A self-sustaining layer of early-life-origin B cells drives steady-state IgA responses in the adult gut

Stefano Vergani; Konjit Getachew Muleta; Clément Da Silva; Alexander Doyle; Trine Ahn Kristiansen; Selene Sodini; Niklas Krausse; Giorgia Montano; Knut Kotarsky; Joy Nakawesi; Hugo Åkerstrand; Stijn Vanhee; Sneh Lata Gupta; David Bryder; William Winston Agace; Katharina Lahl; Joan Yuan

doi:10.1016/j.immuni.2022.08.018

A self-sustaining layer of early-life-origin B cells drives steady-state IgA responses in the adult gut

Stefano Vergani, Konjit Getachew Muleta, Clément Da Silva, Alexander Doyle, Trine Ahn Kristiansen, Selene Sodini, Niklas Krausse, Giorgia Montano, Knut Kotarsky, Joy Nakawesi, Hugo Åkerstrand, Stijn Vanhee, Sneh Lata Gupta, David Bryder, William Winston Agace, Katharina Lahl, Joan Yuan^*

^*Corresponding author for this work

Lund University

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

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Abstract

The adult immune system consists of cells that emerged at various times during ontogeny. We aimed to define the relationship between developmental origin and composition of the adult B cell pool during unperturbed hematopoiesis. Lineage tracing stratified murine adult B cells based on the timing of output, revealing that a substantial portion originated within a restricted neonatal window. In addition to B-1a cells, early-life time-stamped B cells included clonally interrelated IgA plasma cells in the gut and bone marrow. These were actively maintained by B cell memory within gut chronic germinal centers and contained commensal microbiota reactivity. Neonatal rotavirus infection recruited recurrent IgA clones that were distinct from those arising by infection with the same antigen in adults. Finally, gut IgA plasma cells arose from the same hematopoietic progenitors as B-1a cells during ontogeny. Thus, a complex layer of neonatally imprinted B cells confer unique antibody responses later in life.

Original language	English
Journal	Immunity
Volume	55
Issue number	10
Pages (from-to)	1829-1842
ISSN	1074-7613
DOIs	https://doi.org/10.1016/j.immuni.2022.08.018
Publication status	Published - 2022

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Vergani, S., Muleta, K. G., Da Silva, C., Doyle, A., Kristiansen, T. A., Sodini, S., Krausse, N., Montano, G., Kotarsky, K., Nakawesi, J., Åkerstrand, H., Vanhee, S., Gupta, S. L., Bryder, D., Agace, W. W., Lahl, K., & Yuan, J. (2022). A self-sustaining layer of early-life-origin B cells drives steady-state IgA responses in the adult gut. Immunity, 55(10), 1829-1842. https://doi.org/10.1016/j.immuni.2022.08.018

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title = "A self-sustaining layer of early-life-origin B cells drives steady-state IgA responses in the adult gut",

abstract = "The adult immune system consists of cells that emerged at various times during ontogeny. We aimed to define the relationship between developmental origin and composition of the adult B cell pool during unperturbed hematopoiesis. Lineage tracing stratified murine adult B cells based on the timing of output, revealing that a substantial portion originated within a restricted neonatal window. In addition to B-1a cells, early-life time-stamped B cells included clonally interrelated IgA plasma cells in the gut and bone marrow. These were actively maintained by B cell memory within gut chronic germinal centers and contained commensal microbiota reactivity. Neonatal rotavirus infection recruited recurrent IgA clones that were distinct from those arising by infection with the same antigen in adults. Finally, gut IgA plasma cells arose from the same hematopoietic progenitors as B-1a cells during ontogeny. Thus, a complex layer of neonatally imprinted B cells confer unique antibody responses later in life.",

