Microbiota-dependent and -independent postnatal development of salivary immunity

Khaled Zubeidat; Yasmin Jaber; Yasmin Saba; Or Barel; Reem Naamneh; Yasmin Netanely; Yael Horev; Luba Eli-berchoer; Amjad Shhadeh; Omri Yosef; Eliran Arbib; Gili Betser-Cohen; Chen Nadler; Hagit Shapiro; Eran Elinav; Doron J. Aframian; Asaf Wilensky; Avi-Hai Hovav

doi:10.1016/j.celrep.2022.111981

Microbiota-dependent and -independent postnatal development of salivary immunity

Khaled Zubeidat, Yasmin Jaber, Yasmin Saba, Or Barel, Reem Naamneh, Yasmin Netanely, Yael Horev, Luba Eli-berchoer, Amjad Shhadeh, Omri Yosef, Eliran Arbib, Gili Betser-Cohen, Chen Nadler, Hagit Shapiro, Eran Elinav, Doron J. Aframian, Asaf Wilensky, Avi-Hai Hovav

Weizmann Institute of Science, The Hebrew University of Jerusalem

Research output: Contribution to journal › Article › peer-review

Abstract

While saliva regulates the interplay between the microbiota and the oral immune system, the mechanisms establishing postnatal salivary immunity are ill-defined. Here, we show that high levels of neutrophils and neonatal Fc receptor (FcRn)-transferred maternal IgG are temporarily present in the neonatal murine salivary glands in a microbiota-independent manner. During weaning, neutrophils, FcRn, and IgG decrease in the salivary glands, while the polymeric immunoglobulin receptor (pIgR) is upregulated in a growth arrest-specific 6 (GAS6)-dependent manner independent of the microbiota. Production of salivary IgA begins following weaning and relies on CD4-help, IL-17, and the microbiota. The weaning phase is characterized by a transient accumulation of dendritic cells capable of migrating from the oral mucosa to the salivary glands upon exposure to microbial challenges and activating T cells. This study reveals the postnatal mechanisms developed in the salivary glands to induce immunity and proposes the salivary glands as an immune inductive site.

Original language	English
Article number	111981
Number of pages	12
Journal	Cell reports (Cambridge)
Volume	42
Issue number	1
Early online date	7 Jan 2023
DOIs	https://doi.org/10.1016/j.celrep.2022.111981
State	Published - 31 Jan 2023

Keywords

CP: Immunology
CP: Microbiology
IgA
IgG
oral mucosa
postnatal
salivary glands
weaning

All Science Journal Classification (ASJC) codes

General Biochemistry,Genetics and Molecular Biology

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10.1016/j.celrep.2022.111981License: CC BY

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Zubeidat, K., Jaber, Y., Saba, Y., Barel, O., Naamneh, R., Netanely, Y., Horev, Y., Eli-berchoer, L., Shhadeh, A., Yosef, O., Arbib, E., Betser-Cohen, G., Nadler, C., Shapiro, H., Elinav, E., Aframian, D. J., Wilensky, A., & Hovav, A.-H. (2023). Microbiota-dependent and -independent postnatal development of salivary immunity. Cell reports (Cambridge), 42(1), Article 111981. https://doi.org/10.1016/j.celrep.2022.111981

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title = "Microbiota-dependent and -independent postnatal development of salivary immunity",

abstract = "While saliva regulates the interplay between the microbiota and the oral immune system, the mechanisms establishing postnatal salivary immunity are ill-defined. Here, we show that high levels of neutrophils and neonatal Fc receptor (FcRn)-transferred maternal IgG are temporarily present in the neonatal murine salivary glands in a microbiota-independent manner. During weaning, neutrophils, FcRn, and IgG decrease in the salivary glands, while the polymeric immunoglobulin receptor (pIgR) is upregulated in a growth arrest-specific 6 (GAS6)-dependent manner independent of the microbiota. Production of salivary IgA begins following weaning and relies on CD4-help, IL-17, and the microbiota. The weaning phase is characterized by a transient accumulation of dendritic cells capable of migrating from the oral mucosa to the salivary glands upon exposure to microbial challenges and activating T cells. This study reveals the postnatal mechanisms developed in the salivary glands to induce immunity and proposes the salivary glands as an immune inductive site.",

keywords = "CP: Immunology, CP: Microbiology, IgA, IgG, oral mucosa, postnatal, salivary glands, weaning",

author = "Khaled Zubeidat and Yasmin Jaber and Yasmin Saba and Or Barel and Reem Naamneh and Yasmin Netanely and Yael Horev and Luba Eli-berchoer and Amjad Shhadeh and Omri Yosef and Eliran Arbib and Gili Betser-Cohen and Chen Nadler and Hagit Shapiro and Eran Elinav and Aframian, \{Doron J.\} and Asaf Wilensky and Avi-Hai Hovav",

