The maternal gut microbiome during pregnancy and offspring allergy and asthma

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

The maternal gut microbiome during pregnancy and offspring allergy and asthma. / Gao, Yuan; Nanan, Ralph; Macia, Laurence; Tan, Jian; Sominsky, Luba; Quinn, Thomas P.; O'Hely, Martin; Ponsonby, Anne-Louise; Tang, Mimi L. K.; Collier, Fiona; Strickland, Deborah H.; Dhar, Poshmaal; Brix, Susanne; Phipps, Simon; Sly, Peter D.; Ranganathan, Sarath; Stokholm, Jakob; Kristiansen, Karsten; Gray, Lawrence E.K.; Vuillermin, Peter.

In: Journal of Allergy and Clinical Immunology, Vol. 148, No. 3, 2021, p. 669-678.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Gao, Y, Nanan, R, Macia, L, Tan, J, Sominsky, L, Quinn, TP, O'Hely, M, Ponsonby, A-L, Tang, MLK, Collier, F, Strickland, DH, Dhar, P, Brix, S, Phipps, S, Sly, PD, Ranganathan, S, Stokholm, J, Kristiansen, K, Gray, LEK & Vuillermin, P 2021, 'The maternal gut microbiome during pregnancy and offspring allergy and asthma', Journal of Allergy and Clinical Immunology, vol. 148, no. 3, pp. 669-678. https://doi.org/10.1016/j.jaci.2021.07.011

APA

Gao, Y., Nanan, R., Macia, L., Tan, J., Sominsky, L., Quinn, T. P., O'Hely, M., Ponsonby, A-L., Tang, M. L. K., Collier, F., Strickland, D. H., Dhar, P., Brix, S., Phipps, S., Sly, P. D., Ranganathan, S., Stokholm, J., Kristiansen, K., Gray, L. E. K., & Vuillermin, P. (2021). The maternal gut microbiome during pregnancy and offspring allergy and asthma. Journal of Allergy and Clinical Immunology, 148(3), 669-678. https://doi.org/10.1016/j.jaci.2021.07.011

Vancouver

Gao Y, Nanan R, Macia L, Tan J, Sominsky L, Quinn TP et al. The maternal gut microbiome during pregnancy and offspring allergy and asthma. Journal of Allergy and Clinical Immunology. 2021;148(3):669-678. https://doi.org/10.1016/j.jaci.2021.07.011

Author

Gao, Yuan ; Nanan, Ralph ; Macia, Laurence ; Tan, Jian ; Sominsky, Luba ; Quinn, Thomas P. ; O'Hely, Martin ; Ponsonby, Anne-Louise ; Tang, Mimi L. K. ; Collier, Fiona ; Strickland, Deborah H. ; Dhar, Poshmaal ; Brix, Susanne ; Phipps, Simon ; Sly, Peter D. ; Ranganathan, Sarath ; Stokholm, Jakob ; Kristiansen, Karsten ; Gray, Lawrence E.K. ; Vuillermin, Peter. / The maternal gut microbiome during pregnancy and offspring allergy and asthma. In: Journal of Allergy and Clinical Immunology. 2021 ; Vol. 148, No. 3. pp. 669-678.

Bibtex

@article{d05a372c0c7c493f9c3e9d59810570a5,

title = "The maternal gut microbiome during pregnancy and offspring allergy and asthma",

abstract = "Environmental exposures during pregnancy that alter both the maternal gut microbiome and the infant's risk of allergic disease and asthma include a traditional farm environment and consumption of unpasteurized cow's milk, antibiotic use, dietary fiber, and psychosocial stress. Multiple mechanisms acting in concert may underpin these associations and prime the infant to acquire immune competence and homeostasis following exposure to the extrauterine environment. Cellular and metabolic products of the maternal gut microbiome can promote the expression of microbial pattern recognition receptors, as well as thymic and bone marrow hematopoiesis relevant to regulatory immunity. At birth, transmission of maternally derived bacteria likely leverages this in utero programming to accelerate postnatal transition from a TH2- to TH1- and TH17-dominant immune phenotype and maturation of regulatory immune mechanisms, which in turn reduce the child's risk of allergic disease and asthma. Although our understanding of these phenomena is rapidly evolving, the field is relatively nascent, and we are yet to translate existing knowledge into interventions that substantially reduce disease risk in humans. Here, we review evidence that the maternal gut microbiome impacts the offspring's risk of allergic disease and asthma, discuss challenges and future directions for the field, and propose the hypothesis that maternal carriage of Prevotella copri during pregnancy decreases the offspring's risk of allergic disease via production of succinate, which in turn promotes bone marrow myelopoiesis of dendritic cell precursors in the fetus.",

