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IgG Fc sialylation is regulated during the germinal center reaction following immunization with different adjuvants

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IgG Fc sialylation is regulated during the germinal center reaction following immunization with different adjuvants. / Bartsch, Yannic C; Eschweiler, Simon; Leliavski, Alexei; Lunding, Hanna B; Wagt, Sander; Petry, Janina; Lilienthal, Gina-Maria; Rahmöller, Johann; de Haan, Noortje; Hölscher, Alexandra; Erapaneedi, Raghu; Giannou, Anastasios D; Aly, Lilian; Sato, Ryota; de Neef, Louise A; Winkler, André; Braumann, Dominique; Hobusch, Juliane; Kuhnigk, Kyra; Krémer, Vanessa; Steinhaus, Moritz; Blanchard, Véronique; Gemoll, Timo; Habermann, Jens K; Collin, Mattias; Salinas, Gabriela; Manz, Rudolf A; Fukuyama, Hidehiro; Korn, Thomas; Waisman, Ari; Yogev, Nir; Huber, Samuel; Germany, Institute of Biochemistry Kiel University; Rose-John, Stefan; Busch, Hauke; Berberich-Siebelt, Friederike; Hölscher, Christoph; Netherlands, Center for Proteomics and Metabolomics Leiden University Medical Center Leiden; Ehlers, Marc.

In: J ALLERGY CLIN IMMUN, Vol. 146, No. 3, 09.2020, p. 652-666.e11.

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

Harvard

Bartsch, YC, Eschweiler, S, Leliavski, A, Lunding, HB, Wagt, S, Petry, J, Lilienthal, G-M, Rahmöller, J, de Haan, N, Hölscher, A, Erapaneedi, R, Giannou, AD, Aly, L, Sato, R, de Neef, LA, Winkler, A, Braumann, D, Hobusch, J, Kuhnigk, K, Krémer, V, Steinhaus, M, Blanchard, V, Gemoll, T, Habermann, JK, Collin, M, Salinas, G, Manz, RA, Fukuyama, H, Korn, T, Waisman, A, Yogev, N, Huber, S, Germany, IOBKU, Rose-John, S, Busch, H, Berberich-Siebelt, F, Hölscher, C, Netherlands, CFPAMLUMCL & Ehlers, M 2020, 'IgG Fc sialylation is regulated during the germinal center reaction following immunization with different adjuvants', J ALLERGY CLIN IMMUN, vol. 146, no. 3, pp. 652-666.e11. https://doi.org/10.1016/j.jaci.2020.04.059

APA

Bartsch, Y. C., Eschweiler, S., Leliavski, A., Lunding, H. B., Wagt, S., Petry, J., Lilienthal, G-M., Rahmöller, J., de Haan, N., Hölscher, A., Erapaneedi, R., Giannou, A. D., Aly, L., Sato, R., de Neef, L. A., Winkler, A., Braumann, D., Hobusch, J., Kuhnigk, K., ... Ehlers, M. (2020). IgG Fc sialylation is regulated during the germinal center reaction following immunization with different adjuvants. J ALLERGY CLIN IMMUN, 146(3), 652-666.e11. https://doi.org/10.1016/j.jaci.2020.04.059

Vancouver

Bartsch YC, Eschweiler S, Leliavski A, Lunding HB, Wagt S, Petry J et al. IgG Fc sialylation is regulated during the germinal center reaction following immunization with different adjuvants. J ALLERGY CLIN IMMUN. 2020 Sep;146(3):652-666.e11. https://doi.org/10.1016/j.jaci.2020.04.059

