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Immune response and inhibitory effect of ketotifen on the BALB/c and C3H/HeN mice infected with Echinostoma hortense

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Abstract

Although Echinostoma hortense is one of the intestinal trematodes with a high infection rate in South Korea, the exact immune response against E. hortense infection has yet to be fully investigated. In the present study, we investigated differential susceptibilities in two different strains of micenamely, BALB/c (H-2d) and C3H/HeN (H-2k) mice. Likewise, we investigated the effects of ketotifen, an antiallergic drug, on the immune response against E. hortense infection. The worm recovery rate of the C3H/HeN mice was much higher than that of the BALB/c mice. The messenger ribonucleic acid (mRNA) expressions of interleukin (IL)-4 and IL-5 in the BALB/c mice were stronger than that of the C3H/HeN mice after E. hortense infection, but IL-1β and tumor necrosis factor (TNF)-α expressions in the BALB/c mice were weaker than that of the C3H/HeN mice after E. hortense infection. The number of goblet cells and eosinophils increased after E. hortense infection in the BALB/c and the C3H/HeN mice. The worm recovery rate was higher and lasted longer in the ketotifen-treated mice in comparison to the untreated mice. Ketotifen suppressed the mRNA expression of IL-4 and IL-5 in the BALB/c mice, but did not in the C3H/HeN mice. The IL-1β expressions were inhibited by ketotifen in the two strains, but TNF-α expression was inhibited in the C3H/HeN mice after ketotifen treatment. In addition, ketotifen inhibited the increase in eosinophils and goblet cells in varying degrees, depending on the strain. In summary, the immune sensitivity against E. hortense depends on the species of the host. The ketotifen treatment administered on the infected mice differently blocked the immune response against E. hortense infection.

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References

  • Abe T, Sugaya H, Yoshimura K (1993) Different susceptibility to the IL-3 induced protective effects between Strongyloides ratti and Nippostrongylus brasiliensis in C57BL/c mice. Parasitol Immunol 15:645–645

    Article  Google Scholar 

  • Asada S (1926) On a new echinostomatid trematode and its life history. Trans Jpn Pathol Soc 16:293–294

    Google Scholar 

  • Castillo JG, Oehling A, Gamboa PM (1991) Mechanism of ketotifen actin in hypersensitivity reactions. Its effect on cellular enzymatic activities. J Investig Allergol Clin Immunol 1:315–323

    PubMed  CAS  Google Scholar 

  • Chai JY, Kim TH, Kho WG, Chung SW, Hong ST, Lee SH (1993) Mucosal mast cell responses to experimental Metagonimus yokogawai infection in rats. Korean J Parasitol 31(2):129–134

    PubMed  CAS  Google Scholar 

  • Chai JY, Shin EH, Han ET, Guk SM, Choi MH, Lee SH (2000) Genetic difference in susceptibility and fatality of three strains of mice experimentally infected with Neodiplostomum seoulense. J Parasitol 86(5):1140–1144

    PubMed  CAS  Google Scholar 

  • Cho YK, Ryang YS, Kim IS, Park SK, Im JA, Lee KJ (2007) Differential immune profiles following experimental Echinostoma hortense infection in BALB/c and C3H/HeN mice. Parasitol Res 100(5):1053–1061

    Article  PubMed  Google Scholar 

  • Coffman RL, Seymour BWP, Hudak S, Jackson J, Rennick D (1989) Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 245:308–310

    Article  PubMed  CAS  Google Scholar 

  • Conchedda M, Bortoletti G, Gabriele F, Wakelin D, Palmas C (1997) Immune response to the cestode Hymenolepis nana: cytokine production during infection with eggs or cysts. Int J Parasitol 27:321–327

    Article  PubMed  CAS  Google Scholar 

  • Cordoba H, Fernandez M, Santos F, Oehling A (1992) Variations of intracellular histamine basophil levels after treatment with ketotifen. J Investig Allergol Clin Immunol 2:187–190

    PubMed  CAS  Google Scholar 

  • Doligalska M (2000) Immune response to Trichinella spiralis larvae after treatment with the anti-allergic compound ketotifen. Parasitol Res 86:232–238

    Article  PubMed  CAS  Google Scholar 

  • Doligalska M, Laskowska M (2001) The mucosal mast cell and IgA plasma cell responses to primary Trichinelia spiralis infection in BALB/c mice treated with ketotifen. Wiad Parazytol 47(4):597–601

    PubMed  CAS  Google Scholar 

  • Eliakim R, Karmeli F, Okon E, Rachmilewitz D (1992) Ketotifen effectively prevents mucosal damage in experimental colitis. Gut 33:1498–1503

    Article  PubMed  CAS  Google Scholar 

  • Fujino T, Fried B, Tada I (1993) The expulsion of Echinostoma trivolvis: worm kinetics and intestinal cytopathology in conventional and congenitally athymic BALB/c mice. Parasitology 106:297–304

    PubMed  Google Scholar 

  • Folkard SG, Hogarth PJ, Taylor MJ, Bianco AE (1996) Eosinophils are the major effector cells of immunity to microfilariae in a mouse model of onchocerciasis. Parasitology 112:323–239

