Cited by 28

The DOI matches its Crossref record.

Helminth Infection Alters IgE Responses to Allergens Structurally Related to Parasite Proteins

Santiago, Helton da Costa, Ribeiro-Gomes, Flávia L, Bennuru, Sasisekhar, Nutman, Thomas B·2014·The Journal of Immunology

Abstract

Immunological cross-reactivity between environmental allergens and helminth proteins has been demonstrated, although the clinically related implications of this cross-reactivity have not been addressed. To investigate the impact of molecular similarity among allergens and cross-reactive homologous helminth proteins in IgE-based serologic assessment of allergic disorders in a helminth-infected population, we performed ImmunoCAP tests in filarial-infected and noninfected individuals for IgE measurements to allergen extracts that contained proteins with high levels of homology with helminth proteins as well as IgE against representative recombinant allergens with and without helminth homologs. The impact of helminth infection on the levels and function of the IgE to these specific homologous and nonhomologous allergens was corroborated in an animal model. We found that having a tissue-invasive filarial infection increased the serological prevalence of ImmunoCAP-identified IgE directed against house dust mite and cockroach, but not against timothy grass, the latter with few allergens with homologs in helminth infection. IgE ELISA confirmed that filaria-infected individuals had higher IgE prevalences to those recombinant allergens that had homologs in helminths. Mice infected with the helminth Heligmosomoides polygyrus displayed increased levels of IgE and positive skin tests to allergens with homologs in the parasite. These results show that cross-reactivity among allergens and helminth proteins can have practical implications, altering serologic approaches to allergen testing and bringing a new perspective to the “hygiene hypothesis.”

