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Strongyloides ratti: the role of interleukin-5 in protection against tissue migrating larvae and intestinal adult worms

Published online by Cambridge University Press:  12 April 2024

K. Watanabe ,
O. Sasaki ,
S. Hamano ,
K. Kishihara ,
K. Nomoto ,
I. Tada  and
Y. Aoki
K. Watanabe*
Affiliation:
Department of Parasitology, Institute of Tropical Medicine, Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan
O. Sasaki
Affiliation:
Department of Animal Science, Akita Prefectural College of Agriculture, Akita 010-0444, Japan
S. Hamano
Affiliation:
Department of Microbiology and Immunology (Parasitology), Faculty of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
K. Kishihara
Affiliation:
Department of Immunology, Institute of Bioregulation, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
K. Nomoto
Affiliation:
Department of Immunology, Institute of Bioregulation, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
I. Tada
Affiliation:
Department of Microbiology and Immunology (Parasitology), Faculty of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
Y. Aoki
Affiliation:
Department of Parasitology, Institute of Tropical Medicine, Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan
*
*Fax: +81 95 849 7805 E-mail: kanji@net.nagasaki-u.ac.jp
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Abstract

To determine the role of interleukin-5 (IL-5) and eosinophils in protection against Strongyloides ratti, mice treated with anti-IL-5 monoclonal antibody (mAb) were infected with S. ratti larvae. Strongyloides ratti egg numbers in faeces (EPG) in mAb treated mice were higher than those in control mice on days 6 and 7 after inoculation. The numbers of migrating worms in mAb treated mice 36h after inoculation were higher than those observed in control mice. Intestinal worm numbers in mAb treated mice 5 days after inoculation were higher than those in control mice. These results show that eosinophils effectively protected the host against S. ratti infection by mainly the larval stage in primary infections. The involvement of eosinophils in protection against secondary infection was also examined. Before secondary infection, mice were treated with anti-IL-5 mAb and infected with S. ratti. Patent infections were not observed in either mAb treated or control Ab treated mice. The numbers of migrating worms in the head and lungs of mAb treated mice increased to 60% of that in primary infected mice. Intestinal worms were not found in mAb treated mice or in contcrol mice after oral implantation of adult worms. Eosinophils were therefore mainly involved in protection against tissue migrating worms in secondary infections.

Type
Review Article
Information
Journal of Helminthology , Volume 77 , Issue 4 , December 2003 , pp. 355 - 361
Copyright
Copyright © Cambridge University Press 2003

