CoChat
Sign Up
Cited by 65

The DOI matches its Crossref record.

Schistosoma mansoni-Mediated Suppression of Allergic Airway Inflammation Requires Patency and Foxp3+ Treg Cells

Layland, Laura E., Straubinger, Kathrin, Ritter, Manuel, Loffredo-Verde, Eva, Garn, Holger, Sparwasser, Tim, Prazeres da Costa, Clarissa·2013·PLoS Neglected Tropical Diseases
DOI 10.1371/journal.pntd.0002379PMC PMC3744427
Open this paper in CoChat — free account

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pntd.0002379

Cites

Statistics

Figures

Figure 1 Experimental models for examining S. mansoni-mediated suppression of AAI. A Patent Infected Protection (PiP). Groups of BALB/c female mice were infected with S. mansoni. Inf/OVA and OVA groups of mice were then sensitised with OVA either i.p. with Alum or s.c. without adjuvant at the indicated timepoints. Challenge occurred over three consecutive days in the 9th week of infection and analysis 5 days thereafter. B Prepatent (PP). Sensitizations were started in Inf/OVA and OVA groups during the first weeks of infection, before eggs are released from fecund females. Challenge and analysis were performed as in A. C Early Phase (EP). AAI was performed entirely over the first 5 weeks of infection. D Praziquantel therapy. During the 6th week of infection, mice were orally treated with PZQ for 5 consecutive days. AAI was then begun after either 2 weeks (upper track) or 6 weeks (lower track). E Depletion of Treg. Groups of C57BL/6 DEREG mice were infected with S. mansoni. In some groups, Treg were depleted using DT injections prior to OVA sensitization at the indicated timepoints. Challenge and analysis occurred in the 12th week of infection.
Figure 1 Experimental models for examining S. mansoni-mediated suppression of AAI. A Patent Infected Protection (PiP). Groups of BALB/c female mice were infected with S. mansoni. Inf/OVA and OVA groups of mice were then sensitised with OVA either i.p. with Alum or s.c. without adjuvant at the indicated timepoints. Challenge occurred over three consecutive days in the 9th week of infection and analysis 5 days thereafter. B Prepatent (PP). Sensitizations were started in Inf/OVA and OVA groups during the first weeks of infection, before eggs are released from fecund females. Challenge and analysis were performed as in A. C Early Phase (EP). AAI was performed entirely over the first 5 weeks of infection. D Praziquantel therapy. During the 6th week of infection, mice were orally treated with PZQ for 5 consecutive days. AAI was then begun after either 2 weeks (upper track) or 6 weeks (lower track). E Depletion of Treg. Groups of C57BL/6 DEREG mice were infected with S. mansoni. In some groups, Treg were depleted using DT injections prior to OVA sensitization at the indicated timepoints. Challenge and analysis occurred in the 12th week of infection.CC BY · PubMed Central
Figure 2 Suppression of AAI in S. mansoni-infected mice requires patency. Groups of BALB/c female mice were infected with S. mansoni. Left PiP experiments: After the 5th week of infection, OVA sensitizations were administered either i.p. with alum or s.c. in the absence of adjuvant (Figure 1A). Middle PP experiments: sensitizations were given during the first weeks of infection (before patency) but challenge was performed at the same time-point of infection as in PiP investigations (Figure 1B). Right EP studies: both sensitizations and challenge were performed before the onset of patency (Figure 1C). Upon AAI analysis, individual mice were assessed for leucocyte numbers (A–C) and eosinophil levels (D–F). Lung sections were also scored for inflammation (G–I). In i.p.