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Healthy infants harbor intestinal bacteria that protect against food allergy

There has been a striking generational increase in life-threatening food allergies in Westernized societies . One hypothesis to explain this rising prevalence is that twenty-first century lifestyle practices, including misuse of antibiotics, dietary changes, and higher rates of Caesarean birth and f... Full description

Journal Title: Nature medicine 2019-03, Vol.25 (3), p.448-453
Main Author: Feehley, Taylor
Other Authors: Plunkett, Catherine H , Bao, Riyue , Choi Hong, Sung Min , Culleen, Elliot , Belda-Ferre, Pedro , Campbell, Evelyn , Aitoro, Rosita , Nocerino, Rita , Paparo, Lorella , Andrade, Jorge , Antonopoulos, Dionysios A , Berni Canani, Roberto , Nagler, Cathryn R
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: United States: Nature Publishing Group
ID: ISSN: 1078-8956
Link: https://www.ncbi.nlm.nih.gov/pubmed/30643289
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6408964
title: Healthy infants harbor intestinal bacteria that protect against food allergy
format: Article
creator:
  • Feehley, Taylor
  • Plunkett, Catherine H
  • Bao, Riyue
  • Choi Hong, Sung Min
  • Culleen, Elliot
  • Belda-Ferre, Pedro
  • Campbell, Evelyn
  • Aitoro, Rosita
  • Nocerino, Rita
  • Paparo, Lorella
  • Andrade, Jorge
  • Antonopoulos, Dionysios A
  • Berni Canani, Roberto
  • Nagler, Cathryn R
subjects:
  • Allergens
  • Allergies
  • Analysis
  • Anaphylaxis
  • Anaphylaxis - microbiology
  • Animals
  • Antibiotics
  • Antigens
  • Article
  • Bacteria
  • Clostridiales - genetics
  • Communities
  • Cow's milk
  • Diet
  • Dosage and administration
  • Epithelium
  • Fecal Microbiota Transplantation
  • Female
  • Food
  • Food allergies
  • Food allergy
  • Food hypersensitivity
  • Food Hypersensitivity - microbiology
  • Gastrointestinal Microbiome - genetics
  • Gene expression
  • Germ-Free Life
  • Germfree
  • Healthy Volunteers
  • Humans
  • Ileum
  • Ileum - microbiology
  • Infant
  • Infants
  • Intestinal microflora
  • Intestine
  • Male
  • Mice
  • Microbiota (Symbiotic organisms)
  • Milk Hypersensitivity - microbiology
  • Protected species
ispartof: Nature medicine, 2019-03, Vol.25 (3), p.448-453
description: There has been a striking generational increase in life-threatening food allergies in Westernized societies . One hypothesis to explain this rising prevalence is that twenty-first century lifestyle practices, including misuse of antibiotics, dietary changes, and higher rates of Caesarean birth and formula feeding have altered intestinal bacterial communities; early-life alterations may be particularly detrimental . To better understand how commensal bacteria regulate food allergy in humans, we colonized germ-free mice with feces from healthy or cow's milk allergic (CMA) infants . We found that germ-free mice colonized with bacteria from healthy, but not CMA, infants were protected against anaphylactic responses to a cow's milk allergen. Differences in bacterial composition separated the healthy and CMA populations in both the human donors and the colonized mice. Healthy and CMA colonized mice also exhibited unique transcriptome signatures in the ileal epithelium. Correlation of ileal bacteria with genes upregulated in the ileum of healthy or CMA colonized mice identified a clostridial species, Anaerostipes caccae, that protected against an allergic response to food. Our findings demonstrate that intestinal bacteria are critical for regulating allergic responses to dietary antigens and suggest that interventions that modulate bacterial communities may be therapeutically relevant for food allergy.
language: eng
source:
identifier: ISSN: 1078-8956
fulltext: no_fulltext
issn:
  • 1078-8956
  • 1546-170X
url: Link


