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

Published online by Cambridge University Press:  11 October 2006

G. STEPEK
Affiliation:
School of Biology, University of Nottingham NG7 2RD, UK
A. E. LOWE
Affiliation:
School of Biology, University of Nottingham NG7 2RD, UK
D. J. BUTTLE
Affiliation:
Division of Genomic Medicine, University of Sheffield S10 2RX, UK
I. R. DUCE
Affiliation:
School of Biology, University of Nottingham NG7 2RD, UK
J. M. BEHNKE
Affiliation:
School of Biology, University of Nottingham NG7 2RD, UK

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.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Albonico, M., Crompton, D. W. T. and Savioli, L. ( 1999). Control strategies for human intestinal nematode infections. Advances in Parasitology 42, 277341.CrossRefGoogle Scholar
Albonico, M., Bickle, Q., Ramsan, M., Montresor, A., Savioli, L. and Taylor, M. ( 2003). Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bulletin of the World Health Organisation 81, 343352.Google Scholar
Anthony, J.-P., Fyfe, L. and Smith, H. ( 2005). Plant active components – a resource for antiparasitic agents? Trends in Parasitology 21, 462468.Google Scholar
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 Parasitology 99, 205219.CrossRefGoogle Scholar
Behnke, J. M., Barnard, C. J., Mason, N., Harris, P. D., Sherif, N. E., Zalat, S. and Gilbert, F. S. ( 2000). Intestinal helminths of spiny mice (Acomys cahirinus dimidiatus) from St. Katherine's Protectorate in the Sinai, Egypt. Journal of Helminthology 74, 3144.Google Scholar
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 Ethnopharmacology 96, 4955.CrossRefGoogle Scholar
Berger, J. and Asenjo, C. F. ( 1939). Anthelmintic activity of fresh pineapple juice. Science 90, 299300.CrossRefGoogle Scholar
Berger, J. and Asenjo, C. F. ( 1940). Anthelmintic activity of crystalline papain. Science 91, 387388.CrossRefGoogle Scholar
Campos, M. Q. and Vargas, M. V. ( 1977). Biologia de Protospirura muricola Gedoelst, 1916 y Mastophorus muris (Gmelin, 1790) (Nematoda: Spiruridae), en Costa Rica. I. Huespedes intermediarios. Revista de Biologia Tropical 25, 191207.Google Scholar
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 B 656, 203208.CrossRefGoogle Scholar
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-Seyler 369, 733740.Google Scholar
Geerts, S., Coles, G. C. and Gryseels, B. ( 1997). Anthelmintic resistance in human helminths: learning from the problems with worm control in livestock. Parasitology Today 12, 149151.CrossRefGoogle Scholar
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 Ethnopharmacology 85, 4352.CrossRefGoogle Scholar
Gill, J. H. and Lacey, E. ( 1998). Avermectin/milbemycin resistance in trichostrongyloid nematodes. International Journal for Parasitology 28, 863877.CrossRefGoogle Scholar
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 Parasitology 118, 215226.CrossRefGoogle Scholar
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. Parasitology 129, 245253.CrossRefGoogle Scholar
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 Parasitology 29, 781786.CrossRefGoogle Scholar
Hale, L. P. ( 2004). Proteolytic activity and immunogenicity of oral bromelain within the gastrointestinal tract of mice. International Immunopharmacology 4, 255264.CrossRefGoogle Scholar
Hammond, J. A., Fielding, D. and Bishop, S. C. ( 1997). Prospects for plant anthelmintics in tropical veterinary medicine. Veterinary Research Communications 21, 213228.CrossRefGoogle Scholar
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 Parasitology 117, 5160.CrossRefGoogle Scholar
Hounzangbe-Adote, S., Fouraste, I., Moutairou, K. and Hoste, H. ( 2005 a). In vitro effects of four tropical plants on the activity and development of the parasitic nematode, Trichostrongylus colubriformis. Journal of Helminthology 79, 2933.Google Scholar
Hounzangbe-Adote, M. S., Paolini, V., Fouraste, I., Moutairou, K. and Hoste, H. ( 2005 b). In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Research in Veterinary Science 78, 155160.Google Scholar
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 Communications 341, 620626.CrossRefGoogle Scholar
Love, S. ( 1992). The role of equine strongyles in the pathogenesis of colic and the current options for prophylaxis. Equine Veterinary Journal 13, S5S9.Google Scholar
