A distinct microbiota composition is associated with protection from food allergy in an oral mouse immunization model

Clinical Immunology

Volumn 173, Issue , 2016, Pages 10-18

  Diesner, Susanne C ^a,b   Bergmayr, Cornelia ^a   Pfitzner, Barbara ^c   Assmann, Vera ^a   Krishnamurthy, Durga ^a   Starkl, Philipp ^a   Endesfelder, David ^c   Rothballer, Michael ^c   Welzl, Gerhard ^c   Rattei, Thomas ^d   Eiwegger, Thomas ^b   Szépfalusi, Zsolt ^b   Fehrenbach, Heinz ^e   Jensen Jarolim, Erika ^a,f   Hartmann, Anton ^c   Pali Schöll, Isabella ^a,f   Untersmayr, Eva ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIV KLIN KINDER JUGENDHEILKUNDE   (Austria)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF VIENNA   (Austria)

^e RESEARCH CENTER BORSTEL   (Germany)

^f UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Allergen uptake; Bacterial community composition; Cytokines; Food allergy; Intestinal barrier function; Microbiota

Indexed keywords

ALLERGEN; BRINASE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 22; INTERLEUKIN 4; INTERLEUKIN 5; OMEPRAZOLE; OVALBUMIN; SUCRALFATE; ANTIULCER AGENT; CYTOKINE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

ANAPHYLAXIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTERIAL STRAIN; BODY TEMPERATURE; CONTROLLED STUDY; FECES MICROFLORA; FEMALE; FOOD ALLERGY; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNIZATION; INTESTINE EPITHELIUM; MAST CELL; MICROBIAL COMMUNITY; MICROFLORA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; STOMACH ACID; STOMACH PH; SYMPTOM; TH2 CELL; ANATOMY AND HISTOLOGY; ANIMAL; BACTERIUM; BAGG ALBINO MOUSE; BLOOD; CYTOLOGY; DISEASE MODEL; FECES; IMMUNOLOGY; INTESTINE; ISOLATION AND PURIFICATION; MICROBIOLOGY; ORAL DRUG ADMINISTRATION; SPLEEN; STOMACH;

ADMINISTRATION, ORAL; ALLERGENS; ANAPHYLAXIS; ANIMALS; ANTI-ULCER AGENTS; BACTERIA; CYTOKINES; DISEASE MODELS, ANIMAL; FECES; FEMALE; FOOD HYPERSENSITIVITY; GASTRIC ACID; IMMUNIZATION; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTESTINES; MICE, INBRED BALB C; MICROBIOTA; OVALBUMIN; SPLEEN; STOMACH; SUCRALFATE;

EID: 84994361302     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.10.009     Document Type: Article

References (51)

