Overview of in vivo and ex vivo endpoints in murine food allergy models: Suitable for evaluation of the sensitizing capacity of novel proteins?
Jazyk angličtina Země Dánsko Médium print-electronic
Typ dokumentu časopisecké články, přehledy
PubMed
31187876
PubMed Central
PMC7065134
DOI
10.1111/all.13943
Knihovny.cz E-zdroje
- Klíčová slova
- animal models, biomarkers, food allergy, prevention,
- MeSH
- cytokiny biosyntéza MeSH
- fenotyp MeSH
- imunoglobulin E krev MeSH
- imunoglobulin G krev MeSH
- inbrední kmeny myší MeSH
- modely nemocí na zvířatech * MeSH
- myši MeSH
- potravinová alergie krev imunologie MeSH
- T-lymfocyty imunologie MeSH
- tělesná teplota MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- cytokiny MeSH
- imunoglobulin E MeSH
- imunoglobulin G MeSH
Significant efforts are necessary to introduce new dietary protein sources to feed a growing world population while maintaining food supply chain sustainability. Such a sustainable protein transition includes the use of highly modified proteins from side streams or the introduction of new protein sources that may lead to increased clinically relevant allergic sensitization. With food allergy being a major health problem of increasing concern, understanding the potential allergenicity of new or modified proteins is crucial to ensure public health protection. The best predictive risk assessment methods currently relied on are in vivo models, making the choice of endpoint parameters a key element in evaluating the sensitizing capacity of novel proteins. Here, we provide a comprehensive overview of the most frequently used in vivo and ex vivo endpoints in murine food allergy models, addressing their strengths and limitations for assessing sensitization risks. For optimal laboratory-to-laboratory reproducibility and reliable use of predictive tests for protein risk assessment, it is important that researchers maintain and apply the same relevant parameters and procedures. Thus, there is an urgent need for a consensus on key food allergy parameters to be applied in future food allergy research in synergy between both knowledge institutes and clinicians.
Department of Animal Breeding and Production Warsaw University of Life Sciences Warsaw Poland
Department of Medicine APC Microbiome Ireland National University of Ireland Cork Ireland
Department of Microbiology APC Microbiome Ireland National University of Ireland Cork Ireland
INRA UR 1268 BIA Nantes Nantes France
Institute for Risk Assessment Sciences Utrecht University Utrecht The Netherlands
Institute of Microbiology Czech Academy of Sciences Nový Hrádek Czech Republic
Institute of Pathology University of Bern Bern Switzerland
National Food Institute Technical University of Denmark Kgs Lyngby Denmark
Wageningen Food and Biobased Research Wageningen The Netherlands
Zobrazit více v PubMed
Smit JJ, Noti M, O’Mahony L. The use of animal models to discover immunological mechanisms underpinning sensitization to food allergens. Drug Discov Today Dis Model. 2015;17‐18:63‐69.
Hussain M, Epstein MM, Noti M. Experimental food allergy models to study the role of innate immune cells as initiators of allergen‐specific Th2 immune responses. Drug Discov Today Dis Model. 2015;17‐18:55‐62.
Gavrovic‐Jankulovic M, Willemsen L. Epithelial models to study food allergen‐induced barrier disruption and immune activation. Drug Discov Today Dis Model. 2015;17‐18:29‐36.
Cubells‐Baeza N, Verhoeckx K, Larre C, Denery‐Papini S, Gavrovic‐Jankulovic M, Diaz PA. Applicability of epithelial models in protein permeability/transport studies and food allergy. Drug Discov Today Dis Model. 2015;17‐18:13‐21.
