Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-06-02T14:03:43.666Z Has data issue: false hasContentIssue false
  • English
  • Français

The use of albendazole and diammonium glycyrrhizinate in the treatment of eosinophilic meningitis in mice infected with Angiostrongylus cantonensis

Published online by Cambridge University Press:  13 December 2011

Y. Li ,
J.-P. Tang ,
D.-R. Chen ,
C.-Y. Fu ,
P. Wang ,
Z. Li ,
W. Wei ,
H. Li  and
W.-Q. Dong
Y. Li
Affiliation:
Department of Biopharmaceuticals, School of Biotechnology, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China Wuxi Hospital for Infectious Diseases, Wuxi214005, Jiangsu, People's Republic of China Department of General Surgery, The First Hospital of Lanzhou University, Lanzhou730000, Gansu, People's Republic of China
J.-P. Tang
Affiliation:
Department of Biopharmaceuticals, School of Biotechnology, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China
D.-R. Chen
Affiliation:
Department of Pathology, Zhangye Municipality People's Hospital, Zhangye734000, Gansu, People's Republic of China
C.-Y. Fu
Affiliation:
Department of Biopharmaceuticals, School of Biotechnology, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China
P. Wang
Affiliation:
Department of Biopharmaceuticals, School of Biotechnology, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China
Z. Li
Affiliation:
Department of Biopharmaceuticals, School of Biotechnology, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China
W. Wei
Affiliation:
Department of Biopharmaceuticals, School of Biotechnology, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China
H. Li
Affiliation:
Department of Etiology, School of Public Health and Tropical Medicine, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China
W.-Q. Dong*
Affiliation:
Department of Biopharmaceuticals, School of Biotechnology, Southern Medical University, Guangzhou510515, Guangdong, People's Republic of China
*
* Fax: +86 02061648556, E-mail: dongwq63@263.net
Get access Rights & Permissions [Opens in a new window]

Abstract

Angiostrongylus cantonensis (A. cantonensis) infection causes eosinophilic meningitis in humans. Eosinophilia and a Th2-type immune response are the crucial immune mechanisms for eosinophilic meningitis. CD4+CD25+ regulatory T cells (Treg) are involved in the pathogenesis of A. cantonensis. Diammonium glycyrrhizinate (DG) is a compound related to glycyrrhizin (GL), a triterpene glycoside extracted from liquorice root. We investigated the curative effects and probable mechanisms of therapy involving a combination of albendazole and DG in BALB/c mice infected with A. cantonensis, and compared these with therapy involving albendazole and dexamethasone. We analysed survival time, body weight, signs, eosinophil numbers, immunoglobulin E (IgE), interleukin-5 (IL-5), and eotaxin concentrations, numbers and Foxp3 expression of CD4+CD25+ Treg, worm recovery and histopathology. The present results demonstrated that the combination of albendazole and DG could increase survival time more efficiently and relieve neurological dysfunction; decrease weight loss, eosinophil numbers, concentrations of IgE, IL-5 and eotaxin, the number and expression of Foxp3 of CD4+CD25+ Treg; and improve worm recovery and histopathology changes in treated animals, compared with the combination of albendazole and dexamethasone. The observations presented here suggest that the albendazole and dexamethasone combination could be replaced by the combination of albendazole and DG.