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year = "2023",

month = jan,

day = "31",

doi = "10.1016/j.celrep.2022.111981",

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Zubeidat, K, Jaber, Y, Saba, Y, Barel, O, Naamneh, R, Netanely, Y, Horev, Y, Eli-berchoer, L, Shhadeh, A, Yosef, O, Arbib, E, Betser-Cohen, G, Nadler, C, Shapiro, H, Elinav, E , Aframian, DJ, Wilensky, A & Hovav, A-H 2023, 'Microbiota-dependent and -independent postnatal development of salivary immunity', Cell reports (Cambridge), vol. 42, no. 1, 111981. https://doi.org/10.1016/j.celrep.2022.111981

TY - JOUR

T1 - Microbiota-dependent and -independent postnatal development of salivary immunity

AU - Zubeidat, Khaled

AU - Jaber, Yasmin

AU - Saba, Yasmin

AU - Barel, Or

AU - Naamneh, Reem

AU - Netanely, Yasmin

AU - Horev, Yael

AU - Eli-berchoer, Luba

AU - Shhadeh, Amjad

AU - Yosef, Omri

AU - Arbib, Eliran

AU - Betser-Cohen, Gili

AU - Nadler, Chen

AU - Shapiro, Hagit

AU - Elinav, Eran

AU - Aframian, Doron J.

AU - Wilensky, Asaf

AU - Hovav, Avi-Hai

PY - 2023/1/31

Y1 - 2023/1/31

N2 - While saliva regulates the interplay between the microbiota and the oral immune system, the mechanisms establishing postnatal salivary immunity are ill-defined. Here, we show that high levels of neutrophils and neonatal Fc receptor (FcRn)-transferred maternal IgG are temporarily present in the neonatal murine salivary glands in a microbiota-independent manner. During weaning, neutrophils, FcRn, and IgG decrease in the salivary glands, while the polymeric immunoglobulin receptor (pIgR) is upregulated in a growth arrest-specific 6 (GAS6)-dependent manner independent of the microbiota. Production of salivary IgA begins following weaning and relies on CD4-help, IL-17, and the microbiota. The weaning phase is characterized by a transient accumulation of dendritic cells capable of migrating from the oral mucosa to the salivary glands upon exposure to microbial challenges and activating T cells. This study reveals the postnatal mechanisms developed in the salivary glands to induce immunity and proposes the salivary glands as an immune inductive site.

AB - While saliva regulates the interplay between the microbiota and the oral immune system, the mechanisms establishing postnatal salivary immunity are ill-defined. Here, we show that high levels of neutrophils and neonatal Fc receptor (FcRn)-transferred maternal IgG are temporarily present in the neonatal murine salivary glands in a microbiota-independent manner. During weaning, neutrophils, FcRn, and IgG decrease in the salivary glands, while the polymeric immunoglobulin receptor (pIgR) is upregulated in a growth arrest-specific 6 (GAS6)-dependent manner independent of the microbiota. Production of salivary IgA begins following weaning and relies on CD4-help, IL-17, and the microbiota. The weaning phase is characterized by a transient accumulation of dendritic cells capable of migrating from the oral mucosa to the salivary glands upon exposure to microbial challenges and activating T cells. This study reveals the postnatal mechanisms developed in the salivary glands to induce immunity and proposes the salivary glands as an immune inductive site.

KW - CP: Immunology

KW - CP: Microbiology

KW - IgA

KW - IgG

KW - oral mucosa

KW - postnatal

KW - salivary glands

KW - weaning

UR - http://www.scopus.com/inward/record.url?scp=85145865227&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2022.111981

DO - 10.1016/j.celrep.2022.111981

M3 - مقالة

C2 - 36640306

SN - 2211-1247

VL - 42

JO - Cell reports (Cambridge)

JF - Cell reports (Cambridge)

IS - 1

M1 - 111981

ER -

Microbiota-dependent and -independent postnatal development of salivary immunity

Abstract

Keywords

All Science Journal Classification (ASJC) codes

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