Bøgh KL, van Bilsen J, Głogowski R, et al. Current challenges facing the assessment of the allergenic capacity of food allergens in animal models. Clin Transl Allergy. 2016;6:21. PubMed PMC
Mazzucchelli G, Holzhauser T, Cirkovic Velickovic T, et al. Current (Food) allergenic risk assessment: is it fit for novel foods? Status quo and identification of gaps. Mol Nutr Food Res. 2018;62:1700278. PubMed PMC
Hussain M, Borcard L, Walsh KP, et al. Basophil‐derived IL‐4 promotes epicutaneous antigen sensitization concomitant with the development of food allergy. J Allergy Clin Immunol. 2018;141(1):223‐234. PubMed
Blazquez AB, Berin MC. Gastrointestinal dendritic cells promote Th2 Skewing via OX40L. J Immunol. 2008;180:4441‐4450. PubMed
Noval Rivas M, Burton OT, Oettgen HC, Chatila T. IL‐4 production by group 2 innate lymphoid cells promotes food allergy by blocking regulatory T‐cell function. J Allergy Clin Immunol. 2016;138(3):801‐811. PubMed PMC
Khodoun MV, Tomar S, Tocker JE, Wang YH, Finkelman FD. Prevention of food allergy development and suppression of established food allergy by neutralization of thymic stromal lymphopoietin, IL‐25, and IL‐33. J Allergy Clin Immunol. 2018;141(1):171‐179. PubMed
van den Elsen LW, Meulenbroek LA, van Esch BC, et al. CD25+ regulatory T cells transfer n‐3 long chain polyunsaturated fatty acids‐induced tolerance in mice allergic to cow’s milk protein. Allergy. 2013;68:1562‐1570. PubMed
Hogenkamp A, Knippels L, Garssen J, Van EB. Supplementation of mice with specific nondigestible oligosaccharides during pregnancy or lactation leads to diminished sensitization and allergy in the female. J Nutr. 2015;145:996‐1002. PubMed
Thang CL, Boye JI, Shi HN, Zhao X. Effects of supplementing different ratios of omega‐3 and omega‐6 fatty acids in western‐style diets on cow’s milk protein allergy in a mouse model. Mol Nutr Food Res. 2013;57:2029‐2038. PubMed
Manzano‐Szalai K, Pali‐Schöll I, Krishnamurthy D, Stremnitzer C, Flaschberger I, Jensen‐Jarolim E. Anaphylaxis imaging: non‐invasive measurement of surface body temperature and physical activity in small animals. PLoS ONE. 2016;11:e0150819. PubMed PMC
Rodriguez B, Prioult G, Hacini‐Rachinel F, et al. Infant gut microbiota is protective against cow’s milk allergy in mice despite immature ileal T‐cell response. FEMS Microbiol Ecol. 2012;79:192‐202. PubMed
Abril‐Gil M, Garcia‐Just A, Pérez‐Cano FJ, Franch À, Castell M. Development and characterization of an effective food allergy model in Brown Norway rats. PLoS ONE. 2015;10:e0125314. PubMed PMC
Diesner SC, Schultz C, Ackaert C, et al. Nitration of β‐lactoglobulin but not of ovomucoid enhances anaphylactic responses in food allergic mice. PLoS ONE. 2015;10:e0126279. PubMed PMC
Diesner SC, Bergmayr C, Pfitzner B, et al. A distinct microbiota composition is associated with protection from food allergy in an oral mouse immunization model. Clin Immunol. 2016;173:10‐18. PubMed PMC
Diesner SC, Knittelfelder R, Krishnamurthy D, et al. Dose‐dependent food allergy induction against ovalbumin under acid‐suppression: a murine food allergy model. Immunol Lett. 2008;121:45‐51. PubMed PMC
Golias J, Schwarzer M, Wallner M, et al. Heat‐induced structural changes affect OVA‐antigen processing and reduce allergic response in mouse model of food allergy. PLoS ONE. 2012;7:e37156. PubMed PMC