    Article  PubMed  Google Scholar 

  • Gasbarre LC, Leighton EA, Sonstegard T (2001) Role of the bovine immune system and genomic in resistance to gastrointestinal nematodes. Vet Parasitol 98:51–64

    Article  PubMed  CAS  Google Scholar 

  • Grant SM, Goa KL, Fitton A, Sorkin EM (1990) Ketotifen. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic use in asthma and allergic disorders. Drug 40:412–448

    Article  CAS  Google Scholar 

  • Hoffman WH, Pfaff AW, Schulz-Key H, Soboslay PT (2001) Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis. Parasitology 122:641–649

    Article  Google Scholar 

  • Jones N, Roifman CM, Griffiths AM, Sherman P (1998) Ketotifen therapy for acute ulcerative colitis in children, a pilot study. Dig Dis Sci 43(3):609–615

    Article  PubMed  CAS  Google Scholar 

  • King CL, Ottesen EA, Nutman TB (1990) Cytokine regulation of antigen-driven immunoglobulin production in filarial parasite infections in humans. J Clin Invest 85(6):1810–1815

    Article  PubMed  CAS  Google Scholar 

  • Leckie JM, Khan J, O’Connor BJ, Hansel TT, Chung K, Fan DD, Djukanovic PJ, Holgate ST (2000) Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyperresponsiveness, and the late asthmatic response. Lancet 356(9248):2144–2148

    Article  PubMed  CAS  Google Scholar 

  • MacDonaid TT, Ferguson A (1978) Small intestinal epithelial cell kinetics and protozoal infection in mice. Gastroenterology 74(3):496–500

    Google Scholar 

  • Nawa Y, Ishikawa N, Tsuchya K, Hom Y, Abe T, Khan AI, Bingshi, Itoh H, Ide H, Uchiyama F (1994) Selective effector mechanism for the expulsion of intestinal helminths. Parasitol Immunol 16:333–338

    Article  CAS  Google Scholar 

  • Podleski WK, Panaszek BA, Schmidt JL, Burns RB (1984) Inhibition of eosinophils degranulation by ketotifen in a patient with milk allergy, manifested as bronchial asthma-an electron microscopic study. Agents Actions 15:177–181

    Article  PubMed  CAS  Google Scholar 

  • Reite OB, Evensen Ø (2006) Inflammatory cells of teleostean fish: a review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immunol 20(2):192–208

    Article  PubMed  CAS  Google Scholar 

  • Saito S, Hamada A, Watanabe N, Obata T, Katadura K, Otomo H (1996) Eosinophil chemotactic activity in Leishmania amasonesis promastigotes. Parasitol Res 82(6):485–489

    Article  PubMed  CAS  Google Scholar 

  • Seo BS, Chai JK, Hong SJ (1985) Studies on intestinal trematodes in Korea XX. Echinostomus japonicus. Korean J Parasitol 23(2):214–220

    Article  Google Scholar 

  • Shin EH, Yoshio O, Chai JY, Naoki M, Kiyoshi T, Somei K (1997) Protective roles of eosinophils in Nippostrongylus brasiliensis infection. Int Arch Allergy Immunol 114:45–50

    Article  PubMed  Google Scholar 

  • Specian RD, Oliver MG (1991) Functional biology of intestinal goblet cells. Am J Physiol 260:C183–C193

    PubMed  CAS  Google Scholar 

  • Tanaka Y, Nadano S, Koten J (1999) Case of echinostomiasis. Nihon Naika Gakkai Zasshi 88(1):138–140

    PubMed  CAS  Google Scholar 

  • Togawa M, Kiniwa M, Nagai H (2001) The roles of IL-4, IL-5 and mast cells in the accumulation of eosinophils during allergic cutaneous late phage reaction in mice. Life Sci 69(6):699–705

    Article  PubMed  CAS  Google Scholar 

  • Tominaga T, Watanabe A, Tsuji J, Koda A, Nagai H, Kumazawa T, Shimada H (1997) Effect of TYB-2285 on antigen-induced accumulation of eosinophils into the peritoneal cavity of rats sensitized with Ascaris suum extract. Gen Pharmacol 28:411–414

    PubMed  CAS  Google Scholar 

  • Urban JF Jr, Katona IM, Paul WE, Finkelman FD (1991) Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc Natl Acad Sci USA 88(13):5513–5517

    Article  PubMed  CAS  Google Scholar 

  • Wakelin D, Rose ME, Hesketh P, Else KJ, Grencis RK (1993) Immunity to coccidiosis: genetic influences on lymphocyte and cytokine responses of infection with Eimeria vermiformis in inbred mice. Parasitol Immunol 15(1):11–19

    Article  CAS  Google Scholar 

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Acknowledgment

This study was supported by a grant from the Maeji Institute of Academic Research in the fiscal year 2004.

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Correspondence to In Sik Kim.

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Ryang, Y.S., Yang, E.J., Kim, JL. et al. Immune response and inhibitory effect of ketotifen on the BALB/c and C3H/HeN mice infected with Echinostoma hortense . Parasitol Res 101, 1103–1110 (2007). https://doi.org/10.1007/s00436-007-0591-y

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