1. [1] Bock, S.A., Munoz-Furlong, A., Sampson, H.A., Further fatalities caused by anaphylactic reactions to food, 2001–2006. J. Allergy Clin. Immunol. 119 (2007), 1016–1018.
2. [2] Boden, S.R., Wesley Burks, A., Anaphylaxis: a history with emphasis on food allergy. Immunol. Rev. 242 (2011), 247–257.
3. [3] Worm, M., Grunhagen, J., Dolle, S., Food-induced anaphylaxis - data from the anaphylaxis registry. Bundesgesundheitsbl. Gesundheitsforsch. Gesundheitsschutz 59 (2016), 836–840.
4. [4] Brunner, R., Wallmann, J., Szalai, K., Karagiannis, P., Altmeppen, H., Riemer, A.B., Jensen-Jarolim, E., Pali-Scholl, I., Aluminium per se and in the anti-acid drug sucralfate promotes sensitization via the oral route. Allergy 64 (2009), 890–897.
5. [5] Diesner, S.C., Knittelfelder, R., Krishnamurthy, D., Pali-Scholl, I., Gajdzik, L., Jensen-Jarolim, E., Untersmayr, E., Dose-dependent food allergy induction against ovalbumin under acid-suppression: a murine food allergy model. Immunol. Lett. 121 (2008), 45–51.
6. [6] Diesner, S.C., Olivera, A., Dillahunt, S., Schultz, C., Watzlawek, T., Förster-Waldl, E., Pollak, A., Jensen-Jarolim, E., Untersmayr, E., Rivera, J., Sphingosine-kinase 1 and 2 contribute to oral sensitization and effector phase in a mouse model of food allergy. Immunol. Lett. 141 (2012), 210–219.
7. [7] Schöll, I., Ackermann, U., Ozdemir, C., Blumer, N., Dicke, T., Sel, S., Wegmann, M., Szalai, K., Knittelfelder, R., Untersmayr, E., Scheiner, O., Garn, H., Jensen-Jarolim, E., Renz, H., Anti-ulcer treatment during pregnancy induces food allergy in mouse mothers and a Th2-bias in their offspring. FASEB J. 21 (2007), 1264–1270.
8. [8] Untersmayr, E., Bakos, N., Schöll, I., Kundi, M., Roth-Walter, F., Szalai, K., Riemer, A.B., Ankersmit, H.J., Scheiner, O., Boltz-Nitulescu, G., Jensen-Jarolim, E., Anti-ulcer drugs promote IgE formation toward dietary antigens in adult patients. FASEB J. 19 (2005), 656–658.
9. [9] Untersmayr, E., Schöll, I., Swoboda, I., Beil, W.J., Förster-Waldl, E., Walter, F., Riemer, A., Kraml, G., Kinaciyan, T., Spitzauer, S., Boltz-Nitulescu, G., Scheiner, O., Jensen-Jarolim, E., Antacid medication inhibits digestion of dietary proteins and causes food allergy: a fish allergy model in Balb/c mice. J. Allergy Clin. Immunol. 112 (2003), 616–623.
10. [10] Schöll, I., Untersmayr, E., Bakos, N., Roth-Walter, F., Gleiss, A., Boltz-Nitulescu, G., Scheiner, O., Jensen-Jarolim, E., Antiulcer drugs promote oral sensitization and hypersensitivity to hazelnut allergens in BALB/c mice and humans. Am. J. Clin. Nutr. 81 (2005), 154–160.
11. [11] Dehlink, E., Yen, E., Leichtner, A.M., Hait, E.J., Fiebiger, E., First evidence of a possible association between gastric acid suppression during pregnancy and childhood asthma: a population-based register study. Clin. Exp. Allergy 39 (2009), 246–253.
12. [12] DeMuth, K., Stecenko, A., Sullivan, K., Fitzpatrick, A., Relationship between treatment with antacid medication and the prevalence of food allergy in children. Allergy Asthma Proc. 34 (2013), 227–232.
13. [13] Ramirez, E., Cabanas, R., Laserna, L.S., Fiandor, A., Tong, H., Prior, N., Calderon, O., Medrano, N., Bobolea, I., Frias, J., Quirce, S., Proton pump inhibitors are associated with hypersensitivity reactions to drugs in hospitalized patients: a nested case-control in a retrospective cohort study. Clin. Exp. Allergy 43 (2013), 344–352.
14. [14] Trikha, A., Baillargeon, J.G., Kuo, Y.F., Tan, A., Pierson, K., Sharma, G., Wilkinson, G., Bonds, R.S., Development of food allergies in patients with gastroesophageal reflux disease treated with gastric acid suppressive medications. Pediatr. Allergy Immunol. 24 (2013), 582–588.