van Esch B, van Bilsen J, Jeurink PV, et al. Interlaboratory evaluation of a cow's milk allergy mouse model to assess the allergenicity of hydrolysed cow's milk based infant formulas. Toxicol Lett. 2013;220:95‐102. PubMed
van Esch B, Gros‐van Hest M, Westerbeek H, Garssen J. Sensitizing capacity and allergenicity of enzymatically cross‐linked sodium caseinate in comparison to sodium caseinate in a mouse model for cow’s milk allergy. Toxicol Lett. 2013;218:50‐55. PubMed
Noval Rivas M, Burton OT, Wise P, et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol. 2013;131:201‐212. PubMed PMC
Perrier C, Corthésy B. Gut permeability and food allergies. Clin Exp Allergy. 2011;41:20‐28. PubMed
Stefka AT, Feehley T, Tripathi P, et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci USA. 2014;111:13145‐13150. PubMed PMC
Tordesillas L, Rahman AH, Hartmann BM, Sampson HA, Berin MC. Mass cytometry profiling the response of basophils and the complete peripheral blood compartment to peanut. J Allergy Clin Immunol. 2016;138(6):1741‐1744. PubMed PMC
Tordesillas L, Goswami R, Benedé S, et al. Skin exposure promotes a Th2‐dependent sensitization to peanut allergens. J Clin Invest. 2014;124:4965‐4975. PubMed PMC
Roth‐Walter F, Berin MC, Arnaboldi P, et al. Pasteurization of milk proteins promotes allergic sensitization by enhancing uptake through Peyer’s patches. Allergy. 2008;63:882‐890. PubMed
Li X‐M, Srivastava K, Huleatt JW, Bottomly K, Burks AW, Sampson HA. Engineered recombinant peanut protein and heat‐killed Listeria monocytogenes coadministration protects against peanut‐induced anaphylaxis in a murine model. J Immunol. 2003;170:3289‐3295. PubMed
Singh A, Demont A, Actis‐Goretta L, et al. Identification of epicatechin as one of the key bioactive constituents of polyphenol‐enriched extracts that demonstrate an anti‐allergic effect in a murine model of food allergy. Br J Nutr. 2014;112:358‐368. PubMed
Hacini‐Rachinel F, Vissers YM, Doucet‐Ladevéze R, et al. Low‐allergenic hydrolyzed egg induces oral tolerance in mice. Int Arch Allergy Immunol. 2014;164:64‐73. PubMed
Gomes‐Santos AC, Fonseca RC, Lemos L, et al. Hydrolyzed whey protein prevents the development of food allergy to β‐lactoglobulin in sensitized mice. Cell Immunol. 2015;298:47‐53. PubMed
Adel‐Patient K, Nahori M‐A, Proust B, et al. Elicitation of the allergic reaction in beta‐lactoglobulin‐sensitized Balb/c mice: biochemical and clinical manifestations differ according to the structure of the allergen used for challenge. Clin Exp Allergy. 2003;33:376‐385. PubMed
Curciarello R, Smaldini PL, Candreva AM, et al. Targeting a cross‐reactive Gly m 5 soy peptide as responsible for hypersensitivity reactions in a milk allergy mouse model. PLoS ONE. 2014;9:e82341. PubMed PMC
Smit J, de Zeeuw‐Brouwer M, van Roest M, de Jong G, van Bilsen J. Evaluation of the sensitizing potential of food proteins using two mouse models. Toxicol Lett. 2016;262:62‐69. PubMed
Bøgh KL, Barkholt V, Madsen CB. Characterization of the immunogenicity and allergenicity of two cow’s milk hydrolysates – a study in Brown Norway rats. Scand J Immunol. 2015;81:274‐283. PubMed
Adel‐Patient K, Ah‐Leung S, Bernard H, Durieux‐Alexandrenne C, Créminon C, Wal J‐M. Oral sensitization to peanut is highly enhanced by application of peanut extracts to intact skin, but is prevented when CpG and cholera toxin are added. Int Arch Allergy Immunol. 2007;143:10‐20. PubMed