Type
Research Papers
Information
Journal of Helminthology , Volume 87 , Issue 1 , March 2013 , pp. 1 - 11
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abe, K., Ikeda, T., Wake, K., Sato, T., Sato, T. & Inoue, H. (2008) Glycyrrhizin prevents lipopolysaccharide/D-galactosamine-induced liver injury through down-regulation of matrix metalloproteinase-9 in mice. Journal of Pharmacy and Pharmacology 60, 91–97.CrossRefGoogle ScholarPubMed
Alicata, J.E. (1965) Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Advances in Parasitology 3, 223–248.CrossRefGoogle ScholarPubMed
Belkaid, Y. (2007) Regulatory T cells and infection: a dangerous necessity. Nature Reviews Immunology 7, 875–888.CrossRefGoogle ScholarPubMed
Chotmongkol, V., Wongjitrat, C., Sawadpanit, K. & Sawanyawisuth, K. (2004) Treatment of eosinophilic meningitis with a combination of albendazole and corticosteroid. Southeast Asian Journal of Tropical Medicine and Public Health 35, 172–174.Google ScholarPubMed
Chuang, C.C., Su, K.E., Chen, C.W., Fan, C.K., Lin, F.K., Chen, Y.S. & Du, W.Y. (2010) Anti-CCR3 monoclonal antibody inhibits eosinophil infiltration in Angiostrongylus cantonensis-infected ICR mice. Acta Tropica 113, 209–213.CrossRefGoogle ScholarPubMed
Chung, L.Y., Chen, C.H., Wang, L.C., Chang, S.J. & Yen, C.M. (2010) Oxidative stress in mice infected with Angiostrongylus cantonensis coincides with enhanced glutathione-dependent enzymes activity. Experimental Parasitology 126, 178–183.CrossRefGoogle ScholarPubMed
Diao, Z., Chen, X., Yin, C., Wang, J., Qi, H. & Ji, A. (2009) Angiostrongylus cantonensis: effect of combination therapy with albendazole and dexamethasone on Th cytokine gene expression in PBMC from patients with eosinophilic meningitis. Experimental Parasitology 123, 1–5.CrossRefGoogle ScholarPubMed
Eamsobhana, P., Lim, P.E., Zhang, H., Gan, X. & Yong, H.S. (2010) Molecular differentiation and phylogenetic relationships of three Angiostrongylus species and Angiostrongylus cantonensis geographical isolates based on a 66-kDa protein gene of A. cantonensis (Nematoda: Angiostrongylidae). Experimental Parasitology 126, 564–569.CrossRefGoogle ScholarPubMed
Fang, R., Nie, H., Wang, Z., Tu, P., Zhou, D., Wang, L., He, L., Zhou, Y. & Zhao, J. (2009) Protective immune response in BALB/c mice induced by a suicidal DNA vaccine of the MIC3 gene of Toxoplasma gondii. Veterinary Parasitology 164, 134–140.CrossRefGoogle ScholarPubMed
Feng, C., Wang, H., Yao, C., Zhang, J. & Tian, Z. (2007) Diammonium glycyrrhizinate, a component of traditional Chinese medicine Gan-Cao, prevents murine T-cell-mediated fulminant hepatitis in IL-10- and IL-6-dependent manners. International Immunopharmacology 7, 1292–1298.CrossRefGoogle ScholarPubMed
Fontenot, J.D., Gavin, M.A. & Rudensky, A.Y. (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nature Immunology 4, 330–336.CrossRefGoogle ScholarPubMed
He, H.J., Lv, Z.Y., Li, Z.Y., Zhang, L.Y., Liao, Q., Zheng, H.Q., Su, W.Y., Rao, S.Q., Yu, X.B. & Wu, Z.D. (2011) Efficacy of combined treatment with albendazole and baicalein against eosinophilic meningitis induced by Angiostrongylus cantonensis in mice. Journal of Helminthology 85, 92–99.CrossRefGoogle ScholarPubMed
Hogan, S.P., Rosenberg, H.F., Moqbel, R., Phipps, S., Foster, P.S., Lacy, P., Kay, A.B. & Rothenberg, M.E. (2008) Eosinophils: biological properties and role in health and disease. Clinical and Experimental Allergy 38, 709–750.CrossRefGoogle ScholarPubMed
Intapan, P.M., Niwattayakul, K., Sawanyawisuth, K., Chotmongkol, V. & Maleewong, W. (2007) Cerebrospinal fluid eotaxin and eotaxin-2 levels in human eosinophilic meningitis associated with angiostrongyliasis. Cytokine 39, 138–141.CrossRefGoogle ScholarPubMed
