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Cited by 96Parasites and Host InteractionsT-cell and B-cell ImmunologyIL-33, ST2, and ILC Pathways

Schistosome egg antigens, including the glycoprotein IPSE/alpha-1, trigger the development of regulatory B cells

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Haeberlein, Simone, Obieglo, Katja, Ozir-Fazalalikhan, Arifa, Chayé, Mathilde A. M., Veninga, Henrike, van der Vlugt, Luciën E. P. M., Voskamp, Astrid, Boon, Louis +7 more·2017·PLOS Pathogens
DOI 10.1371/journal.ppat.1006539PMC PMC5550006
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Abstract

Infection with the helminth Schistosoma (S.) mansoni drives the development of interleukin (IL)-10-producing regulatory B (Breg) cells in mice and man, which have the capacity to reduce experimental allergic airway inflammation and are thus of high therapeutic interest. However, both the involved antigen and cellular mechanisms that drive Breg cell development remain to be elucidated. Therefore, we investigated whether S. mansoni soluble egg antigens (SEA) directly interact with B cells to enhance their regulatory potential, or act indirectly on B cells via SEA-modulated macrophage subsets. Intraperitoneal injections of S. mansoni eggs or SEA significantly upregulated IL-10 and CD86 expression by marginal zone B cells. Both B cells as well as macrophages of the splenic marginal zone efficiently bound SEA in vivo, but macrophages were dispensable for Breg cell induction as shown by macrophage depletion with clodronate liposomes. SEA was internalized into acidic cell compartments of B cells and induced a 3-fold increase of IL-10, which was dependent on endosomal acidification and was further enhanced by CD40 ligation. IPSE/alpha-1, one of the major antigens in SEA, was also capable of inducing IL-10 in naïve B cells, which was reproduced by tobacco plant-derived recombinant IPSE. Other major schistosomal antigens, omega-1 and kappa-5, had no effect. SEA depleted of IPSE/alpha-1 was still able to induce Breg cells indicating that SEA contains more Breg cell-inducing components. Importantly, SEA- and IPSE-induced Breg cells triggered regulatory T cell development in vitro. SEA and recombinant IPSE/alpha-1 also induced IL-10 production in human CD1d+ B cells. In conclusion, the mechanism of S. mansoni-induced Breg cell development involves a direct targeting of B cells by SEA components such as the secretory glycoprotein IPSE/alpha-1.

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  • The secreted products of S. mansoni eggs can induce a regulatory B cell phenotype in murine and human cells, through or independently of the action of IPSE.

    “The secreted products of S. mansoni eggs can induce a regulatory B (Breg) cell phenotype in murine and human cells, through or independently of the action of IPSE (Haeberlein et al., 2017).”

    From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Haeberlein et al., 2017

    The Results section, “The secretory schistosome egg antigen IPSE/alpha-1 induces Breg cell development in mice and humans” (page unavailable), reports that soluble egg antigens and IPSE induce regulatory B-cell responses in mouse and human cells. It also reports that IPSE-depleted egg antigens retain this effect in mouse B cells, but does not establish IPSE-independent induction in human B cells. (LLM, conf=0.83)

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  • Uptake of IPSE is necessary to induce B cell IL-10 and Treg cell development in vitro.

    “Uptake of IPSE is necessary to induce B cell IL-10 and Treg cell development in vitro (Haeberlein et al., 2017).”

    From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Haeberlein et al., 2017

    The Discussion reports that IPSE directly interacts with murine B cells and induces B-cell IL-10 secretion and Treg development in vitro. The Results link internalization and endosomal processing to IL-10 induction by the broader schistosome egg antigen mixture (SEA), but do not establish that uptake of IPSE itself is necessary for either outcome. Page numbers are unavailable in our copy. (LLM, conf=0.88)

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Authors
Haeberlein, S., Obieglo, K., Ozir-Fazalalikhan, A., Chayé, M. A. M., Veninga, H., van der Vlugt, L. E. P. M., Voskamp, A., Boon, L., den Haan, J. M. M., Westerhof, L. B., Wilbers, R. H. P., Schots, A., Schramm, G., Hokke, C. H., & Smits, H. H.
Affiliations
  • Leiden University Medical Center (NL)
  • Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
  • Polpharma Biologics (Netherlands) (NL)
  • Wageningen University & Research (NL)
  • Research Center Borstel - Leibniz Lung Center (DE)
Corresponding author
Smits, Hermelijn H.
ORCID
Venue
PLOS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2017-07-28
Volume
13
Issue
7
Pages
e1006539
ISSN
  • 1553-7366 (ISSN-L)
  • 1553-7374
DOI
10.1371/journal.ppat.1006539
PMC
PMC5550006
OpenAlex
W2739939395
Cited by
96
References
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FWCI
9.47
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journal article
Language
en
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new_version (2017-08-09)
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Funders
  • Deutsche Forschungsgemeinschaft (SCHR608/4-1)
  • ZonMw (91714352, 91214131)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (91214131, 91714352)
Topics
  • Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Keywords
Schistosoma mansoni, soluble egg antigen, regulatory B cells, IL-10, schistosomiasis, marginal zone B cells, endosomal acidification, CD40 ligation, macrophage depletion, clodronate liposomes, regulatory T cells, allergic airway inflammation, helminthiasis, antigen uptake
MeSH terms
Animals, Antigens, Helminth, Egg Proteins, Female, Humans, Mice, Inbred C57BL, Ovum, Schistosoma mansoni, Schistosomiasis mansoni, Helminth Proteins, Interleukin-10, Mice, B-Lymphocytes, Regulatory

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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