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descriptionThere has been a striking generational increase in life-threatening food allergies in Westernized societies . One hypothesis to explain this rising prevalence is that twenty-first century lifestyle practices, including misuse of antibiotics, dietary changes, and higher rates of Caesarean birth and formula feeding have altered intestinal bacterial communities; early-life alterations may be particularly detrimental . To better understand how commensal bacteria regulate food allergy in humans, we colonized germ-free mice with feces from healthy or cow's milk allergic (CMA) infants . We found that germ-free mice colonized with bacteria from healthy, but not CMA, infants were protected against anaphylactic responses to a cow's milk allergen. Differences in bacterial composition separated the healthy and CMA populations in both the human donors and the colonized mice. Healthy and CMA colonized mice also exhibited unique transcriptome signatures in the ileal epithelium. Correlation of ileal bacteria with genes upregulated in the ileum of healthy or CMA colonized mice identified a clostridial species, Anaerostipes caccae, that protected against an allergic response to food. Our findings demonstrate that intestinal bacteria are critical for regulating allergic responses to dietary antigens and suggest that interventions that modulate bacterial communities may be therapeutically relevant for food allergy.
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subjectAllergens ; Allergies ; Analysis ; Anaphylaxis ; Anaphylaxis - microbiology ; Animals ; Antibiotics ; Antigens ; Article ; Bacteria ; Clostridiales - genetics ; Communities ; Cow's milk ; Diet ; Dosage and administration ; Epithelium ; Fecal Microbiota Transplantation ; Female ; Food ; Food allergies ; Food allergy ; Food hypersensitivity ; Food Hypersensitivity - microbiology ; Gastrointestinal Microbiome - genetics ; Gene expression ; Germ-Free Life ; Germfree ; Healthy Volunteers ; Humans ; Ileum ; Ileum - microbiology ; Infant ; Infants ; Intestinal microflora ; Intestine ; Male ; Mice ; Microbiota (Symbiotic organisms) ; Milk Hypersensitivity - microbiology ; Protected species
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descriptionThere has been a striking generational increase in life-threatening food allergies in Westernized societies . One hypothesis to explain this rising prevalence is that twenty-first century lifestyle practices, including misuse of antibiotics, dietary changes, and higher rates of Caesarean birth and formula feeding have altered intestinal bacterial communities; early-life alterations may be particularly detrimental . To better understand how commensal bacteria regulate food allergy in humans, we colonized germ-free mice with feces from healthy or cow's milk allergic (CMA) infants . We found that germ-free mice colonized with bacteria from healthy, but not CMA, infants were protected against anaphylactic responses to a cow's milk allergen. Differences in bacterial composition separated the healthy and CMA populations in both the human donors and the colonized mice. Healthy and CMA colonized mice also exhibited unique transcriptome signatures in the ileal epithelium. Correlation of ileal bacteria with genes upregulated in the ileum of healthy or CMA colonized mice identified a clostridial species, Anaerostipes caccae, that protected against an allergic response to food. Our findings demonstrate that intestinal bacteria are critical for regulating allergic responses to dietary antigens and suggest that interventions that modulate bacterial communities may be therapeutically relevant for food allergy.
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1Plunkett, Catherine H
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7Aitoro, Rosita
8Nocerino, Rita
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notes
0C.R.N. is President and co-founder of ClostraBio, Inc. The other authors declare that they have no competing financial interests. Correspondence and requests for materials should be addressed to C.R.N. (cnagler@bsd.uchicago.edu).
1Author Information
2Author contributions
3T.F., C.H.P, R.B. R.B.C. and C.R.N. designed the study. C.H.P. and T.F performed mouse experiments with help from P.B.F., R.A, E.C., E.C. and S.C.H. R.B., P.B.F and J.A. performed bioinformatics analysis. T.F., C.H.P., R.B., P.B.F. and C.R.N. analyzed results. R.B.C., R.N. and L.A. cared for patients and provided donor fecal samples. D.A.A. provided protocols and assisted with the colonization of GF mice with human feces and A. caccae. T.F., C.H.P., R.B., R.B.C. and C.R.N. wrote the manuscript. All authors read and commented on manuscript.
abstractThere has been a striking generational increase in life-threatening food allergies in Westernized societies . One hypothesis to explain this rising prevalence is that twenty-first century lifestyle practices, including misuse of antibiotics, dietary changes, and higher rates of Caesarean birth and formula feeding have altered intestinal bacterial communities; early-life alterations may be particularly detrimental . To better understand how commensal bacteria regulate food allergy in humans, we colonized germ-free mice with feces from healthy or cow's milk allergic (CMA) infants . We found that germ-free mice colonized with bacteria from healthy, but not CMA, infants were protected against anaphylactic responses to a cow's milk allergen. Differences in bacterial composition separated the healthy and CMA populations in both the human donors and the colonized mice. Healthy and CMA colonized mice also exhibited unique transcriptome signatures in the ileal epithelium. Correlation of ileal bacteria with genes upregulated in the ileum of healthy or CMA colonized mice identified a clostridial species, Anaerostipes caccae, that protected against an allergic response to food. Our findings demonstrate that intestinal bacteria are critical for regulating allergic responses to dietary antigens and suggest that interventions that modulate bacterial communities may be therapeutically relevant for food allergy.
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