Intapan, P.M., Kittimongkolma, S., Niwattayakul, K., Sawanyawisuth, K. & Maleewong, W. (2008) Cerebrospinal fluid cytokine responses in human eosinophilic meningitis associated with angiostrongyliasis. Journal of the Neurological Sciences 267, 17–21.CrossRefGoogle ScholarPubMed
Ismael, A.B., Dimier-Poisson, I., Lebrun, M., Dubremetz, J.F., Bout, D. & Mevelec, M.N. (2006) Mic1-3 knockout of Toxoplasma gondii is a successful vaccine against chronic and congenital toxoplasmosis in mice. Journal of Infectious Diseases 194, 1176–1183.CrossRefGoogle ScholarPubMed
Ismael, A.B., Hedhli, D., Cerede, O., Lebrun, M., Dimier-Poisson, I. & Mevelec, M.N. (2009) Further analysis of protection induced by the MIC3 DNA vaccine against T. gondii: CD4 and CD8 T cells are the major effectors of the MIC3 DNA vaccine-induced protection, both lectin-like and EGF-like domains of MIC3 conferred protection. Vaccine 27, 2959–2966.CrossRefGoogle ScholarPubMed
Jindrak, K. & Alicata, J.E. (1968) Comparative pathology in experimental infection of pigs and calves with larvae of Angiostrongylus cantonensis. Journal of Comparative Pathology 78, 371–382.CrossRefGoogle ScholarPubMed
Kwon, O.J., Au, B.T., Collins, P.D., Adcock, I.M., Mak, J.C., Robbins, R.R., Chung, K.F. & Barnes, P.J. (1994) Tumor necrosis factor-induced interleukin-8 expression in cultured human airway epithelial cells. American Journal of Physiology 267, L398–L405.Google ScholarPubMed
Lai, S.C., Chen, K.M., Chang, Y.H. & Lee, H.H. (2008) Comparative efficacies of albendazole and the Chinese herbal medicine long-dan-xie-gan-tan, used alone or in combination, in the treatment of experimental eosinophilic meningitis induced by Angiostrongylus cantonensis. Annals of Tropical Medicine and Parasitology 102, 143–150.CrossRefGoogle ScholarPubMed
Lan, K.P. & Lai, S.C. (2009) Differences of proteolytic enzymes and pathological changes in permissive and nonpermissive animal hosts for Angiostrongylus cantonensis infection. Veterinary Parasitology 165, 265–272.CrossRefGoogle ScholarPubMed
Lin, K.Y., Chen, K.M., Lan, K.P., Lee, H.H. & Lai, S.C. (2010) Alterations of myelin proteins in inflammatory demyelination of BALB/c mice caused by Angiostrongylus cantonensis. Veterinary Parasitology 171, 74–80.CrossRefGoogle ScholarPubMed
Matsui, S., Matsumoto, H., Sonoda, Y., Ando, K., Aizu-Yokota, E., Sato, T. & Kasahara, T. (2004) Glycyrrhizin and related compounds down-regulate production of inflammatory chemokines IL-8 and eotaxin 1 in a human lung fibroblast cell line. International Immunopharmacology 4, 1633–1644.CrossRefGoogle Scholar
Matsui, S., Sonoda, Y., Sekiya, T., Aizu-Yokota, E. & Kasahara, T. (2006) Glycyrrhizin derivative inhibits eotaxin 1 production via STAT6 in human lung fibroblasts. International Immunopharmacology 6, 369–375.CrossRefGoogle ScholarPubMed
Narala, V.R., Ranga, R., Smith, M.R., Berlin, A.A., Standiford, T.J., Lukacs, N.W. & Reddy, R.C. (2007) Pioglitazone is as effective as dexamethasone in a cockroach allergen-induced murine model of asthma. Respiritory Research 8, 90.CrossRefGoogle Scholar
Ni, Y.F., Kuai, J.K., Lu, Z.F., Yang, G.D., Fu, H.Y., Wang, J., Tian, F., Yan, X.L., Zhao, Y.C., Wang, Y.J. & Jiang, T. (2011) Glycyrrhizin treatment is associated with attenuation of lipopolysaccharide-induced acute lung injury by inhibiting cyclooxygenase-2 and inducible nitric oxide synthase expression. Journal of Surgical Research 165, e29–e35.CrossRefGoogle ScholarPubMed
Padilla-Docal, B., Dorta-Contreras, A.J., Bu-Coifiu-Fanego, R., Rodriguez-Rey, A., Gutierrez-Hernandez, J.C. & De Paula-Almeida, S.O. (2010) Reibergram of intrathecal synthesis of C4 in patients with eosinophilic meningitis caused by Angiostrongylus cantonensis. American Journal of Tropical Medicine and Hygiene 82, 1094–1098.CrossRefGoogle ScholarPubMed
Parsons, J.C. & Grieve, R.B. (1990) Effect of egg dosage and host genotype on liver trapping in murine larval toxocariasis. Journal of Parasitology 76, 53–58.CrossRefGoogle ScholarPubMed
