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Epicutaneous sensitization with nematode antigens of fish parasites results in the production of specific IgG and IgE

Published online by Cambridge University Press:  07 August 2017

G. Fontenelle ,
M. Knoff ,
M.A. Verícimo  and
S.C. São Clemente
G. Fontenelle
Affiliation:
Pós-Graduação de Higiene Veterinária e Processamento Tecnológico de Produtos de Origem Animal, Faculdade de Medicina Veterinária, Universidade Federal Fluminense, Niterói, RJ, Brazil
M. Knoff*
Affiliation:
Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil
M.A. Verícimo
Affiliation:
Departamento de Imunobiologia, Instituto de Biologia, Campus do Valonguinho, Universidade Federal Fluminense, Niterói, RJ, Brazil
S.C. São Clemente
Affiliation:
Laboratório de Inspeção e Tecnologia do Pescado, Departamento de Tecnologia de Alimentos, Faculdade de Medicina Veterinária, Universidade Federal Fluminense, Niterói, RJ, Brazil
*
*E-mail: knoffm@ioc.fiocruz.br
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Abstract

Fish consumption plays an important role in the human diet. Hoplias malabaricus, trahira, is a freshwater fish widely appreciated in several Brazilian states and it is frequently infected by Contracaecum multipapillatum third-instar larvae (L3). The aim of the present study was to evaluate the allergenic potential of the C. multipapillatum L3 crude extract (CECM). BALB/c mice were immunized intraperitoneally (ip) with 10 or 50 μg CECM associated with 2 mg of aluminium hydroxide on days 0, 14 and 48. The determination of specific IgG and IgE antibody levels was done after immunization, and the late immunity was evaluated by the intradermal reaction in the ear pavilion. Epicutaneous sensitization was performed in the dorsal region, with antigenic exposure via a Finn-type chamber, containing 100 μg of chicken ovum albumin (OVA) or 100 μg CECM. After the exposures, the specific antibody levels were determined. In the ip immunization, there was a gradual increase in IgG antibody levels, independent of CECM concentration. In relation to IgE production, it was transitory, and immunization with 10 μg was more efficient than that of 50 μg. The same result was observed in the cellular hypersensitivity reaction. In the case of antigen exposure by the epicutaneous route, it was verified that only CECM was able to induce detectable levels of specific IgG and IgE antibodies. In the present study it was demonstrated that both intraperitoneal immunization and epicutaneous contact with C. multipapillatum larval antigens are potentially capable of inducing allergic sensitization in mice.

Type
Research Paper
Information
Journal of Helminthology , Volume 92 , Issue 4 , July 2018 , pp. 403 - 409
Copyright
Copyright © Cambridge University Press 2017 

