrointest Endosc . 2002;56:260–270
  7. Liacouras CA . Eosinophilic esophagitis in children and adults . J Pediatr Gastroenterol Nutr . 2003;37(Suppl 1):S23–S28
  8. Straumann A , Spichtin HP , Grize L , Bucher KA , Beglinger C , Simon HU . Natural history of primary eosinophilic esophagitis (a follow-up of 30 adult patients for up to 11.5 years) . Gastroenterology . 2003;125:1660–1669
  9. Noel RJ , Putnam PE , Rothenberg ME . Eosinophilic esophagitis . N Engl J Med . 2004;351:940–941
  10. Sampson HA . Food allergy. Part 1: immunopathogenesis and clinical disorders . J Allergy Clin Immunol . 1999;103:717–728
  11. Mishra A , Hogan SP , Brandt EB , Rothenberg ME . IL-5 promotes eosinophil trafficking to the esophagus . J Immunol . 2002;168:2464–2469
  12. Eichenfield LF, Hanifin JM, Beck LA, Lemanske RF, Sampson HA, Weiss ST, et al. Atopic dermatitis and asthma (parallels in the evolution of treatment) . Pediatrics . 2003;111:608–616
  13. Spergel JM , Paller AS . Atopic dermatitis and the atopic march . J Allergy Clin Immunol . 2003;112:S118–S127
  14. Leung DY , Boguniewicz M , Howell MD , Nomura I , Hamid QA . New insights into atopic dermatitis . J Clin Invest . 2004;113:651–657
  15. Saloga J , Renz H , Larsen GL , Gelfand EW . Increased airways responsiveness in mice depends on local challenge with antigen . Am J Respir Crit Care Med . 1994;149:65–70
  16. Spergel JM , Mizoguchi E , Brewer JP , Martin TR , Bhan AK , Geha RS . Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice . J Clin Invest . 1998;101:1614–1622
  17. Herrick CA , MacLeod H , Glusac E , Tigelaar RE , Bottomly K . Th2 responses induced by epicutaneous or inhalational protein exposure are differentially dependent on IL-4 . J Clin Invest . 2000;105:765–775
  18. Ma W, Bryce PJ, Humbles AA, Laouini D, Yalcindag A, Alenius H, et al. CCR3 is essential for skin eosinophilia and airway hyperresponsiveness in a murine model of allergic skin inflammation . J Clin Invest . 2002;109:621–628
  19. Walsh SV, Antonioli DA, Goldman H, Fox VL, Bousvaros A, Leichtner AM, et al. Allergic esophagitis in children (a clinicopathological entity) . Am J Surg Pathol . 1999;23:390–396
  20. Spergel JM , Beausoleil JL , Mascarenhas M , Liacouras CA . The use of skin prick tests and patch tests to identify causative foods in eosinophilic esophagitis . J Allergy Clin Immunol . 2002;109:363–368
  21. Guajardo JR , Plotnick LM , Fende JM , Collins MH , Putnam PE , Rothenberg ME . Eosinophil-associated gastrointestinal disorders (a world-wide-web based registry) . J Pediatr . 2002;141:576–581
  22. Busse WW , Holgate ST . Asthma and rhinitis . In:  Howarth PH ,  Saito H editor. 2nd ed.. Animal models of asthma . Volume 2: Oxford, England: Blackwell Science; 2000;p. 1205–1227
  23. Hamelmann E , Gelfand EW . IL-5-induced airway eosinophilia—the key to asthma? . Immunol Rev . 2001;179:182–191
  24. Lee NA , Gelfand EW , Lee JJ . Pulmonary T cells and eosinophils (coconspirators or independent triggers of allergic respiratory pathology?) . J Allergy Clin Immunol . 2001;107:945–957
  25. Kumar RK , Foster PS . Modeling allergic asthma in mice (pitfalls and opportunities) . Am J Respir Cell Mol Biol . 2002;27:267–272
  26. Mishra A , Hogan SP , Brandt EB , Rothenberg ME . An etiological role for aeroallergens and eosinophils in experimental esophagitis . J Clin Invest . 2001;107:83–90
  27. Zurawski G , de Vries JE . Interleukin 13 elicits a subset of the activities of its close relative interleukin 4 . Stem Cells . 1994;12:169–174
  28. Lai SY , Molden J , Liu KD , Puck JM , White MD , Goldsmith MA . Interleukin-4-specific signal transduction events are driven by homotypic interactions of the interleukin-4 receptor alpha subunit . EMBO J . 1996;15:4506–4514
  29. Murata T , Noguchi PD , Puri RK . IL-13 induces phosphorylation and activation of JAK2 Janus kinase in human colon carcinoma cell lines (similarities between IL-4 and IL-13 signaling) . J Immunol . 1996;156:2972–2978
  30. Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, et al. Essential role of Stat6 in IL-4 signalling . Nature . 1996;380:627–630
  31. Takeda K , Kamanaka M , Tanaka T , Kishimoto T , Akira S . Impaired IL-13-mediated functions of macrophages in STAT6-deficient mice . J Immunol . 1996;157:3220–3222
  32. Corry DB , Kheradmand F . Biology and therapeutic potential of the interleukin-4/interleukin-13 signaling pathway in asthma . Am J Respir Med . 2002;1:185–193
  33. Akimoto T, Numata F, Tamura M, Takata Y, Higashida N, Takashi T, et al. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice . J Exp Med . 1998;187:1537–1542
