CoChat
Sign Up
Cited by 11

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Antigenic cross-reactivity between Schistosoma mansoni and pollen allergens from the birch tree (Betula verrucosa) and Timothy grass (Phleum pratense): involvement of shared glycan epitopes and implications for the hygiene hypothesis

Igetei, Joseph E., El-Faham, Marwa, Liddell, Susan, Schramm, Gabriele, Doenhoff, Michael J.·2018·International Journal for Parasitology
DOI 10.1016/j.ijpara.2017.12.005
Open this paper in CoChat — free account

Abstract

Previous studies have shown that schistosome infection can protect against allergic symptoms, but the underlying mechanisms are still not fully understood. Here we have shown that rabbit IgG antibodies raised against Schistosoma mansoni soluble egg antigens (SmSEA) are cross-reactive with a wide array of molecules in Timothy grass pollen (TGP) and birch tree pollen (BTP). Five of the cross-reactive pollen molecules (two from TGP and three from BTP) were selected randomly and identified by tandem mass spectrometric (TMS) analysis to be, respectively, the TGP allergens Phl p 1 and Phl p 5b, and BTP glutathione S-transferase (GST), and the BTP allergens Bet v 1 and Bet v 6.0102. Rabbit anti-SmSEA IgG antibodies that cross-reacted with each of the five allergens were found to be reactive with three major S. mansoni egg antigens, IPSE/alpha-1, omega-1 and kappa-5. Pairwise alignment of the amino acid sequences of each of the five TMS-identified pollen allergens with each of the three egg antigens revealed a low level of amino acid sequence identity. Further experiments indicated that the schistosome antigen/allergen cross-reactivity was mostly due to similar glycans present in helminths and plants, but not in mammals: so called cross-reactive carbohydrate determinants (CCDs). Previously, CCDs have been implicated in the cross-reactivity between many plants and invertebrates. Furthermore, pollen-induced anti-CCD IgGs have been found in sera of patients undergoing allergen-specific…