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References

Abe, T., Sugaya, H., Ishida, K., Khan, W.I., Tasdemir, I. & Yoshimura, K. (1993) Intestinal protection against Strongyloides ratti and mastocytosis induced by administration of interleukin-3 in mice. Immunology 80, 116–121.Google ScholarPubMed
Behm, C.A. & Ovington, K.S. (2000) The role of eosinophils in parasitic helminth infections: insights from genetically modified mice. Parasitology Today 16, 202–209.CrossRefGoogle ScholarPubMed
Butterworth, A.E., Sturrock, R.F., Houba, V., Mahmouda, A.F., Sher, A. & Rees, P.H. (1975) Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature 256, 727–729.CrossRefGoogle ScholarPubMed
Coffman, R.L., Seymour, B.W., Hudak, S., Jackson, J. & Rennick, D. (1989) Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 245, 308–310.CrossRefGoogle ScholarPubMed
Dawkins, H.J.S., Muir, G.M. & Grove, D.I. (1981) Histopathological appearances in primary and secondary infection with Strongyloides ratti in mice. International Journal for Parasitology 11, 97–103.CrossRefGoogle Scholar
Herbert, D.R., Lee, J.J., Lee, N.A., Nolan, T.J., Schad, G.A. & Abraham, D. (2000) Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. Journal of Immunology 165, 4544–4551.CrossRefGoogle ScholarPubMed
Hitoshi, Y., Yamaguchi, N., Korenaga, M., Mita, S., Tominaga, A. & Takatsu, K. (1991) In vivo administration of antibody to murine IL-5 receptor inhibits eosinophilia of IL-5 transgenic mice. International Immunology 3, 135–139.CrossRefGoogle ScholarPubMed
Korenaga, M., Hitoshi, Y., Yamaguchi, N., Sato, Y., Takatsu, K. & Tada, I. (1991) The role of interleukin-5 in protective immunity to Strongyloides venezuelensis infection in mice. Immunology 72, 502–507.Google ScholarPubMed
Maruyama, H., Yabu, Y., Yoshida, A., Nawa, Y. & Ohta, N. (2000) A role of mast cell glycosaminoglycans for the immunological expulsion of the intestinal nematode, Strongyloides venezuelensis . Journal of Immunology 164, 3749–3754.CrossRefGoogle ScholarPubMed
Meeusen, E.N.T. & Balic, A. (2000) Do eosinophils have a role in the killing of helminth parasites? Parasitology Today 16, 95–101.CrossRefGoogle ScholarPubMed
Mould, A.W., Matthaei, K.I., Young, I.G. & Foster, P.S. (1997) Relationship between interleukin-5 and eotaxin in regulating blood and tissue eosinophilia in mice. Journal of Clinical Investigation 99, 1064–1071.CrossRefGoogle ScholarPubMed
Nawa, Y., Kiyota, M., Korenaga, M. & Kotani, M. (1985) Defective protective capacity of W/Wv mice against Strongyloides ratti infection and its reconstitution with bone marrow cells. Parasite Immunology 7, 429–438.CrossRefGoogle ScholarPubMed
Newlands, G.F.J., Gibson, S., Knox, D.P., Grenics, R., Wakelin, D. & Miller, H.R.P. (1987) Characterization and mast cell origin of a chymotrypsin-like protease isolated from intestines of mice infected with Trichinella spiralis . Immunology 62, 629–634.Google ScholarPubMed
Onah, D.N., Uchiyama, F., Nagakui, Y., Ono, M., Takai, T. & Nawa, Y. (2000) Mucosal defense against a gastrointestinal nematode: response of mucosal mast cells and mouse mast cell protease 1 during primary Strongyloides venezuelensis infection in FcR gamma-knockout mice. Infection and Immunity 68, 4968–4971.CrossRefGoogle Scholar
Ovington, K.S., McKie, K., Matthaei, K.I., Young, I.G. & Behm, C.A. (1998) Regulation of primary Strongyloides ratti infections in mice: a role for interleukin-5. Immunology 95, 488–493.CrossRefGoogle ScholarPubMed
Shin, S.H., Osada, Y., Chai, J.Y., Matsumoto, N., Takatsu, K. & Kojima, S. (1997) Protective roles of eosinophils in Nippostrongylus braziliensis infection. International Archives of Allergy and Immunology 114, Supplement 1, 45–50.CrossRefGoogle Scholar
Sugaya, H., Aoki, M., Yoshida, T., Takatsu, K. & Yoshimura, K. (1997) Eosinophilia and intracranial worm recovery in interleukin-5 transgenic and interleukin-5 receptor alpha chain-knockout mice infected with Angiostrongylus cantonensis . Parasitology Research 83, 583–590.CrossRefGoogle ScholarPubMed
Tada, I., Mimori, T. & Nakai, M. (1979) Migration route of Strongyloides ratti in albino rats. Japanese Journal of Parasitology 28, 219–227.Google Scholar
Takatsu, K. (1998) Interleukin-5 and B cell differentiation. Cytokine and Growth Factor Reviews 9, 25–35.CrossRefGoogle ScholarPubMed
Watanabe, K., Hamano, S., Noda, K., Koga, M. & Tada, I. (1999) Strongyloides ratti. Additive effect of testosterone implantation and carbon injection on the susceptibility of female mice. Parasitology Research 85, 522–526.CrossRefGoogle ScholarPubMed
Watanabe, K., Noda, K., Hamano, S., Koga, M., Kishihara, K., Nomoto, K. & Tada, I. (2000) The crucial role of granulocytes in the early host defense against Strongyloides ratti infection in mice. Parasitology Research 86, 188–193.CrossRefGoogle ScholarPubMed
Watanabe, K., Hamano, S., Yada, S., Noda, K., Kishihara, K., Nomoto, K. & Tada, I. (2001) The effect of interleukin-4 on the induction of intestinal mast cells and chronological cytokine profiles during intestinal nematode Strongyloides ratti infection. Parasitology Research 87, 149–154.CrossRefGoogle ScholarPubMed