+Alum experiments displayed in A, D and G, bars show mean + SD of individual mice from 5 independent infection/allergy experiments (PBS, n = 21; OVA, n = 34; Inf/OVA, n = 29 and Inf., n = 28). In s.c.-Alum experiments OVA, n = 8 and Inf/OVA, n = 7. In PP experiments B, E and H, bars show mean + SD of individual mice from 2 independent infection/allergy experiments (PBS, n = 2; OVA, n = 14; Inf/OVA, n = 13 and Inf., n = 10). In EP experiments C, F and I, bars show mean + SD of individual mice from 1 or 3 similar independent infection/allergy experiments (PBS, n = 2; OVA, n = 10; Inf/OVA, n = 10 and Inf., n = 4). Asterisks show statistical differences (ANOVA or Student's t test) between the groups indicated by the brackets (*p<0.05, **p<0.01, ***p<0.001).
Figure 2 Suppression of AAI in S. mansoni-infected mice requires patency. Groups of BALB/c female mice were infected with S. mansoni. Left PiP experiments: After the 5th week of infection, OVA sensitizations were administered either i.p. with alum or s.c. in the absence of adjuvant (Figure 1A). Middle PP experiments: sensitizations were given during the first weeks of infection (before patency) but challenge was performed at the same time-point of infection as in PiP investigations (Figure 1B). Right EP studies: both sensitizations and challenge were performed before the onset of patency (Figure 1C). Upon AAI analysis, individual mice were assessed for leucocyte numbers (A–C) and eosinophil levels (D–F). Lung sections were also scored for inflammation (G–I). In i.p.+Alum experiments displayed in A, D and G, bars show mean + SD of individual mice from 5 independent infection/allergy experiments (PBS, n = 21; OVA, n = 34; Inf/OVA, n = 29 and Inf., n = 28). In s.c.-Alum experiments OVA, n = 8 and Inf/OVA, n = 7. In PP experiments B, E and H, bars show mean + SD of individual mice from 2 independent infection/allergy experiments (PBS, n = 2; OVA, n = 14; Inf/OVA, n = 13 and Inf., n = 10). In EP experiments C, F and I, bars show mean + SD of individual mice from 1 or 3 similar independent infection/allergy experiments (PBS, n = 2; OVA, n = 10; Inf/OVA, n = 10 and Inf., n = 4). Asterisks show statistical differences (ANOVA or Student's t test) between the groups indicated by the brackets (*p<0.05, **p<0.01, ***p<0.001).CC BY · PubMed Central
Figure 3 Increased Foxp3+ Treg frequency in the draining lymph nodes of Inf/OVA mice is not reflected in lung sections. A) Total cell counts and B) the number of CD4+Foxp3+ T cells in the draining lymph nodes of individual mice on the day of analysis in PiP studies. Symbols depict the levels in each mouse and data shows values from 5 independent infection studies (PBS, n = 21; OVA, n = 34; Inf/OVA, n = 29 and Inf., n = 28). CD3+Foxp3+ T cells in the lung sections of C) OVA mice, D) Inf/OVA mice and E) control groups (PBS) were determined by immunohistochemical staining. Arrows depict positive cells. F) Quantification of CD3+Foxp3+ T cells in individual lung sections was determined within a 1 mm2 area. Asterisks show statistical differences (ANOVA) between the groups indicated by the brackets (*p<0.05, **p<0.01, ***p<0.001).