Wavrin S, Bernard H, Wal JM, Adel‐Patient K. Cutaneous or respiratory exposures to peanut allergens in mice and their impacts on subsequent oral exposure. Int Arch Allergy Immunol. 2014;164:189‐199. PubMed
Guillon B, Bernard H, Drumare MF, Hazebrouck S, Adel‐Patient K. Heat processing of peanut seed enhances the sensitization potential of the major peanut allergen Ara h 6. Mol Nutr Food Res. 2016;60:2722‐2735. PubMed PMC
van Wijk F, Hartgring S, Koppelman SJ, Pieters R, Knippels L. Mixed antibody and T cell responses to peanut and the peanut allergens Ara h 1, Ara h 2, Ara h 3 and Ara h 6 in an oral sensitization model. Clin Exp Allergy. 2004;34:1422‐1428. PubMed
Li X‐M, Serebrisky D, Lee S‐Y, et al. A murine model of peanut anaphylaxis: T‐ and B‐cell responses to a major peanut allergen mimic human responses. J Allergy Clin Immunol. 2000;106:150‐158. PubMed
Kroghsbo S, Bøgh KL, Rigby NM, Mills E, Rogers A, Madsen CB. Sensitization with 7S globulins from peanut, hazelnut, soy or pea induces IgE with different biological activities which are modified by soy tolerance. Int Arch Allergy Immunol. 2011;155:212‐224. PubMed
Bøgh KL, Kroghsbo S, Dahl L, et al. Digested Ara h 1 has sensitizing capacity in Brown Norway rats. Clin Exp Allergy. 2009;39:1611‐1621. PubMed
Madsen JL, Kroghsbo S, Madsen CB, Pozdnyakova I, Barkholt V, Bøgh KL. The impact of structural integrity and route of administration on the antibody specificity against three cow’s milk allergens – a study in Brown Norway rats. Clin Transl Allergy. 2014;4:25. PubMed PMC
Gould HJ, Sutton BJ. IgE in allergy and asthma today. Nat Rev Immunol. 2008;8:205‐217. PubMed
El‐Khouly F, Lewis SA, Pons L, Burks AW, Hourihane JO. IgG and IgE avidity characteristics of peanut allergic individuals. Pediatr Allergy Immunol. 2007;18:607‐613. PubMed
Wang J, Lin J, Bardina L, et al. Correlation of IgE/IgG4 milk epitopes and affinity of milk‐specific IgE antibodies with different phenotypes of clinical milk allergy. J Allergy Clin Immunol. 2010;125(3):695‐702. PubMed PMC
Pullen GR, Fitzgerald MG, Hosking CS. Antibody avidity determination by ELISA using thiocyanate elution. J Immunol Methods. 1986;86(1):83‐90. PubMed
Lew AM, Anders RF, Edwards SJ, Langford CJ. Comparison of antibody avidity and titre elicited by peptide as a protein conjugate or as expressed in vaccinia. Immunology. 1988;65:311. PubMed PMC
Noti M, Kim BS, Siracusa MC, et al. Exposure to food allergens through inflamed skin promotes intestinal food allergy through the thymic stromal lymphopoietin‐basophil axis. J Allergy Clin Immunol. 2014;133(5):1390‐1399. PubMed PMC
Moghaddam AE, Hillson WR, Noti M, et al. Dry roasting enhances peanut‐induced allergic sensitization across mucosal and cutaneous routes in mice. J Allergy Clin Immunol. 2014;134:1453‐1456. PubMed PMC
Han H, Thelen TD, Comeau MR, Ziegler SF. Thymic stromal lymphopoietin‐mediated epicutaneous inflammation promotes acute diarrhea and anaphylaxis. J Clin Invest. 2014;124:5442‐5452. PubMed PMC
Forbes EE, Groschwitz K, Abonia JP, et al. IL‐9– and mast cell–mediated intestinal permeability predisposes to oral antigen hypersensitivity. J Exp Med. 2008;205:897‐913. PubMed PMC
Bartnikas LM, Gurish MF, Burton OT, et al. Epicutaneous sensitization results in IgE‐dependent intestinal mast cell expansion and food‐induced anaphylaxis. J Allergy Clin Immunol. 2013;131(2):451‐460. PubMed PMC
