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A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis

Rivas, Magali Noval and Burton, Oliver T. and Wise, Petra and Zhang, Yu-gian and Hobson, Suejy A. and Lloret, Maria Garcia and Cheoud, Christel and Kuzynski, Justin and DeSantis, Todd and Warrington, Janet and Hyde, Embriette R. and Petrosino, Joseph F. and Gerber, Georg K. and Bry, Lynn and Oettgen, Hans C. and Mazmanian, Sarkis K. and Chatila, Talal A. (2013) A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. Journal of Allergy and Clinical Inmunology, 131 (1). pp. 201-212. ISSN 0091-6749. PMCID PMC3860814. https://resolver.caltech.edu/CaltechAUTHORS:20130206-080531622

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Abstract

Background: Commensal microbiota play a critical role in maintaining oral tolerance. The effect of food allergy on the gut microbial ecology remains unknown. Methods: Food allergy–prone mice with a gain-of-function mutation in the IL-4 receptor α chain (Il4raF709) and wild-type (WT) control animals were subjected to oral sensitization with chicken egg ovalbumin (OVA). Enforced tolerance was achieved by using allergen-specific regulatory T (Treg) cells. Community structure analysis of gut microbiota was performed by using a high-density 16S rDNA oligonucleotide microarrays (PhyloChip) and massively parallel pyrosequencing of 16S rDNA amplicons. Results: OVA-sensitized Il4raF709 mice exhibited a specific microbiota signature characterized by coordinate changes in the abundance of taxa of several bacterial families, including the Lachnospiraceae, Lactobacillaceae, Rikenellaceae, and Porphyromonadaceae. This signature was not shared by similarly sensitized WT mice, which did not exhibit an OVA-induced allergic response. Treatment of OVA-sensitized Il4raF709 mice with OVA-specific Treg cells led to a distinct tolerance-associated signature coincident with the suppression of the allergic response. The microbiota of allergen-sensitized Il4raF709 mice differentially promoted OVA-specific IgE responses and anaphylaxis when reconstituted in WT germ-free mice. Conclusion: Mice with food allergy exhibit a specific gut microbiota signature capable of transmitting disease susceptibility and subject to reprogramming by enforced tolerance. Disease-associated microbiota may thus play a pathogenic role in food allergy.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.jaci.2012.10.026DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3860814PubMed CentralArticle
ORCID:
AuthorORCID
Hyde, Embriette R.0000-0002-9370-0051
Petrosino, Joseph F.0000-0002-4046-6898
Mazmanian, Sarkis K.0000-0003-2713-1513
Additional Information:© 2012 American Academy of Allergy, Asthma & Immunology. Received 31 January 2012; received in revised form 18 October 2012; accepted 22 October 2012. published online 03 December 2012. Supported by National Institutes of Health grants AI 080002 (to T.A.C.), AI007512 (to O.T.B.), DK034854 and DK078938 (to L.B.), HL07627 (to G.K.G.), AI100889 (to H.C.O.), and DK078938 (to S.K.M.); a grant from the Alkek Foundation (to J.F.P.); and the Department of Defense Congressionally Directed Medical Research Program in Food allergy grant FA100085 (to T.A.C.). Disclosure of potential conflict of interest: C. Chehoud, J. Kuczynski, T. DeSantis, and J. Warrington are employees of Second Genome. E. R. Hyde has received support from The Alkek Foundation. G. K. Gerber, L. Bry, and H. C. Oettgen have received research support from the National Institutes of Health. The rest of the authors declare that they have no relevant conflicts of interest.
Funders:
Funding AgencyGrant Number
NIHAI 080002
NIHAI007512
NIHDK034854
NIHDK078938
NIHHL07627
NIHAI100889
NIHDK078938
Alkek FoundationUNSPECIFIED
Department of Defense Congressionally Directed Medical Research Program in Food allergyFA100085
Subject Keywords:Food allergy, microbiome, microbiota, regulatory T cells, tolerance, anaphylaxis, IgE, 16S rDNA, IL-4 receptor
Issue or Number:1
PubMed Central ID:PMC3860814
Record Number:CaltechAUTHORS:20130206-080531622
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130206-080531622
Official Citation:A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis Magali Noval Rivas, Oliver T. Burton, Petra Wise, Yu-qian Zhang, Suejy A. Hobson, Maria Garcia Lloret, Christel Chehoud, Justin Kuczynski, Todd DeSantis, Janet Warrington, Embriette R. Hyde, Joseph F. Petrosino, Georg K. Gerber, Lynn Bry, Hans C. Oettgen, Sarkis K. Mazmanian, Talal A. Chatila The Journal of allergy and clinical immunology 1 January 2013 (volume 131 issue 1 Pages 201-212 DOI: 10.1016/j.jaci.2012.10.026)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:36791
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:08 Feb 2013 18:28
Last Modified:15 Apr 2020 18:15

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