Overview

Integrity signals

Registry

Crossref · 10.1016/j.ijpara.2017.12.005

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Citations

Cites

Show all 1 references

Research works printed but not linked: 89

  1. Aalberse, 1997, Crossreactive carbohydrate determinants, Clin. Rev. Allergy Immunol., 15, 375, 10.1007/BF02737733 · DOI
  2. Altmann, 2016, Coping with cross-reactive carbohydrate determinants in allergy diagnosis, Allergo. J. Int., 25, 98, 10.1007/s40629-016-0115-3 · DOI · Paper page
  3. Andersson, 2003, Characteristics and immunobiology of grass pollen allergens, Int. Arch. Allergy Immunol., 130, 87, 10.1159/000069013 · DOI
  4. Araujo, 2006, Human schistosomiasis decreases immune responses to allergens and clinical manifestations of asthma, Chem. Immunol. Allergy, 90, 29
  5. Araujo, 2004, Schistosoma mansoni infection modulates the immune response against allergic and auto-immune diseases, Mem. Inst. Oswaldo Cruz, 99, 27, 10.1590/S0074-02762004000900005 · DOI
  6. Bach, 2002, The effect of infections on susceptibility to autoimmune and allergic diseases, N. Engl. J. Med., 347, 911, 10.1056/NEJMra020100 · DOI
  7. Bellinghausen, 1997, Insect venom immunotherapy induces interleukin-10 production and a Th2-to-Th1 shift, and changes surface marker expression in venom-allergic subjects, Eur. J. Immunol., 27, 1131, 10.1002/eji.1830270513 · DOI
  8. Bencurova, 2004, Specificity of IgG and IgE antibodies against plant and insect glycoprotein glycans determined with artificial glycoforms of human transferrin, Glycobiology, 14, 457, 10.1093/glycob/cwh058 · DOI
  9. Breiteneder, 1989, The gene coding for the major birch pollen allergen Betv1, is highly homologous to a pea disease resistance response gene, EMBO J., 8, 1935, 10.1002/j.1460-2075.1989.tb03597.x · DOI
  10. Bufe, 1995, Major allergen Phl p Vb in timothy grass is a novel pollen RNase, FEBS Lett., 363, 6, 10.1016/0014-5793(95)00259-C · DOI
  11. Bullimore, 2012, Cross-reactivity in grasses: biochemical attributes define exemplar relevance, World Allergy Organ J., 5, 111, 10.1097/WOX.0b013e31826a10cf · DOI
  12. Cadot, 2003, Oral allergy syndrome to chicory associated with birch pollen allergy, Int. Arch. Allergy Immunol., 131, 19, 10.1159/000070430 · DOI
  13. Caldas, 2008, Human schistosomiasis mansoni: Immune responses during acute and chronic phases of the infection, Acta Trop., 108, 109, 10.1016/j.actatropica.2008.05.027 · DOI
  14. Casset, 2012, Varying allergen composition and content affects the in vivo allergenic activity of commercial Dermatophagoides pteronyssinus extracts, Int. Arch. Allergy Immunol., 1593, 253, 10.1159/000337654 · DOI
  15. Chauhan, 2013, In silico platform for prediction of N- O- and C-glycosites in eukaryotic protein sequences, PLoS One, 8, e67008, 10.1371/journal.pone.0067008 · DOI
  16. Collot, 2011, Synthesis of cross-reactive carbohydrate determinants fragments as tools for in vitro allergy diagnosis, Bioorg. Med. Chem., 19, 1306, 10.1016/j.bmc.2010.12.001 · DOI
  17. Darani, 2008, An association between Schistosoma mansoni worms and an enzymatically-active protease/peptidase in mouse blood, Parasitology, 135, 467, 10.1017/S0031182007003988 · DOI
  18. Deifl, 2014, Glutathione-S-transferase: A minor allergen in birch pollen due to limited release from hydrated pollen, PLoS One, 9, e109075, 10.1371/journal.pone.0109075 · DOI
  19. Doenhoff, 2016, Cross-reactivity between Schistosoma mansoni antigens and the latex allergen Hev b 7: putative implication of cross-reactive carbohydrate determinants (CCDs), PLoS One, 11, e0159542, 10.1371/journal.pone.0159542 · DOI
  20. Doenhoff, 1988, Immunological identification of Schistosoma mansoni peptidases, Mol. Biochem. Parasitol., 313, 233, 10.1016/0166-6851(88)90153-3 · DOI
  21. Dunne, 1986, Schistosoma mansoni egg antigens: preparation of rabbit antisera with monospecific immunoprecipitating activity, and their use in antigen characterization, Parasite Immunol., 8, 575, 10.1111/j.1365-3024.1986.tb00871.x · DOI
  22. Durham, 1996, Grass pollen immunotherapy inhibits allergen-induced infiltration of CD4+ T lymphocytes and eosinophils in the nasal mucosa and increases the number of cells expressing messenger RNA for interferon-gamma, J. Allergy Clin. Immunol., 97, 1356, 10.1016/S0091-6749(96)70205-1 · DOI
