Food allergy enhances allergic asthma in mice

Respiratory Research

Antoine Magnan²  Marie Bodinier⁵  Sophie Brouard³  Michel Neunlist¹  Christine Sagan⁴  Guillaume Mahay²  Philippe Aubert¹  Marie-Aude Cheminant²  Faouzi Braza²  Camille Rolland-Debord²  David Lair²  Julie Chesné²  Gregory Bouchaud⁵  Tiphaine Bihouée² 

[1] INSERM, UMR U913, Nantes F-44000, France;DHU2020 médecine personnalisée des maladies chroniques, Nantes F-44000, France;INSERM, UMR U1064 and Institut de Transplantation Urologie, Néphrologie (ITUN), Nantes F44093, France;CHU de Nantes, Service d’anatomie et cytologique pathologiques, Nantes, France;INRA, UR1268 BIA, Nantes F-44316, France

关键词: Ovalbumin;    Mouse;    Immunity;    House dust mite;    Gut;    Th2 cytokines;    Allergy;    Asthma;   

Others  :  1137226
DOI  :  10.1186/s12931-014-0142-x

 received in 2014-09-03, accepted in 2014-11-01,  发布年份 2014

【 摘 要 】

Background

Atopic march refers to the typical transition from a food allergy in early childhood to allergic asthma in older children and adults. However the precise interplay of events involving gut, skin and pulmonary inflammation in this process is not completely understood.

Objectives

To develop a mouse model of mixed food and respiratory allergy mimicking the atopic march and better understand the impact of food allergies on asthma.

Methods

Food allergy to ovalbumin (OVA) was induced through intra-peritoneal sensitization and intra-gastric challenge, and/or a respiratory allergy to house dust mite (HDM) was obtained through percutaneous sensitization and intra-nasal challenges with dermatophagoides farinae (Der f) extract. Digestive, respiratory and systemic parameters were analyzed.

Results

OVA-mediated gut allergy was associated with an increase in jejunum permeability, and a worsening of Der f-induced asthma with stronger airway hyperresponsiveness and pulmonary cell infiltration, notably eosinophils. There was overproduction of the pro-eosinophil chemokine RANTES in broncho-alveolar lavages associated with an enhanced Th2 cytokine secretion and increased total and Der f-specific IgE when the two allergies were present. Both AHR and lung inflammation increased after a second pulmonary challenge.

Conclusion

Gut sensitization to OVA amplifies Der f-induced asthma in mice.