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 · 10.4049/jimmunol.1401638

Cites

Statistics

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: 54

  1. Pearce, 2007, Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC), Thorax, 62, 758, 10.1136/thx.2006.070169 · DOI
  2. Bach, 2002, The effect of infections on susceptibility to autoimmune and allergic diseases, N. Engl. J. Med., 347, 911, 10.1056/NEJMra020100 · DOI
  3. Maizels, 2005, Infections and allergy: helminths, hygiene and host immune regulation, Curr. Opin. Immunol., 17, 656, 10.1016/j.coi.2005.09.001 · DOI
  4. 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
  5. Cooper, 2003, Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics, J. Allergy Clin. Immunol., 111, 995, 10.1067/mai.2003.1348 · DOI
  6. Dagoye, 2003, Wheezing, allergy, and parasite infection in children in urban and rural Ethiopia, Am. J. Respir. Crit. Care Med., 167, 1369, 10.1164/rccm.200210-1204OC · DOI
  7. Flohr, 2006, Poor sanitation and helminth infection protect against skin sensitization in Vietnamese children: a cross-sectional study, J. Allergy Clin. Immunol., 118, 1305, 10.1016/j.jaci.2006.08.035 · DOI
  8. Scrivener, 2001, Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study, Lancet, 358, 1493, 10.1016/S0140-6736(01)06579-5 · DOI
  9. Cooper, 2003, Allergic symptoms, atopy, and geohelminth infections in a rural area of Ecuador, Am. J. Respir. Crit. Care Med., 168, 313, 10.1164/rccm.200211-1320OC · DOI
  10. Rodrigues, 2008, Early infection with Trichuris trichiura and allergen skin test reactivity in later childhood, Clin. Exp. Allergy, 38, 1769, 10.1111/j.1365-2222.2008.03027.x · DOI · Paper page
  11. Huang, 2002, Negative association of Enterobius infestation with asthma and rhinitis in primary school children in Taipei, Clin. Exp. Allergy, 32, 1029, 10.1046/j.1365-2745.2002.01424.x · DOI
  12. Araujo, 2000, Inverse association between skin response to aeroallergens and Schistosoma mansoni infection, Int. Arch. Allergy Immunol., 123, 145, 10.1159/000024433 · DOI
  13. Rujeni, 2012, Atopy is inversely related to schistosome infection intensity: a comparative study in Zimbabwean villages with distinct levels of Schistosoma haematobium infection, Int. Arch. Allergy Immunol., 158, 288, 10.1159/000332949 · DOI · Paper page
  14. Choi, 2011, Clonorchis sinensis infection is positively associated with atopy in endemic area, Clin. Exp. Allergy, 41, 697, 10.1111/j.1365-2222.2011.03746.x · DOI
  15. Dold, 1998, Ascaris-specific IgE and allergic sensitization in a cohort of school children in the former East Germany, J. Allergy Clin. Immunol., 102, 414, 10.1016/S0091-6749(98)70129-0 · DOI
  16. Alshishtawy, 1991, Asthma in Tanta, Egypt: serologic analysis of total and specific IgE antibody levels and their relationship to parasite infection, Int. Arch. Allergy Appl. Immunol., 96, 348, 10.1159/000235520 · DOI
  17. Hunninghake, 2007, Sensitization to Ascaris lumbricoides and severity of childhood asthma in Costa Rica, J. Allergy Clin. Immunol., 119, 654, 10.1016/j.jaci.2006.12.609 · DOI · Paper page
  18. Palmer, 2002, Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China, Am. J. Respir. Crit. Care Med., 165, 1489, 10.1164/rccm.2107020 · DOI
  19. Buijs, 1997, Relationship between allergic manifestations and Toxocara seropositivity: a cross-sectional study among elementary school children, Eur. Respir. J., 10, 1467, 10.1183/09031936.97.10071467 · DOI
  20. Moncayo, 2013, Effects of geohelminth infection and age on the associations between allergen-specific IgE, skin test reactivity and wheeze: a case-control study, Clin. Exp. Allergy, 43, 60, 10.1111/cea.12040 · DOI
  21. Babu, 2006, Regulatory networks induced by live parasites impair both Th1 and Th2 pathways in patent lymphatic filariasis: implications for parasite persistence, J. Immunol., 176, 3248, 10.4049/jimmunol.176.5.3248 · DOI
  22. Metenou, 2012, Impact of filarial infections on coincident intracellular pathogens: Mycobacterium tuberculosis and Plasmodium falciparum, Curr. Opin. HIV AIDS, 7, 231, 10.1097/COH.0b013e3283522c3d · DOI
  23. Metenou, 2009, Patent filarial infection modulates malaria-specific type 1 cytokine responses in an IL-10-dependent manner in a filaria/malaria-coinfected population, J. Immunol., 183, 916, 10.4049/jimmunol.0900257 · DOI
  24. Sabin, 1996, Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni, J. Infect. Dis., 173, 269, 10.1093/infdis/173.1.269 · DOI · Paper page
  25. Cooper, 2001, Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR, Infect. Immun., 69, 1574, 10.1128/IAI.69.3.1574-1580.2001 · DOI
  26. Cooper, 1999, Human onchocerciasis and tetanus vaccination: impact on the postvaccination antitetanus antibody response, Infect. Immun., 67, 5951, 10.1128/IAI.67.11.5951-5957.1999 · DOI
  27. Jarrett, 1974, Elevation of total serum IgE in rats following helminth parasite infection, Nature, 251, 613, 10.1038/251613a0 · DOI
  28. Urban, 1982, Cellular basis of the non-specific potentiation of the immunoglobulin E response after helminth parasite infection, Vet. Parasitol., 10, 131, 10.1016/0304-4017(82)90019-X · DOI
