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Anthelmintic action of plant cysteine proteinases against the rodent stomach nematode, Protospirura muricola, in vitro and in vivo

  • G. STEPEK (a1), A. E. LOWE (a1), D. J. BUTTLE (a2), I. R. DUCE (a1) and J. M. BEHNKE (a1)...
Abstract

Cysteine proteinases from the fruit and latex of plants, including papaya, pineapple and fig, were previously shown to have a rapid detrimental effect, in vitro, against the rodent gastrointestinal nematodes, Heligmosomoides polygyrus (which is found in the anterior small intestine) and Trichuris muris (which resides in the caecum). Proteinases in the crude latex of papaya also showed anthelmintic efficacy against both nematodes in vivo. In this paper, we describe the in vitro and in vivo effects of these plant extracts against the rodent nematode, Protospirura muricola, which is found in the stomach. As in earlier work, all the plant cysteine proteinases examined, with the exception of actinidain from the juice of kiwi fruit, caused rapid loss of motility and digestion of the cuticle, leading to death of the nematode in vitro. In vivo, in contrast to the efficacy against H. polygyrus and T. muris, papaya latex only showed efficacy against P. muricola adult female worms when the stomach acidity had been neutralized prior to administration of papaya latex. Therefore, collectively, our studies have demonstrated that, with the appropriate formulation, plant cysteine proteinases have efficacy against nematodes residing throughout the rodent gastrointestinal tract.

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Corresponding author
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK. Tel: 44 115 951 3208. Fax: 44 115 951 3251. E-mail: jerzy.behnke@nottingham.ac.uk
Current address: Department of Veterinary Parasitology, Institute of Comparative Medicine, Faculty of Veterinary Medicine, University of Glasgow G61 1QH, UK.
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Albonico, M., Crompton, D. W. T. and Savioli, L. ( 1999). Control strategies for human intestinal nematode infections. Advances in Parasitology42, 277341.

Anthony, J.-P., Fyfe, L. and Smith, H. ( 2005). Plant active components – a resource for antiparasitic agents? Trends in Parasitology21, 462468.

Athanasiadou, S., Kyriazakis, I., Jackson, F. and Coop, R. L. ( 2001). Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: in vitro and in vivo studies. Veterinary Parasitology99, 205219.

Beloin, N., Gbeassor, M., Akpagana, K., Hudson, J., de Soussa, K., Koumaglo, K. and Arnason, J. T. ( 2005). Ethnomedicinal uses of Momordica charantia (Cucurbitaceae) in Togo and relation to its phytochemistry and biological activity. Journal of Ethnopharmacology96, 4955.

Berger, J. and Asenjo, C. F. ( 1939). Anthelmintic activity of fresh pineapple juice. Science90, 299300.

Berger, J. and Asenjo, C. F. ( 1940). Anthelmintic activity of crystalline papain. Science91, 387388.

Dekeyser, P. M., de Smedt, S., Demeester, J. and Lauwers, A. ( 1994). Fractionation and purification of the thiol proteinases from papaya latex. Journal of Chromatography B656, 203208.

Dubois, T., Jacquet, A., Schnek, A. G. and Looze, Y. ( 1988). The thiol proteinases from the latex of Carica papaya L. I. Fractionation, purification and preliminary characterisation. Biological Chemistry Hoppe-Seyler369, 733740.

Giday, M., Asfaw, Z., Elmqvist, T. and Woldu, Z. ( 2003). An ethnobotanical study of medicinal plants used by the Zay people in Ethiopia. Journal of Ethnopharmacology85, 4352.

Gill, J. H. and Lacey, E. ( 1998). Avermectin/milbemycin resistance in trichostrongyloid nematodes. International Journal for Parasitology28, 863877.

Githiori, J. B., Hoglund, J., Waller, P. J. and Baker, R. L. ( 2003). Evaluation of anthelmintic properties of extracts from some plants used as livestock dewormers by pastoralist and smallholder farmers in Kenya against Heligmosomoides polygyrus infections in mice. Veterinary Parasitology118, 215226.

Githiori, J. B., Hoglund, J., Waller, P. J. and Baker, R. L. ( 2004). Evaluation of anthelmintic properties of some plants used as livestock dewormers against Haemonchus contortus infections in sheep. Parasitology129, 245253.

Gopal, R. M., Pomroy, W. E. and West, D. M. ( 1999). Resistance of field isolates of Trichostrongylus colubriformis and Ostertagia circumcincta to ivermectin. International Journal for Parasitology29, 781786.

Hale, L. P. ( 2004). Proteolytic activity and immunogenicity of oral bromelain within the gastrointestinal tract of mice. International Immunopharmacology4, 255264.