Figure 3 Increased Foxp3+ Treg frequency in the draining lymph nodes of Inf/OVA mice is not reflected in lung sections. A) Total cell counts and B) the number of CD4+Foxp3+ T cells in the draining lymph nodes of individual mice on the day of analysis in PiP studies. Symbols depict the levels in each mouse and data shows values from 5 independent infection studies (PBS, n = 21; OVA, n = 34; Inf/OVA, n = 29 and Inf., n = 28). CD3+Foxp3+ T cells in the lung sections of C) OVA mice, D) Inf/OVA mice and E) control groups (PBS) were determined by immunohistochemical staining. Arrows depict positive cells. F) Quantification of CD3+Foxp3+ T cells in individual lung sections was determined within a 1 mm2 area. Asterisks show statistical differences (ANOVA) between the groups indicated by the brackets (*p<0.05, **p<0.01, ***p<0.001).CC BY · PubMed Central
Figure 4 Depletion of Treg during sensitization reverts schistosome-mediated dampening of AAI. As depicted in Figure 1F, groups of C57BL/6 DEREG mice were infected with S. mansoni. On the 9th and 10th week of infection mice were sensitized i.p. with OVA in the presence of alum. Prior to sensitization, Treg were depleted by the administration of DT. During the 12th week of infection, mice were challenged and assessed for the number of leucocytes (A) and eosinophils (B) in the BAL. Levels of inflammation were also scored using lung sections stained with PAS (C–G). OVA-specific IgE levels were measured in the sera of individual mice via ELISA (H). OVA-specific responses were measured following stimulation of spleen cells (2×105) with 10 µg/ml OVA (I). In addition, schistosome-specific responses were evaluated upon re-stimulation of spleen cells with SEA (25 µg/ml) (J). After 72 hours, IL-5 levels were determined in the culture supernatant by ELISA (I and J). Egg burden was measured in livers of individually infected mice (K). Bars show data from one of two similar experiments (OVA, n = 7; OVADT, n = 7; Inf/OVADT, n = 5; Inf/OVA n = 8; PBSDT n = 3). Asterisks show statistical differences (ANOVA or Student's t test) between the groups indicated by the brackets (*p<0.05, p<0.01, ***p<0.001).
Figure 4 Depletion of Treg during sensitization reverts schistosome-mediated dampening of AAI. As depicted in Figure 1F, groups of C57BL/6 DEREG mice were infected with S. mansoni. On the 9th and 10th week of infection mice were sensitized i.p. with OVA in the presence of alum. Prior to sensitization, Treg were depleted by the administration of DT. During the 12th week of infection, mice were challenged and assessed for the number of leucocytes (A) and eosinophils (B) in the BAL. Levels of inflammation were also scored using lung sections stained with PAS (C–G). OVA-specific IgE levels were measured in the sera of individual mice via ELISA (H). OVA-specific responses were measured following stimulation of spleen cells (2×105) with 10 µg/ml OVA (I). In addition, schistosome-specific responses were evaluated upon re-stimulation of spleen cells with SEA (25 µg/ml) (J). After 72 hours, IL-5 levels were determined in the culture supernatant by ELISA (I and J). Egg burden was measured in livers of individually infected mice (K). Bars show data from one of two similar experiments (OVA, n = 7; OVADT, n = 7; Inf/OVADT, n = 5; Inf/OVA n = 8; PBSDT n = 3). Asterisks show statistical differences (ANOVA or Student's t test) between the groups indicated by the brackets (*p<0.05, p<0.01, ***p<0.001).CC BY · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 43