Raghavan, S. & Holmgren, J. (2005) CD4+CD25+ suppressor T cells regulate pathogen induced inflammation and disease. FEMS Immunology and Medical Microbiology 44, 121–127.CrossRefGoogle ScholarPubMed
Ram, A., Mabalirajan, U., Das, M., Bhattacharya, I., Dinda, A.K., Gangal, S.V. & Ghosh, B. (2006) Glycyrrhizin alleviates experimental allergic asthma in mice. International Immunopharmacology 6, 1468–1477.CrossRefGoogle ScholarPubMed
Ramos, A.L., Discipio, R.G. & Ferreira, A.M. (2006) Eosinophil cationic protein damages protoscoleces in vitro and is present in the hydatid cyst. Parasite Immunology 28, 347–355.CrossRefGoogle ScholarPubMed
Rosenberg, H.F., Phipps, S. & Foster, P.S. (2007) Eosinophil trafficking in allergy and asthma. Journal of Allergy and Clinical Immunology 119, 1303–1312.CrossRefGoogle ScholarPubMed
Sasaki, O., Sugaya, H., Ishida, K. & Yoshimura, K. (1993) Ablation of eosinophils with anti-IL-5 antibody enhances the survival of intracranial worms of Angiostrongylus cantonensis in the mouse. Parasite Immunology 15, 349–354.CrossRefGoogle ScholarPubMed
Sato, H., Goto, W., Yamamura, J., Kurokawa, M., Kageyama, S., Takahara, T., Watanabe, A. & Shiraki, K. (1996) Therapeutic basis of glycyrrhizin on chronic hepatitis B. Antiviral Research 30, 171–177.CrossRefGoogle ScholarPubMed
Seminario, M.C., Saini, S.S. Jr, Macglashan, D. & Bochner, B.S. (1999) Intracellular expression and release of Fc epsilon RI alpha by human eosinophils. Journal of Immunology 162, 6893–6900.CrossRefGoogle ScholarPubMed
Shaio, M.F., Hou, S.C., Chen, J.G., Wu, C.C., Yang, K.D. & Chang, F.Y. (1990) Immunoglobulin G-dependent classical complement pathway activation in neutrophil-mediated cytotoxicity to infective larvae of Angiostrongylus cantonensis. Annals of Tropical Medicine and Parasitology 84, 185–191.CrossRefGoogle ScholarPubMed
Someya, A., Nishijima, K., Nunoi, H., Irie, S. & Nagaoka, I. (1997) Study on the superoxide-producing enzyme of eosinophils and neutrophils–comparison of the NADPH oxidase components. Archives of Biochemistry and Biophysics 345, 207–213.CrossRefGoogle Scholar
Song, L.J., Wang, Z.X., Chi, B.R. & Yang, G.Z. (2007) Regulatory effect of diammonium glycyrrhizinate on Th1/Th2 deviation in bronchial asthma: experiment with rats. Zhonghua Yi Xue Za Zhi 87, 2865–2867(in Chinese).Google ScholarPubMed
Takei, H., Baba, Y., Hisatsune, A., Katsuki, H., Miyata, T., Yokomizo, K. & Isohama, Y. (2008) Glycyrrhizin inhibits interleukin-8 production and nuclear factor-kappaB activity in lung epithelial cells, but not through glucocorticoid receptors. Journal of Pharmacological Sciences 106, 460–468.CrossRefGoogle Scholar
Tu, W.C. & Lai, S.C. (2006) Angiostrongylus cantonensis: efficacy of albendazole-dexamethasone co-therapy against infection-induced plasminogen activators and eosinophilic meningitis. Experimental Parasitology 113, 8–15.CrossRefGoogle ScholarPubMed
Wang, J.M., Rambaldi, A., Biondi, A., Chen, Z.G., Sanderson, C.J. & Mantovani, A. (1989) Recombinant human interleukin 5 is a selective eosinophil chemo-attractant. European Journal of Immunology 19, 701–705.CrossRefGoogle Scholar
Wang, Q.P., Lai, D.H., Zhu, X.Q., Chen, X.G. & Lun, Z.R. (2008) Human angiostrongyliasis. Lancet Infectious Diseases 8, 621–630.CrossRefGoogle ScholarPubMed
Yamaguchi, Y., Hayashi, Y., Sugama, Y., Miura, Y., Kasahara, T., Kitamura, S., Torisu, M., Mita, S., Tominaga, A. & Takatsu, K. (1988) Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor. Journal of Experimental Medicine 167, 1737–1742.CrossRefGoogle ScholarPubMed
Yen, C.M. & Chen, E.R. (1991) Detection of antibodies to Angiostrongylus cantonensis in serum and cerebrospinal fluid of patients with eosinophilic meningitis. International Journal for Parasitology 21, 17–21.Google ScholarPubMed