  23. Eberl, 2001, Antibodies to glycans dominate the host response to schistosome larvae and eggs: is their role protective or subversive?, J. Infect. Dis., 183, 1238, 10.1086/319691 · DOI
  24. Faveeuw, 2003, Schistosome N-glycans containing core alpha 3-fucose and core beta 2-xylose epitopes are strong inducers of Th2 responses in mice, Eur. J. Immunol., 33, 1271, 10.1002/eji.200323717 · DOI · Paper page
  25. Figueiredo, 2012, Adult worm-specific IgE/IgG4 balance is associated with low infection levels of Schistosoma mansoni in an endemic area, Parasite Immunol., 34, 604, 10.1111/pim.12001 · DOI
  26. Fitzsimmons, 2005, Molecular characterization of omega-1: a hepatotoxic ribonuclease from Schistosoma mansoni eggs, Mol. Biochem. Parasitol., 144, 123, 10.1016/j.molbiopara.2005.08.003 · DOI
  27. Freidhoff, 1986, A study of the human immune response to Lolium perenne (rye) pollen and its components, Lol p I and Lol p II (rye I and rye II). I Prevalence of reactivity to the allergens and correlations among skin test, IgE antibody, and IgG antibody data, J. Allergy Clin. Immunol., 78, 1190, 10.1016/0091-6749(86)90271-X · DOI
  28. Fujita, 2012, Mechanisms of allergen-specific immunotherapy, Clin. Transl. Allergy, 2, 2, 10.1186/2045-7022-2-2 · DOI
  29. Hamid, 1997, Increases in IL-12 messenger RNA+ cells accompany inhibition of allergen-induced late skin responses after successful grass pollen immunotherapy, J. Allergy Clin. Immunol., 99, 254, 10.1016/S0091-6749(97)70106-4 · DOI
  30. Hamilton, 1999, Periodate-sensitive immunological cross-reactivity between keyhole limpet haemocyanin (KLH) and serodiagnostic Schistosoma mansoni egg antigens, Parasitology, 118, 83, 10.1017/S0031182098003461 · DOI
  31. Himly, 2002, Art v 1, the major allergen of mugwort pollen, is a modular glycoprotein with a defensin-like and a hydroxyproline-rich domain, FASEB J., 17, 106, 10.1096/fj.02-0472fje · DOI
  32. Hino, 2009, Periodate-resistant carbohydrate epitopes recognized by IgG and IgE antibodies from some of the immunized mice and patients with allergy, Biochem. Biophys. Res. Commun., 380, 632, 10.1016/j.bbrc.2009.01.138 · DOI
  33. Hoffmann-Sommergruber, 2011, Glycomarkers in parasitic infections and allergy, Biochem. Soc. Trans., 39, 360, 10.1042/BST0390360 · DOI
  34. Homann, 2017, Glycans and glycan-specific IgE in clinical and molecular allergology: Sensitization, diagnostics, and clinical symptoms, J. Allergy Clin. Immunol., 140, 356, 10.1016/j.jaci.2017.04.019 · DOI
  35. Igetei, 2016, Purification of a chymotrypsin-like enzyme present on adult Schistosoma mansoni worms from infected mice and its characterization as a host carboxylesterase, Parasitology, 143, 646, 10.1017/S0031182016000184 · DOI
  36. Igetei, 2017, Antigenic cross-reactivity between Schistosoma mansoni and peanut: a role for cross-reactive carbohydrate determinants (CCDs) and implications for the hygiene hypothesis, Immunology, 150, 506, 10.1111/imm.12711 · DOI · Paper page
  37. Jin, 2008, Affinity of IgE and IgG against cross-reactive carbohydrate determinants on plant and insect glycoproteins, J. Allergy Clin. Immunol., 121, 185, 10.1016/j.jaci.2007.07.047 · DOI
  38. Johnson, 1965, Isoallergens from rye grass pollen, Nature, 206, 935, 10.1038/206935b0 · DOI
  39. Karamloo, 1999, Molecular cloning and characterization of a birch pollen minor allergen, Bet v 5, belonging to a family of isoflavone reductase-related proteins, J. Allergy Clin. Immunol., 104, 991, 10.1016/S0091-6749(99)70080-1 · DOI
  40. Koloski, 2008, Hygiene hypothesis in inflammatory bowel disease: a critical review of the literature, World J. Gastroenterol., 14, 165, 10.3748/wjg.14.165 · DOI
  41. Kwaasi, 2002, Cross-reactivities between date palm (Phoenix dactylifera L.) polypeptides and foods implicated in the oral allergy syndrome, Allergy, 57, 508, 10.1034/j.1398-9995.2002.23308.x · DOI
  42. Laemmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0 · DOI · Paper page
  43. Laffer, 1994, Complementary DNA cloning of the major allergen Phl p I from timothy grass (Phleum pratense); recombinant Phl p I inhibits IgE binding to group I allergens from eight different grass species, J. Allergy Clin. Immunol., 94, 689, 10.1016/0091-6749(94)90176-7 · DOI