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References

Alonso-Gomez, A., Moreno-Ancillo, A., Lopez-Serrano, M.C., Suarez-de-Parga, J.M., Daschner, A., Caballero, M.T., Barranco, P. & Cabanas, R. (2004) Anisakis simplex only provokes allergic symptoms when the worm parasitises the gastrointestinal tract. Parasitology Research 93, 378–384.Google Scholar
Audicana, M.T., Ansotegui, I.J., De Corres, L.F. & Kennedy, M.W. (2002) Anisakis simplex: dangerous – dead and alive? Trends in Parasitology 18, 20–25.Google Scholar
Baeza, M.L., Conejero, L., Higaki, Y., Martin, E., Perez, C., Infante, S., Rubio, M. & Zubeldia, J.M. (2005) Anisakis simplex allergy: a murine model of anaphylaxis induced by parasitic proteins displays a mixed Th1/Th2 pattern. Clinical & Experimental Immunology 142, 433–440.Google Scholar
Birmingham, N.P., Parvataneni, S., Hassan, H.M., Harkema, J., Samineni, S., Navuluri, L., Kelly, C.J. & Gangur, V. (2007) An adjuvant-free mouse model of tree nut allergy using hazelnut as a model tree nut. International Archives of Allergy and Immunology 144, 203–210.CrossRefGoogle Scholar
Cho, M.K., Park, M.K., Kang, S.A., Caballero, M.L., Perez-Pinar, T., Rodriguez-Perez, R., Ock, M.S., Cha, H.J., Hong, Y.C. & Yu, H.S. (2014) Allergenicity of two Anisakis simplex allergens evaluated in vivo using an experimental mouse model. Experimental Parasitology 146, 71–77.Google Scholar
Daschner, A., Alonso-Gomez, A., Cabañas, R., Suarez-de-Parga, J.M. & Lopez-Serrano, M.C. (2000) Gastroallergic anisakiasis: borderline between food allergy and parasitic disease – clinical and allergologic evaluation of 20 patients with confirmed acute parasitism by Anisakis simplex. Journal of Allergy and Clinical Immunology 105, 176–181.CrossRefGoogle ScholarPubMed
De Rossell, R.A., Bray, R.S. & Alexander, J. (1987) The correlation between delayed hypersensitivity, lymphocyte activation and protective immunity in experimental murine leishmaniasis. Parasite Immunology 9, 105–115.CrossRefGoogle ScholarPubMed
Del Pozo, M.D., Audicana, M., Diez, J.M., Munoz, D., Ansotegui, I.J., Fernandez, E., Garcia, M., Etxenagusia, M., Moneo, I. & De Corres, L.F. (1997) Anisakis simplex, a relevant etiologic factor in acute urticaria. Allergy 52, 576–579.Google Scholar
Dunkin, D., Berin, M.C. & Mayer, L. (2011) Allergic sensitization can be induced via multiple physiologic routes in an adjuvant-dependent manner. Journal of Allergy and Clinical Immunology 128, 1251–1258.Google Scholar
Gonipeta, B., Parvataneni, S., Tempelman, R.J. & Gangur, V. (2009) An adjuvant-free mouse model to evaluate the allergenicity of milk whey protein. Journal of Dairy Science 92, 4738–4744.Google Scholar
He, R., Oyoshi, M.K., Jin, H. & Geha, R.S. (2007) Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proceedings of the National Academy of Sciences, USA 104, 15817–15822.Google Scholar
Hsieh, K.Y., Tsai, C.C., Wu, C.H. & Lin, R.H. (2003) Epicutaneous exposure to protein antigen and food allergy. Clinical & Experimental Allergy 33, 1067–1075.Google Scholar
Iglesias, R., Leiro, J., Ubeira, F.M., Santamarina, M.T. & Sanmartin, M.L. (1993) Anisakis simplex: antigen recognition and antibody production in experimentally infected mice. Parasite Immunology 15, 243–250.Google Scholar
Jofre, M.L., Neira, O.P., Noemi, H.I. & Cerva, C.J. (2008) Pseudoterranovosis and sushi. Revista Chilena de Infectologia 25, 200–205.Google Scholar
Koyasu, S., Moro, K., Tanabe, M. & Takeuchi, T. (2010) Natural helper cells: a new player in the innate immune response against helminth infection. Advances in Immunology 108, 21–44.Google Scholar
Lack, G., Fox, D., Northstone, K., Golding, J., Avon Longitudinal Study of Parents and Children StudyTeam. (2003) Factors associated with the development of peanut allergy in childhood. New England Journal of Medicine 348, 977–985.Google Scholar
Leung, D.Y. (2000) Atopic dermatitis: new insights and opportunities for therapeutic intervention. Journal of Allergy and Clinical Immunology 105, 860–876.Google Scholar
