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In vitro anthelmintic effects of cysteine proteinases from plants against intestinal helminths of rodents

Published online by Cambridge University Press:  01 December 2007

Gillian Stepek ,
Ann E. Lowe ,
David J. Buttle ,
Ian R. Duce  and
Jerzy M. Behnke
Gillian Stepek
Affiliation:
School of Biology, University of Nottingham, NG7 2RD, UK
Ann E. Lowe
Affiliation:
School of Biology, University of Nottingham, NG7 2RD, UK
David J. Buttle
Affiliation:
Academic Unit of Molecular Medicine, University of Sheffield Medical School, S10 2RX, UK
Ian R. Duce
Affiliation:
School of Biology, University of Nottingham, NG7 2RD, UK
Jerzy M. Behnke*
Affiliation:
School of Biology, University of Nottingham, NG7 2RD, UK
*
*Fax +44 115 951 3251 E-mail: [email protected]
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Abstract

Infections with gastrointestinal (GI) nematodes are amongst the most prevalent worldwide, especially in tropical climates. Control of these infections is primarily through treatment with anthelmintic drugs, but the rapid development of resistance to all the currently available classes of anthelmintic means that alternative treatments are urgently required. Cysteine proteinases from plants such as papaya, pineapple and fig are known to be substantially effective against three rodent GI nematodes, Heligmosomoides polygyrus, Trichuris muris and Protospirura muricola, both in vitro and in vivo. Here, based on in vitro motility assays and scanning electron microscopy, we extend these earlier reports, demonstrating the potency of this anthelmintic effect of plant cysteine proteinases against two GI helminths from different taxonomic groups – the canine hookworm, Ancylostoma ceylanicum, and the rodent cestode, Rodentolepis microstoma. In the case of hookworms, a mechanism of action targeting the surface layers of the cuticle indistinguishable from that reported earlier appears to be involved, and in the case of cestodes, the surface of the tegumental layers was also the principal location of damage. Hence, plant cysteine proteinases have a broad spectrum of activity against intestinal helminths (both nematodes and cestodes), a quality that reinforces their suitability for development as a much-needed novel treatment against GI helminths of humans and livestock.

Type
Research Papers
Information
Journal of Helminthology , Volume 81 , Issue 4 , December 2007 , pp. 353 - 360
Copyright
Copyright © Cambridge University Press 2007

