B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen

Irene Puga; Montserrat Cols; Carolina M. Barra; Bing He; Linda Cassis; Maurizio Gentile; Laura Comerma; Alejo Chorny; Meimei Shan; Weifeng Xu; Giuliana Magri; Daniel M. Knowles; Wayne Tam; April Chiu; James B. Bussel; Sergi Serrano; José Antonio Lorente; Beatriz Bellosillo; Josep Lloreta; Nuria Juanpere; Francesc Alameda; Teresa Baró; Cristina Díaz De Heredia; Núria Torán; Albert Català; Montserrat Torrebadell; Claudia Fortuny; Victoria Cusí; Carmen Carreras; George A. Diaz; J. Magarian Blander; Claire Michèle Farber; Guido Silvestri; Charlotte Cunningham-Rundles; Michaela Calvillo; Carlo Dufour; Lucia Dora Notarangelo; Vassilios Lougaris; Alessandro Plebani; Jean Laurent Casanova; Stephanie C. Ganal; Andreas Diefenbach; Juan Ignacio Aróstegui; Manel Juan; Jordi Yagüe; Nizar Mahlaoui; Jean Donadieu; Kang Chen; Andrea Cerutti

doi:10.1038/ni.2194

B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen

Irene Puga, Montserrat Cols, Carolina M. Barra, Bing He, Linda Cassis, Maurizio Gentile, Laura Comerma, Alejo Chorny, Meimei Shan, Weifeng Xu, Giuliana Magri, Daniel M. Knowles, Wayne Tam, April Chiu, James B. Bussel, Sergi Serrano, José Antonio Lorente, Beatriz Bellosillo, Josep Lloreta, Nuria JuanpereFrancesc Alameda, Teresa Baró, Cristina Díaz De Heredia, Núria Torán, Albert Català, Montserrat Torrebadell, Claudia Fortuny, Victoria Cusí, Carmen Carreras, George A. Diaz, J. Magarian Blander, Claire Michèle Farber, Guido Silvestri, Charlotte Cunningham-Rundles, Michaela Calvillo, Carlo Dufour, Lucia Dora Notarangelo, Vassilios Lougaris, Alessandro Plebani, Jean Laurent Casanova, Stephanie C. Ganal, Andreas Diefenbach, Juan Ignacio Aróstegui, Manel Juan, Jordi Yagüe, Nizar Mahlaoui, Jean Donadieu, Kang Chen, Andrea Cerutti

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

416 Citations (Scopus)

Abstract

Neutrophils use immunoglobulins to clear antigen, but their role in immunoglobulin production is unknown. Here we identified neutrophils around the marginal zone (MZ) of the spleen, a B cell area specialized in T cell-independent immunoglobulin responses to circulating antigen. Neutrophils colonized peri-MZ areas after postnatal mucosal colonization by microbes and enhanced their B cell-helper function after receiving reprogramming signals, including interleukin 10 (IL-10), from splenic sinusoidal endothelial cells. Splenic neutrophils induced immunoglobulin class switching, somatic hypermutation and antibody production by activating MZ B cells through a mechanism that involved the cytokines BAFF, APRIL and IL-21. Neutropenic patients had fewer and hypomutated MZ B cells and a lower abundance of preimmune immunoglobulins to T cell-independent antigens, which indicates that neutrophils generate an innate layer of antimicrobial immunoglobulin defense by interacting with MZ B cells. © 2012 Nature America, Inc. All rights reserved.

Original language	English
Pages (from-to)	170-180
Journal	Nature Immunology
Volume	13
Issue number	2
DOIs	https://doi.org/10.1038/ni.2194
Publication status	Published - 1 Feb 2012

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Puga, I., Cols, M., Barra, C. M., He, B., Cassis, L., Gentile, M., Comerma, L., Chorny, A., Shan, M., Xu, W., Magri, G., Knowles, D. M., Tam, W., Chiu, A., Bussel, J. B., Serrano, S., Lorente, J. A., Bellosillo, B., Lloreta, J., ... Cerutti, A. (2012). B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nature Immunology, 13(2), 170-180. https://doi.org/10.1038/ni.2194

Puga, Irene ; Cols, Montserrat ; Barra, Carolina M. ; He, Bing ; Cassis, Linda ; Gentile, Maurizio ; Comerma, Laura ; Chorny, Alejo ; Shan, Meimei ; Xu, Weifeng ; Magri, Giuliana ; Knowles, Daniel M. ; Tam, Wayne ; Chiu, April ; Bussel, James B. ; Serrano, Sergi ; Lorente, José Antonio ; Bellosillo, Beatriz ; Lloreta, Josep ; Juanpere, Nuria ; Alameda, Francesc ; Baró, Teresa ; De Heredia, Cristina Díaz ; Torán, Núria ; Català, Albert ; Torrebadell, Montserrat ; Fortuny, Claudia ; Cusí, Victoria ; Carreras, Carmen ; Diaz, George A. ; Blander, J. Magarian ; Farber, Claire Michèle ; Silvestri, Guido ; Cunningham-Rundles, Charlotte ; Calvillo, Michaela ; Dufour, Carlo ; Notarangelo, Lucia Dora ; Lougaris, Vassilios ; Plebani, Alessandro ; Casanova, Jean Laurent ; Ganal, Stephanie C. ; Diefenbach, Andreas ; Aróstegui, Juan Ignacio ; Juan, Manel ; Yagüe, Jordi ; Mahlaoui, Nizar ; Donadieu, Jean ; Chen, Kang ; Cerutti, Andrea. / B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. In: Nature Immunology. 2012 ; Vol. 13, No. 2. pp. 170-180.

