The shaping of immunological responses through natural selection after the Roma Diaspora

Autoinflammatory diseases (AIDs) were first described as clinical disorders characterized by recurrent episodes of seemingly unprovoked sterile inflammation. In the past few years, the identification of novel AIDs expanded their phenotypes toward more complex clinical pictures associating vasculopat...

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Detalhes bibliográficos
Autores: Dobón Berenguer, Begoña, 1987-, Ter Horst, Rob, Laayouni, Hafid, 1968-, Mondal, Mayukh, 1989-, Bianco, Erica, Comas, David, 1969-, Ioana, Mihai, Bosch Fusté, Elena, Bertranpetit, Jaume, 1952-, Netea, Mihai G.
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Recursos:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/45591
Acesso em linha:http://hdl.handle.net/10230/45591
http://dx.doi.org/10.1038/s41598-020-73182-1
Access Level:acceso abierto
Palavra-chave:APLAID
Autoinflammatory diseases
PLCγ2
Agammaglobulinemia
Caspase-1
Inflammasome
Interleukin-1
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oai_identifier_str oai:recercat.cat:10230/45591
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv The shaping of immunological responses through natural selection after the Roma Diaspora
title The shaping of immunological responses through natural selection after the Roma Diaspora
spellingShingle The shaping of immunological responses through natural selection after the Roma Diaspora
Dobón Berenguer, Begoña, 1987-
APLAID
Autoinflammatory diseases
PLCγ2
Agammaglobulinemia
Caspase-1
Inflammasome
Interleukin-1
title_short The shaping of immunological responses through natural selection after the Roma Diaspora
title_full The shaping of immunological responses through natural selection after the Roma Diaspora
title_fullStr The shaping of immunological responses through natural selection after the Roma Diaspora
title_full_unstemmed The shaping of immunological responses through natural selection after the Roma Diaspora
title_sort The shaping of immunological responses through natural selection after the Roma Diaspora
dc.creator.none.fl_str_mv Dobón Berenguer, Begoña, 1987-
Ter Horst, Rob
Laayouni, Hafid, 1968-
Mondal, Mayukh, 1989-
Bianco, Erica
Comas, David, 1969-
Ioana, Mihai
Bosch Fusté, Elena
Bertranpetit, Jaume, 1952-
Netea, Mihai G.
author Dobón Berenguer, Begoña, 1987-
author_facet Dobón Berenguer, Begoña, 1987-
Ter Horst, Rob
Laayouni, Hafid, 1968-
Mondal, Mayukh, 1989-
Bianco, Erica
Comas, David, 1969-
Ioana, Mihai
Bosch Fusté, Elena
Bertranpetit, Jaume, 1952-
Netea, Mihai G.
author_role author
author2 Ter Horst, Rob
Laayouni, Hafid, 1968-
Mondal, Mayukh, 1989-
Bianco, Erica
Comas, David, 1969-
Ioana, Mihai
Bosch Fusté, Elena
Bertranpetit, Jaume, 1952-
Netea, Mihai G.
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv APLAID
Autoinflammatory diseases
PLCγ2
Agammaglobulinemia
Caspase-1
Inflammasome
Interleukin-1
topic APLAID
Autoinflammatory diseases
PLCγ2
Agammaglobulinemia
Caspase-1
Inflammasome
Interleukin-1
description Autoinflammatory diseases (AIDs) were first described as clinical disorders characterized by recurrent episodes of seemingly unprovoked sterile inflammation. In the past few years, the identification of novel AIDs expanded their phenotypes toward more complex clinical pictures associating vasculopathy, autoimmunity, or immunodeficiency. Herein, we describe two unrelated patients suffering since the neonatal period from a complex disease mainly characterized by severe sterile inflammation, recurrent bacterial infections, and marked humoral immunodeficiency. Whole-exome sequencing detected a novel, de novo heterozygous PLCG2 variant in each patient (p.Ala708Pro and p.Leu845_Leu848del). A clear enhanced PLCγ2 activity for both variants was demonstrated by both ex vivo calcium responses of the patient's B cells to IgM stimulation and in vitro assessment of PLC activity. These data supported the autoinflammation and PLCγ2-associated antibody deficiency and immune dysregulation (APLAID) diagnosis in both patients. Immunological evaluation revealed a severe decrease of immunoglobulins and B cells, especially class-switched memory B cells, with normal T and NK cell counts. Analysis of bone marrow of one patient revealed a reduced immature B cell fraction compared with controls. Additional investigations showed that both PLCG2 variants activate the NLRP3-inflammasome through the alternative pathway instead of the canonical pathway. Collectively, the evidences here shown expand APLAID diversity toward more severe phenotypes than previously reported including dominantly inherited agammaglobulinemia, add novel data about its genetic basis, and implicate the alternative NLRP3-inflammasome activation pathway in the basis of sterile inflammation.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/45591
