Cargando…

The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells

Pentraxin 3 (PTX3) is a fluid-phase pattern recognition receptor of the humoral innate immune system with ancestral antibody-like properties but unknown antibody-inducing function. In this study, we found binding of PTX3 to splenic marginal zone (MZ) B cells, an innate-like subset of antibody-produc...

Descripción completa

Detalles Bibliográficos
Autores principales: Chorny, Alejo, Casas-Recasens, Sandra, Sintes, Jordi, Shan, Meimei, Polentarutti, Nadia, García-Escudero, Ramón, Walland, A. Cooper, Yeiser, John R., Cassis, Linda, Carrillo, Jorge, Puga, Irene, Cunha, Cristina, Bastos, Hélder, Rodrigues, Fernando, Lacerda, João F., Morais, António, Dieguez-Gonzalez, Rebeca, Heeger, Peter S., Salvatori, Giovanni, Carvalho, Agostinho, Garcia-Sastre, Adolfo, Blander, J. Magarian, Mantovani, Alberto, Garlanda, Cecilia, Cerutti, Andrea
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5030794/
https://www.ncbi.nlm.nih.gov/pubmed/27621420
http://dx.doi.org/10.1084/jem.20150282
_version_ 1782454739198279680
author Chorny, Alejo
Casas-Recasens, Sandra
Sintes, Jordi
Shan, Meimei
Polentarutti, Nadia
García-Escudero, Ramón
Walland, A. Cooper
Yeiser, John R.
Cassis, Linda
Carrillo, Jorge
Puga, Irene
Cunha, Cristina
Bastos, Hélder
Rodrigues, Fernando
Lacerda, João F.
Morais, António
Dieguez-Gonzalez, Rebeca
Heeger, Peter S.
Salvatori, Giovanni
Carvalho, Agostinho
Garcia-Sastre, Adolfo
Blander, J. Magarian
Mantovani, Alberto
Garlanda, Cecilia
Cerutti, Andrea
author_facet Chorny, Alejo
Casas-Recasens, Sandra
Sintes, Jordi
Shan, Meimei
Polentarutti, Nadia
García-Escudero, Ramón
Walland, A. Cooper
Yeiser, John R.
Cassis, Linda
Carrillo, Jorge
Puga, Irene
Cunha, Cristina
Bastos, Hélder
Rodrigues, Fernando
Lacerda, João F.
Morais, António
Dieguez-Gonzalez, Rebeca
Heeger, Peter S.
Salvatori, Giovanni
Carvalho, Agostinho
Garcia-Sastre, Adolfo
Blander, J. Magarian
Mantovani, Alberto
Garlanda, Cecilia
Cerutti, Andrea
author_sort Chorny, Alejo
collection PubMed
description Pentraxin 3 (PTX3) is a fluid-phase pattern recognition receptor of the humoral innate immune system with ancestral antibody-like properties but unknown antibody-inducing function. In this study, we found binding of PTX3 to splenic marginal zone (MZ) B cells, an innate-like subset of antibody-producing lymphocytes strategically positioned at the interface between the circulation and the adaptive immune system. PTX3 was released by a subset of neutrophils that surrounded the splenic MZ and expressed an immune activation–related gene signature distinct from that of circulating neutrophils. Binding of PTX3 promoted homeostatic production of IgM and class-switched IgG antibodies to microbial capsular polysaccharides, which decreased in PTX3-deficient mice and humans. In addition, PTX3 increased IgM and IgG production after infection with blood-borne encapsulated bacteria or immunization with bacterial carbohydrates. This immunogenic effect stemmed from the activation of MZ B cells through a neutrophil-regulated pathway that elicited class switching and plasmablast expansion via a combination of T cell–independent and T cell–dependent signals. Thus, PTX3 may bridge the humoral arms of the innate and adaptive immune systems by serving as an endogenous adjuvant for MZ B cells. This property could be harnessed to develop more effective vaccines against encapsulated pathogens.
format Online
Article
Text
id pubmed-5030794
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher The Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-50307942017-03-19 The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells Chorny, Alejo Casas-Recasens, Sandra Sintes, Jordi Shan, Meimei Polentarutti, Nadia García-Escudero, Ramón Walland, A. Cooper Yeiser, John R. Cassis, Linda Carrillo, Jorge Puga, Irene Cunha, Cristina Bastos, Hélder Rodrigues, Fernando Lacerda, João F. Morais, António Dieguez-Gonzalez, Rebeca Heeger, Peter S. Salvatori, Giovanni Carvalho, Agostinho Garcia-Sastre, Adolfo Blander, J. Magarian Mantovani, Alberto Garlanda, Cecilia Cerutti, Andrea J Exp Med Research Articles Pentraxin 3 (PTX3) is a fluid-phase pattern recognition receptor of the humoral innate immune system with ancestral antibody-like properties but unknown antibody-inducing function. In this study, we found binding of PTX3 to splenic marginal zone (MZ) B cells, an innate-like subset of antibody-producing lymphocytes strategically positioned at the interface between the circulation and the adaptive immune system. PTX3 was released by a subset of neutrophils that surrounded the splenic MZ and expressed an immune activation–related gene signature distinct from that of circulating neutrophils. Binding of PTX3 promoted homeostatic production of IgM and class-switched IgG antibodies to microbial capsular polysaccharides, which decreased in PTX3-deficient mice and humans. In addition, PTX3 increased IgM and IgG production after infection with blood-borne encapsulated bacteria or immunization with bacterial carbohydrates. This immunogenic effect stemmed from the activation of MZ B cells through a neutrophil-regulated pathway that elicited class switching and plasmablast expansion via a combination of T cell–independent and T cell–dependent signals. Thus, PTX3 may bridge the humoral arms of the innate and adaptive immune systems by serving as an endogenous adjuvant for MZ B cells. This property could be harnessed to develop more effective vaccines against encapsulated pathogens. The Rockefeller University Press 2016-09-19 /pmc/articles/PMC5030794/ /pubmed/27621420 http://dx.doi.org/10.1084/jem.20150282 Text en © 2016 Chorny et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Articles