@article{2c37b119191b4707b095458abeca4722,

title = "B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen",

abstract = "Neutrophils use immunoglobulins to clear antigen, but their role in immunoglobulin production is unknown. Here we identified neutrophils around the marginal zone (MZ) of the spleen, a B cell area specialized in T cell-independent immunoglobulin responses to circulating antigen. Neutrophils colonized peri-MZ areas after postnatal mucosal colonization by microbes and enhanced their B cell-helper function after receiving reprogramming signals, including interleukin 10 (IL-10), from splenic sinusoidal endothelial cells. Splenic neutrophils induced immunoglobulin class switching, somatic hypermutation and antibody production by activating MZ B cells through a mechanism that involved the cytokines BAFF, APRIL and IL-21. Neutropenic patients had fewer and hypomutated MZ B cells and a lower abundance of preimmune immunoglobulins to T cell-independent antigens, which indicates that neutrophils generate an innate layer of antimicrobial immunoglobulin defense by interacting with MZ B cells. {\textcopyright} 2012 Nature America, Inc. All rights reserved.",

author = "Irene Puga and Montserrat Cols and Barra, {Carolina M.} and Bing He and Linda Cassis and Maurizio Gentile and Laura Comerma and Alejo Chorny and Meimei Shan and Weifeng Xu and Giuliana Magri and Knowles, {Daniel M.} and Wayne Tam and April Chiu and Bussel, {James B.} and Sergi Serrano and Lorente, {Jos{\'e} Antonio} and Beatriz Bellosillo and Josep Lloreta and Nuria Juanpere and Francesc Alameda and Teresa Bar{\'o} and {De Heredia}, {Cristina D{\'i}az} and N{\'u}ria Tor{\'a}n and Albert Catal{\`a} and Montserrat Torrebadell and Claudia Fortuny and Victoria Cus{\'i} and Carmen Carreras and Diaz, {George A.} and Blander, {J. Magarian} and Farber, {Claire Mich{\`e}le} and Guido Silvestri and Charlotte Cunningham-Rundles and Michaela Calvillo and Carlo Dufour and Notarangelo, {Lucia Dora} and Vassilios Lougaris and Alessandro Plebani and Casanova, {Jean Laurent} and Ganal, {Stephanie C.} and Andreas Diefenbach and Ar{\'o}stegui, {Juan Ignacio} and Manel Juan and Jordi Yag{\"u}e and Nizar Mahlaoui and Jean Donadieu and Kang Chen and Andrea Cerutti",

year = "2012",

month = feb,

day = "1",

doi = "10.1038/ni.2194",

language = "English",

volume = "13",

pages = "170--180",

journal = "Nature Immunology",

issn = "1529-2908",

number = "2",

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Puga, I, Cols, M, Barra, CM, He, B, Cassis, L, Gentile, M, Comerma, L, Chorny, A, Shan, M, Xu, W, Magri, G, Knowles, DM, Tam, W, Chiu, A, Bussel, JB, Serrano, S, Lorente, JA, Bellosillo, B, Lloreta, J, Juanpere, N, Alameda, F, Baró, T, De Heredia, CD, Torán, N, Català, A, Torrebadell, M, Fortuny, C, Cusí, V, Carreras, C, Diaz, GA, Blander, JM, Farber, CM, Silvestri, G, Cunningham-Rundles, C, Calvillo, M, Dufour, C, Notarangelo, LD, Lougaris, V, Plebani, A, Casanova, JL, Ganal, SC, Diefenbach, A, Aróstegui, JI, Juan, M, Yagüe, J, Mahlaoui, N, Donadieu, J, Chen, K & Cerutti, A 2012, 'B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen', Nature Immunology, vol. 13, no. 2, pp. 170-180. https://doi.org/10.1038/ni.2194