author = "Stefano Vergani and Muleta, {Konjit Getachew} and {Da Silva}, Cl{\'e}ment and Alexander Doyle and Kristiansen, {Trine Ahn} and Selene Sodini and Niklas Krausse and Giorgia Montano and Knut Kotarsky and Joy Nakawesi and Hugo {\AA}kerstrand and Stijn Vanhee and Gupta, {Sneh Lata} and David Bryder and Agace, {William Winston} and Katharina Lahl and Joan Yuan",

note = "Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2022",

doi = "10.1016/j.immuni.2022.08.018",

language = "English",

volume = "55",

pages = "1829--1842",

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Vergani, S, Muleta, KG, Da Silva, C, Doyle, A, Kristiansen, TA, Sodini, S, Krausse, N, Montano, G, Kotarsky, K, Nakawesi, J, Åkerstrand, H, Vanhee, S, Gupta, SL, Bryder, D, Agace, WW, Lahl, K & Yuan, J 2022, 'A self-sustaining layer of early-life-origin B cells drives steady-state IgA responses in the adult gut', Immunity, vol. 55, no. 10, pp. 1829-1842. https://doi.org/10.1016/j.immuni.2022.08.018

TY - JOUR

T1 - A self-sustaining layer of early-life-origin B cells drives steady-state IgA responses in the adult gut

AU - Vergani, Stefano

AU - Muleta, Konjit Getachew

AU - Da Silva, Clément

AU - Doyle, Alexander

AU - Kristiansen, Trine Ahn

AU - Sodini, Selene

AU - Krausse, Niklas

AU - Montano, Giorgia

AU - Kotarsky, Knut

AU - Nakawesi, Joy

AU - Åkerstrand, Hugo

AU - Vanhee, Stijn

AU - Gupta, Sneh Lata

AU - Bryder, David

AU - Agace, William Winston

AU - Lahl, Katharina

AU - Yuan, Joan

PY - 2022

Y1 - 2022

N2 - The adult immune system consists of cells that emerged at various times during ontogeny. We aimed to define the relationship between developmental origin and composition of the adult B cell pool during unperturbed hematopoiesis. Lineage tracing stratified murine adult B cells based on the timing of output, revealing that a substantial portion originated within a restricted neonatal window. In addition to B-1a cells, early-life time-stamped B cells included clonally interrelated IgA plasma cells in the gut and bone marrow. These were actively maintained by B cell memory within gut chronic germinal centers and contained commensal microbiota reactivity. Neonatal rotavirus infection recruited recurrent IgA clones that were distinct from those arising by infection with the same antigen in adults. Finally, gut IgA plasma cells arose from the same hematopoietic progenitors as B-1a cells during ontogeny. Thus, a complex layer of neonatally imprinted B cells confer unique antibody responses later in life.

AB - The adult immune system consists of cells that emerged at various times during ontogeny. We aimed to define the relationship between developmental origin and composition of the adult B cell pool during unperturbed hematopoiesis. Lineage tracing stratified murine adult B cells based on the timing of output, revealing that a substantial portion originated within a restricted neonatal window. In addition to B-1a cells, early-life time-stamped B cells included clonally interrelated IgA plasma cells in the gut and bone marrow. These were actively maintained by B cell memory within gut chronic germinal centers and contained commensal microbiota reactivity. Neonatal rotavirus infection recruited recurrent IgA clones that were distinct from those arising by infection with the same antigen in adults. Finally, gut IgA plasma cells arose from the same hematopoietic progenitors as B-1a cells during ontogeny. Thus, a complex layer of neonatally imprinted B cells confer unique antibody responses later in life.

U2 - 10.1016/j.immuni.2022.08.018

DO - 10.1016/j.immuni.2022.08.018

M3 - Journal article

C2 - 36115337

AN - SCOPUS:85139337509

SN - 1074-7613

VL - 55

SP - 1829

EP - 1842

JO - Immunity

JF - Immunity

IS - 10

ER -

A self-sustaining layer of early-life-origin B cells drives steady-state IgA responses in the adult gut

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