The use of animal models to discover immunological mechanisms underpinning sensitization to food allergens

Drug Discovery Today: Disease Models

Volumn 17-18, Issue , 2015, Pages 63-69

  Smit, Joost J ^a   Noti, Mario ^b   O'Mahony, Liam ^c  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FOOD ALLERGEN;

ADAPTIVE IMMUNITY; ALLERGENICITY; ALLERGIC REACTION; ANIMAL MODEL; BALB/C NUDE MOUSE; FOOD ALLERGY; IMMUNE RESPONSE; IMMUNE SYSTEM; INNATE IMMUNITY; MOUSE MODEL; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN INTAKE; RAT MODEL; REVIEW; RISK ASSESSMENT;

EID: 85008703813     PISSN: None     EISSN: 17406757     Source Type: Journal    
DOI: 10.1016/j.ddmod.2016.09.001     Document Type: Review

References (49)

1. [1] Eigenmann, P.A., T lymphocytes in food allergy: overview of an intricate network of circulating and organ-resident cells. Pediatr Allergy Immunol 13 (2002), 162–171.
2. [2] Gould, H.J., Ramadani, F., IgE responses in mouse and man and the persistence of IgE memory. Trends Immunol 36 (2015), 40–48, 10.1016/j.it.2014.11.002.
3. [3] Strobel, S., Ferguson, A., Immune responses to fed protein antigens in mice. 3. Systemic tolerance or priming is related to age at which antigen is first encountered. Pediatr Res 18 (1984), 588–594, 10.1203/00006450-198407000-00004.
4. [4] Verhasselt, V., Oral tolerance in neonates: from basics to potential prevention of allergic disease. Mucosal Immunol 3 (2010), 326–333, 10.1038/mi.2010.25.
5. [5] Dupont, D., Mackie, A.R., Static and dynamic in vitro digestion models to study protein stability in the gastrointestinal tract and help predict allergenicity. Drug Discov Today Dis Models, 2016 [in press].
6. [6] Frei, R., Lauener, R.P., Crameri, R., O'Mahony, L., Microbiota and dietary interactions: an update to the hygiene hypothesis?. Allergy 67 (2012), 451–461, 10.1111/j.1398-9995.2011.02783.x.
7. [7] Palomares, O., Martín-Fontecha, M., Lauener, R., Traidl-Hoffmann, C., Cavkaytar, O., Akdis, M., et al. Regulatory T cells and immune regulation of allergic diseases: roles of IL-10 and TGF-β. Genes Immun 15 (2014), 511–520, 10.1038/gene.2014.45.
8. [8] Noval Rivas, M., Burton, O.T., Oettgen, H.C., 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, 10.1016/j.jaci.2016.02.030.
9. [9] Schulz, O., Jaensson, E., Persson, E.K., Liu, X., Worbs, T., Agace, W.W., et al. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 206 (2009), 3101–3114, 10.1084/jem.20091925.
10. [10] Saenz, S.A., Noti, M., Artis, D., Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends Immunol 31 (2010), 407–413, 10.1016/j.it.2010.09.001.
11. [11] Chu, D.K., Llop-Guevara, A., Walker, T.D., Flader, K., Goncharova, S., Boudreau, J.E., et al. IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol, 131, 2013, 10.1016/j.jaci.2012.08.002 187–200.e1–8.
12. [12] Schiavi, E., Smolinska, S., O'Mahony, L., Intestinal dendritic cells. Curr Opin Gastroenterol 31 (2015), 98–103, 10.1097/MOG.0000000000000155.
13. [13] Pabst, O., Mowat, A.M., Oral tolerance to food protein. Mucosal Immunol 5 (2012), 232–239, 10.1038/mi.2012.4.
14. [14] Bol-Schoenmakers, M., Marcondes Rezende, M., Bleumink, R., Boon, L., Man, S., Hassing, I., et al. Regulation by intestinal γδ T cells during establishment of food allergic sensitization in mice. Allergy 66 (2011), 331–340, 10.1111/j.1398-9995.2010.02479.x.
15. [15] Hussain, M., Epstein, M.M., Noti, M., Noti, Experimental food allergy models to study the role of innate immune cells as initiators of allergen specific Th2 immune responses. Drug Discov Today Dis Models, 2016 [in press].
16. [16] Knight, A.K., Blázquez, A.B., Zhang, S., Mayer, L., Sampson, H.A., Berin, M.C., CD4 T cells activated in the mesenteric lymph node mediate gastrointestinal food allergy in mice. Am J Physiol Gastrointest Liver Physiol 293 (2007), G1234–G1243, 10.1152/ajpgi.00323.2007.