15. [15] Pali-Schöll, I., Yildirim, A.O., Ackermann, U., Knauer, T., Becker, C., Garn, H., Renz, H., Jensen-Jarolim, E., Fehrenbach, H., Anti-acids lead to immunological and morphological changes in the intestine of BALB/c mice similar to human food allergy. Exp. Toxicol. Pathol. 60 (2008), 337–345.
16. [16] Lane, D.J., 16S/23S rRNA sequencing. Stackebrandt, E., Goodfellow, M., (eds.) Nucleic Acid Techniques in Bacterial Systematics, 1991, Wiley, New York, 115–175.
17. [17] Juretschko, S., Timmermann, G., Schmid, M., Schleifer, K.-H., Pommerening-Röser, A., Koops, H.-P., Wagner, M., Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and nitrospira-like bacteria as dominant populations. Appl. Environ. Microbiol. 64 (1998), 3042–3051.
18. [18] Schloss, P.D., Gevers, D., Westcott, S.L., Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One, 6, 2011, e27310.
19. [19] Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J., Weber, C.F., Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 (2009), 7537–7541.
20. [20] Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41 (2013), D590–D596.
21. [21] Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (2011), 2194–2200.
22. [22] Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., Kulam-Syed-Mohideen, A.S., McGarrell, D.M., Marsh, T., Garrity, G.M., Tiedje, J.M., The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37 (2009), D141–D145.
23. [23] Dixon, P., VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14 (2003), 927–930.
24. [24] Dray, S., Doufour, A.B., The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22 (2007), 1–20.
25. [25] Gupta, R., Holdford, D., Bilaver, L., Dyer, A., Holl, J.L., Meltzer, D., The economic impact of childhood food allergy in the United States. JAMA Pediatr. 167 (2013), 1026–1031.
26. [26] Graham, M.T., Nadeau, K.C., Lessons learned from mice and man: mimicking human allergy through mouse models. Clin. Immunol. 155 (2014), 1–16.
27. [27] Oyoshi, M.K., Oettgen, H.C., Chatila, T.A., Geha, R.S., Bryce, P.J., Food allergy: insights into etiology, prevention, and treatment provided by murine models. J. Allergy Clin. Immunol. 133 (2014), 309–317.
28. [28] Bogh, K.L., van Bilsen, J., Glogowski, R., Lopez-Exposito, I., Bouchaud, G., Blanchard, C., Bodinier, M., Smit, J., Pieters, R., Bastiaan-Net, S., de Wit, N., Untersmayr, E., Adel-Patient, K., Knippels, L., Epstein, M.M., Noti, M., Nygaard, U.C., Kimber, I., Verhoeckx, K., O'Mahony, L., Current challenges facing the assessment of the allergenic capacity of food allergens in animal models. Clin. Transl. Allergy, 6, 2016, 21.
29. [29] Brunner, R., Wallmann, J., Szalai, K., Karagiannis, P., Kopp, T., Scheiner, O., Jensen-Jarolim, E., Pali-Scholl, I., The impact of aluminium in acid-suppressing drugs on the immune response of BALB/c mice. Clin. Exp. Allergy 37 (2007), 1566–1573.
30. [30] Untersmayr, E., Diesner, S.C., Bramswig, K.H., Knittelfelder, R., Bakos, N., Gundacker, C., Lukschal, A., Wallmann, J., Szalai, K., Pali-Scholl, I., Boltz-Nitulescu, G., Scheiner, O., Duschl, A., Jensen-Jarolim, E., Characterization of intrinsic and extrinsic risk factors for celery allergy in immunosenescence. Mech. Ageing Dev. 129 (2008), 120–128.
31. [31] Pali-Schöll, I., Herzog, R., Wallmann, J., Szalai, K., Brunner, R., Lukschal, A., Karagiannis, P., Diesner, S.C., Jensen-Jarolim, E., Antacids and dietary supplements with an influence on the gastric pH increase the risk for food sensitization. Clin. Exp. Allergy 40 (2010), 1091–1098.
32. [32] Untersmayr, E., Diesner, S.C., Oostingh, G.J., Selzle, K., Pfaller, T., Schultz, C., Zhang, Y., Krishnamurthy, D., Starkl, P., Knittelfelder, R., Forster-Waldl, E., Pollak, A., Scheiner, O., Poschl, U., Jensen-Jarolim, E., Duschl, A., Nitration of the egg-allergen ovalbumin enhances protein allergenicity but reduces the risk for oral sensitization in a murine model of food allergy. PLoS One, 5, 2010, e14210.
