Cutting Edge: IPSE/alpha-1, a Glycoprotein from Schistosoma mansoni Eggs, Induces IgE-Dependent, Antigen-Independent IL-4 Production by Murine Basophils In Vivo
Abstract
During infection with the helminth parasite Schistosoma mansoni, the deposition of eggs coincides with the onset of IL-4 production and Th2 development. Although IL-4 is known as a potent inducer of Th2 differentiation, the mechanism by which schistosome eggs induce IL-4 production is not clear. In this study, we demonstrate that the S. mansoni egg Ag (SmEA) induces IgE-dependent IL-4 production by basophils derived from Heligmosomoides polygyrus-infected or OVA/alum-immunized mice in the absence of pathogen-specific IgE. The effect is mediated by the secretory glycoprotein IPSE/alpha-1, because IPSE/alpha-1-depleted SmEA no longer induces cytokine production. Conversely, recombinant IPSE/alpha-1 is sufficient to induce IL-4 production. Importantly, the injection of SmEA or recombinant IPSE/alpha-1 into H. polygyrus-infected 4get/KN2 IL-4 reporter mice rapidly induces the dose-dependent IL-4 production by basophils in the liver, a major site of egg deposition. Thus, IPSE/alpha-1 induces basophils to produce IL-4 even in the absence of Ag-specific IgE.
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IPSE supports type 2 cell responses through induction of IL-4 release from basophils that is IgE dependent but antigen independent and does not require uptake of IPSE by basophils.
“IPSE also supports type 2 cell responses, through induction of IL-4 release from basophils that is IgE dependent but antigen independent and does not require uptake of IPSE by basophils, so this single protein has multiple functions and activation routes (Schramm et al., 2007).”
From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Schramm et al., 2007
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BackgroundInduction of Type 2 Responses by Schistosome Worms during Prepatent Infection
Fraga, L. A. D. O., Torrero, M. N., Tocheva, A. S., Mitre, E. E. S., & Davies, S. J. A. (2009) · The Journal of Infectious Diseases · doi:10.1086/649841 · Cited by 49 · see citing works
Schistosoma mansoni infection reduces the incidence of murine cerebral malaria
Waknine-Grinberg, J. H., Gold, D., Ohayon, A., Flescher, E., Heyfets, A., Doenhoff, M. J., Schramm, G., Haas, H., & Golenser, J. (2010) · Malaria Journal · doi:10.1186/1475-2875-9-5 · Cited by 49 · see citing works
“Alternatively, mice were first infected with P. berghei and subsequently administered complete S. mansoni egg extract (SmEA) [12], egg extract from which IPSE/alpha-1 was removed (SmEA ΔIPSE/alpha- 1) [ 16 ] (45 μg/mouse/day on days -7, 0, and 3 postinfection; 22.5 μg/mouse on day 6 post-infection), or IPSE/alpha-1 [8…”
InfluentialSelf-citationHelminth Modulation of Lung Inflammation
Schwartz, C., Hams, E., & Fallon, P. G. (2018) · Trends in Parasitology · doi:10.1016/j.pt.2017.12.007 · Cited by 49 · see citing works
Knuhr, K., Langhans, K., Nyenhuis, S., Viertmann, K., Kildemoes, A. O., Doenhoff, M. J., Haas, H., & Schramm, G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02293 · Cited by 49 · see citing works
Self-citationMeevissen, M. H. J., Driessen, N. N., Smits, H. H., Versteegh, R., van Vliet, S. J., van Kooyk, Y., Schramm, G., Deelder, A. M., Haas, H., Yazdanbakhsh, M., et al. (2012) · International Journal for Parasitology · doi:10.1016/j.ijpara.2012.01.004 · Cited by 48 · see citing works
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Innate immunostimulatory properties of allergens and their relevance to food allergy
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“mansoni-specific IgE, and is likely to amplify Th2 priming by DCs [83].”
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Antibodies and IL-3 support helminth-induced basophil expansion
Herbst, T., Esser, J., Prati, M., Kulagin, M., Stettler, R., Zaiss, M. M., Hewitson, J. P., Merky, P., Verbeek, J. S., Bourquin, C., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1117584109 · Cited by 46 · see citing works
“In support of this possibility, Schistosoma mansoni egg antigens can elicit IL-4 secretion from basophils following nonspecific interactions with surface bound IgE (31), and Hill et al.”
