Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells.

2.50
HDL Handle:
http://hdl.handle.net/10033/254929
Title:
Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells.
Authors:
van der Vlugt, Luciën E P M; Labuda, Lucja A; Ozir-Fazalalikhan, Arifa; Lievers, Ellen; Gloudemans, Anouk K; Liu, Kit-Yeng; Barr, Tom A; Sparwasser, Tim; Boon, Louis; Ngoa, Ulysse Ateba; Feugap, Eliane Ngoune; Adegnika, Ayola A; Kremsner, Peter G; Gray, David; Yazdanbakhsh, Maria; Smits, Hermelijn H
Abstract:
Chronic helminth infections, such as schistosomes, are negatively associated with allergic disorders. Here, using B cell IL-10-deficient mice, Schistosoma mansoni-mediated protection against experimental ovalbumin-induced allergic airway inflammation (AAI) was shown to be specifically dependent on IL-10-producing B cells. To study the organs involved, we transferred B cells from lungs, mesenteric lymph nodes or spleen of OVA-infected mice to recipient OVA-sensitized mice, and showed that both lung and splenic B cells reduced AAI, but only splenic B cells in an IL-10-dependent manner. Although splenic B cell protection was accompanied by elevated levels of pulmonary FoxP3(+) regulatory T cells, in vivo ablation of FoxP3(+) T cells only moderately restored AAI, indicating an important role for the direct suppressory effect of regulatory B cells. Splenic marginal zone CD1d(+) B cells proved to be the responsible splenic B cell subset as they produced high levels of IL-10 and induced FoxP3(+) T cells in vitro. Indeed, transfer of CD1d(+) MZ-depleted splenic B cells from infected mice restored AAI. Markedly, we found a similarly elevated population of CD1d(hi) B cells in peripheral blood of Schistosoma haematobium-infected Gabonese children compared to uninfected children and these cells produced elevated levels of IL-10. Importantly, the number of IL-10-producing CD1d(hi) B cells was reduced after anti-schistosome treatment. This study points out that in both mice and men schistosomes have the capacity to drive the development of IL-10-producing regulatory CD1d(hi) B cells and furthermore, these are instrumental in reducing experimental allergic inflammation in mice.
Affiliation:
Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands.
Citation:
Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. 2012, 7 (2):e30883 PLoS ONE
Journal:
PloS one
Issue Date:
2012
URI:
http://hdl.handle.net/10033/254929
DOI:
10.1371/journal.pone.0030883
PubMed ID:
22347409
Type:
Article
Language:
en
ISSN:
1932-6203
Appears in Collections:
publications of the TwinCore unit Infection immunology

Full metadata record

DC FieldValueLanguage
dc.contributor.authorvan der Vlugt, Luciën E P Men_GB
dc.contributor.authorLabuda, Lucja Aen_GB
dc.contributor.authorOzir-Fazalalikhan, Arifaen_GB
dc.contributor.authorLievers, Ellenen_GB
dc.contributor.authorGloudemans, Anouk Ken_GB
dc.contributor.authorLiu, Kit-Yengen_GB
dc.contributor.authorBarr, Tom Aen_GB
dc.contributor.authorSparwasser, Timen_GB
dc.contributor.authorBoon, Louisen_GB
dc.contributor.authorNgoa, Ulysse Atebaen_GB
dc.contributor.authorFeugap, Eliane Ngouneen_GB
dc.contributor.authorAdegnika, Ayola Aen_GB
dc.contributor.authorKremsner, Peter Gen_GB
dc.contributor.authorGray, Daviden_GB
dc.contributor.authorYazdanbakhsh, Mariaen_GB
dc.contributor.authorSmits, Hermelijn Hen_GB
dc.date.accessioned2012-12-07T15:29:08Z-
dc.date.available2012-12-07T15:29:08Z-
dc.date.issued2012-
dc.identifier.citationSchistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. 2012, 7 (2):e30883 PLoS ONEen_GB
dc.identifier.issn1932-6203-
dc.identifier.pmid22347409-
dc.identifier.doi10.1371/journal.pone.0030883-
dc.identifier.urihttp://hdl.handle.net/10033/254929-
dc.description.abstractChronic helminth infections, such as schistosomes, are negatively associated with allergic disorders. Here, using B cell IL-10-deficient mice, Schistosoma mansoni-mediated protection against experimental ovalbumin-induced allergic airway inflammation (AAI) was shown to be specifically dependent on IL-10-producing B cells. To study the organs involved, we transferred B cells from lungs, mesenteric lymph nodes or spleen of OVA-infected mice to recipient OVA-sensitized mice, and showed that both lung and splenic B cells reduced AAI, but only splenic B cells in an IL-10-dependent manner. Although splenic B cell protection was accompanied by elevated levels of pulmonary FoxP3(+) regulatory T cells, in vivo ablation of FoxP3(+) T cells only moderately restored AAI, indicating an important role for the direct suppressory effect of regulatory B cells. Splenic marginal zone CD1d(+) B cells proved to be the responsible splenic B cell subset as they produced high levels of IL-10 and induced FoxP3(+) T cells in vitro. Indeed, transfer of CD1d(+) MZ-depleted splenic B cells from infected mice restored AAI. Markedly, we found a similarly elevated population of CD1d(hi) B cells in peripheral blood of Schistosoma haematobium-infected Gabonese children compared to uninfected children and these cells produced elevated levels of IL-10. Importantly, the number of IL-10-producing CD1d(hi) B cells was reduced after anti-schistosome treatment. This study points out that in both mice and men schistosomes have the capacity to drive the development of IL-10-producing regulatory CD1d(hi) B cells and furthermore, these are instrumental in reducing experimental allergic inflammation in mice.en_GB
dc.language.isoenen
dc.rightsArchived with thanks to PloS oneen_GB
dc.subject.meshAnimalsen_GB
dc.subject.meshAntigens, CD1den_GB
dc.subject.meshB-Lymphocytesen_GB
dc.subject.meshChilden_GB
dc.subject.meshGabonen_GB
dc.subject.meshHelminthsen_GB
dc.subject.meshHumansen_GB
dc.subject.meshHypersensitivityen_GB
dc.subject.meshInflammationen_GB
dc.subject.meshInterleukin-10en_GB
dc.subject.meshMiceen_GB
dc.subject.meshMice, Knockouten_GB
dc.subject.meshSchistosomaen_GB
dc.subject.meshT-Lymphocytes, Regulatoryen_GB
dc.titleSchistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells.en
dc.typeArticleen
dc.contributor.departmentDepartment of Parasitology, Leiden University Medical Center, Leiden, The Netherlands.en_GB
dc.identifier.journalPloS oneen_GB

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