The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells
Autor(a) principal: | |
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Data de Publicação: | 2016 |
Outros Autores: | , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/1822/44876 |
Resumo: | 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. |
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The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cellsCiências Médicas::Medicina BásicaScience & TechnologyPentraxin 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.European Advanced grant ERC-2011-ADG-20110310, Ministerio de Ciencia e Innovación grant SAF2011-25241, and Marie Curie reintegra -tion grant PIRG-08-GA-2010-276928 to A. Cerutti; Sara Borrell post-doctoral fellow -ships to A. Chorny; and US National Institutes of Health grants R01 AI57653, U01 AI95613, P01 AI61093, and U19 096187 to A. Cerutti. C. Cunha and A. Carvalho were funded by grants from Fundação para a Ciência e Tecnologia, co-funded by Programa Operacional Regional do Norte (ON.2—O Novo Norte)., and from the Quadro de Referência Estratégico Nacional (SFRH/BPD/96176/2013 to C. Cunha and grant IF/00735/2014 to A. Carvalho) through the Fundo Europeu de Desenvolvimento Regional and Projeto Estratégico (LA 26 – 2013–2014; PEst-C/SAU/LA0026/2013)Rockefeller University PressUniversidade do MinhoChorny, AlejoCasas‑Recasens, SandraSintes, JordiShan, MeimeiPolentarutti, NadiaGarcía‑Escudero, RamónCunha, Cristina AmorimBastos, Hélder NovaisRodrigues, Fernando José dos SantosCarvalho, Agostinho Albérico Rodrigues2016-092016-09-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/1822/44876engChorny, A., Casas-Recasens, S., Sintes, J., Shan, M., et. al.(2016). The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells. The Journal of experimental medicine, 213(10), 2167-21850022-100710.1084/jem.2015028227621420http://jem.rupress.org/content/213/10/2167info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-21T12:48:54Zoai:repositorium.sdum.uminho.pt:1822/44876Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T19:47:14.436877Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
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 |
spellingShingle |
The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells Chorny, Alejo Ciências Médicas::Medicina Básica Science & Technology |
title_short |
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_sort |
The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells |
author |
Chorny, Alejo |
author_facet |
Chorny, Alejo Casas‑Recasens, Sandra Sintes, Jordi Shan, Meimei Polentarutti, Nadia García‑Escudero, Ramón Cunha, Cristina Amorim Bastos, Hélder Novais Rodrigues, Fernando José dos Santos Carvalho, Agostinho Albérico Rodrigues |
author_role |
author |
author2 |
Casas‑Recasens, Sandra Sintes, Jordi Shan, Meimei Polentarutti, Nadia García‑Escudero, Ramón Cunha, Cristina Amorim Bastos, Hélder Novais Rodrigues, Fernando José dos Santos Carvalho, Agostinho Albérico Rodrigues |
author2_role |
author author author author author author author author author |
dc.contributor.none.fl_str_mv |
Universidade do Minho |
dc.contributor.author.fl_str_mv |
Chorny, Alejo Casas‑Recasens, Sandra Sintes, Jordi Shan, Meimei Polentarutti, Nadia García‑Escudero, Ramón Cunha, Cristina Amorim Bastos, Hélder Novais Rodrigues, Fernando José dos Santos Carvalho, Agostinho Albérico Rodrigues |
dc.subject.por.fl_str_mv |
Ciências Médicas::Medicina Básica Science & Technology |
topic |
Ciências Médicas::Medicina Básica Science & Technology |
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. |
publishDate |
2016 |
dc.date.none.fl_str_mv |
2016-09 2016-09-01T00:00:00Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/1822/44876 |
url |
http://hdl.handle.net/1822/44876 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Chorny, A., Casas-Recasens, S., Sintes, J., Shan, M., et. al.(2016). The soluble pattern recognition receptor PTX3 links humoral innate and adaptive immune responses by helping marginal zone B cells. The Journal of experimental medicine, 213(10), 2167-2185 0022-1007 10.1084/jem.20150282 27621420 http://jem.rupress.org/content/213/10/2167 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
Rockefeller University Press |
publisher.none.fl_str_mv |
Rockefeller University Press |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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RCAAP |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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