BackgroundMwinzi, P. N. M., Ganley-Leal, L. M., Black, C. L., Secor, W. E., Karanja, D. M. S., & Colley, D. G. (2008) · The Journal of Infectious Diseases · doi:10.1086/595792 · Cited by 46 · see citing works
Monomeric IgE and Mast Cell Development, Survival and Function
Kashiwakura, J., Otani, I. M., & Kawakami, T. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-9533-9_3 · Cited by 43 · see citing works
Ferguson, B. J., Newland, S. A., Gibbs, S. E., Tourlomousis, P., dos Santos, P. F., Patel, M. N., Hall, S. W., Walczak, H., Schramm, G., Haas, H., et al. (2015) · International Journal for Parasitology · doi:10.1016/j.ijpara.2015.08.005 · Cited by 42 · see citing works
Self-citationMeevissen, M. H. J., Balog, C., Koeleman, C., Doenhoff, M., Schramm, G., Haas, H., Deelder, A., Wuhrer, M., & Hokke, C. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.005710 · Cited by 52 · see citing works
“The structural elucidation of kappa-5 glycans, and the previously reported studies on the glycosylation of IPSE/alpha-1 (12), a basophil modulator (39) and of omega-1 (11), an SEA component recently described to condition DC to drive Th2 responses (40), provide a starting point to further detail the contribution of th…”
BackgroundSelf-citationThe Mannose Receptor in Regulation of Helminth-Mediated Host Immunity
van Die, I., & Cummings, R. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01677 · Cited by 38 · see citing works
Hasby, E. A., Saad, M. A. H., Shohieb, Z. S., & Noby, K. E. (2015) · Cellular Immunology · doi:10.1016/j.cellimm.2015.02.013 · Cited by 40 · see citing works
Sotillo, J., Pearson, M. S., Becker, L., Mekonnen, G. G., Amoah, A. S., van Dam, G. J., Corstjens, P. L. A. M., Murray, J., Mduluza, T., Mutapi, F., et al. (2019) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0007362 · Cited by 38 · see citing works
Early Events Triggering the Initiation of a Type 2 Immune Response
El-Naccache, D. W., Haskó, G., & Gause, W. C. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.11.006 · Cited by 38 · see citing works
Vaccine against autoimmune disease: can helminths or their products provide a therapy?
Zaccone, P., & Cooke, A. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.02.006 · Cited by 37 · see citing works
Type 2 immunity: a two-edged sword in schistosomiasis immunopathology
Aziz, N. A., Musaigwa, F., Mosala, P., Berkiks, I., & Brombacher, F. (2022) · Trends in Immunology · doi:10.1016/j.it.2022.06.005 · Cited by 36 · see citing works
Oliveira, R. R., de Figueiredo, J. P., Cardoso, L. S., Jabar, R. L., de Souza, R. P., Wells, M. T., Carvalho, E. M., Fitzgerald, D. W., Barnes, K. C., Araújo, M. I., et al. (2012) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2012.11-0204 · Cited by 35 · see citing works
Immune responses to S chistosoma haematobium infection
Odegaard, J. I., & Hsieh, M. H. (2014) · Parasite Immunology · doi:10.1111/pim.12084 · Cited by 34 · see citing works
Kaur, I., Schramm, G., Everts, B., Scholzen, T. E., Kindle, K. B., Beetz, C., Montiel‐Duarte, C., Blindow, S., Jones, A. T., Haas, H., et al. (2011) · Infection and Immunity · doi:10.1128/iai.01048-10 · Cited by 34 · see citing works
Self-citationTurner, J. D., Narang, P., Coles, M. C., & Mountford, A. P. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003063 · Cited by 34 · see citing works
“alternative activation of macrophages in the gut via their secretions to initiate egg egress [8,9,23], escape via PP represents a unique”
BackgroundEmerging roles of basophils in protective immunity against parasites
Karasuyama, H., Wada, T., Yoshikawa, S., & Obata‐Ninomiya, K. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.11.006 · Cited by 31 · see citing works
Schistosome Eggs Impair Protective Th1/Th17 Immune Responses Against Salmonella Infection
Schramm, G., Suwandi, A., Galeev, A., Sharma, S., Braun, J., Claes, A.-K., Braubach, P., & Graßl, G. A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02614 · Cited by 31 · see citing works
Self-citationMeyer, N. H., Mayerhofer, H., Tripsianes, K., Blindow, S., Barths, D., Mewes, A., Weimar, T., Köhli, T., Bade, S., Madl, T., et al. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.675066 · Cited by 31 · see citing works
“mansoni eggs, which induces the release of IL-4 from human and murine basophils (7, 8).”