  34. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, et al. Interleukin-13 (central mediator of allergic asthma) . Science . 1998;282:2258–2261
  35. Trifilieff A , El Hasim A , Corteling R , Owen CE . Abrogation of lung inflammation in sensitized Stat6-deficient mice is dependent on the allergen inhalation procedure . Br J Pharmacol . 2000;130:1581–1588
  36. Pope SM, Brandt EB, Mishra A, Hogan SP, Zimmermann N, Matthaei KI, et al. IL-13 induces eosinophil recruitment into the lung by an IL-5- and eotaxin-dependent mechanism . J Allergy Clin Immunol . 2001;108:594–601
  37. Zimmermann N, Mishra A, King NE, Fulkerson PC, Doepker MP, Nikolaidis NM, et al. Transcript signatures in experimental asthma (identification of STAT6-dependent and -independent pathways) . J Immunol . 2004;172:1815–1824
  38. Mishra A , Rothenberg ME . Intratracheal IL-13 induces eosinophilic esophagitis by an IL-5, eotaxin-1, and STAT6-dependent mechanism . Gastroenterology . 2003;125:1419–1427
  39. Blease K, Schuh JM, Jakubzick C, Lukacs NW, Kunkel SL, Joshi BH, et al. Stat6-deficient mice develop airway hyperresponsiveness and peribronchial fibrosis during chronic fungal asthma . Am J Pathol . 2002;160:481–490
  40. Wang LF , Lin JY , Hsieh KH , Lin RH . Epicutaneous exposure of protein antigen induces a predominant Th2-like response with high IgE production in mice . J Immunol . 1996;156:4077–4082
  41. Brandt EB , Rothenberg ME . Eosinophil levels in mice are significantly higher in small blood vessels than in large blood vessels . J Allergy Clin Immunol . 2001;108:142–143
  42. Hogan SP , Mishra A , Brandt EB , Foster PS , Rothenberg ME . A critical role for eotaxin in experimental oral antigen-induced eosinophilic gastrointestinal allergy . Proc Natl Acad Sci U S A . 2000;97:6681–6686
  43. Saito H, Matsumoto K, Denburg AE, Crawford L, Ellis R, Inman MD, et al. Pathogenesis of murine experimental allergic rhinitis (a study of local and systemic consequences of IL-5 deficiency) . J Immunol . 2002;168:3017–3023
  44. Lee NA , McGarry MP , Larson KA , Horton MA , Kristensen AB , Lee JJ . Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies . J Immunol . 1997;158:1332–1344
  45. Spergel JM , Mizoguchi E , Oettgen H , Bhan AK , Geha RS . Roles of TH1 and TH2 cytokines in a murine model of allergic dermatitis . J Clin Invest . 1999;103:1103–1111
  46. Ruchelli E , Wenner W , Voytek T , Brown K , Liacouras C . Severity of esophageal eosinophilia predicts response to conventional gastroesophageal reflux therapy . Pediatr Dev Pathol . 1999;2:15–18
  47. Justinich CJ , Ricci A , Kalafus DA , Treem WR , Hyams JS , Kreutzer DL . Activated eosinophils in esophagitis in children (a transmission electron microscopic study) . J Pediatr Gastroenterol Nutr . 1997;25:194–198
  48. van Neste D , Douka M , Rahier J , Staquet MJ . Epidermal changes in atopic dermatitis . Acta Derm Venereol Suppl (Stockh) . 1985;114:67–71
  49. Leung DY . Atopic dermatitis (the skin as a window into the pathogenesis of chronic allergic diseases) . J Allergy Clin Immunol . 1995;96:302–318
  50. Noel RJ, Putnam PE, Collins MH, Assa’ad AH, Guajardo JR, Jameson SC, et al. Clinical and immunopathologic effects of swallowed fluticasone for eosinophilic esophagitis . Clin Gastroenterol Hepatol . 2004;2:568–575
  51. Bochner BS , Schleimer RP . Mast cells, basophils, and eosinophils (distinct but overlapping pathways for recruitment) . Immunol Rev . 2001;179:5–15
  52. Mishra A , Hogan SP , Lee JJ , Foster PS , Rothenberg ME . Fundamental signals that regulate eosinophil homing to the gastrointestinal tract . J Clin Invest . 1999;103:1719–1727
  53. Straumann A , Bauer M , Fischer B , Blaser K , Simon HU . Idiopathic eosinophilic esophagitis is associated with a T(H)2-type allergic inflammatory response . J Allergy Clin Immunol . 2001;108:954–961
  54. Garrett JK, Jameson SC, Thomson B, Collins MH, Wagoner LE, Freese DK, et al. Anti-interleukin-5 (mepolizumab) therapy for hypereosinophilic syndromes . J Allergy Clin Immunol . 2004;113:115–119
  55. Nicholson AG , Li D , Pastorino U , Goldstraw P , Jeffery PK . Full thickness eosinophilia in oesophageal leiomyomatosis and idiopathic eosinophilic oesophagitis. A common allergic inflammatory profile? . J Pathol . 1997;183:233–236

 Supported in part by National Institutes of Health grants R01 AI42242 and AI45898 and the Burroughs Welcome Fund Translational Research Grant (to M.E.R.).

PII: S0016-5085(05)01129-7

doi: 10.1053/j.gastro.2005.06.027

Gastroenterology
Volume 129, Issue 3 , Pages 985-994 , September 2005

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