Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice

BackgroundEarly dietary introduction of peanut has shown efficacy in clinical trials and driven pediatric recommendations for early introduction of peanut to children with heightened allergy risk worldwide. Unfortunately, tolerance is not induced in every case, and a subset of patients are allergic...

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Main Authors: Robert M. Immormino, Johanna M. Smeekens, Priscilla I. Mathai, Janelle R. Kesselring, Andrew V. Turner, Michael D. Kulis, Timothy P. Moran
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Allergy
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/falgy.2023.1219268/full
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author Robert M. Immormino
Johanna M. Smeekens
Johanna M. Smeekens
Priscilla I. Mathai
Janelle R. Kesselring
Janelle R. Kesselring
Andrew V. Turner
Andrew V. Turner
Michael D. Kulis
Michael D. Kulis
Timothy P. Moran
author_facet Robert M. Immormino
Johanna M. Smeekens
Johanna M. Smeekens
Priscilla I. Mathai
Janelle R. Kesselring
Janelle R. Kesselring
Andrew V. Turner
Andrew V. Turner
Michael D. Kulis
Michael D. Kulis
Timothy P. Moran
author_sort Robert M. Immormino
collection DOAJ
description BackgroundEarly dietary introduction of peanut has shown efficacy in clinical trials and driven pediatric recommendations for early introduction of peanut to children with heightened allergy risk worldwide. Unfortunately, tolerance is not induced in every case, and a subset of patients are allergic prior to introduction. Here we assess peanut allergic sensitization and oral tolerance in genetically diverse mouse strains.ObjectiveWe aimed to determine whether environmental adjuvant-driven airway sensitization and oral tolerance to peanut could be induced in various genetically diverse mouse strains.MethodsC57BL/6J and 12 Collaborative Cross (CC) mouse strains were fed regular chow or ad libitum peanut butter to induce tolerance. Tolerance was tested by attempting to sensitize mice via intratracheal exposure to peanut and lipopolysaccharide (LPS), followed by intraperitoneal peanut challenge. Peanut-specific immunoglobulins and peanut-induced anaphylaxis were assessed.ResultsWithout oral peanut feeding, most CC strains (11/12) and C57BL/6J induced peanut-specific IgE and IgG1 following airway exposure to peanut and LPS. With oral peanut feeding none of the CC strains nor C57BL/6J mice became sensitized to peanut or experienced anaphylaxis following peanut challenge.ConclusionAllergic sensitization and oral tolerance to peanut can be achieved across a range of genetically diverse mice. Notably, the same strains that became allergic via airway sensitization were tolerized by feeding high doses of peanut butter before sensitization, suggesting that the order and route of peanut exposure are critical for determining the allergic fate.
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spelling doaj.art-592b64addfd6418d96db6ce758376f7e2023-07-17T09:45:12ZengFrontiers Media S.A.Frontiers in Allergy2673-61012023-07-01410.3389/falgy.2023.12192681219268Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross miceRobert M. Immormino0Johanna M. Smeekens1Johanna M. Smeekens2Priscilla I. Mathai3Janelle R. Kesselring4Janelle R. Kesselring5Andrew V. Turner6Andrew V. Turner7Michael D. Kulis8Michael D. Kulis9Timothy P. Moran10Department of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesDepartment of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesUNC Food Allergy Initiative, Department of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesDepartment of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesDepartment of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesUNC Food Allergy Initiative, Department of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesDepartment of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesUNC Food Allergy Initiative, Department of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesDepartment of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesUNC Food Allergy Initiative, Department of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesDepartment of Pediatrics, UNC School of Medicine, Chapel Hill, NC, United StatesBackgroundEarly dietary introduction of peanut has shown efficacy in clinical trials and driven pediatric recommendations for early introduction of peanut to children with heightened allergy risk worldwide. Unfortunately, tolerance is not induced in every case, and a subset of patients are allergic prior to introduction. Here we assess peanut allergic sensitization and oral tolerance in genetically diverse mouse strains.ObjectiveWe aimed to determine whether environmental adjuvant-driven airway sensitization and oral tolerance to peanut could be induced in various genetically diverse mouse strains.MethodsC57BL/6J and 12 Collaborative Cross (CC) mouse strains were fed regular chow or ad libitum peanut butter to induce tolerance. Tolerance was tested by attempting to sensitize mice via intratracheal exposure to peanut and lipopolysaccharide (LPS), followed by intraperitoneal peanut challenge. Peanut-specific immunoglobulins and peanut-induced anaphylaxis were assessed.ResultsWithout oral peanut feeding, most CC strains (11/12) and C57BL/6J induced peanut-specific IgE and IgG1 following airway exposure to peanut and LPS. With oral peanut feeding none of the CC strains nor C57BL/6J mice became sensitized to peanut or experienced anaphylaxis following peanut challenge.ConclusionAllergic sensitization and oral tolerance to peanut can be achieved across a range of genetically diverse mice. Notably, the same strains that became allergic via airway sensitization were tolerized by feeding high doses of peanut butter before sensitization, suggesting that the order and route of peanut exposure are critical for determining the allergic fate.https://www.frontiersin.org/articles/10.3389/falgy.2023.1219268/fullfood allergypeanut allergyoral tolerancecollaborative crossairway sensitization
spellingShingle Robert M. Immormino
Johanna M. Smeekens
Johanna M. Smeekens
Priscilla I. Mathai
Janelle R. Kesselring
Janelle R. Kesselring
Andrew V. Turner
Andrew V. Turner
Michael D. Kulis
Michael D. Kulis
Timothy P. Moran
Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice
Frontiers in Allergy
food allergy
peanut allergy
oral tolerance
collaborative cross
airway sensitization
title Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice
title_full Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice
title_fullStr Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice
title_full_unstemmed Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice
title_short Peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice
title_sort peanut butter feeding induces oral tolerance in genetically diverse collaborative cross mice
topic food allergy
peanut allergy
oral tolerance
collaborative cross
airway sensitization
url https://www.frontiersin.org/articles/10.3389/falgy.2023.1219268/full
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