Li, X.M., Kleiner, G., Huang, C.K., Lee, S.Y., Schofield, B., Soter, N.A. & Sampson, H.A. (2001) Murine model of atopic dermatitis associated with food hypersensitivity. Journal of Allergy and Clinical Immunology 107, 693–702.Google Scholar
Liu, T., Navarro, S. & Lopata, A.L. (2016) Current advances of murine models for food allergy. Molecular Immunology 70, 104–117.Google Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275.Google Scholar
Lozano, M.J., Martin, H.L., Diaz, S.V., Manas, A.I., Valero, L.A. & Campos, B.M. (2004) Cross-reactivity between antigens of Anisakis simplex s.l. and other ascarid nematodes. Parasite 11, 219–223.Google Scholar
Maizels, R.M. & Yazdanbakhsh, M. (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews. Immunology 3, 733–744.Google Scholar
Mattos, D.P., Vericimo, M.A., Lopes, L.M. & São Clemente, S.C. (2015) Immunogenic activity of the fish tapeworm Pterobothrium heteracanthum (Trypanorhyncha: Pterobothriidae) in BALB/c mice. Journal of Helminthology 89, 203–207.Google Scholar
Moravec, F. (1998) Nematodes of freshwater fishes of the Neotropical region. 464 pp. Praha, Academia.Google Scholar
Murakawa, M., Yamaoka, K., Tanaka, Y. & Fukuda, Y. (2006) Involvement of tumor necrosis factor (TNF)-alpha in phorbol ester 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced skin edema in mice. Biochemical Pharmacology 71, 1331–1336.Google Scholar
Na, H.K., Seo, M., Chai, J.Y., Lee, E.K. & Jeon, S.M. (2013) A case of anisakidosis caused by Pseudoterranova decipiens larva. Korean Journal of Parasitology 51, 115–117.Google Scholar
Neill, D.R. & McKenzie, A.N. (2011) Nuocytes and beyond: new insights into helminth expulsion. Trends in Parasitology 27, 214–221.Google Scholar
Nieuwenhuizen, N., Lopata, A.L., Jeebhay, M.F., Herbert, D.R., Robins, T.G. & Brombacher, F. (2006) Exposure to the fish parasite Anisakis causes allergic airway hyperreactivity and dermatitis. Journal of Allergy and Clinical Immunology 117, 1098–1105.Google Scholar
Perteguer, M.J., Rodero, M., Flores, J.M., Dorea, R.C. & Cuellar, C. (2001) Cellular immune responses in mice immunized with Anisakis simplex larval antigens. Parasitology Research 87, 396–404.Google Scholar
Santamaria Babi, L.F., Picker, L.J., Perez Soler, M.T., Drzimalla, K., Flohr, P., Blaser, K. & Hauser, C. (1995) Circulating allergen-reactive T cells from patients with atopic dermatitis and allergic contact dermatitis express the skin-selective homing receptor, the cutaneous lymphocyte-associated antigen. Journal of Experimental Medicine 181, 1935–1940.Google Scholar
Shamsi, S. & Butcher, A.R. (2011) First report of human anisakidosis in Australia. Medical Journal of Australia 194, 199–200.Google Scholar
Sicherer, S.H. (2002) Food allergy. Lancet 360, 701–710.Google Scholar
Sicherer, S.H. & Sampson, H.A. (2006) Food allergy. Journal of Allergy and Clinical Immunology 117, S470–475.Google Scholar
Spencer, L.A. & Weller, P.F. (2010) Eosinophils and Th2 immunity: contemporary insights. Immunology & Cell Biology 88, 250–256.Google Scholar
Spergel, J.M., Mizoguchi, E., Brewer, J.P., Martin, T.R., Bhan, A.K. & Geha, R.S. (1998) Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice. Journal of Clinical Investigation 101, 1614–1622.Google Scholar
Teraki, Y., Hotta, T. & Shiohara, T. (2000) Increased circulating skin-homing cutaneous lymphocyte-associated antigen (CLA)+ type 2 cytokine-producing cells, and decreased CLA+ type 1 cytokine-producing cells in atopic dermatitis. British Journal of Dermatology 143, 373–378.Google Scholar
Vericimo, M.A., Figueiredo, I., Teixeira, G.A. & São Clemente, S.C. (2015) Experimental anisakid infections in mice. Journal of Helminthology 89, 620–624.Google Scholar
Wang, L.F., Lin, J.Y., Hsieh, K.H. & Lin, R.H. (1996) Epicutaneous exposure of protein antigen induces a predominant Th2-like response with high IgE production in mice. Journal of Immunology 156, 4077–4082.Google Scholar
Wang, L.F., Chiu, H.C., Hsu, C.J., Liu, C.Y., Hsueh, Y.H. & Miaw, S.C. (2009) Epicutaneous sensitization with a protein antigen induces Th17 cells. Journal of Dermatological Science 54, 192–197.Google Scholar