  1. M Masoli, 2004, The global burden of asthma: executive summary of the GINA Dissemination Committee report, Allergy, 59, 469, 10.1111/j.1398-9995.2004.00526.x · DOI
  2. R Beasley, 2000, Prevalence and etiology of asthma, J Allergy Clin Immunol, 105, S466, 10.1016/S0091-6749(00)90044-7 · DOI
  3. PJ Barnes, 2008, Immunology of asthma and chronic obstructive pulmonary disease, Nat Rev Immunol, 8, 183, 10.1038/nri2254 · DOI
  4. EM Carvalho, 2006, Worms and allergy, Parasite Immunol, 28, 525, 10.1111/j.1365-3024.2006.00894.x · DOI
  5. J Leonardi-Bee, 2006, Asthma and current intestinal parasite infection: systematic review and meta-analysis, Am J Respir Crit Care Med, 174, 514, 10.1164/rccm.200603-331OC · DOI · Paper page
  6. P Zaccone, 2009, Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice, Eur J Immunol, 39, 1098, 10.1002/eji.200838871 · DOI
  7. HH Smits, 2007, Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection, J Allergy Clin Immunol, 120, 932, 10.1016/j.jaci.2007.06.009 · DOI
  8. X Song, 2011, Impact of Schistosoma japonicum infection on collagen-induced arthritis in DBA/1 mice: a murine model of human rheumatoid arthritis, PLoS One, 6, e23453, 10.1371/journal.pone.0023453 · DOI
  9. J Correale, 2009, Helminth antigens modulate immune responses in cells from multiple sclerosis patients through TLR2-dependent mechanisms, J Immunol, 183, 5999, 10.4049/jimmunol.0900897 · DOI
  10. M Medeiros Jr, 2003, Schistosoma mansoni infection is associated with a reduced course of asthma, J Allergy Clin Immunol, 111, 947, 10.1067/mai.2003.1381 · DOI · Paper page
  11. CM Lloyd, 2009, Regulatory T cells in asthma, Immunity, 31, 438, 10.1016/j.immuni.2009.08.007 · DOI
  12. T Yamaguchi, 2011, Two modes of immune suppression by Foxp3(+) regulatory T cells under inflammatory or non-inflammatory conditions, Semin Immunol, 23, 424, 10.1016/j.smim.2011.10.002 · DOI
  13. LE Layland, 2007, Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2, Eur J Immunol, 37, 2174, 10.1002/eji.200737063 · DOI
  14. LE Layland, 2010, Pronounced phenotype in activated regulatory T cells during a chronic helminth infection, J Immunol, 184, 713, 10.4049/jimmunol.0901435 · DOI
  15. J Kearley, 2008, CD4+CD25+ regulatory T cells reverse established allergic airway inflammation and prevent airway remodeling, J Allergy Clin Immunol, 122, 617, 10.1016/j.jaci.2008.05.048 · DOI
  16. AM Baru, 2010, Selective depletion of Foxp3+ Treg during sensitization phase aggravates experimental allergic airway inflammation, Eur J Immunol, 40, 2259, 10.1002/eji.200939972 · DOI
  17. LE van der Vlugt, 2012, Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells, PLoS One, 7, e30883, 10.1371/journal.pone.0030883 · DOI
  18. S Amu, 2010, Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model, J Allergy Clin Immunol, 125, 1114, 10.1016/j.jaci.2010.01.018 · DOI
  19. LG Pacifico, 2009, Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4+ CD25+ Foxp3+ T cells independent of interleukin-10, Infect Immun, 77, 98, 10.1128/IAI.00783-07 · DOI
  20. K Lahl, 2007, Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease, J Exp Med, 204, 57, 10.1084/jem.20061852 · DOI
  21. LE Layland, 2005, Lack of antigen-specific Th1 response alters granuloma formation and composition in Schistosoma mansoni-infected MyD88-/- mice, Eur J Immunol, 35, 3248, 10.1002/eji.200526273 · DOI
  22. PJ Busse, 2007, Effect of ageing on pulmonary inflammation, airway hyperresponsiveness and T and B cell responses in antigen-sensitized and -challenged mice, Clinical and Experimental Allergy, 37, 1392, 10.1111/j.1365-2222.2007.02775.x · DOI
  23. ML Conrad, 2009, Comparison of adjuvant and adjuvant-free murine experimental asthma models, Clin Exp Allergy, 39, 1246, 10.1111/j.1365-2222.2009.03260.x · DOI
  24. SM Hsu, 1981, The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics, Am J Clin Pathol, 75, 816, 10.1093/ajcp/75.6.816 · DOI
