Review
. 2013 May; 23(9):R389-400.
doi: 10.1016/j.cub.2013.02.043.

Mucosal immunology of food allergy

M Cecilia Berin 1 Hugh A Sampson  
Affiliations
  • PMID: 23660362
  •     140 References
  •     43 citations

Abstract

Food allergies are increasing in prevalence at a higher rate than can be explained by genetic factors, suggesting a role for as yet unidentified environmental factors. In this review, we summarize the state of knowledge about the healthy immune response to antigens in the diet and the basis of immune deviation that results in immunoglobulin E (IgE) sensitization and allergic reactivity to foods. The intestinal epithelium forms the interface between the external environment and the mucosal immune system, and emerging data suggest that the interaction between intestinal epithelial cells and mucosal dendritic cells is of particular importance in determining the outcome of immune responses to dietary antigens. Exposure to food allergens through non-oral routes, in particular through the skin, is increasingly recognized as a potentially important factor in the increasing rate of food allergy. There are many open questions on the role of environmental factors, such as dietary factors and microbiota, in the development of food allergy, but data suggest that both have an important modulatory effect on the mucosal immune system. Finally, we discuss recent developments in our understanding of immune mechanisms of clinical manifestations of food allergy. New experimental tools, particularly in the field of genomics and the microbiome, are likely to shed light on factors responsible for the growing clinical problem of food allergy.

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Predicting a human gut microbiota's response to diet in gnotobiotic mice.
Jeremiah J Faith, Nathan P McNulty, Federico E Rey, Jeffrey I Gordon.
Science, 2011 May 21; 333(6038). PMID: 21596954    Free PMC article.
Highly Cited.
Ingested allergens must be absorbed systemically to induce systemic anaphylaxis.
Richard T Strait, Ashley Mahler, +3 authors, Fred D Finkelman.
J Allergy Clin Immunol, 2011 Mar 01; 127(4). PMID: 21354602    Free PMC article.
The human gut virome: inter-individual variation and dynamic response to diet.
Samuel Minot, Rohini Sinha, +5 authors, Frederic D Bushman.
Genome Res, 2011 Sep 02; 21(10). PMID: 21880779    Free PMC article.
Highly Cited.
Loss-of-function variants in the filaggrin gene are a significant risk factor for peanut allergy.
Sara J Brown, Yuka Asai, +20 authors, W H Irwin McLean.
J Allergy Clin Immunol, 2011 Mar 08; 127(3). PMID: 21377035    Free PMC article.
Highly Cited.
The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice.
Peter J Turnbaugh, Vanessa K Ridaura, +3 authors, Jeffrey I Gordon.
Sci Transl Med, 2010 Apr 07; 1(6). PMID: 20368178    Free PMC article.
Highly Cited.
Allergen-responsive CD4+CD25+ regulatory T cells in children who have outgrown cow's milk allergy.
Malin R Karlsson, Jarle Rugtveit, Per Brandtzaeg.
J Exp Med, 2004 Jun 16; 199(12). PMID: 15197226    Free PMC article.
Gastrointestinal dendritic cells promote Th2 skewing via OX40L.
Ana Belén Blázquez, M Cecilia Berin.
J Immunol, 2008 Mar 21; 180(7). PMID: 18354165
Rising prevalence of allergy to peanut in children: Data from 2 sequential cohorts.
Jane Grundy, Sharon Matthews, +2 authors, Syed Hasan Arshad.
J Allergy Clin Immunol, 2002 Nov 06; 110(5). PMID: 12417889
CD4 T cells activated in the mesenteric lymph node mediate gastrointestinal food allergy in mice.
Adina Kay Knight, Ana Belén Blázquez, +3 authors, M Cecilia Berin.
Am J Physiol Gastrointest Liver Physiol, 2007 Oct 06; 293(6). PMID: 17916645
Vitamin D levels and food and environmental allergies in the United States: results from the National Health and Nutrition Examination Survey 2005-2006.
Shimi Sharief, Sunit Jariwala, +2 authors, Michal L Melamed.
J Allergy Clin Immunol, 2011 Feb 19; 127(5). PMID: 21329969    Free PMC article.
Induction and suppression of allergic diarrhea and systemic anaphylaxis in a murine model of food allergy.
Zeynep Yesim Kucuk, Richard Strait, +3 authors, Fred D Finkelman.