Noval Rivas M, Burton O, Wise P, et al. Regulatory T cell reprogramming toward a Th2‐cell‐like lineage impairs oral tolerance and promotes food allergy. Immunity. 2015;42:512‐523. PubMed PMC
Ganeshan K, Neilsen CV, Hadsaitong A, Schleimer RP, Luo X, Bryce PJ. Impairing oral tolerance promotes allergy and anaphylaxis: a new murine food allergy model. J Allergy Clin Immunol. 2009;123(1):231‐238. PubMed PMC
Galand C, Leyva‐Castillo JM, Yoon J, et al. IL‐33 promotes food anaphylaxis in epicutaneously sensitized mice by targeting mast cells. J Allergy Clin Immunol. 2016;138:1356‐1366. PubMed PMC
Tordesillas L, Mondoulet L, Blazquez AB, Benhamou P‐H, Sampson HA, Berin MC. Epicutaneous immunotherapy induces gastrointestinal LAP + regulatory T cells and prevents food‐induced anaphylaxis. J Allergy Clin Immunol. 2017;139(1):189‐201. PubMed PMC
Frossard CP, Zimmerli SC, Rincon Garriz JM, Eigenmann PA. Food allergy in mice is modulated through the thymic stromal lymphopoietin pathway. Clin Transl Allergy. 2015;6:2. PubMed PMC
Nakajima‐Adachi H, Kikuchi A, Fujimura Y, et al. Peyer’s patches and mesenteric lymph nodes cooperatively promote enteropathy in a mouse model of food allergy. PLoS ONE. 2014;9:e107492. PubMed PMC
Knight AK, Bele A, Zhang S, Mayer L, Sampson HA, Berin MC. CD4 T cells activated in the mesenteric lymph node mediate gastrointestinal food allergy in mice. Am J Physiol Gastrointest Liver Physiol. 2007;293(6):G1234‐G1243. PubMed
DeLong JH, Hetherington KA, Wambre E, James EA, Robinson D, Ara W. 1‐Reactive T cells in peanut allergic individuals. J Allergy Clin Immunol. 2011;127:1211‐1219. PubMed PMC
Brough HA, Cousins DJ, Munteanu A, et al. IL‐9 is a key component of memory THcell peanut‐specific responses from children with peanut allergy. J Allergy Clin Immunol. 2014;134(6):1329‐1338. PubMed
Akdis M, Burgler S, Crameri R, et al. to 37, and interferon‐γ: receptors, functions, and roles in diseases. J Allergy Clin Immunol. 2011;127:701‐721. PubMed
Frossard CP, Asigbetse KE, Burger D, Eigenmann PA. Gut T cell receptor‐γδ + intraepithelial lymphocytes are activated selectively by cholera toxin to break oral tolerance in mice. Clin Exp Immunol. 2015;180:118‐130. PubMed PMC
Saidova A, Hershkop AM, Ponce M, Eiwegger T. Allergen‐specific T cells in IgE‐mediated food allergy. Arch Immunol Ther Exp (Warsz). 2018;66:161‐170. PubMed
Haller D, Bode C, Hammes WP, Pfeifer AM, Schiffrin EJ, Blum S. Non‐pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co‐cultures. Gut. 2000;47:79‐87. PubMed PMC
Tsilingiri K, Barbosa T, Penna G, et al. Probiotic and postbiotic activity in health and disease: comparison on a novel polarised ex‐vivo organ culture model. Gut. 2012;61:1007‐1015. PubMed
Sato T, Vries RG, Snippert HJ, et al. Single Lgr5 stem cells build crypt‐villus structures in vitro without a mesenchymal niche. Nature. 2009;459:262‐265. PubMed
Clevers H. Modeling development and disease with organoids. Cell. 2016;165:1586‐1597. PubMed
Kim HJ, Li H, Collins JJ, Ingber DE. Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut‐on‐a‐chip. Proc Natl Acad Sci. 2016;113:E7‐E15. PubMed PMC
Kim HJ, Huh D, Hamilton G, Ingber DE. Human gut‐on‐a‐chip inhabited by microbial flora that experiences intestinal peristalsis‐like motions and flow. Lab Chip. 2012;12:2165. PubMed
Yissachar N, Zhou Y, Ung L, et al. An intestinal organ culture system uncovers a role for the nervous system in microbe‐immune crosstalk. Cell. 2017;168(6):1135‐1148. PubMed PMC