  44. Larche, 2006, Peptide immunotherapy, Immunol. Allergy Clin. North Am., 26, 321, 10.1016/j.iac.2006.02.005 · DOI
  45. Larche, 2006, Immunological mechanisms of allergen-specific immunotherapy, Nat. Rev. Immunol., 6, 761, 10.1038/nri1934 · DOI
  46. Larsen, 1992, PCR based cloning and sequencing of isogenes encoding the tree pollen major allergen Car b I from Carpinus betulus, hornbeam, Mol. Immunol., 29, 703, 10.1016/0161-5890(92)90180-6 · DOI
  47. Lowry, 1951, Protein measurement with the Folin phenol reagent, J. Biol. Chem., 193, 265, 10.1016/S0021-9258(19)52451-6 · DOI
  48. Marth, 2013, A nonallergenic birch pollen allergy vaccine consisting of hepatitis PreS-fused Bet v 1 peptides focuses blocking IgG toward IgE epitopes and shifts immune responses to a tolerogenic and Th1 phenotype, J. Immunol., 190, 3068, 10.4049/jimmunol.1202441 · DOI
  49. Meevissen, 2011, Targeted glycoproteomic analysis reveals that kappa-5 is a major, uniquely glycosylated component of Schistosoma mansoni egg antigens, Mol. Cell Proteomics, 10, 1, 10.1074/mcp.M110.005710 · DOI
  50. Meevissen, 2010, Structural characterization of glycans on omega-1, a major Schistosoma mansoni egg glycoprotein that drives Th2 responses, J. Proteome Res., 9, 2630, 10.1021/pr100081c · DOI
  51. Meyer, 2015, A crystallin fold in the interleukin-4-inducing principle of Schistosoma mansoni eggs (IPSE/alpha-1) mediates IgE binding for antigen-independent basophil activation, J. Biol. Chem., 290, 22111, 10.1074/jbc.M115.675066 · DOI
  52. Mitre, 2005, Saturation of immunoglobulin E (IgE) binding sites by polyclonal IgE does not explain the protective effect of helminth infections against atopy, Infect. Immun., 73, 4106, 10.1128/IAI.73.7.4106-4111.2005 · DOI
  53. Mobs, 2012, Birch pollen immunotherapy results in long-term loss of Bet v 1-specific TH2 responses, transient TR1 activation, and synthesis of IgE-blocking antibodies, J. Allergy Clin. Immunol., 130, 1108, 10.1016/j.jaci.2012.07.056 · DOI
  54. Modha, 1988, An association between schistosomes and contrapsin, a mouse serine protease inhibitor (serpin), Parasitology, 96, 99, 10.1017/S0031182000081683 · DOI
  55. Nouri-Aria, 2004, Grass pollen immunotherapy induces mucosal and peripheral IL-10 responses and blocking IgG activity, J. Immunol., 172, 3252, 10.4049/jimmunol.172.5.3252 · DOI
  56. Nyame, 2000, Antibody responses to the fucosylated LacdiNAc glycan antigen in Schistosoma mansoni-infected mice and expression of the glycan among schistosomes, Exp. Parasitol., 96, 202, 10.1006/expr.2000.4573 · DOI
  57. Papayannopoulos, 1995, The interpretation of collision-induced dissociation tandem mass-spectra of peptides, Mass Spectrom. Rev., 14, 49, 10.1002/mas.1280140104 · DOI
  58. Paschinger, 2009, Revealing the anti-HRP epitope in Drosophila and Caenorhabditis, Glycoconj J., 26, 385, 10.1007/s10719-008-9155-3 · DOI
  59. Petersen, 1995, Studies on the carbohydrate moieties of the timothy grass pollen allergen Phl p I, Electrophoresis, 16, 869, 10.1002/elps.11501601144 · DOI
  60. Price, 2015, Oral allergy syndrome (pollen-food allergy syndrome), Dermatitis, 26, 78, 10.1097/DER.0000000000000087 · DOI
  61. Radauer, 2008, The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands, BMC Evol. Biol., 8, 286, 10.1186/1471-2148-8-286 · DOI
  62. Rook, 2007, The hygiene hypothesis and the increasing prevalence of chronic inflammatory disorders, Trans. R. Soc. Trop. Med. Hyg., 101, 1072, 10.1016/j.trstmh.2007.05.014 · DOI
  63. Rook, 1998, Give us this day our daily germs, Immunol. Today, 19, 113, 10.1016/S0167-5699(98)80008-X · DOI
  64. Rujeni, 2012, Human schistosome infection and allergic sensitisation, J. Parasitol. Res., 2012, 1, 10.1155/2012/154743 · DOI
  65. Rybicki, 1986, Affinity purification of specific antibodies from plant virus capsid protein immobilised on nitrocellulose, J. Phytopathol., 116, 30, 10.1111/j.1439-0434.1986.tb00891.x · DOI
  66. Schenk, 2009, Characterization of PR-10 genes from eight Betula species and detection of Bet v 1 isoforms in birch pollen, BMC Plant Biol., 9, 1, 10.1186/1471-2229-9-24 · DOI
  67. Schnoeller, 2008, A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages, J. Immunol., 180, 4265, 10.4049/jimmunol.180.6.4265 · DOI