Bibtex

@article{cb5d401714f043718ab786cda5e0f1c5,
title = "IgG Fc sialylation is regulated during the germinal center reaction following immunization with different adjuvants",
abstract = "BACKGROUND: Effector functions of IgG Abs are regulated by their Fc N-glycosylation pattern. IgG Fc glycans that lack galactose and terminal sialic acid residues correlate with the severity of inflammatory (auto)immune disorders and have also been linked to protection against viral infection and discussed in the context of vaccine-induced protection. In contrast, sialylated IgG Abs have shown immunosuppressive effects.OBJECTIVE: We sought to investigate IgG glycosylation programming during the germinal center (GC) reaction following immunization of mice with a foreign protein antigen and different adjuvants.METHODS: Mice were analyzed for GC T-cell, B-cell, and plasma cell responses, as well as for antigen-specific serum IgG subclass titers and Fc glycosylation patterns.RESULTS: Different adjuvants induce distinct IgG+ GC B-cell responses with specific transcriptomes and expression levels of the α2,6-sialyltransferase responsible for IgG sialylation that correspond to distinct serum IgG Fc glycosylation patterns. Low IgG Fc sialylation programming in GC B cells was overall highly dependent on the Foxp3- follicular helper T (TFH) cell-inducing cytokine IL-6, here in particular induced by water-in-oil adjuvants and Mycobacterium tuberculosis. Furthermore, low IgG Fc sialylation programming was dependent on adjuvants that induced IL-27 receptor-dependent IFN-γ+ TFH1 cells, IL-6/IL-23-dependent IL-17A+ TFH17 cells, and high ratios of TFH cells to Foxp3+ follicular regulatory T cells. Here, the 2 latter were dependent on M tuberculosis and its cord factor.CONCLUSION: This study's findings regarding adjuvant-dependent GC responses and IgG glycosylation programming may aid in the development of novel vaccination strategies to induce IgG Abs with both high affinity and defined Fc glycosylation patterns in the GC.",
author = "Bartsch, {Yannic C} and Simon Eschweiler and Alexei Leliavski and Lunding, {Hanna B} and Sander Wagt and Janina Petry and Gina-Maria Lilienthal and Johann Rahm{\"o}ller and {de Haan}, Noortje and Alexandra H{\"o}lscher and Raghu Erapaneedi and Giannou, {Anastasios D} and Lilian Aly and Ryota Sato and {de Neef}, {Louise A} and Andr{\'e} Winkler and Dominique Braumann and Juliane Hobusch and Kyra Kuhnigk and Vanessa Kr{\'e}mer and Moritz Steinhaus and V{\'e}ronique Blanchard and Timo Gemoll and Habermann, {Jens K} and Mattias Collin and Gabriela Salinas and Manz, {Rudolf A} and Hidehiro Fukuyama and Thomas Korn and Ari Waisman and Nir Yogev and Samuel Huber and Germany, {Institute of Biochemistry Kiel University} and Stefan Rose-John and Hauke Busch and Friederike Berberich-Siebelt and Christoph H{\"o}lscher and Netherlands, {Center for Proteomics and Metabolomics Leiden University Medical Center Leiden} and Marc Ehlers",
note = "Copyright {\textcopyright} 2020 The Authors. Published by Elsevier Inc. All rights reserved.",
year = "2020",
month = sep,
doi = "10.1016/j.jaci.2020.04.059",
language = "English",
volume = "146",
pages = "652--666.e11",
journal = "J ALLERGY CLIN IMMUN",
issn = "0091-6749",
publisher = "Mosby Inc.",
number = "3",

}

RIS

TY - JOUR

T1 - IgG Fc sialylation is regulated during the germinal center reaction following immunization with different adjuvants

AU - Bartsch, Yannic C

AU - Eschweiler, Simon

AU - Leliavski, Alexei

AU - Lunding, Hanna B

AU - Wagt, Sander

AU - Petry, Janina

AU - Lilienthal, Gina-Maria

AU - Rahmöller, Johann

AU - de Haan, Noortje

AU - Hölscher, Alexandra

AU - Erapaneedi, Raghu

AU - Giannou, Anastasios D

AU - Aly, Lilian

AU - Sato, Ryota

AU - de Neef, Louise A

AU - Winkler, André

AU - Braumann, Dominique

AU - Hobusch, Juliane

AU - Kuhnigk, Kyra

AU - Krémer, Vanessa

AU - Steinhaus, Moritz

AU - Blanchard, Véronique

AU - Gemoll, Timo

AU - Habermann, Jens K

AU - Collin, Mattias

AU - Salinas, Gabriela

AU - Manz, Rudolf A

AU - Fukuyama, Hidehiro

AU - Korn, Thomas

AU - Waisman, Ari

AU - Yogev, Nir

AU - Huber, Samuel

AU - Germany, Institute of Biochemistry Kiel University

AU - Rose-John, Stefan

AU - Busch, Hauke

AU - Berberich-Siebelt, Friederike

AU - Hölscher, Christoph

AU - Netherlands, Center for Proteomics and Metabolomics Leiden University Medical Center Leiden

