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Effect of the Eubothrium rugosum (Cestoda) Extract on Intestinal Proteolytic Activity in Various Fish Species

  • Comparative and Ontogenic Biochemistry
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Abstract

The extract of the fish tapeworm Eubothrium rugosum was found to inhibit activity of intestinal proteases in its host, the burbot. A decrease in proteolytic activity of the intestinal mucosa, when using the E. rugosum extract as an inhibitor, is comparable with that of a serine protease inhibitor PMSF. This implies that the tapeworm-produced inhibitor inactivates major intestinal serine proteases, trypsin and chymotrypsin. The tapeworm extract was also demonstrated to inhibit proteolytic activity in the intestinal mucosa of the two other fish species, zope and bream. Using the Gini index, it was found that the distribution of percent inhibition levels shows some nonuniformity across the given set of species. Namely, the tapeworm extract exerts a more selective inhibitory effect on intestinal proteases in different fish species as compared to PMSF. This indicates a partial though quite explicit species-specific selectivity of the tapeworm-produced inhibitor toward the host’s proteolytic activity which may contribute to the formation of specific host-parasite interrelationships.

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References

  1. Pappas, P.W. and Uglem, G.L., Hymenolepis diminuta (Cestoda) liberates an inhibitor of proteolytic enzymes during in vitro incubation, Parasitol., 1990, vol. 101, pp. 455–464.

    Article  CAS  Google Scholar 

  2. Rawlings, N.D., Tolle, D.P., and Barrett, A.J., Evolutionary families of peptidase inhibitors, Biochem. J., 2004, vol. 378, pp. 705–716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Molehin, A.J., Gobert, G.N., and McManus, D.P., Serine protease inhibitors of parasitic helminthes, Parasitol., 2012, vol. 139, no. 6, pp. 681–95.

    Article  CAS  Google Scholar 

  4. Izvekova, G.I. and Frolova, T.V., Proteolytic enzymes and their inhibitors in Cestodes, Biol. Bull. Rev., 2017, vol. 7, pp. 150–159.

    Article  Google Scholar 

  5. Pappas, P.W. and Read, C.P., Trypsin inactivation by intact Hymenolepis diminuta, J. Parasitol., 1972, vol. 58, pp. 864–871.

    Article  CAS  Google Scholar 

  6. Schroeder, L.L., Pappas, P.W., and Means, G.E., Trypsin inactivation by intact Hymenolepis diminuta (Cestoda): some characteristics of the inactivated enzyme, J. Parasitol., 1981, vol. 67, no. 3, pp. 378–385.

    Article  CAS  PubMed  Google Scholar 

  7. Klimenko, V.V. and Ķĕniņa, V.A., On the influence of phylogeny and ecology on some biochemical mechanisms of helminth adaptation, Izv. Akad. Nauk Latv. SSR, 1971, no. 11, pp. 93–96.

    Google Scholar 

  8. Dubovskaya, A.Ya., A study of proteolytic activity in some species of Cestoda, Parazitol., 1973, vol. VII, no. 2, pp. 154–159.

    Google Scholar 

  9. Alarcón, F.J., Martínez, T.F., Barranco, P., Cabello, T., Díaz, M., and Moyano, F.J., Digestive proteases during development of larvae of red palm weevil, Rhynchophorus errugineus (Olivier, 1790) (Coleoptera: Curculionidae), Insect Biochem. Mol. Biol., 2002, vol. 32, pp. 265–274.

    Article  PubMed  Google Scholar 

  10. Graczyk, P., Gini coefficient: a new way to express kinase selectivity against a family of kinases, J. Med. Chem., 2007, vol. 50, pp. 5773–5779.

    Article  CAS  PubMed  Google Scholar 

  11. Natalia, Y., Hashim, R., Ali, A., and Chong, A., Characterization of digestive enzymes in a carnivorous ornamental fish, the Asian bony tongue Scleropages formosus (Osteoglossidae), Aquacult., 2004, vol. 233, pp. 305–320.

    Article  CAS  Google Scholar 

  12. Ugolev, A.M. and Kuz’mina, V.V., Pishchevaritel’nye protsessy i adaptatsii u ryb (Digestive Processes and Fish Adaptations), St. Petersburg, 1993.

    Google Scholar 

  13. Solovyev, M.M., Kashinskaya, E.N., Izvekova, G.I., Gisbert, E., and Glupov, V.V., Feeding habits and ontogenic changes in digestive enzyme patterns in five freshwater teleosts, J. Fish Biol., 2014, vol. 85, no. 5, pp. 1395–412.

    Article  CAS  PubMed  Google Scholar 

  14. Dimes, L.E., Garcia-Carreno, F.L., and Haard, N.F., Estimation of protein digestibility-III. Studies on the digestive enzymes from the pyloric ceca of rainbow trout and salmon, Comp. Biochem. Physiol., 1994, vol. 109A, no. 2, pp. 349–360.