B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. / Puga, Irene; Cols, Montserrat; Barra, Carolina M.; He, Bing; Cassis, Linda; Gentile, Maurizio; Comerma, Laura; Chorny, Alejo; Shan, Meimei; Xu, Weifeng; Magri, Giuliana; Knowles, Daniel M.; Tam, Wayne; Chiu, April; Bussel, James B.; Serrano, Sergi; Lorente, José Antonio; Bellosillo, Beatriz; Lloreta, Josep; Juanpere, Nuria; Alameda, Francesc; Baró, Teresa; De Heredia, Cristina Díaz; Torán, Núria; Català, Albert; Torrebadell, Montserrat; Fortuny, Claudia; Cusí, Victoria; Carreras, Carmen; Diaz, George A.; Blander, J. Magarian; Farber, Claire Michèle; Silvestri, Guido; Cunningham-Rundles, Charlotte; Calvillo, Michaela; Dufour, Carlo; Notarangelo, Lucia Dora; Lougaris, Vassilios; Plebani, Alessandro; Casanova, Jean Laurent; Ganal, Stephanie C.; Diefenbach, Andreas; Aróstegui, Juan Ignacio; Juan, Manel; Yagüe, Jordi; Mahlaoui, Nizar; Donadieu, Jean; Chen, Kang; Cerutti, Andrea.

In: Nature Immunology, Vol. 13, No. 2, 01.02.2012, p. 170-180.

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

TY - JOUR

T1 - B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen

AU - Puga, Irene

AU - Cols, Montserrat

AU - Barra, Carolina M.

AU - He, Bing

AU - Cassis, Linda

AU - Gentile, Maurizio

AU - Comerma, Laura

AU - Chorny, Alejo

AU - Shan, Meimei

AU - Xu, Weifeng

AU - Magri, Giuliana

AU - Knowles, Daniel M.

AU - Tam, Wayne

AU - Chiu, April

AU - Bussel, James B.

AU - Serrano, Sergi

AU - Lorente, José Antonio

AU - Bellosillo, Beatriz

AU - Lloreta, Josep

AU - Juanpere, Nuria

AU - Alameda, Francesc

AU - Baró, Teresa

AU - De Heredia, Cristina Díaz

AU - Torán, Núria

AU - Català, Albert

AU - Torrebadell, Montserrat

AU - Fortuny, Claudia

AU - Cusí, Victoria

AU - Carreras, Carmen

AU - Diaz, George A.

AU - Blander, J. Magarian

AU - Farber, Claire Michèle

AU - Silvestri, Guido

AU - Cunningham-Rundles, Charlotte

AU - Calvillo, Michaela

AU - Dufour, Carlo

AU - Notarangelo, Lucia Dora

AU - Lougaris, Vassilios

AU - Plebani, Alessandro

AU - Casanova, Jean Laurent

AU - Ganal, Stephanie C.

AU - Diefenbach, Andreas

AU - Aróstegui, Juan Ignacio

AU - Juan, Manel

AU - Yagüe, Jordi

AU - Mahlaoui, Nizar

AU - Donadieu, Jean

AU - Chen, Kang

AU - Cerutti, Andrea

PY - 2012/2/1

Y1 - 2012/2/1

N2 - Neutrophils use immunoglobulins to clear antigen, but their role in immunoglobulin production is unknown. Here we identified neutrophils around the marginal zone (MZ) of the spleen, a B cell area specialized in T cell-independent immunoglobulin responses to circulating antigen. Neutrophils colonized peri-MZ areas after postnatal mucosal colonization by microbes and enhanced their B cell-helper function after receiving reprogramming signals, including interleukin 10 (IL-10), from splenic sinusoidal endothelial cells. Splenic neutrophils induced immunoglobulin class switching, somatic hypermutation and antibody production by activating MZ B cells through a mechanism that involved the cytokines BAFF, APRIL and IL-21. Neutropenic patients had fewer and hypomutated MZ B cells and a lower abundance of preimmune immunoglobulins to T cell-independent antigens, which indicates that neutrophils generate an innate layer of antimicrobial immunoglobulin defense by interacting with MZ B cells. © 2012 Nature America, Inc. All rights reserved.

AB - Neutrophils use immunoglobulins to clear antigen, but their role in immunoglobulin production is unknown. Here we identified neutrophils around the marginal zone (MZ) of the spleen, a B cell area specialized in T cell-independent immunoglobulin responses to circulating antigen. Neutrophils colonized peri-MZ areas after postnatal mucosal colonization by microbes and enhanced their B cell-helper function after receiving reprogramming signals, including interleukin 10 (IL-10), from splenic sinusoidal endothelial cells. Splenic neutrophils induced immunoglobulin class switching, somatic hypermutation and antibody production by activating MZ B cells through a mechanism that involved the cytokines BAFF, APRIL and IL-21. Neutropenic patients had fewer and hypomutated MZ B cells and a lower abundance of preimmune immunoglobulins to T cell-independent antigens, which indicates that neutrophils generate an innate layer of antimicrobial immunoglobulin defense by interacting with MZ B cells. © 2012 Nature America, Inc. All rights reserved.

U2 - 10.1038/ni.2194

DO - 10.1038/ni.2194

M3 - Article

VL - 13

SP - 170

EP - 180

JO - Nature Immunology

JF - Nature Immunology

SN - 1529-2908

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ER -