AU - Ehlers, Marc

N1 - Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

PY - 2020/9

Y1 - 2020/9

N2 - BACKGROUND: Effector functions of IgG Abs are regulated by their Fc N-glycosylation pattern. IgG Fc glycans that lack galactose and terminal sialic acid residues correlate with the severity of inflammatory (auto)immune disorders and have also been linked to protection against viral infection and discussed in the context of vaccine-induced protection. In contrast, sialylated IgG Abs have shown immunosuppressive effects.OBJECTIVE: We sought to investigate IgG glycosylation programming during the germinal center (GC) reaction following immunization of mice with a foreign protein antigen and different adjuvants.METHODS: Mice were analyzed for GC T-cell, B-cell, and plasma cell responses, as well as for antigen-specific serum IgG subclass titers and Fc glycosylation patterns.RESULTS: Different adjuvants induce distinct IgG+ GC B-cell responses with specific transcriptomes and expression levels of the α2,6-sialyltransferase responsible for IgG sialylation that correspond to distinct serum IgG Fc glycosylation patterns. Low IgG Fc sialylation programming in GC B cells was overall highly dependent on the Foxp3- follicular helper T (TFH) cell-inducing cytokine IL-6, here in particular induced by water-in-oil adjuvants and Mycobacterium tuberculosis. Furthermore, low IgG Fc sialylation programming was dependent on adjuvants that induced IL-27 receptor-dependent IFN-γ+ TFH1 cells, IL-6/IL-23-dependent IL-17A+ TFH17 cells, and high ratios of TFH cells to Foxp3+ follicular regulatory T cells. Here, the 2 latter were dependent on M tuberculosis and its cord factor.CONCLUSION: This study's findings regarding adjuvant-dependent GC responses and IgG glycosylation programming may aid in the development of novel vaccination strategies to induce IgG Abs with both high affinity and defined Fc glycosylation patterns in the GC.

AB - BACKGROUND: Effector functions of IgG Abs are regulated by their Fc N-glycosylation pattern. IgG Fc glycans that lack galactose and terminal sialic acid residues correlate with the severity of inflammatory (auto)immune disorders and have also been linked to protection against viral infection and discussed in the context of vaccine-induced protection. In contrast, sialylated IgG Abs have shown immunosuppressive effects.OBJECTIVE: We sought to investigate IgG glycosylation programming during the germinal center (GC) reaction following immunization of mice with a foreign protein antigen and different adjuvants.METHODS: Mice were analyzed for GC T-cell, B-cell, and plasma cell responses, as well as for antigen-specific serum IgG subclass titers and Fc glycosylation patterns.RESULTS: Different adjuvants induce distinct IgG+ GC B-cell responses with specific transcriptomes and expression levels of the α2,6-sialyltransferase responsible for IgG sialylation that correspond to distinct serum IgG Fc glycosylation patterns. Low IgG Fc sialylation programming in GC B cells was overall highly dependent on the Foxp3- follicular helper T (TFH) cell-inducing cytokine IL-6, here in particular induced by water-in-oil adjuvants and Mycobacterium tuberculosis. Furthermore, low IgG Fc sialylation programming was dependent on adjuvants that induced IL-27 receptor-dependent IFN-γ+ TFH1 cells, IL-6/IL-23-dependent IL-17A+ TFH17 cells, and high ratios of TFH cells to Foxp3+ follicular regulatory T cells. Here, the 2 latter were dependent on M tuberculosis and its cord factor.CONCLUSION: This study's findings regarding adjuvant-dependent GC responses and IgG glycosylation programming may aid in the development of novel vaccination strategies to induce IgG Abs with both high affinity and defined Fc glycosylation patterns in the GC.

U2 - 10.1016/j.jaci.2020.04.059

DO - 10.1016/j.jaci.2020.04.059

M3 - SCORING: Journal article

C2 - 32445838

VL - 146

SP - 652-666.e11

JO - J ALLERGY CLIN IMMUN

JF - J ALLERGY CLIN IMMUN

SN - 0091-6749

IS - 3

ER -