J Allergy Clin Immunol, 2012 Apr 03; 129(5). PMID: 22465213    Free PMC article.
Maternal consumption of peanut during pregnancy is associated with peanut sensitization in atopic infants.
Scott H Sicherer, Robert A Wood, +7 authors, Hugh A Sampson.
J Allergy Clin Immunol, 2010 Nov 03; 126(6). PMID: 21035177    Free PMC article.
A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis.
Magali Noval Rivas, Oliver T Burton, +14 authors, Talal A Chatila.
J Allergy Clin Immunol, 2012 Dec 04; 131(1). PMID: 23201093    Free PMC article.
Highly Cited.
Cutting edge: Langerin+ dendritic cells in the mesenteric lymph node set the stage for skin and gut immune system cross-talk.
Sun-Young Chang, Hye-Ran Cha, +6 authors, Mi-Na Kweon.
J Immunol, 2008 Mar 21; 180(7). PMID: 18354155
Intestinal CD103(-) dendritic cells migrate in lymph and prime effector T cells.
V Cerovic, S A Houston, +4 authors, S W F Milling.
Mucosal Immunol, 2012 Jun 22; 6(1). PMID: 22718260
Highly Cited.
A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism.
Janine L Coombes, Karima R R Siddiqui, +4 authors, Fiona Powrie.
J Exp Med, 2007 Jul 11; 204(8). PMID: 17620361    Free PMC article.
Highly Cited.
Factors associated with the development of peanut allergy in childhood.
Gideon Lack, Deborah Fox, +2 authors, Avon Longitudinal Study of Parents and Children Study Team.
N Engl J Med, 2003 Mar 15; 348(11). PMID: 12637607
Highly Cited.
Pasteurization of milk proteins promotes allergic sensitization by enhancing uptake through Peyer's patches.
F Roth-Walter, M C Berin, +5 authors, L Mayer.
Allergy, 2008 Jul 01; 63(7). PMID: 18588554
Intrauterine sensitization of allergen-specific IgE analyzed by a highly sensitive new allergen microarray.
Norio Kamemura, Hitomi Tada, +7 authors, Hiroshi Kido.
J Allergy Clin Immunol, 2012 Apr 03; 130(1). PMID: 22464644
Immunomodulatory dendritic cells in intestinal lamina propria.
Fernando G Chirdo, Owain R Millington, Helen Beacock-Sharp, Allan McI Mowat.
Eur J Immunol, 2005 Jul 13; 35(6). PMID: 16010704
Mechanisms underlying differential food allergy response to heated egg.
Gustavo Martos, Ivan Lopez-Exposito, +2 authors, Anna Nowak-Węgrzyn.
J Allergy Clin Immunol, 2011 Mar 08; 127(4). PMID: 21377717    Free PMC article.
Lymphotoxin regulates commensal responses to enable diet-induced obesity.
Vaibhav Upadhyay, Valeriy Poroyko, +10 authors, Yang-Xin Fu.
Nat Immunol, 2012 Aug 28; 13(10). PMID: 22922363    Free PMC article.
Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells.
Tim Worbs, Ulrike Bode, +5 authors, Oliver Pabst.
J Exp Med, 2006 Mar 15; 203(3). PMID: 16533884    Free PMC article.
Highly Cited.
Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy.
Mohamed Elfatih H Bashir, Steve Louie, Hai Ning Shi, Cathryn Nagler-Anderson.
J Immunol, 2004 May 22; 172(11). PMID: 15153518
Highly Cited.
A functional role for CCR6 on proallergic T cells in the gastrointestinal tract.
Ana Belén Blázquez, Adina Kay Knight, +4 authors, M Cecilia Berin.
Gastroenterology, 2009 Sep 29; 138(1). PMID: 19782082    Free PMC article.
Allergic sensitization can be induced via multiple physiologic routes in an adjuvant-dependent manner.
David Dunkin, M Cecilia Berin, Lloyd Mayer.
J Allergy Clin Immunol, 2011 Jul 19; 128(6). PMID: 21762973    Free PMC article.
Intestinal microbiota and immunoglobulin E responses in 5-year-old Estonian children.
E Sepp, K Julge, M Mikelsaar, B Björkstén.
Clin Exp Allergy, 2005 Sep 17; 35(9). PMID: 16164439
Suppression of Th1 and Th17, but not Th2, responses in a CD8(+) T cell-mediated model of oral tolerance.