33. [33] Brandtzaeg, P., Update on mucosal immunoglobulin A in gastrointestinal disease. Curr. Opin. Gastroenterol. 26 (2010), 554–563.
34. [34] Johansen, F.E., Pekna, M., Norderhaug, I.N., Haneberg, B., Hietala, M.A., Krajci, P., Betsholtz, C., Brandtzaeg, P., Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component-deficient mice. J. Exp. Med. 190 (1999), 915–922.
35. [35] Finkelman, F.D., Rothenberg, M.E., Brandt, E.B., Morris, S.C., Strait, R.T., Molecular mechanisms of anaphylaxis: lessons from studies with murine models. J. Allergy Clin. Immunol. 115 (2005), 449–457 (quiz 458).
36. [36] Frossard, C.P., Hauser, C., Eigenmann, P.A., Antigen-specific secretory IgA antibodies in the gut are decreased in a mouse model of food allergy. J. Allergy Clin. Immunol. 114 (2004), 377–382.
37. [37] Corazza, N., Kaufmann, T., Novel insights into mechanisms of food allergy and allergic airway inflammation using experimental mouse models. Allergy 67 (2012), 1483–1490.
38. [38] Karlsson, M.R., Johansen, F.E., Kahu, H., Macpherson, A., Brandtzaeg, P., Hypersensitivity and oral tolerance in the absence of a secretory immune system. Allergy 65 (2010), 561–570.
39. [39] Bailon, E., Cueto-Sola, M., Utrilla, P., Rodriguez-Ruiz, J., Garrido-Mesa, N., Zarzuelo, A., Xaus, J., Galvez, J., Comalada, M., A shorter and more specific oral sensitization-based experimental model of food allergy in mice. J. Immunol. Methods 381 (2012), 41–49.
40. [40] Gill, N., Finlay, B.B., The gut microbiota: challenging immunology. Nature 11 (2011), 636–637.
41. [41] Penders, J., Thijs, C., van den Brandt, P.A., Kummeling, I., Snijders, B., Stelma, F., Adams, H., van Ree, R., Stobberingh, E.E., Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 56 (2007), 661–667.
42. [42] Rodriguez, B., Prioult, G., Bibiloni, R., Nicolis, I., Mercenier, A., Butel, M.J., Waligora-Dupriet, A.J., Germ-free status and altered caecal subdominant microbiota are associated with a high susceptibility to cow's milk allergy in mice. FEMS Microbiol. Ecol. 76 (2011), 133–144.
43. [43] Strachan, D.P., Hay fever, hygiene, and household size. BMJ 299 (1989), 1259–1260.
44. [44] Bjorksten, B., The hygiene hypothesis: do we still believe in it?. Nestle Nutr. Workshop Ser. Pediatr. Program 64 (2009), 11–18 (discussion 18–22, 251–257).
45. [45] Ivanov, I.I., Rde, L.F., Manel, N., Yoshinaga, K., Rifkin, D.B., Sartor, R.B., Finlay, B.B., Littman, D.R., Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4 (2008), 337–349.
46. [46] Friswell, M.K., Gika, H., Stratford, I.J., Theodoridis, G., Telfer, B., Wilson, I.D., McBain, A.J., Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS One, 5, 2010, e8584.
47. [47] Grant, M.M., Kolamunne, R.T., Lock, F.E., Matthews, J.B., Chapple, I.L., Griffiths, H.R., Oxygen tension modulates the cytokine response of oral epithelium to periodontal bacteria. J. Clin. Periodontol. 37 (2010), 1039–1048.
48. [48] Noval Rivas, M., Burton, O.T., Wise, P., Zhang, Y.Q., Hobson, S.A., Garcia Lloret, M., Chehoud, C., Kuczynski, J., DeSantis, T., Warrington, J., Hyde, E.R., Petrosino, J.F., Gerber, G.K., Bry, L., Oettgen, H.C., Mazmanian, S.K., Chatila, T.A., A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J. Allergy Clin. Immunol. 131 (2013), 201–212.
49. [49] Stefka, A.T., Feehley, T., Tripathi, P., Qiu, J., McCoy, K., Mazmanian, S.K., Tjota, M.Y., Seo, G.Y., Cao, S., Theriault, B.R., Antonopoulos, D.A., Zhou, L., Chang, E.B., Fu, Y.X., Nagler, C.R., Commensal bacteria protect against food allergen sensitization. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 13145–13150.
50. [50] Sonnenberg, G.F., Fouser, L.A., Artis, D., Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12 (2011), 383–390.
51. [51] Honda, K., Littman, D.R., The microbiota in adaptive immune homeostasis and disease. Nature 535 (2016), 75–84.