http://dx.doi.org/10.1038/s41598-020-73182-1
url http://hdl.handle.net/10230/45591
http://dx.doi.org/10.1038/s41598-020-73182-1
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Sci Rep. 2020; 10(1):16134
info:eu-repo/grantAgreement/ES/1PE/BFU2016-77961-P
info:eu-repo/grantAgreement/ES/1PE/CGL2016-75389-P
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Research
publisher.none.fl_str_mv Nature Research
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling The shaping of immunological responses through natural selection after the Roma DiasporaDobón Berenguer, Begoña, 1987-Ter Horst, RobLaayouni, Hafid, 1968-Mondal, Mayukh, 1989-Bianco, EricaComas, David, 1969-Ioana, MihaiBosch Fusté, ElenaBertranpetit, Jaume, 1952-Netea, Mihai G.APLAIDAutoinflammatory diseasesPLCγ2AgammaglobulinemiaCaspase-1InflammasomeInterleukin-1Autoinflammatory diseases (AIDs) were first described as clinical disorders characterized by recurrent episodes of seemingly unprovoked sterile inflammation. In the past few years, the identification of novel AIDs expanded their phenotypes toward more complex clinical pictures associating vasculopathy, autoimmunity, or immunodeficiency. Herein, we describe two unrelated patients suffering since the neonatal period from a complex disease mainly characterized by severe sterile inflammation, recurrent bacterial infections, and marked humoral immunodeficiency. Whole-exome sequencing detected a novel, de novo heterozygous PLCG2 variant in each patient (p.Ala708Pro and p.Leu845_Leu848del). A clear enhanced PLCγ2 activity for both variants was demonstrated by both ex vivo calcium responses of the patient's B cells to IgM stimulation and in vitro assessment of PLC activity. These data supported the autoinflammation and PLCγ2-associated antibody deficiency and immune dysregulation (APLAID) diagnosis in both patients. Immunological evaluation revealed a severe decrease of immunoglobulins and B cells, especially class-switched memory B cells, with normal T and NK cell counts. Analysis of bone marrow of one patient revealed a reduced immature B cell fraction compared with controls. Additional investigations showed that both PLCG2 variants activate the NLRP3-inflammasome through the alternative pathway instead of the canonical pathway. Collectively, the evidences here shown expand APLAID diversity toward more severe phenotypes than previously reported including dominantly inherited agammaglobulinemia, add novel data about its genetic basis, and implicate the alternative NLRP3-inflammasome activation pathway in the basis of sterile inflammation.This work has been partially funded by the following: CERCA Programme/Generalitat de Catalunya (JIA), SAF2015-68472-C2-1-R grant from the Spanish Ministry of Economy and Competitiveness co-financed by European Regional Development Fund (ERDF) (JIA), RTI2018-096824-B-C21 grant from the Spanish Ministry of Science, Innovation and Universities co-financed by ERDF (JIA), AC15/00027 grant from the Instituto de Salud Carlos III/Transnational Research Projects on Rare Diseases (JIA), PI14/00405 grant from the Instituto de Salud Carlos III co-financed by ERDF (RC), PI13/00174 grant from the Spanish Ministry of Economy and Competitiveness co-financed by ERDF (PP), SAF2017-88276-R grant from the Spanish Ministry of Economy, Industry and Competitiveness co-financed by ERDF (PP), ERC-2013-CoG project 614578 from the European Research Council (PP), 20859/PI/18 grant from Fundación Séneca (PP), SAF2015-68472-C2-2-R grant from the Spanish Ministry of Economy and Competitiveness co-financed by ERDF (FC) and RTI2018-096824-B-C22 grant from the Spanish Ministry of Science, Innovation and Universities co-financed by ERDF (FC). MK acknowledges support from CRUK (A16567) and MRC (P028160). H M-B is a Rio Hortega fellowship from Instituto de Salud Carlos III (CM14/00008) and DB acknowledges support from the UCL Impact Studentship.Nature Research202020202020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/45591http://dx.doi.org/10.1038/s41598-020-73182-1reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésSci Rep. 2020; 10(1):16134info:eu-repo/grantAgreement/ES/1PE/BFU2016-77961-Pinfo:eu-repo/grantAgreement/ES/1PE/CGL2016-75389-P© The Author(s) 2020. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/455912026-05-29T05:05:01Z
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