P M Arnaboldi, F Roth-Walter, L Mayer.
Mucosal Immunol, 2009 Jul 03; 2(5). PMID: 19571798    Free PMC article.
Peanut-induced intestinal allergy is mediated through a mast cell-IgE-FcepsilonRI-IL-13 pathway.
Meiqin Wang, Katsuyuki Takeda, +4 authors, Erwin W Gelfand.
J Allergy Clin Immunol, 2010 Jul 14; 126(2). PMID: 20624645    Free PMC article.
The immunology of food allergy.
Laura K Johnston, Karen B Chien, Paul J Bryce.
J Immunol, 2014 Mar 13; 192(6). PMID: 24610821    Free PMC article.
Review.
A major population of mucosal memory CD4+ T cells, coexpressing IL-18Rα and DR3, display innate lymphocyte functionality.
P Holmkvist, K Roepstorff, +10 authors, W W Agace.
Mucosal Immunol, 2014 Oct 02; 8(3). PMID: 25269704    Free PMC article.
Gut microbes and adverse food reactions: Focus on gluten related disorders.
Heather J Galipeau, Elena F Verdu.
Gut Microbes, 2014 Dec 09; 5(5). PMID: 25483329    Free PMC article.
Review.
Gene, environment, microbiome and mucosal immune tolerance in rheumatoid arthritis.
Anca I Catrina, Kevin D Deane, Jose U Scher.
Rheumatology (Oxford), 2014 Dec 30; 55(3). PMID: 25539828    Free PMC article.
Review.
Dietary ω3 fatty acid exerts anti-allergic effect through the conversion to 17,18-epoxyeicosatetraenoic acid in the gut.
Jun Kunisawa, Makoto Arita, +12 authors, Hiroshi Kiyono.
Sci Rep, 2015 Jun 13; 5. PMID: 26065911    Free PMC article.
Toll-like receptor 2 activators modulate oral tolerance in mice.
M C Tunis, B Dawod, +2 authors, J S Marshall.
Clin Exp Allergy, 2015 Aug 06; 45(11). PMID: 26242919    Free PMC article.
Immunotherapy using algal-produced Ara h 1 core domain suppresses peanut allergy in mice.
James A Gregory, Ariel Shepley-McTaggart, +5 authors, M Cecilia Berin.
Plant Biotechnol J, 2016 Jan 24; 14(7). PMID: 26801740    Free PMC article.
Antibody Production, Anaphylactic Signs, and T-Cell Responses Induced by Oral Sensitization With Ovalbumin in BALB/c and C3H/HeOuJ Mice.
Alba Pablos-Tanarro, Ivan López-Expósito, +2 authors, Elena Molina.
Allergy Asthma Immunol Res, 2016 Mar 01; 8(3). PMID: 26922934    Free PMC article.
Regulation of Exacerbated Immune Responses in Human Peripheral Blood Cells by Hydrolysed Egg White Proteins.
Daniel Lozano-Ojalvo, Elena Molina, Rosina López-Fandiño.
PLoS One, 2016 Mar 24; 11(3). PMID: 27007699    Free PMC article.
Early-life gut microbiome composition and milk allergy resolution.
Supinda Bunyavanich, Nan Shen, +8 authors, Jose C Clemente.
J Allergy Clin Immunol, 2016 Jun 14; 138(4). PMID: 27292825    Free PMC article.
Highly Cited.
Food allergy: immune mechanisms, diagnosis and immunotherapy.
Wong Yu, Deborah M Hussey Freeland, Kari C Nadeau.
Nat Rev Immunol, 2016 Nov 01; 16(12). PMID: 27795547    Free PMC article.
Highly Cited. Review.
Food allergy and the gut.
Anna Nowak-Wegrzyn, Hania Szajewska, Gideon Lack.
Nat Rev Gastroenterol Hepatol, 2016 Dec 22; 14(4). PMID: 27999436
Review.
Critical role of intestinal interleukin-4 modulating regulatory T cells for desensitization, tolerance, and inflammation of food allergy.
Haruyo Nakajima-Adachi, Kyoko Shibahara, +12 authors, Satoshi Hachimura.
PLoS One, 2017 Feb 25; 12(2). PMID: 28234975    Free PMC article.