  68. Schramm, 2009, Molecular characterisation of kappa-5, a major antigenic glycoprotein from Schistosoma mansoni eggs, Mol. Biochem. Parasitol., 166, 4, 10.1016/j.molbiopara.2009.02.003 · DOI
  69. Silveira, 2002, High levels of IgG4 to Schistosoma mansoni egg antigens in individuals with periportal fibrosis, Am. J. Trop. Med. Hyg., 66, 542, 10.4269/ajtmh.2002.66.542 · DOI
  70. Siman, 2013, Allergen-specific IgG antibodies purified from mite-allergic patients sera block the IgE recognition of Dermatophagoides pteronyssinus antigens: an in vitro study, Clin. Dev. Immunol., 2013, 1, 10.1155/2013/657424 · DOI
  71. Steen, 2004, The ABCs (and XYZs) of peptide sequencing, Nat. Rev. Mol. Cell Biol., 5, 699, 10.1038/nrm1468 · DOI
  72. Steinke, 2008, 5. Genetics of allergic disease, J. Allergy Clin. Immunol., 121, S384, 10.1016/j.jaci.2007.07.029 · DOI
  73. Studier, 1973, Analysis of bacteriophage T7 early RNAs and proteins on slab gels, J. Mol. Biol., 79, 237, 10.1016/0022-2836(73)90003-X · DOI
  74. Stumvoll, 2002, Purification, structural and immunological characterization of a timothy grass (Phleum pratense) pollen allergen, Phl p 4, with cross-reactive potential, Biol. Chem., 383, 1383, 10.1515/BC.2002.157 · DOI
  75. Subbarayal, 2013, Kinetics, cross-reactivity, and specificity of Bet v 1-specific IgG4 antibodies induced by immunotherapy with birch pollen, Allergy, 68, 1377, 10.1111/all.12236 · DOI
  76. Swoboda, 1995, Isoforms of Bet v 1, the major birch pollen allergen, analyzed by liquid chromatography, mass spectrometry, and cDNA cloning, J. Biol. Chem., 270, 2607, 10.1074/jbc.270.6.2607 · DOI
  77. Towbin, 1979, Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications, Proc. Natl. Acad. Sci. U.S.A., 76, 4350, 10.1073/pnas.76.9.4350 · DOI
  78. Tretter, 1993, Fucose alpha-1,3-linked to the core region of glycoprotein N-glycans creates an important epitope for Ige from honeybee venom allergic individuals, Int. Arch. Allergy Immunol., 102, 259, 10.1159/000236534 · DOI
  79. van Die, 2006, Glycans modulate immune responses in helminth infections and allergy, Chem. Immunol. Allergy, 90, 91
  80. van Ree, 2002, Carbohydrate epitopes and their relevance for the diagnosis and treatment of allergic diseases, Int. Arch. Allergy Immunol., 129, 189, 10.1159/000066770 · DOI
  81. van Ree, 1995, Demonstration of carbohydrate-specific immunoglobulin G4 antibodies in sera of patients receiving grass pollen immunotherapy, Int. Arch. Allergy Immunol., 106, 146, 10.1159/000236835 · DOI
  82. van Ree, 2000, Beta(1,2)-xylose and alpha(1,3)-fucose residues have a strong contribution in IgE binding to plant glycoallergens, J. Biol. Chem., 275, 11451, 10.1074/jbc.275.15.11451 · DOI
  83. Wicklein, 2004, Carbohydrate moieties can induce mediator release: a detailed characterization of two major timothy grass pollen allergens, Biol. Chem., 385, 397, 10.1515/BC.2004.044 · DOI
  84. Wilson, 1998, Core alpha 1,3-fucose is a key part of the epitope recognized by antibodies reacting against plant N-linked oligosaccharides and is present in a wide variety of plant extracts, Glycobiology, 8, 651, 10.1093/glycob/8.7.651 · DOI
  85. Winther, 2006, Side-effects of allergen-specific immunotherapy: a prospective multi-centre study, Clin. Exp. Allergy, 36, 254, 10.1111/j.1365-2222.2006.02340.x · DOI
  86. Wuhrer, 2006, IPSE/alpha-1, a major secretory glycoprotein antigen from schistosome eggs, expresses the Lewis X motif on core-difucosylated N-glycans, FEBS J., 273, 2276, 10.1111/j.1742-4658.2006.05242.x · DOI
  87. Yazdanbakhsh, 2005, The role of helminth infections in protection from atopic disorders, Curr. Opin. Allergy Clin. Immunol., 5, 386, 10.1097/01.all.0000182541.52971.eb · DOI
  88. Young, 2012, Whole-genome sequence of Schistosoma haematobium, Nat. Genet., 44, 221, 10.1038/ng.1065 · DOI
  89. Zaccone, 2006, Parasitic worms and inflammatory diseases, Parasite Immunol., 28, 515, 10.1111/j.1365-3024.2006.00879.x · DOI

Cited by

Sorted by citations

Metadata

Authors
Igetei, J. E., El-Faham, M., Liddell, S., Schramm, G., & Doenhoff, M. J.
Venue
International Journal for Parasitology
Publisher
Elsevier BV
Published
2018-04
Volume
48
Issue
5
Pages
345-357
ISSN
0020-7519
DOI
10.1016/j.ijpara.2017.12.005
Cited by
11
References
1
Language
en
Licence
Funders
University of Nottingham

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