Hammond, J. A., Fielding, D. and Bishop, S. C. ( 1997). Prospects for plant anthelmintics in tropical veterinary medicine. Veterinary Research Communications21, 213228.

Hördegen, P., Hertzberg, H., Heilmann, J., Langhans, W. and Maurer, V. ( 2003). The anthelmintic efficacy of five plant products against gastrointestinal trichostrongylids in artificially infected lambs. Veterinary Parasitology117, 5160.

Hounzangbe-Adote, M. S., Paolini, V., Fouraste, I., Moutairou, K. and Hoste, H. ( 2005b). In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Research in Veterinary Science78, 155160.

Huet, J., Looze, Y., Bartik, K., Raussens, V., Wintjens, R. and Boussard, P. ( 2006). Structural characterisation of the papaya cysteine proteinases at low pH. Biochemical and Biophysical Research Communications341, 620626.

McDowall, M. A. ( 1970). Anionic proteinase from Actinidia chinensis: preparation and properties of the crystalline enzyme. European Journal of Biochemistry14, 214221.

Mole, J. E. and Horton, H. R. ( 1973). Kinetics of papain-catalysed hydrolysis of α-N-benzoyl-L-arginine-p-nitroanilide. Biochemistry12, 816822.

Mwamachi, D. M., Audho, J. O., Thorpe, W. and Baker, R. L. ( 1995). Evidence for multiple anthelmintic resistance in sheep and goats reared under the same management in coastal Kenya. Veterinary Parasitology60, 303313.

Napper, A. D., Bennett, S. P., Borowski, M., Holdridge, M. B., Leonard, M. J. C., Rogers, E. E., Duan, Y., Laursen, R. A., Reinhold, B. and Shames, S. L. ( 1994). Purification and characterisation of multiple forms of the pineapple-stem-derived cysteine proteinases ananain and comosain. The Biochemical Journal301, 727735.

Paolini, V., Frayssines, A., de la Farge, F., Dorchies, P. and Hoste, H. ( 2003). Effects of condensed tannins on established populations and on incoming larvae of Trichostrongylus colubriformis and Teladorsagia circumcincta in goats. Veterinary Research34, 331339.

Rowan, A. D., Buttle, D. J. and Barrett, A. J. ( 1988). Ananain: a novel cysteine proteinase found in pineapple stem. Archives of Biochemistry and Biophysics267, 262270.

Stepek, G., Buttle, D. J., Duce, I. R., Lowe, A. and Behnke, J. M. ( 2005). Assessment of the anthelmintic effect of natural plant cysteine proteinases against the gastrointestinal nematode, Heligmosomoides polygyrus, in vitro. Parasitology130, 203211.

Stepek, G., Lowe, A. E., Buttle, D. J., Duce, I. R. and Behnke, J. M. ( 2006). In vitro and in vivo anthelmintic efficacy of plant cysteine proteinases against the rodent gastrointestinal nematode, Trichuris muris. Parasitology132, 681689.

Tagboto, S. and Townson, S. ( 2001). Antiparasitic properties of medicinal plants and other naturally occurring products. Advances in Parasitology50, 199295.

Tandon, V., Pal, P., Roy, B., Rao, H. S. P. and Reddy, K. S. ( 1997). In vitro anthelmintic activity of root-tuber extract of Flemingia vestita, an indigenous plant in Shillong, India. Parasitology Research83, 492498.

Uhlinger, C. ( 1990). Effects of three anthelmintic schedules on the incidence of colic in horses. Equine Veterinary Journal22, 251254.

Varughese, K. I., Ahmed, F. R., Carey, P. R., Hasnain, S., Huber, C. P. and Storer, A. C. ( 1989). Crystal structure of a papain-E-64 complex. Biochemistry28, 13301332.

Varughese, K. I., Su, Y., Cromwell, D., Hasnain, S. and Xuong, N. ( 1992). Crystal structure of an actinidin-E-64 complex. Biochemistry31, 51725176.

Waller, P. J., Echevarria, F., Eddi, C., Maciel, S., Nari, A. and Hansen, J. W. ( 1996). The prevalence of anthelmintic resistance in nematode parasites of sheep in Southern Latin America: general overview. Veterinary Parasitology62, 181187.

Waller, P. J., Bernes, G., Thamsborg, S. M., Sukura, A., Richter, S. H., Ingebrigtsen, K. and Hoglund, J. ( 2001). Plants as de-worming agents of livestock in the Nordic countries: historical perspective, popular beliefs and prospects for the future. Acta Veterinaria Scandinavica42, 3144.

Yamada, F., Takahashi, N. and Murachi, T. ( 1976). Purification and characterisation of a proteinase from pineapple fruit, fruit bromelain FA2. Journal of Biochemistry79, 12231234.

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Parasitology
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