The microbiome in allergic disease: Current understanding and future opportunities-2017 PRACTALL document of the American Academy of Allergy, Asthma & Immunology and the European Academy of Allergy and Clinical Immunology.
Yvonne J Huang, Benjamin J Marsland, +4 authors, Thomas A Fleisher.
J Allergy Clin Immunol, 2017 Mar 05; 139(4). PMID: 28257972    Free PMC article.
Highly Cited. Review.
Air Pollution and Climate Change Effects on Allergies in the Anthropocene: Abundance, Interaction, and Modification of Allergens and Adjuvants.
Kathrin Reinmuth-Selzle, Christopher J Kampf, +17 authors, Ulrich Pöschl.
Environ Sci Technol, 2017 Mar 23; 51(8). PMID: 28326768    Free PMC article.
Multifactorial Modulation of Food-Induced Anaphylaxis.
Sara Benedé, María Garrido-Arandia, +3 authors, Mayte Villalba.
Front Immunol, 2017 Jun 01; 8. PMID: 28559894    Free PMC article.
Review.
Spontaneous food allergy in Was-/- mice occurs independent of FcεRI-mediated mast cell activation.
W S Lexmond, J A Goettel, +6 authors, E Fiebiger.
Allergy, 2017 Jun 11; 72(12). PMID: 28600891    Free PMC article.
Genomic dissection of conserved transcriptional regulation in intestinal epithelial cells.
Colin R Lickwar, J Gray Camp, +5 authors, John F Rawls.
PLoS Biol, 2017 Aug 30; 15(8). PMID: 28850571    Free PMC article.
Immune mechanisms of food allergy and its prevention by early intervention.
Victor Turcanu, Helen A Brough, +4 authors, Gideon Lack.
Curr Opin Immunol, 2017 Sep 12; 48. PMID: 28892729    Free PMC article.
Review.
Oral Tolerance Development and Maintenance.
Erik Wambre, David Jeong.
Immunol Allergy Clin North Am, 2017 Nov 15; 38(1). PMID: 29132672    Free PMC article.
Review.
Managing Rheumatoid Arthritis with Dietary Interventions.
Shweta Khanna, Kumar Sagar Jaiswal, Bhawna Gupta.
Front Nutr, 2017 Nov 24; 4. PMID: 29167795    Free PMC article.
Review.
Allergen-Specific Immunotherapies for Food Allergy.
Elizabeth Feuille, Anna Nowak-Wegrzyn.
Allergy Asthma Immunol Res, 2018 Apr 21; 10(3). PMID: 29676066    Free PMC article.
Review.
Debates in Allergy Medicine: Does oral immunotherapy shorten the duration of milk and egg allergy? The pro argument.
Valentina Pecora, Rocco Luigi Valluzzi, +2 authors, Lamia Dahdah.
World Allergy Organ J, 2018 Jul 07; 11(1). PMID: 29977438    Free PMC article.
Review.
IL-10 Receptor or TGF-β Neutralization Abrogates the Protective Effect of a Specific Nondigestible Oligosaccharide Mixture in Cow-Milk-Allergic Mice.
JoAnn Kerperien, Désirée Veening-Griffioen, +8 authors, Linette E M Willemsen.
J Nutr, 2018 Jul 10; 148(8). PMID: 29986071    Free PMC article.
Immunomodulatory Protein Hydrolysates and Their Application.
Mensiena B G Kiewiet, Marijke M Faas, Paul de Vos.
Nutrients, 2018 Jul 18; 10(7). PMID: 30011891    Free PMC article.
Review.
Gut Mucosal Antibody Responses and Implications for Food Allergy.
Ramona A Hoh, Scott D Boyd.
Front Immunol, 2018 Oct 16; 9. PMID: 30319658    Free PMC article.
Review.
A New Approach of Extraction of α-Amylase/trypsin Inhibitors from Wheat (Triticum aestivum L.), Based on Optimization Using Plackett-Burman and Box-Behnken Designs.
Sorel Tchewonpi Sagu, Gerd Huschek, +2 authors, Harshadrai M Rawel.
Molecules, 2019 Oct 09; 24(19). PMID: 31590396    Free PMC article.
Early-life gut microbiome and egg allergy.
M Fazlollahi, Y Chun, +8 authors, S Bunyavanich.
Allergy, 2018 Jan 11; 73(7). PMID: 29318631    Free PMC article.
Germ-Free Mice Exhibit Mast Cells With Impaired Functionality and Gut Homing and Do Not Develop Food Allergy.
