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The anthelmintic efficacy of natural plant cysteine proteinases against Hymenolepis microstoma in vivo

Published online by Cambridge University Press:  16 September 2014

F. Mansur ,
W. Luoga ,
D.J. Buttle ,
I.R. Duce ,
A. Lowe  and
J.M. Behnke
F. Mansur
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK Faculty of Medicine and Health Sciences, Universiti Sains Islam Malaysia (USIM), Kuala Lumpur, Malaysia
W. Luoga
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK Department of Life Sciences, Mkwawa University College of Education, Iringa, Tanzania
D.J. Buttle
Affiliation:
Department of Infection and Immunity, University of Sheffield Medical School, Beech Hill Road, Sheffield, S10 2RX, UK
I.R. Duce
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
A. Lowe
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
J.M. Behnke*
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK
*
*Fax: 44 115 951 3251 E-mail: jerzy.behnke@nottingham.ac.uk
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Abstract

Little is known about the efficacy of cysteine proteinases (CP) as anthelmintics for cestode infections in vivo. Hymenolepis microstoma is a natural parasite of house mice, and provides a convenient model system for the assessment of novel drugs for anthelmintic activity against cestodes. The experiments described in this paper indicate that treatment of H. microstoma infections in mice with the supernatant of papaya latex (PLS), containing active cysteine proteinases, is only minimally efficacious. The statistically significant effects seen on worm burden and biomass showed little evidence of dose dependency, were temporary and the role of cysteine proteinases as the active principles in PLS was not confirmed by specific inhibition with E-64. Worm fecundity was not affected by treatment at the doses used. We conclude also that this in vivo host–parasite system is not sensitive enough to be used reliably for the detection of cestocidal activity of compounds being screened as potential, novel anthelmintics.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 5 , September 2015 , pp. 601 - 611
Copyright
Copyright © Cambridge University Press 2014 