Chorny, Alejo
Casas-Recasens, Sandra
Sintes, Jordi
Shan, Meimei
Polentarutti, Nadia
García-Escudero, Ramón
Walland, A. Cooper
Yeiser, John R.
Cassis, Linda
Carrillo, Jorge
Puga, Irene
Cunha, Cristina
Bastos, Hélder
Rodrigues, Fernando
Lacerda, João F.
Morais, António
Dieguez-Gonzalez, Rebeca
Heeger, Peter S.
Salvatori, Giovanni
Carvalho, Agostinho
Garcia-Sastre, Adolfo
Blander, J. Magarian
Mantovani, Alberto
Garlanda, Cecilia
Cerutti, Andrea
The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells
title The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells
title_full The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells
title_fullStr The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells
title_full_unstemmed The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells
title_short The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells
title_sort soluble pattern recognition receptor ptx3 links humoral innate and adaptive immune responses by helping marginal zone b cells
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5030794/
https://www.ncbi.nlm.nih.gov/pubmed/27621420
http://dx.doi.org/10.1084/jem.20150282
work_keys_str_mv AT chornyalejo thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT casasrecasenssandra thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT sintesjordi thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT shanmeimei thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT polentaruttinadia thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT garciaescuderoramon thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT wallandacooper thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT yeiserjohnr thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT cassislinda thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT carrillojorge thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT pugairene thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT cunhacristina thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT bastoshelder thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT rodriguesfernando thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT lacerdajoaof thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT moraisantonio thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT dieguezgonzalezrebeca thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT heegerpeters thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT salvatorigiovanni thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT carvalhoagostinho thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT garciasastreadolfo thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT blanderjmagarian thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT mantovanialberto thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT garlandacecilia thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT ceruttiandrea thesolublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT chornyalejo solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT casasrecasenssandra solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT sintesjordi solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT shanmeimei solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT polentaruttinadia solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT garciaescuderoramon solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT wallandacooper solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT yeiserjohnr solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT cassislinda solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT carrillojorge solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT pugairene solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT cunhacristina solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT bastoshelder solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT rodriguesfernando solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT lacerdajoaof solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT moraisantonio solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT dieguezgonzalezrebeca solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT heegerpeters solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT salvatorigiovanni solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT carvalhoagostinho solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT garciasastreadolfo solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT blanderjmagarian solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT mantovanialberto solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT garlandacecilia solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells
AT ceruttiandrea solublepatternrecognitionreceptorptx3linkshumoralinnateandadaptiveimmuneresponsesbyhelpingmarginalzonebcells