The distinctive germinal center phase of IgE+ B lymphocytes limits their contribution to the classical memory response

Jin-Shu He; Michael Meyer-Hermann; Deng Xiangying; Lim Yok Zuan; Leigh Ann Jones; Lakshmi Ramakrishna; Victor C de Vries; Jayashree Dolpady; Hoi Aina; Sabrina Joseph; Sriram Narayanan; Sharrada Subramaniam; Manoj Puthia; Glenn Wong; Huizhong Xiong; Michael Poidinger; Joseph F Urban; Juan J Lafaille; Maria A Curotto de Lafaille

doi:10.1084/jem.20131539

The distinctive germinal center phase of IgE+ B lymphocytes limits their contribution to the classical memory response

Jin-Shu He, Michael Meyer-Hermann, Deng Xiangying, Lim Yok Zuan, Leigh Ann Jones, Lakshmi Ramakrishna, Victor C de Vries, Jayashree Dolpady, Hoi Aina, Sabrina Joseph, Sriram Narayanan, Sharrada Subramaniam, Manoj Puthia, Glenn Wong, Huizhong Xiong, Michael Poidinger, Joseph F Urban, Juan J Lafaille, Maria A Curotto de Lafaille

A*STAR Singapore Immunology Network (SIgN)

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

Abstract

The mechanisms involved in the maintenance of memory IgE responses are poorly understood, and the role played by germinal center (GC) IgE(+) cells in memory responses is particularly unclear. IgE(+) B cell differentiation is characterized by a transient GC phase, a bias toward the plasma cell (PC) fate, and dependence on sequential switching for the production of high-affinity IgE. We show here that IgE(+) GC B cells are unfit to undergo the conventional GC differentiation program due to impaired B cell receptor function and increased apoptosis. IgE(+) GC cells fail to populate the GC light zone and are unable to contribute to the memory and long-lived PC compartments. Furthermore, we demonstrate that direct and sequential switching are linked to distinct B cell differentiation fates: direct switching generates IgE(+) GC cells, whereas sequential switching gives rise to IgE(+) PCs. We propose a comprehensive model for the generation and memory of IgE responses.

Original language	English
Pages (from-to)	2755-2771
Journal	Journal of Experimental Medicine
Volume	210
Issue number	12
DOIs	https://doi.org/10.1084/jem.20131539
Publication status	Published - 2013 Nov 18
Externally published	Yes

Subject classification (UKÄ)

Cell and Molecular Biology

Keywords

Animals
Apoptosis
B-Lymphocytes/cytology
Cell Differentiation
Germinal Center/cytology
Green Fluorescent Proteins/genetics
Immunoglobulin Class Switching
Immunoglobulin E/metabolism
Immunoglobulin G/metabolism
Immunologic Memory
Mice
Mice, Inbred BALB C
Mice, Transgenic
Models, Immunological
Nippostrongylus
Plasma Cells/cytology
Receptors, Antigen, B-Cell/metabolism
Signal Transduction
Strongylida Infections/immunology

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10.1084/jem.20131539Licence: CC BY-NC-SA

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He, J-S., Meyer-Hermann, M., Xiangying, D., Zuan, L. Y., Jones, L. A., Ramakrishna, L., de Vries, V. C., Dolpady, J., Aina, H., Joseph, S., Narayanan, S., Subramaniam, S., Puthia, M., Wong, G., Xiong, H., Poidinger, M., Urban, J. F., Lafaille, J. J., & Curotto de Lafaille, M. A. (2013). The distinctive germinal center phase of IgE+ B lymphocytes limits their contribution to the classical memory response. Journal of Experimental Medicine, 210(12), 2755-2771. https://doi.org/10.1084/jem.20131539

@article{e26eca08a3ca40118fccd8251e69779b,

title = "The distinctive germinal center phase of IgE+ B lymphocytes limits their contribution to the classical memory response",

abstract = "The mechanisms involved in the maintenance of memory IgE responses are poorly understood, and the role played by germinal center (GC) IgE(+) cells in memory responses is particularly unclear. IgE(+) B cell differentiation is characterized by a transient GC phase, a bias toward the plasma cell (PC) fate, and dependence on sequential switching for the production of high-affinity IgE. We show here that IgE(+) GC B cells are unfit to undergo the conventional GC differentiation program due to impaired B cell receptor function and increased apoptosis. IgE(+) GC cells fail to populate the GC light zone and are unable to contribute to the memory and long-lived PC compartments. Furthermore, we demonstrate that direct and sequential switching are linked to distinct B cell differentiation fates: direct switching generates IgE(+) GC cells, whereas sequential switching gives rise to IgE(+) PCs. We propose a comprehensive model for the generation and memory of IgE responses. ",

keywords = "Animals, Apoptosis, B-Lymphocytes/cytology, Cell Differentiation, Germinal Center/cytology, Green Fluorescent Proteins/genetics, Immunoglobulin Class Switching, Immunoglobulin E/metabolism, Immunoglobulin G/metabolism, Immunologic Memory, Mice, Mice, Inbred BALB C, Mice, Transgenic, Models, Immunological, Nippostrongylus, Plasma Cells/cytology, Receptors, Antigen, B-Cell/metabolism, Signal Transduction, Strongylida Infections/immunology",