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References

Abbott, J.B. & Barrett, E.J. (2008) The problem of diagnosing tapeworm infections in horses. Equine Veterinary Journal 40, 5–6.CrossRefGoogle ScholarPubMed
Andreassen, J. (1991) Immunity to adult cestodes: basic knowledge and vaccination problems. A review. Parassitologia 33, 45–53.Google ScholarPubMed
Barrett, A.J., Kembhavi, A.A. & Hanada, K. (1981) E-64 [L-trans-epoxysuccinyl-leucyl-amido(4-guanidino)butane] and related epoxides as inhibitors of cysteine proteinases. Acta Biologica et Medica Germanica 40, 1513–1517.Google Scholar
Befus, A.D. & Threadgold, L.T. (1975) Possible immunological damage to the tegument of Hymenolepis diminuta in mice and rats. Parasitology 71, 525–534.CrossRefGoogle Scholar
Behnke, J.M. (2001) Hymenolepis species (Cestoda). pp. 115–121in Halton, D.W., Behnke, J.M. & Marshall, I. (Eds) Practical exercises in parasitology. British Society for Parasitology. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Behnke, J.M. & Parish, H.A. (1979) Nematospiroides dubius: arrested development of larvae in immune mice. Experimental Parasitology 47, 116–127.CrossRefGoogle ScholarPubMed
Behnke, J.M., Buttle, D.J., Stepek, G., Lowe, A. & Duce, I.R. (2008) Developing novel anthelmintics from plant cysteine proteinases. Parasites & Vectors 1, 29.CrossRefGoogle ScholarPubMed
Buttle, D.J., Dando, P.M., Coe, P.F., Sharp, S.L., Shepherd, S.T. & Barrett, A.J. (1990) The preparation of fully active chymopapain free of contaminating proteinases. Biological Chemistry 371, 1083–1088.Google ScholarPubMed
Buttle, D.J., Behnke, J.M., Bartley, Y., Elsheikha, H.M., Bartley, D.J., Garnett, M.C., Donnan, A.A., Jackson, F., Lowe, A. & Duce, I.R. (2011) Oral dosing with papaya latex is an effective anthelmintic treatment for sheep infected with Haemonchus contortus. Parasites & Vectors 4, 36.CrossRefGoogle ScholarPubMed
Caldwell, F.C. & Caldwell, F.L. (1929) A study of the anthelmintic efficacy of Higuerolatex in the treatment of trichuriasis, with comment as to its effectiveness against Ascaris infestation. American Journal of Tropical Medicine 9, 471–482.Google Scholar
Coles, G.C. (1983) Chemotherapy and the effects of chemotherapeutic agents. pp. 581–628in Arme, C. & Pappas, C.W. (Eds) Biology of the Eucestoda. London, Academic Press.Google Scholar
Cunningham, L.J. & Olson, P.D. (2010) Description of Hymenolepis microstoma (Nottingham strain): a classical tapeworm model for research in the genomic era. Parasites & Vectors 3, 123.CrossRefGoogle Scholar
de Amorin, A., Borba, H.R., Carauta, J.P., Lopes, D. & Kaplan, M.A. (1999) Anthelmintic activity of the latex of Ficus species. Journal of Ethnopharmacology 64, 255–258.CrossRefGoogle ScholarPubMed
de Rycke, P. (1966) Development of the cestode Hymenolepis microstoma in Mus musculus. Zeitschrift für Parasitenkunde 27, 350–354.CrossRefGoogle ScholarPubMed
Evans, W.S., Gray, B. & Novak, M. (1979) Effect of mebendazole on the larval development of three Hymenolepidid cestodes. Journal of Parasitology 65, 31–34.CrossRefGoogle ScholarPubMed
Evans, W.S., Hardy, M. & Novak, M. (1980) A comparison of the effect of albendazole, cambendazole, and thiabendazole on the larval development of three hymenolepidid cestodes. Journal of Parasitology 66, 935–940.CrossRefGoogle ScholarPubMed
Hansson, A., Veliz, G., Naquira, C., Amren, M., Arroyo, M. & Arevalo, G. (1986) Preclinical and clinical studies with latex from Ficus glabrata HBK, a traditional intestinal anthelminthic in the Amazonian area. Journal of Ethnopharmacology 17, 105–138.CrossRefGoogle ScholarPubMed
He, S., Tiuria, R. & Retnani, B.E. (1992) Uji biologis aktivitas anthelmintik sari buah nanas muda, daun miana dan ranting puring terhadap cacing Aspiculuris tetraptera (Nematoda) dan Hymenolepis nana pada mencit putih (Mus musculus albinus). Hemera Zoa 75, 94–110(in Indonesian).Google Scholar
Heyneman, D. (1961) Studies on helminth immunity. III. Experimental verification of autoinfection from cysticercoids of Hymenolepis nana in the white mouse. Journal of Infectious Diseases 109, 10–18.CrossRefGoogle ScholarPubMed