Lowrie, F. M., Behnke, J. M. and Barnard, C. J. ( 2004). Density-dependent effects on the survival and growth of the rodent stomach worm Protospirura muricola in laboratory mice. Journal of Helminthology 78, 121128.CrossRefGoogle Scholar
McDowall, M. A. ( 1970). Anionic proteinase from Actinidia chinensis: preparation and properties of the crystalline enzyme. European Journal of Biochemistry 14, 214221.CrossRefGoogle Scholar
Mole, J. E. and Horton, H. R. ( 1973). Kinetics of papain-catalysed hydrolysis of α-N-benzoyl-L-arginine-p-nitroanilide. Biochemistry 12, 816822.CrossRefGoogle Scholar
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 Parasitology 60, 303313.CrossRefGoogle Scholar
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 Journal 301, 727735.CrossRefGoogle Scholar
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 Research 34, 331339.CrossRefGoogle Scholar
Quentin, J.-C. ( 1969). Cycle biologique de Protospirura muricola Gedoelst, 1916 Nematoda Spiruridae. Annales de Parasitologie (Paris) 44, 485504.CrossRefGoogle Scholar
Raj, R. K. ( 1974). Screening of some indigenous plants for anthelmintic action against human Ascaris lumbricoides. Indian Journal of Physiology and Pharmacology 18, 129131.Google Scholar
Robbins, B. H. ( 1930). A proteolytic enzyme in ficin, the anthelmintic principle of Leche de Higueron. Journal of Biological Chemistry 87, 251257.Google Scholar
Rowan, A. D., Buttle, D. J. and Barrett, A. J. ( 1988). Ananain: a novel cysteine proteinase found in pineapple stem. Archives of Biochemistry and Biophysics 267, 262270.CrossRefGoogle Scholar
Rowan, A. D., Buttle, D. J. and Barrett, A. J. ( 1990). The cysteine proteinases of the pineapple plant. Biochemical Journal 266, 869875.Google Scholar
Salih, E., Malthouse, J. P. G., Kowlessur, D., Jarvis, M., O'Driscoll, M. and Brocklehurst, K. ( 1987). Differences in the chemical and catalytic characteristics of two crystallographically “identical” enzyme catalytic sites. Characterisation of actinidin and papain by a combination of pH-dependent substrate catalysis kinetics and reactivity probe studies targeted on the catalytic-site thiol group and its immediate environment. The Biochemical Journal 247, 181193.Google Scholar
Satrija, F., Retnani, E. B., Ridwan, Y. and Tiuria, R. ( 2001). Potential use of herbal anthelmintics as alternative antiparasitic drugs for small holder farms in developing countries. Livestock Community and Environment. Proceedings of the 10th Conference of the Association of Institutions for Tropical Veterinary Medicine (Copenhagen, Denmark). http://www.aitvm.kvl.dk/E_periurban/E6Satrija.htm
Sgarbieri, V. C., Gupte, S. M., Kramer, D. E. and Whitaker, J. R. ( 1964). Ficus enzymes. I: Separation of the proteolytic enzymes of Ficus carica and Ficus glabrata latices. Journal of Biological Chemistry 239, 21702177.Google Scholar
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. Parasitology 130, 203211.CrossRefGoogle Scholar
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. Parasitology 132, 681689.CrossRefGoogle Scholar
Tagboto, S. and Townson, S. ( 2001). Antiparasitic properties of medicinal plants and other naturally occurring products. Advances in Parasitology 50, 199295.CrossRefGoogle Scholar
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 Research 83, 492498.CrossRefGoogle Scholar
Uhlinger, C. ( 1990). Effects of three anthelmintic schedules on the incidence of colic in horses. Equine Veterinary Journal 22, 251254.CrossRefGoogle Scholar
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. Biochemistry 28, 13301332.CrossRefGoogle Scholar
Varughese, K. I., Su, Y., Cromwell, D., Hasnain, S. and Xuong, N. ( 1992). Crystal structure of an actinidin-E-64 complex. Biochemistry 31, 51725176.CrossRefGoogle Scholar
Waller, P. J. ( 1986). Anthelmintic resistance in nematode parasites of sheep. Agricultural Zoology Reviews 1, 333373.Google Scholar
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 Parasitology 62, 181187.CrossRefGoogle Scholar
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 Scandinavica 42, 3144.CrossRefGoogle Scholar
Yamada, F., Takahashi, N. and Murachi, T. ( 1976). Purification and characterisation of a proteinase from pineapple fruit, fruit bromelain FA2. Journal of Biochemistry 79, 12231234.Google Scholar