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References

Anthony, J.-P., Fyfe, L. & Smith, H. (2005) Plant active components – a resource for antiparasitic agents? Trends in Parasitology 21, 462–468.CrossRefGoogle ScholarPubMed
Berger, J. & Asenjo, C.F. (1939) Anthelmintic activity of fresh pineapple juice. Science 90, 299–300.CrossRefGoogle ScholarPubMed
Berger, J. & Asenjo, C.F. (1940) Anthelmintic activity of crystalline papain. Science 91, 387–388.CrossRefGoogle ScholarPubMed
Garside, P. & Behnke, J.M. (1989) Ancylostoma ceylanicum: observations on host–parasite relationship during primary infection. Parasitology 98, 283–289.CrossRefGoogle ScholarPubMed
Geerts, S. & Gryseels, B. (2000) Drug resistance in human helminths: current situation and lessons from livestock. Clinical and Microbiological Reviews 13, 207–222.CrossRefGoogle ScholarPubMed
Giday, M., Asfaw, Z., Elmqvist, T. & Woldu, Z. (2003) An ethnobotanical study of medicinal plants used by the Zay people in Ethiopia. Journal of Ethnopharmacology 85, 43–52.CrossRefGoogle ScholarPubMed
Gill, J.H. & Lacey, E. (1998) Avermectin/milbemycin resistance in trichostrongyloid nematodes. International Journal of Parasitology 28, 863–877.CrossRefGoogle ScholarPubMed
Githiori, J.B., Höglund, J., Waller, P.J. & 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, 215–226.CrossRefGoogle ScholarPubMed
Hammond, J.A., Fielding, D. & Bishop, S.C. (1997) Prospects for plant anthelmintics in tropical veterinary medicine. Veterinary Research Communications 21, 213–228.CrossRefGoogle ScholarPubMed
Hounzangbe-Adote, S., Fouraste, I., Moutairou, K. & Hoste, H. (2005) In vitro effects of four tropical plants on the activity and development of the parasitic nematode, Trichostrongylus colubriformis. Journal of Helminthology 79, 29–33.CrossRefGoogle ScholarPubMed
Kaminsky, R. (2003) Drug resistance in nematodes: a paper tiger or a real problem? Current Opinion in Infectious Diseases 16, 559–564.CrossRefGoogle ScholarPubMed
Kowlessur, D., O'Driscol, M., Topham, M., Templeton, W., Thomas, E.W. & Brocklehurst, K. (1989) The interplay of electrostatic fields and binding interactions determining catalytic-site reactivity in actinidin. Biochemical Journal 259, 443–452.CrossRefGoogle ScholarPubMed
Robbins, B.H. (1930) A proteolytic enzyme in ficin, the anthelmintic principle of leche de higueron. Journal of Biological Chemistry 87, 251–257.CrossRefGoogle Scholar
Satrija, F., Nansen, P., Bjorn, H., Murtini, S. & He, S. (1994) Effect of papaya latex against Ascaris suum in naturally infected pigs. Journal of Helminthology 68, 343–346.CrossRefGoogle ScholarPubMed
Satrija, F., Nansen, P., Murtini, S. & He, S. (1995) Anthelmintic activity of papaya latex against patent Heligmosomoides polygyrus infections in mice. Journal of Ethnopharmacology 48, 161–164.CrossRefGoogle ScholarPubMed
Stepek, G., Buttle, D.J., Duce, I.R., Lowe, A. & Behnke, J.M. (2005) Assessment of the anthelmintic effect of natural plant cysteine proteinases against the gastrointestinal nematode, Heligmosomoides polygyrus, in vitro. Parasitology 130, 203–211.CrossRefGoogle ScholarPubMed
Stepek, G., Lowe, A.E., Buttle, D.J., Duce, I.R. & Behnke, J.M. (2006) In vitro and in vivo anthelmintic efficacy of plant cysteine proteinases against the rodent gastrointestinal nematode, Trichuris muris. Parasitology 132, 681–689.CrossRefGoogle ScholarPubMed
Stepek, G., Lowe, A.E., Buttle, D.J., Duce, I.R. & Behnke, J.M. (2007a) Anthelmintic action of plant cysteine proteinases against the rodent stomach nematode, Protospirura muricola, in vitro and in vivo. Parasitology 134, 103–112.CrossRefGoogle ScholarPubMed
Stepek, G., Lowe, A.E., Buttle, D.J., Duce, I.R. & Behnke, J.M. (2007b) The anthelmintic efficacy of plant-derived cysteine proteinases against the rodent gastrointestinal nematode. Heligmosomoides Polygyrus, in vivo. Parasitology 134, 1409–1419.CrossRefGoogle ScholarPubMed
Varughese, K.I., Ahmed, F.R., Carey, P.R., Hasnain, S., Huber, C.P. & Storer, A.C. (1989) Crystal structure of a papain–E-64 complex. Biochemistry 28, 1330–1332.CrossRefGoogle ScholarPubMed
Varughese, K.I., Su, Y., Cromwell, D., Hasnain, S. & Xuong, N. (1992) Crystal structure of an actinidin–E-64 complex. Biochemistry 31, 5172–5176.CrossRefGoogle ScholarPubMed
Waller, P.J. (1986) Anthelmintic resistance in nematode parasites of sheep. Agricultural Zoology Reviews 1, 333–373.Google Scholar
Waller, P.J., Bernes, G., Thamsborg, S.M., Sukura, A., Richter, S.H., Ingebrigtsen, K. & Höglund, 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, 31–44.CrossRefGoogle ScholarPubMed