【 授权许可】

   
2014 Bihouée et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Global Strategy for Asthma Management and Prevention 2012.
• [2]Fanta CH: Asthma. N Engl J Med 2009, 360:1002-1014.
• [3]Haldar P, Pavord ID, Shaw DE, Berry MA, Thomas M, Brightling CE, Wardlaw AJ, Green RH: Cluster analysis and clinical asthma phenotypes. Am J Respir Crit Care Med 2008, 178:218-224.
• [4]Dharmage SC, Lowe AJ, Matheson MC, Burgess JA, Allen KJ, Abramson MJ: Atopic dermatitis and the atopic march revisited. Allergy 2014, 69:17-27.
• [5]Lin YT, Wu CT, Huang JL, Cheng JH, Yeh KW: Correlation of ovalbumin of egg white components with allergic diseases in children.J Microbiol Immunol Infect 2014. epub 03/26.
• [6]Bieber T, Cork M, Reitamo S: Atopic dermatitis: a candidate for disease-modifying strategy. Allergy 2012, 67:969-975.
• [7]Brooks C, Pearce N, Douwes J: The hygiene hypothesis in allergy and asthma: an update. Curr Opin Allergy Clin Immunol 2013, 13:70-77.
• [8]Bohle B: T lymphocytes and food allergy. Mol Nutr Food Res 2004, 48:424-433.
• [9]Campbell DE, Hill DJ, Kemp AS: Enhanced IL-4 but normal interferon-gamma production in children with isolated IgE mediated food hypersensitivity. Pediatr Allergy Immunol 1998, 9:68-72.
• [10]Gregory LG, Lloyd CM: Orchestrating house dust mite-associated allergy in the lung. Trends Immunol 2011, 32:402-411.
• [11]Boralevi F, Hubiche T, Leaute-Labreze C, Saubusse E, Fayon M, Roul S, Maurice-Tison S, Taieb A: Epicutaneous aeroallergen sensitization in atopic dermatitis infants - determining the role of epidermal barrier impairment. Allergy 2008, 63:205-210.
• [12]Kubo A, Nagao K, Amagai M: Epidermal barrier dysfunction and cutaneous sensitization in atopic diseases. J Clin Invest 2012, 122:440-447.
• [13]Hammad H, Plantinga M, Deswarte K, Pouliot P, Willart MA, Kool M, Muskens F, Lambrecht BN: Inflammatory dendritic cells–not basophils–are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J Exp Med 2010, 207:2097-2111.
• [14]Tourdot S, Airouche S, Berjont N, Da Silveira A, Mascarell L, Jacquet A, Caplier L, Langelot M, Baron-Bodo V, Moingeon P: Evaluation of therapeutic sublingual vaccines in a murine model of chronic house dust mite allergic airway inflammation. Clin Exp Allergy 2011, 41:1784-1792.
• [15]Lewkowich IP, Lajoie S, Clark JR, Herman NS, Sproles AA, Wills-Karp M: Allergen uptake, activation, and IL-23 production by pulmonary myeloid DCs drives airway hyperresponsiveness in asthma-susceptible mice. PLoS One 2008, 3:e3879.
• [16]Rolland-Debord C, Lair D, Roussey-Bihouee T, Hassoun D, Evrard J, Cheminant MA, Chesne J, Braza F, Mahay G, Portero V, Sagan C, Pitard B, Magnan A: Block copolymer/DNA vaccination induces a strong allergen-specific local response in a mouse model of house dust mite asthma. PLoS One 2014, 9:e85976.
• [17]Zhang G, Wang P, Yang G, Cao Q, Wang R: The inhibitory role of hydrogen sulfide in airway hyperresponsiveness and inflammation in a mouse model of asthma. Am J Pathol 2013, 182:1188-1195.
• [18]Perrier C, Thierry AC, Mercenier A, Corthesy B: Allergen-specific antibody and cytokine responses, mast cell reactivity and intestinal permeability upon oral challenge of sensitized and tolerized mice. Clin Exp Allergy 2010, 40:153-162.
• [19]Hennino A, Vocanson M, Toussaint Y, Rodet K, Benetiere J, Schmitt AM, Aries MF, Berard F, Rozieres A, Nicolas JF: Skin-infiltrating CD8+ T cells initiate atopic dermatitis lesions. J Immunol 2007, 178:5571-5577.
• [20]Moore WC: The natural history of asthma phenotypes identified by cluster analysis. Looking for chutes and ladders. Am J Respir Crit Care Med 2013, 188:521-522.
• [21]Venge J, Lampinen M, Hakansson L, Rak S, Venge P: Identification of IL-5 and RANTES as the major eosinophil chemoattractants in the asthmatic lung. J Allergy Clin Immunol 1996, 97:1110-1115.
• [22]Brandt EB, Scribner TA, Akei HS, Rothenberg ME: Experimental gastrointestinal allergy enhances pulmonary responses to specific and unrelated allergens. J Allergy Clin Immunol 2006, 118:420-427.
• [23]Amat F. Boutmy-Deslandes E. DK, Nemni A., Bourrat E., Sarahoui F., Pansé I., Fouere S., Bagot M., Just J.: Multiple sensitization to food allergens predisposes to develop sensitization to inhaled allergens in infants with early-onset atopic dermatitis: evidence from the ORCA prospective cohort.EAACI 2014, Oral Abstract Session, OAS 35, Pediatric epidemiology, B10.