  25. RA Wilson, 2009, Immune effector mechanisms against schistosomiasis: looking for a chink in the parasite's armour, Trends Parasitol, 25, 423, 10.1016/j.pt.2009.05.011 · DOI
  26. S Schulte, 2008, Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis, American Journal of Pathology, 172, 1500, 10.2353/ajpath.2008.070776 · DOI
  27. M Lohoff, 1998, Experimental murine leishmaniasis and the Th1/Th2 cell concept, Tokai J Exp Clin Med, 23, 347
  28. M Baumgart, 2006, Naturally occurring CD4+Foxp3+ regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation, J Immunol, 176, 5374, 10.4049/jimmunol.176.9.5374 · DOI
  29. CM Kane, 2004, Helminth antigens modulate TLR-initiated dendritic cell activation, J Immunol, 173, 7454, 10.4049/jimmunol.173.12.7454 · DOI
  30. NE Mangan, 2006, Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness, J Immunol, 176, 138, 10.4049/jimmunol.176.1.138 · DOI
  31. D Cioli, 2004, Determination of ED50 values for praziquantel in praziquantel-resistant and -susceptible Schistosoma mansoni isolates, Int J Parasitol, 34, 979, 10.1016/j.ijpara.2004.05.001 · DOI
  32. MS Wilson, 2011, IL-10 Blocks the Development of Resistance to Re-Infection with Schistosoma mansoni, Plos Pathogens, 7, e1002171, 10.1371/journal.ppat.1002171 · DOI
  33. AH van den Biggelaar, 2000, Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10, Lancet, 356, 1723, 10.1016/S0140-6736(00)03206-2 · DOI
  34. AH van den Biggelaar, 2001, The prevalence of parasite infestation and house dust mite sensitization in Gabonese schoolchildren, Int Arch Allergy Immunol, 126, 231, 10.1159/000049519 · DOI
  35. AH van den Biggelaar, 2004, Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren, J Infect Dis, 189, 892, 10.1086/381767 · DOI · Paper page
  36. NR Lynch, 1993, Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum, J Allergy Clin Immunol, 92, 404, 10.1016/0091-6749(93)90119-Z · DOI
  37. M Yu, 2006, Mast cells can promote the development of multiple features of chronic asthma in mice, J Clin Invest, 116, 1633, 10.1172/JCI25702 · DOI
  38. S Nakae, 2007, Mast cell-derived TNF contributes to airway hyperreactivity, inflammation, and TH2 cytokine production in an asthma model in mice, J Allergy Clin Immunol, 120, 48, 10.1016/j.jaci.2007.02.046 · DOI
  39. DM Zhao, 2006, Activated CD4+CD25+ T cells selectively kill B lymphocytes, Blood, 107, 3925, 10.1182/blood-2005-11-4502 · DOI
  40. Y Zheng, 2007, Foxp3 in control of the regulatory T cell lineage, Nat Immunol, 8, 457, 10.1038/ni1455 · DOI
  41. JA Hall, 2008, Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses, Immunity, 29, 637, 10.1016/j.immuni.2008.08.009 · DOI
  42. K Lahl, 2011, In vivo depletion of FoxP3+ Tregs using the DEREG mouse model, Methods Mol Biol, 707, 157, 10.1007/978-1-61737-979-6_10 · DOI
  43. H Maazi, 2012, Contribution of regulatory T cells to alleviation of experimental allergic asthma after specific immunotherapy, Clinical and Experimental Allergy, 42, 1519, 10.1111/j.1365-2222.2012.04064.x · DOI

Cited by

Sorted by citations

See all 65

Metadata

Authors
Layland, L. E., Straubinger, K., Ritter, M., Loffredo-Verde, E., Garn, H., Sparwasser, T., & Prazeres da Costa, C.
Venue
PLoS Neglected Tropical Diseases
Publisher
Public Library of Science (PLoS)
Published
2013-08-15
Volume
7
Issue
8
Pages
e2379
ISSN
1935-2735
DOI
10.1371/journal.pntd.0002379
PMC
PMC3744427
Cited by
65
References
0
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (unspecified)

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 ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Schistosoma mansoni-Mediated Suppression of Allergic Airway Inflammation Requires Patency and Foxp3+ Treg Cells. https://app.cochat.ai/papers/10.1371/journal.pntd.0002379
The paper
Layland, L. E., Straubinger, K., Ritter, M., Loffredo-Verde, E., Garn, H., Sparwasser, T., & Prazeres da Costa, C. (2013). Schistosoma mansoni-Mediated Suppression of Allergic Airway Inflammation Requires Patency and Foxp3+ Treg Cells. PLoS Neglected Tropical Diseases. https://doi.org/10.1371/journal.pntd.0002379