author = "Jin-Shu He and Michael Meyer-Hermann and Deng Xiangying and Zuan, {Lim Yok} and Jones, {Leigh Ann} and Lakshmi Ramakrishna and {de Vries}, {Victor C} and Jayashree Dolpady and Hoi Aina and Sabrina Joseph and Sriram Narayanan and Sharrada Subramaniam and Manoj Puthia and Glenn Wong and Huizhong Xiong and Michael Poidinger and Urban, {Joseph F} and Lafaille, {Juan J} and {Curotto de Lafaille}, {Maria A}",

year = "2013",

month = nov,

day = "18",

doi = "10.1084/jem.20131539",

language = "English",

volume = "210",

pages = "2755--2771",

journal = "Journal of Experimental Medicine",

issn = "1540-9538",

publisher = "Rockefeller University Press",

number = "12",

}

He, J-S, Meyer-Hermann, M, Xiangying, D, Zuan, LY, Jones, LA, Ramakrishna, L, de Vries, VC, Dolpady, J, Aina, H, Joseph, S, Narayanan, S, Subramaniam, S, Puthia, M, Wong, G, Xiong, H, Poidinger, M, Urban, JF, Lafaille, JJ & Curotto de Lafaille, MA 2013, 'The distinctive germinal center phase of IgE+ B lymphocytes limits their contribution to the classical memory response', Journal of Experimental Medicine, vol. 210, no. 12, pp. 2755-2771. https://doi.org/10.1084/jem.20131539

TY - JOUR

T1 - The distinctive germinal center phase of IgE+ B lymphocytes limits their contribution to the classical memory response

AU - He, Jin-Shu

AU - Meyer-Hermann, Michael

AU - Xiangying, Deng

AU - Zuan, Lim Yok

AU - Jones, Leigh Ann

AU - Ramakrishna, Lakshmi

AU - de Vries, Victor C

AU - Dolpady, Jayashree

AU - Aina, Hoi

AU - Joseph, Sabrina

AU - Narayanan, Sriram

AU - Subramaniam, Sharrada

AU - Puthia, Manoj

AU - Wong, Glenn

AU - Xiong, Huizhong

AU - Poidinger, Michael

AU - Urban, Joseph F

AU - Lafaille, Juan J

AU - Curotto de Lafaille, Maria A

PY - 2013/11/18

Y1 - 2013/11/18

N2 - The mechanisms involved in the maintenance of memory IgE responses are poorly understood, and the role played by germinal center (GC) IgE(+) cells in memory responses is particularly unclear. IgE(+) B cell differentiation is characterized by a transient GC phase, a bias toward the plasma cell (PC) fate, and dependence on sequential switching for the production of high-affinity IgE. We show here that IgE(+) GC B cells are unfit to undergo the conventional GC differentiation program due to impaired B cell receptor function and increased apoptosis. IgE(+) GC cells fail to populate the GC light zone and are unable to contribute to the memory and long-lived PC compartments. Furthermore, we demonstrate that direct and sequential switching are linked to distinct B cell differentiation fates: direct switching generates IgE(+) GC cells, whereas sequential switching gives rise to IgE(+) PCs. We propose a comprehensive model for the generation and memory of IgE responses.

AB - The mechanisms involved in the maintenance of memory IgE responses are poorly understood, and the role played by germinal center (GC) IgE(+) cells in memory responses is particularly unclear. IgE(+) B cell differentiation is characterized by a transient GC phase, a bias toward the plasma cell (PC) fate, and dependence on sequential switching for the production of high-affinity IgE. We show here that IgE(+) GC B cells are unfit to undergo the conventional GC differentiation program due to impaired B cell receptor function and increased apoptosis. IgE(+) GC cells fail to populate the GC light zone and are unable to contribute to the memory and long-lived PC compartments. Furthermore, we demonstrate that direct and sequential switching are linked to distinct B cell differentiation fates: direct switching generates IgE(+) GC cells, whereas sequential switching gives rise to IgE(+) PCs. We propose a comprehensive model for the generation and memory of IgE responses.

KW - Animals

KW - Apoptosis

KW - B-Lymphocytes/cytology

KW - Cell Differentiation

KW - Germinal Center/cytology

KW - Green Fluorescent Proteins/genetics

KW - Immunoglobulin Class Switching

KW - Immunoglobulin E/metabolism

KW - Immunoglobulin G/metabolism

KW - Immunologic Memory

KW - Mice

KW - Mice, Inbred BALB C

KW - Mice, Transgenic

KW - Models, Immunological

KW - Nippostrongylus

KW - Plasma Cells/cytology

KW - Receptors, Antigen, B-Cell/metabolism

KW - Signal Transduction

KW - Strongylida Infections/immunology

U2 - 10.1084/jem.20131539

DO - 10.1084/jem.20131539

M3 - Article

C2 - 24218137

VL - 210

SP - 2755

EP - 2771

JO - Journal of Experimental Medicine

JF - Journal of Experimental Medicine

SN - 1540-9538

IS - 12

ER -

The distinctive germinal center phase of IgE+ B lymphocytes limits their contribution to the classical memory response

Abstract

Subject classification (UKÄ)

Keywords

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