Heyneman, D. (1962) Studies on helminth immunity. I. Comparison between luminal and tissue phases of infection in the white mouse by Hymenolepis nana (Cestoda: Hymenolepididae). American Journal of Tropical Medicine and Hygiene 11, 46–63.CrossRefGoogle Scholar
Hopkins, C.A., Subramanian, G. & Stallard, H. (1972) The effect of immunosuppressants on the development of Hymenolepis diminuta in mice. Parasitology 65, 111–120.CrossRefGoogle ScholarPubMed
Isaak, D.D., Jacobson, R.H. & Reed, N.D. (1977) The course of Hymenolepis nana infections in thymus-deficient mice. International Archives of Allergy and Applied Immunology 55, 504–513.CrossRefGoogle ScholarPubMed
Levecke, B., Buttle, D.J., Behnke, J.M., Duce, I.R. & Vercruysse, J. (2014) Cysteine proteinases from papaya (Carica papaya) in the treatment of experimental Trichuris suis infection in pigs: two randomized controlled trials. Parasites & Vectors 7, 255.CrossRefGoogle ScholarPubMed
Luoga, W., Mansur, F., Buttle, D.J., Duce, I.R., Garnett, M.C. & Behnke, J.M. (2012) The anthelmintic efficacy of papaya latex in a rodent–nematode model is not dependent on fasting before treatment. Journal of Helminthology 86, 311–316.CrossRefGoogle Scholar
Luoga, W., Mansur, F., Buttle, D.J., Duce, I.R., Garnett, M.C., Lowe, A. & Behnke, J.M. (2014) The relative anthelmintic efficacy of plant-derived cysteine proteinases on intestinal nematodes. Journal of Helminthology in press.Google Scholar
Mansur, F., Luoga, W., Buttle, D.J., Duce, I.R., Lowe, A. & Behnke, J.M. (2014) The anthelmintic efficacy of natural plant cysteine proteinases against two rodent cestodes Hymenolepis diminuta and Hymenolepis microstoma in vitro. Veterinary Parasitology 201, 48–58.CrossRefGoogle ScholarPubMed
McCracken, R.O., Lipkowitz, K.B. & Dronen, N.O. (1992) Efficacy of albendazole and mebendazole against Hymenolepis microstoma and Hymenolepis diminuta. Parasitology Research 78, 108–111.CrossRefGoogle ScholarPubMed
Meana, A., Luzon, M., Corchero, J. & Gomez-Bautista, M. (1998) Reliability of coprological diagnosis of Anoplocephala perfoliata infection. Veterinary Parasitology 74, 79–83.CrossRefGoogle ScholarPubMed
Moss, G.D. (1971) The nature of the immune response of the mouse to the bile duct cestode, Hymenolepis microstoma. Parasitology 62, 285–294.CrossRefGoogle Scholar
Mursof, E.P. & He, S. (1991) A potential role of papaya latex as an anthelmintic against patent Ascaridia galli infection in chicken. Hemera Zoa 74, 11–20.Google Scholar
Nilsson, O., Ljungstrom, B.L., Hoglund, J., Lundquist, H. & Uggla, A. (1995) Anoplocephala perfoliata in horses in Sweden: prevalence, infection levels and intestinal lesions. Acta Veterinaria Scandinavica 36, 319–328.CrossRefGoogle ScholarPubMed
Proudman, C.J. & Edwards, G.B. (1992) Validation of a centrifugation/flotation technique for the diagnosis of equine cestodiasis. Veterinary Record 131, 71–72.CrossRefGoogle ScholarPubMed
Rawlings, N.D., Barrett, A.J. & Bateman, A. (2012) MERIOS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Research 40, D343–D350.CrossRefGoogle ScholarPubMed
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
Siles-Lucas, M. & Hemphill, A. (2002) Cestode parasites: application of in vivo and in vitro models for studies on the host–parasite relationship. Advances in Parasitology 51, 133–230.CrossRefGoogle ScholarPubMed
Smyth, J.D. & Clegg, J.A. (1959) Egg-shell formation in trematodes and cestodes. Experimental Parasitology 8, 286–323.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
Stepek, G., Lowe, A.E., Buttle, D.J., Duce, I.R. & Behnke, J.M. (2007c) In vitro anthelmintic effects of cysteine proteinases from plants against intestinal helminths of rodents. Journal of Helminthology 81, 353–360.CrossRefGoogle ScholarPubMed
Wharton, D. (1980) Nematode egg-shells. Parasitology 81, 447–463.CrossRefGoogle ScholarPubMed
Zucker, S., Buttle, D.J., Nicklin, M.J.H. & Barrett, A.J. (1985) The proteolytic activities of chymopapain, papain, and papaya proteinase III. Biochimica et Biophysica Acta (BBA) – Protein Structure and Molecular Enzymology 828, 196–204.CrossRefGoogle ScholarPubMed