BackgroundSelf-citationRicciardi, A., Dalton, J. P., & Ndao, M. (2014) · Vaccine · doi:10.1016/j.vaccine.2014.11.016 · Cited by 31 · see citing works
Macroparasites, innate immunity and immunoregulation: developing natural models
Friberg, I. M., Bradley, J. E., & Jackson, J. A. (2010) · Trends in Parasitology · doi:10.1016/j.pt.2010.06.010 · Cited by 30 · see citing works
Hambrook, J. R., Kaboré, A. L., Pila, E. A., & Hanington, P. C. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007393 · Cited by 30 · see citing works
Helminth mediated modulation of Type 1 diabetes (T1D)
Zaccone, P., & Cooke, A. (2013) · International Journal for Parasitology · doi:10.1016/j.ijpara.2012.12.004 · Cited by 29 · see citing works
“IPSE/a 1 has been shown to induce IL-4 from basophils and skew T cell immune responses towards Th2 (Schramm et al., 2007).”
BackgroundSchistosome: Its Benefit and Harm in Patients Suffering from Concomitant Diseases
Osada, Y., & Kanazawa, T. (2011) · BioMed Research International · doi:10.1155/2011/264173 · Cited by 27 · see citing works
“Moreover, the administration of IPSE/alpha-1, a Th2inducing schistosomal egg protein [9, 10], also delayed death.”
BackgroundSundstrom, J. B., Hair, G. A., Ansari, A. A., Secor, W. E., Gilfillan, A. M., Metcalfe, D. D., & Kirshenbaum, A. S. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0801481 · Cited by 25 · see citing works
The Tao survivorship of schistosomes: implications for schistosomiasis control
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The Evolution of Human Basophil Biology from Neglect towards Understanding of Their Immune Functions
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“This major immunogenic trematode egg glycoprotein induces IL-4 secretion from basophils by binding nonspecifically to cell-bound IgE [154].”
BackgroundBasophils, IgE, and Autoantibody-Mediated Kidney Disease
Bosch, X., Lozano, F., Cervera, R., Ramos‐Casals, M., & Min, B. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002648 · Cited by 24 · see citing works
“IPSE/a-1, a glycoprotein from Schistosoma egg Ags, induces IL-4 production in basophils (27).”
BackgroundCutting Edge: Helminth Infection Induces IgE in the Absence of μ- or δ-Chain Expression
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Below the belt: new insights into potential complications of HIV-1/schistosome coinfections
Secor, W. E., & Sundstrom, J. B. (2007) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0b013e3282e9ac03 · Cited by 23 · see citing works
Contributions to the study of Trichinella spiralis TSL‐1 antigens in host immunity
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- Authors
- Schramm, G., Mohrs, K., Wodrich, M., Doenhoff, M. J., Pearce, E. J., Haas, H., & Mohrs, M.
- Affiliations
- Research Center Borstel - Leibniz Lung Center (DE)
- Trudeau Institute (US)
- Bangor University (GB)
- University of Pennsylvania (US)
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-05
- Volume
- 178
- Issue
- 10
- Pages
- 6023-6027
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2114089512
- Cited by
- 163
- References
- 24
- Citations by year
- 2026: 2 · 2024: 2 · 2023: 4 · 2022: 5 · 2021: 8 · 2020: 3 · 2019: 6 · 2018: 9 · 2017: 7 · 2016: 11 · 2015: 8 · 2014: 12 · 2013: 10 · 2012: 15
- FWCI
- 10.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (N0 155270)
- National Institute of Allergy and Infectious Diseases (AI32573, AI 45666, R01AI072296, P01AI045666, AI072296)
- Topics
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
- Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
- Keywords
- Schistosoma mansoni eggs, IL-4 production, basophils, Th2 differentiation, secretory glycoproteins, Heligmosomoides polygyrus, schistosomiasis, helminthiasis
- MeSH terms
- Animals, Antigens, Helminth, Basophils, Cell Line, Cells, Cultured, Egg Proteins, Humans, Immunoglobulin E, Mice, Inbred BALB C, Orosomucoid, Schistosoma mansoni, Helminth Proteins, Interleukin-4, Mice, Knockout, Mice
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