keywords = "allergy, asthma, fetal immunity, Gut microbiome",

author = "Yuan Gao and Ralph Nanan and Laurence Macia and Jian Tan and Luba Sominsky and Quinn, {Thomas P.} and Martin O'Hely and Anne-Louise Ponsonby and Tang, {Mimi L. K.} and Fiona Collier and Strickland, {Deborah H.} and Poshmaal Dhar and Susanne Brix and Simon Phipps and Sly, {Peter D.} and Sarath Ranganathan and Jakob Stokholm and Karsten Kristiansen and Gray, {Lawrence E.K.} and Peter Vuillermin",

note = "Publisher Copyright: {\textcopyright} 2021 American Academy of Allergy, Asthma & Immunology",

year = "2021",

doi = "10.1016/j.jaci.2021.07.011",

language = "English",

volume = "148",

pages = "669--678",

journal = "Journal of Allergy and Clinical Immunology",

issn = "0091-6749",

publisher = "Mosby Inc.",

number = "3",

}

RIS

TY - JOUR

T1 - The maternal gut microbiome during pregnancy and offspring allergy and asthma

AU - Gao, Yuan

AU - Nanan, Ralph

AU - Macia, Laurence

AU - Tan, Jian

AU - Sominsky, Luba

AU - Quinn, Thomas P.

AU - O'Hely, Martin

AU - Ponsonby, Anne-Louise

AU - Tang, Mimi L. K.

AU - Collier, Fiona

AU - Strickland, Deborah H.

AU - Dhar, Poshmaal

AU - Brix, Susanne

AU - Phipps, Simon

AU - Sly, Peter D.

AU - Ranganathan, Sarath

AU - Stokholm, Jakob

AU - Kristiansen, Karsten

AU - Gray, Lawrence E.K.

AU - Vuillermin, Peter

PY - 2021

Y1 - 2021

N2 - Environmental exposures during pregnancy that alter both the maternal gut microbiome and the infant's risk of allergic disease and asthma include a traditional farm environment and consumption of unpasteurized cow's milk, antibiotic use, dietary fiber, and psychosocial stress. Multiple mechanisms acting in concert may underpin these associations and prime the infant to acquire immune competence and homeostasis following exposure to the extrauterine environment. Cellular and metabolic products of the maternal gut microbiome can promote the expression of microbial pattern recognition receptors, as well as thymic and bone marrow hematopoiesis relevant to regulatory immunity. At birth, transmission of maternally derived bacteria likely leverages this in utero programming to accelerate postnatal transition from a TH2- to TH1- and TH17-dominant immune phenotype and maturation of regulatory immune mechanisms, which in turn reduce the child's risk of allergic disease and asthma. Although our understanding of these phenomena is rapidly evolving, the field is relatively nascent, and we are yet to translate existing knowledge into interventions that substantially reduce disease risk in humans. Here, we review evidence that the maternal gut microbiome impacts the offspring's risk of allergic disease and asthma, discuss challenges and future directions for the field, and propose the hypothesis that maternal carriage of Prevotella copri during pregnancy decreases the offspring's risk of allergic disease via production of succinate, which in turn promotes bone marrow myelopoiesis of dendritic cell precursors in the fetus.

AB - Environmental exposures during pregnancy that alter both the maternal gut microbiome and the infant's risk of allergic disease and asthma include a traditional farm environment and consumption of unpasteurized cow's milk, antibiotic use, dietary fiber, and psychosocial stress. Multiple mechanisms acting in concert may underpin these associations and prime the infant to acquire immune competence and homeostasis following exposure to the extrauterine environment. Cellular and metabolic products of the maternal gut microbiome can promote the expression of microbial pattern recognition receptors, as well as thymic and bone marrow hematopoiesis relevant to regulatory immunity. At birth, transmission of maternally derived bacteria likely leverages this in utero programming to accelerate postnatal transition from a TH2- to TH1- and TH17-dominant immune phenotype and maturation of regulatory immune mechanisms, which in turn reduce the child's risk of allergic disease and asthma. Although our understanding of these phenomena is rapidly evolving, the field is relatively nascent, and we are yet to translate existing knowledge into interventions that substantially reduce disease risk in humans. Here, we review evidence that the maternal gut microbiome impacts the offspring's risk of allergic disease and asthma, discuss challenges and future directions for the field, and propose the hypothesis that maternal carriage of Prevotella copri during pregnancy decreases the offspring's risk of allergic disease via production of succinate, which in turn promotes bone marrow myelopoiesis of dendritic cell precursors in the fetus.

KW - allergy

KW - asthma

KW - fetal immunity

KW - Gut microbiome

U2 - 10.1016/j.jaci.2021.07.011

DO - 10.1016/j.jaci.2021.07.011

M3 - Journal article

C2 - 34310928

AN - SCOPUS:85113312173

VL - 148

SP - 669

EP - 678

JO - Journal of Allergy and Clinical Immunology

JF - Journal of Allergy and Clinical Immunology

SN - 0091-6749

IS - 3

ER -

ID: 279253862

Department of Biology