Martin Schwarzer, Petra Hermanova, +9 authors, Irma Schabussova.
Front Immunol, 2019 Feb 28; 10. PMID: 30809227    Free PMC article.
Murine models for mucosal tolerance in allergy.
Ursula Smole, Irma Schabussova, Winfried F Pickl, Ursula Wiedermann.
Semin Immunol, 2017 Aug 16; 30. PMID: 28807539    Free PMC article.
Review.
A Comprehensive Review on Natural Bioactive Compounds and Probiotics as Potential Therapeutics in Food Allergy Treatment.
Kunal Pratap, Aya C Taki, +2 authors, Sandip D Kamath.
Front Immunol, 2020 Jul 17; 11. PMID: 32670266    Free PMC article.
Review.
Dietary Glucose Consumption Promotes RALDH Activity in Small Intestinal CD103+CD11b+ Dendritic Cells.
Hyun-Ja Ko, Sung-Wook Hong, +8 authors, Sin-Hyeog Im.
Front Immunol, 2020 Aug 28; 11. PMID: 32849649    Free PMC article.
Epicutaneous sensitization in the development of food allergy: What is the evidence and how can this be prevented?
Helen A Brough, Kari C Nadeau, +5 authors, Gideon Lack.
Allergy, 2020 Apr 07; 75(9). PMID: 32249942    Free PMC article.
Review.
Dynamic Interplay Between Microbiota and Mucosal Immunity in Early Shaping of Asthma and its Implication for the COVID-19 Pandemic.
Suzan A AlKhater.
J Asthma Allergy, 2020 Oct 17; 13. PMID: 33061464    Free PMC article.
Review.
Mechanisms by which gut microorganisms influence food sensitivities.
Alberto Caminero, Marlies Meisel, Bana Jabri, Elena F Verdu.
Nat Rev Gastroenterol Hepatol, 2018 Sep 15; 16(1). PMID: 30214038    Free PMC article.
Review.
Personalized Nutrition Approach in Food Allergy: Is It Prime Time Yet?
Enza D'Auria, Mariette Abrahams, Gian Vincenzo Zuccotti, Carina Venter.
Nutrients, 2019 Feb 13; 11(2). PMID: 30744105    Free PMC article.
Review.
Intestinal transcriptional profiling reveals fava bean-induced immune response in DBA/1 mice.
Guankui Du, Man Xiao, +3 authors, Wangwei Cai.
Biol Res, 2019 Mar 03; 52(1). PMID: 30823938    Free PMC article.
Differences in Regulatory Mechanisms Induced by β-Lactoglobulin and κ-Casein in Cow's Milk Allergy Mouse Model-In Vivo and Ex Vivo Studies.
Dagmara Złotkowska, Emilia Stachurska, +3 authors, Ewa Wasilewska.
Nutrients, 2021 Jan 29; 13(2). PMID: 33503831    Free PMC article.
Vitamin D and Allergy Susceptibility during Gestation and Early Life.
Daniela Briceno Noriega, Huub F J Savelkoul.
Nutrients, 2021 Apr 04; 13(3). PMID: 33801051    Free PMC article.
Review.
Vitamin D and Microbiota: Is There a Link with Allergies?
Giuseppe Murdaca, Alessandra Gerosa, +3 authors, Sebastiano Gangemi.
Int J Mol Sci, 2021 May 01; 22(8). PMID: 33924232    Free PMC article.
Review.
Oral Mucosa as a Potential Site for Diagnosis and Treatment of Allergic and Autoimmune Diseases.
Cristina Gomez-Casado, Javier Sanchez-Solares, +3 authors, María M Escribese.
Foods, 2021 May 01; 10(5). PMID: 33925074    Free PMC article.
Review.
Novel Topical Treatment for Dandruff & Dry Scalp Through Sustained Balance in Skin Microbiome.
Alexander Xiao, Christopher Warren, Waheeda Samady, Lucy Bilaver.
Clin Cosmet Investig Dermatol, 2021 Aug 03; 14. PMID: 34335039    Free PMC article.
The promise of the gut microbiome as part of individualized treatment strategies.
Daniel A Schupack, Ruben A T Mars, +2 authors, Purna C Kashyap.
Nat Rev Gastroenterol Hepatol, 2021 Aug 29;. PMID: 34453142
Review.