    Article  CAS  Google Scholar 

  15. Kumar, S., Garcia-Carreño, F.L., Chakrabarti, R., Toro, M.A.N., and Córdova-Murueta, J.H., Digestive proteases of three carps Catla catla, Labeo rohita and Hypophthalmichthys molitrix: partial characterization and protein hydrolysis efficiency, Aquacult. Nut., 2007, vol. 13, pp. 381–388.

    Article  CAS  Google Scholar 

  16. Concha-Frias, B., Alvarez-González, C.A., Gaxiola-Cortes, M.G., Silva-Arancibia, A.E., Toledo-Agüero, P.H., Martínez-García, R., Camarillo-Coop, S., Jimenez-Martinez, L.D., and Arias-Moscoso, J.L., Partial characterization of digestive proteases in the common snook Centropomus undecimalis, Int. J. Biol., 2016, vol. 8, no. 4, pp. 1–11.

    Article  CAS  Google Scholar 

  17. Pujante, I.M., Díaz-López, M., Mancera, J.M., and Moyano, F.J., Characterization of digestive enzymes protease and alpha-amylase activities in the thick-lipped grey mullet (Chelon labrosus, Risso 1827), Aquacult. Res., 2016, pp. 1–10.

    Google Scholar 

  18. Munilla-Morán, R. and Saborido-Rey, F., Digestive enzymes in marine species. I. Proteinase activities in gut from redfish (Sebastes mentella), seabream (Sparus aurata) and turbot (Scophthalmus maximus), Comp. Biochem. Physiol., 1996, vol. 113B, no. 2, pp. 395–402.

    Article  Google Scholar 

  19. GarcΓía-Carreño, F.L., Albuquerque-Cavalcanti, C., Navarrete del Toroa, M.A., and Zaniboni-Filho, E., Digestive proteinases of Brycon orbignyanus (Characidae, Teleostei): characteristics and effects of protein quality, Comp. Biochem. Physiol., 2002, vol. 132B, pp. 343–352.

    Article  Google Scholar 

  20. Martzen, M.R., Geise, G.L., Hogan, B.J., and Peanasky, A.J., Ascaris suum: localization by lmmunochemical and fluorescent probes of host proteases and parasite proteinase inhibitors in cross-sections, Exp. Parasitol., 1985, vol. 60, pp. 139–149.

    Article  CAS  PubMed  Google Scholar 

  21. Matskási, I. and Juhász, S., Ligula intestinalis (L., 1758): investigation on plerocercoids and adults for protease and protease inhibitor activities, Parasitol. Hung., 1977, vol. 10, pp. 51–60.

    Google Scholar 

  22. Matskási, I., The effect of Bothriocephalus acheilognati Yamaguti, 1934, infection on the protease activity in the gut of carp fry, Parasitol. Hung., 1978, vol. 11, pp. 51–56.

    Google Scholar 

  23. Hawley, J.H. and Peanasky, A.J., Ascaris suum: are trypsin inhibitors involved in species specificity of ascarid nematodes? Exp. Parasitol., 1992, vol. 75, pp. 112–118.

    Article  CAS  PubMed  Google Scholar 

  24. Németh, I., Juhász, S., and Baintner, K., A trypsin and chymotrypsin inhibitor from Taenia pisiformis, Int. J. Parasitol., 1979, vol. 9, iss. 6, pp. 515–522.

    Article  PubMed  Google Scholar 

  25. Merckelbach, A. and Ruppel, A., Biochemical properties of an intracellular serpin from Echinococcus multilocularis, Mol. Biochem. Parasitol., 2007, vol. 156, pp. 84–88.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Russia

    G. I. Izvekova, T. V. Frolova & E. I. Izvekov

  2. Institute of Biology, Karelian Research Center, Russian Academy of Sciences, Petrozavodsk, Russia

    A. N. Parshukov

  3. Institute of Animal Systematics and Ecology, Russian Academy of Sciences, Novosibirsk, Russia

    M. M. Solovyev

  4. Tomsk State University, Tomsk, Russia

    M. M. Solovyev

Authors
  1. G. I. Izvekova
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  2. T. V. Frolova
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  3. E. I. Izvekov
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  4. A. N. Parshukov
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  5. M. M. Solovyev
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Correspondence to E. I. Izvekov.

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Russian Text © G.I. Izvekova, T.V. Frolova, E. I. Izvekov, A.N. Parshukov, M.M. Solovyev, 2019, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2019, Vol. 55, No. 1, pp. 4350.

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Izvekova, G.I., Frolova, T.V., Izvekov, E.I. et al. Effect of the Eubothrium rugosum (Cestoda) Extract on Intestinal Proteolytic Activity in Various Fish Species. J Evol Biochem Phys 55, 47–54 (2019). https://doi.org/10.1134/S002209301901006X

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  • DOI: https://doi.org/10.1134/S002209301901006X

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