17. [17] Oettgen, H.C., Fifty years later: emerging functions of IgE antibodies in host defense, immune regulation, and allergic diseases. J Allergy Clin Immunol 137 (2016), 1631–1645, 10.1016/j.jaci.2016.04.009.
18. [18] Stanic, B., van de Veen, W., Wirz, O.F., Rückert, B., Morita, H., Söllner, S., et al. IL-10-overexpressing B cells regulate innate and adaptive immune responses. J Allergy Clin Immunol 135 (2015), 771–778, 10.1016/j.jaci.2014.07.041.
19. [19] Bloomfield, S.F., Stanwell-Smith, R., Crevel, R.W.R., Pickup, J., Too clean, or not too clean: the hygiene hypothesis and home hygiene. Clin Exp Allergy 36 (2006), 402–425, 10.1111/j.1365-2222.2006.02463.x.
20. [20] Van Gramberg, J.L., de Veer, M.J., O'Hehir, R.E., Meeusen, E.N.T., Bischof, R.J., Use of animal models to investigate major allergens associated with food allergy. J Allergy (Cairo), 2013, 2013, 10.1155/2013/635695 635695–10.
21. [21] Atkinson, H.A., Miller, K., Assessment [correction of Assessment] of the brown Norway rat as a suitable model for the investigation of food allergy. Toxicology 91 (1994), 281–288.
22. [22] Kool, M., Soullié, T., van Nimwegen, M., Willart, M.A.M., Muskens, F., Jung, S., et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 205 (2008), 869–882, 10.1084/jem.20071087.
23. [23] Chu, D.K., Mohammed-Ali, Z., Jiménez-Saiz, R., Walker, T.D., Goncharova, S., Llop-Guevara, A., et al. T helper cell IL-4 drives intestinal Th2 priming to oral peanut antigen, under the control of OX40L and independent of innate-like lymphocytes. Mucosal Immunol 7 (2014), 1395–1404, 10.1038/mi.2014.29.
24. [24] Smit, J.J., Bol-Schoenmakers, M., Hassing, I., Fiechter, D., Boon, L., Bleumink, R., et al. The role of intestinal dendritic cells subsets in the establishment of food allergy. Clin Exp Allergy 41 (2011), 890–898, 10.1111/j.1365-2222.2011.03738.x.
25. [25] Berin, M.C., Mayer, L., Immunophysiology of experimental food allergy. Mucosal Immunol 2 (2009), 24–32, 10.1038/mi.2008.72.
26. [26] Arias, K., Chu, D.K., Flader, K., Botelho, F., Walker, T., Arias, N., et al. Distinct immune effector pathways contribute to the full expression of peanut-induced anaphylactic reactions in mice. J Allergy Clin Immunol, 127, 2011, 10.1016/j.jaci.2011.03.044 1552–61.e1.
27. [27] Bol-Schoenmakers, M., Braber, S., Akbari, P., de Graaff, P., van Roest, M., Kruijssen, L., et al. The mycotoxin deoxynivalenol facilitates allergic sensitization to whey in mice. Mucosal Immunol, 2016, 10.1038/mi.2016.13.
28. [28] Srivastava, K.D., Siefert, A., Fahmy, T.M., Caplan, M.J., Li, X-M., Sampson, H.A., Investigation of peanut oral immunotherapy with CpG/peanut nanoparticles in a murine model of peanut allergy. J Allergy Clin Immunol, 2016, 10.1016/j.jaci.2016.01.047.
29. [29] Ladics, G.S., Fry, J., Goodman, R., Herouet-Guicheney, C., Hoffmann-Sommergruber, K., Madsen, C.B., et al. Allergic sensitization: screening methods. Clin Transl Allergy, 4, 2014, 13, 10.1186/2045-7022-4-13.
30. [30] Liu, T., Navarro, S., Lopata, A.L., Current advances of murine models for food allergy. Mol Immunol 70 (2016), 104–117, 10.1016/j.molimm.2015.11.011.
31. [31] Bøgh, K.L., van Bilsen, J., Głogowski, R., López-Expósito, I., Bouchaud, G., Blanchard, C., et al. Current challenges facing the assessment of the allergenic capacity of food allergens in animal models. Clin Transl Allergy, 6, 2016, 21, 10.1186/s13601-016-0110-2.
32. [32] Wavrin, S., Bernard, H., Wal, J-M., Adel-Patient, K., Influence of the route of exposure and the matrix on the sensitisation potency of a major cows’ milk allergen. Clin Transl Allergy, 5, 2015, 3, 10.1186/s13601-015-0047-x.