  29. Fitzsimmons, 2009, Survival of the fittest: allergology or parasitology?, Trends Parasitol., 25, 447, 10.1016/j.pt.2009.07.004 · DOI · Paper page
  30. Santiago, 2012, Structural differences between human proteins and aero- and microbial allergens define allergenicity, PLoS ONE, 7, e40552, 10.1371/journal.pone.0040552 · DOI
  31. Sereda, 2008, Helminths and allergy: the example of tropomyosin, Trends Parasitol., 24, 272, 10.1016/j.pt.2008.03.006 · DOI
  32. Acevedo, 2009, IgE cross-reactivity between Ascaris and domestic mite allergens: the role of tropomyosin and the nematode polyprotein ABA-1, Allergy, 64, 1635, 10.1111/j.1398-9995.2009.02084.x · DOI
  33. Santos, 2008, Cross-reactive IgE antibody responses to tropomyosins from Ascaris lumbricoides and cockroach, J. Allergy Clin. Immunol., 121, 1040, 10.1016/j.jaci.2007.12.1147 · DOI
  34. Santiago, 2011, Structural and immunologic cross-reactivity among filarial and mite tropomyosin: implications for the hygiene hypothesis, J. Allergy Clin. Immunol., 127, 479, 10.1016/j.jaci.2010.11.007 · DOI
  35. Valmonte, 2012, IgE cross-reactivity between house dust mite allergens and Ascaris lumbricoides antigens, Asia Pac. Allergy, 2, 35, 10.5415/apallergy.2012.2.1.35 · DOI
  36. Nakazawa, 2013, Immunization of rabbits with nematode Ascaris lumbricoides antigens induces antibodies cross-reactive to house dust mite Dermatophagoides farinae antigens, Biosci. Biotechnol. Biochem., 77, 145, 10.1271/bbb.120626 · DOI
  37. Santiago, 2012, Molecular mimicry between cockroach and helminth glutathione S-transferases promotes cross-reactivity and cross-sensitization, J. Allergy Clin. Immunol., 130, 248, 10.1016/j.jaci.2012.02.045 · DOI
  38. 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
  39. Proust, 2008, A single oral sensitization to peanut without adjuvant leads to anaphylaxis in mice, Int. Arch. Allergy Immunol., 146, 212, 10.1159/000115889 · DOI
  40. Ljungström, 1988, The sequential appearance of IgG subclasses and IgE during the course of Trichinella spiralis infection, Clin. Exp. Immunol., 74, 230
  41. Hussaarts, 2011, Regulatory B-cell induction by helminths: implications for allergic disease, J. Allergy Clin. Immunol., 128, 733, 10.1016/j.jaci.2011.05.012 · DOI · Paper page
  42. Maizels, 2011, Regulatory T cells in infection, Adv. Immunol., 112, 73, 10.1016/B978-0-12-387827-4.00003-6 · DOI
  43. Aalberse, 2009, Immunoglobulin G4: an odd antibody, Clin. Exp. Allergy, 39, 469, 10.1111/j.1365-2222.2009.03207.x · DOI
  44. Hussain, 1992, Control of allergic reactivity in human filariasis. Predominant localization of blocking antibody to the IgG4 subclass, J. Immunol., 148, 2731, 10.4049/jimmunol.148.9.2731 · DOI
  45. Matsui, 2005, Mouse allergen-specific immunoglobulin G and immunoglobulin G4 and allergic symptoms in immunoglobulin E-sensitized laboratory animal workers, Clin. Exp. Allergy, 35, 1347, 10.1111/j.1365-2222.2005.02331.x · DOI
  46. Harnett, 2010, Helminth-derived immunomodulators: can understanding the worm produce the pill?, Nat. Rev. Immunol., 10, 278, 10.1038/nri2730 · DOI
  47. Bager, 2011, Symptoms after ingestion of pig whipworm Trichuris suis eggs in a randomized placebo-controlled double-blind clinical trial, PLoS ONE, 6, e22346, 10.1371/journal.pone.0022346 · DOI
  48. Feary, 2010, Experimental hookworm infection: a randomized placebo-controlled trial in asthma, Clin. Exp. Allergy, 40, 299, 10.1111/j.1365-2222.2009.03433.x · DOI · Paper page
  49. Elliott, 2012, Where are we on worms?, Curr. Opin. Gastroenterol., 28, 551, 10.1097/MOG.0b013e3283572f73 · DOI
  50. Blount, 2009, Immunologic profiles of persons recruited for a randomized, placebo-controlled clinical trial of hookworm infection, Am. J. Trop. Med. Hyg., 81, 911, 10.4269/ajtmh.2009.09-0237 · DOI · Paper page
  51. Caraballo, 2011, Allergy in the tropics: the impact of cross-reactivity between mites and ascaris, Front. Biosci. (Elite Ed.), 3, 51, 10.2741/e219 · DOI
  52. Scala, 2013, Allergen microbead arrays: the future of allergy diagnostics?, Expert Rev. Clin. Immunol., 9, 1, 10.1586/eci.12.81 · DOI
  53. Morens, 2010, The wages of original antigenic sin, Emerg. Infect. Dis., 16, 1023, 10.3201/eid1606.100453 · DOI
  54. van Neerven, 1999, Blocking antibodies induced by specific allergy vaccination prevent the activation of CD4+ T cells by inhibiting serum-IgE-facilitated allergen presentation, J. Immunol., 163, 2944, 10.4049/jimmunol.163.5.2944 · DOI

Cited by

Sorted by citations

See all 28

Metadata

Authors
Santiago, H. D. C., Ribeiro-Gomes, F. L., Bennuru, S., & Nutman, T. B.
Venue
The Journal of Immunology
Published
2014-01-01
Volume
194
Issue
1
Pages
93-100
ISSN
  • 0022-1767
  • 1550-6606
Cited by
28
References
0
Language
en

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: Helminth Infection Alters IgE Responses to Allergens Structurally Related to Parasite Proteins. https://app.cochat.ai/papers/10.4049/jimmunol.1401638
The paper
Santiago, H. D. C., Ribeiro-Gomes, F. L., Bennuru, S., & Nutman, T. B. (2014). Helminth Infection Alters IgE Responses to Allergens Structurally Related to Parasite Proteins. The Journal of Immunology. https://doi.org/10.4049/jimmunol.1401638