33. [33] Dearman, R.J., Kimber, I., Determination of protein allergenicity: studies in mice. Toxicol Lett 120 (2001), 181–186.
34. [34] Barcik, W., Untersmayr, E., Pali-Schöll, I., O'Mahony, L., Frei, R., Influence of microbiome and diet on immune responses in food allergy models. Drug Discov Today Dis Models, 2016.
35. [35] Smit, J.J., Willemsen, K., Hassing, I., Fiechter, D., Storm, G., van Bloois, L., et al. Contribution of classic and alternative effector pathways in peanut-induced anaphylactic responses. PLoS ONE, 6, 2011, e28917, 10.1371/journal.pone.0028917.
36. [36] Li, X.M., Serebrisky, D., Lee, S.Y., Huang, C.K., Bardina, L., Schofield, B.H., 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 106 (2000), 150–158, 10.1067/mai.2000.107395.
37. [37] Evans, H., Killoran, K.E., Mitre, E., Measuring local anaphylaxis in mice. J Vis Exp, 2014, e52005, 10.3791/52005.
38. [38] Bowman, C.C., Selgrade, M.K., Differences in allergenic potential of food extracts following oral exposure in mice reflect differences in digestibility: potential approaches to safety assessment. Toxicol Sci 102 (2008), 100–109, 10.1093/toxsci/kfm288.
39. [39] Smit, J., Zeeuw-Brouwer, M.L., van Roest, M., de Jong, G., van Bilsen, J., Evaluation of the sensitizing potential of food proteins using two mouse models. Toxicol Lett 262 (2016), 62–69, 10.1016/j.toxlet.2016.09.005.
40. [40] Velickovic, T.C., Jankov, R.M., Design and modifications of allergens for improving specific immunotherapy. Inflamm Allergy Drug Targets 7 (2008), 270–278.
41. [41] Smit, J.J., Pennings, M.T., Willemsen, K., van Roest, M., van Hoffen, E., Pieters, R.H., Heterogeneous responses and cross reactivity between the major peanut allergens Ara h 1, 2,3 and 6 in a mouse model for peanut allergy. Clin Transl Allergy, 5, 2015, 13, 10.1186/s13601-015-0056-9.
42. [42] Kucuk, Z.Y., Strait, R., Khodoun, M.V., Mahler, A., Hogan, S., Finkelman, F.D., Induction and suppression of allergic diarrhea and systemic anaphylaxis in a murine model of food allergy. J Allergy Clin Immunol 129 (2012), 1343–1348, 10.1016/j.jaci.2012.03.004.
43. [43] Tordesillas, L., Goswami, R., Benedé, S., Grishina, G., Dunkin, D., Järvinen, K.M., et al. Skin exposure promotes a Th2-dependent sensitization to peanut allergens. J Clin Invest 124 (2014), 4965–4975, 10.1172/JCI75660.
44. [44] Wavrin, S., Bernard, H., Wal, J.-M., Adel-Patient, K., Influence of the route of exposure and the matrix on the sensitisation potency of a major cows’ milk allergen. Clin Transl Allergy, 5, 2015, 3, 10.1186/s13601-015-0047-x.
45. [45] Gonipeta, B., Parvataneni, S., Tempelman, R.J., Gangur, V., An adjuvant-free mouse model to evaluate the allergenicity of milk whey protein. J Dairy Sci 92 (2009), 4738–4744, 10.3168/jds.2008-1927.
46. [46] Li, X.-M., Srivastava, K., Huleatt, J.W., Bottomly, K., Burks, A.W., Sampson, H.A., Engineered recombinant peanut protein and heat-killed Listeria monocytogenes coadministration protects against peanut-induced anaphylaxis in a murine model. J Immunol 170 (2003), 3289–3295.
47. [47] Frossard, C.P., Zimmerli, S.C., Rincon Garriz, J.M., Eigenmann, P.A., Food allergy in mice is modulated through the thymic stromal lymphopoietin pathway. Clin Transl Allergy, 6, 2015, 2, 10.1186/s13601-016-0090-2.
48. [48] van Esch, B.C.A.M., van Bilsen, J.H.M., Jeurink, P.V., Garssen, J., Penninks, A.H., Smit, J.J., 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 220 (2013), 95–102, 10.1016/j.toxlet.2013.04.008.
49. [49] Ganeshan, K., Neilsen, C.V., Hadsaitong, A., Schleimer, R.P., Luo, X., Bryce, P.J., Impairing oral tolerance promotes allergy and anaphylaxis: a new murine food allergy model. J Allergy Clin Immunol 123 (2009), 231–238.e4, 10.1016/j.jaci.2008.10.011.