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Involvement of cysteine proteinases in excystment of Paragonimus ohirai metacercariae induced by sodium cholate and A23187

Published online by Cambridge University Press:  12 April 2024

T. Ikeda*
Affiliation:
Department of Medical Zoology, Kanazawa Medical University, Uchinada, Ishikawa, 920-0293, Japan
*
*Fax: +81 76 218 8336 Email: ikeda@kanazawa-med.ac.jp

Abstract

The involvement of intrinsic proteinases in the excystment of Paragonimus ohirai metacercariae was studied in in vitro excystment induced by sodium (Na) cholate, a bile salt and A23187, a Ca2+ ionophore. The effects of various proteinase inhibitors on the in vitro excystment were examined and similar inhibitory profiles were obtained. Benzyloxycarbonyl-L-leucyl-L-leucinal (Z-Leu-Leu-H), a cysteine proteinase inhibitor and 4-(2-aminoethyl)-benzenesulfonyl fluoride (Pefabloc SC), a serine proteinase inhibitor completely inhibited excystment, while L-3-carboxy-2,3-trans-epoxypropionyl-leucylamido (4-guanidino)-butane (E-64), a cysteine proteinase inhibitor and leupeptin, a cysteine/serine proteinase inhibitor permitted partial excystment at a lower rate, but inhibited it from proceeding from the partial excystment stage. In secretions released from metacercariae during excystment, proteinase activities detected towards various fluorogenic peptidyl substrates were almost completely inhibited by Z-Leu-Leu-H and E-64, but not by Pefabloc SC. Sodium cholate induced a higher secretion of cysteine proteinases and a higher rate of excystment than A23187. Profiles of cysteine proteinase activities towards five peptidyl substrates detected were markedly different among the two secretions and the lysate of newly excysted juveniles. Newly excysted juveniles released cysteine proteinases with similar activity profiles and levels to metacercariae induced by Na cholate-incubation, whereas the release of cysteine proteinases was reduced compared with metacercariae induced by A23187-incubation. These results provide valuable information about the involvement of intrinsic proteinases in metacercarial excystment.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2003

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References

Bock, D. (1989) Hatching mechanism of the metacercaria of Plagiorchis species 1 (Trematoda: Plagiorchiidae). Journal of Helminthology 63, 153171.CrossRefGoogle Scholar
Butler, R., Michel, A., Kunz, W. & Klinkert, M.Q. (1995) Sequence of Schistosoma mansoni cathepsin C and its structural comparison with papain and cathepsins B and L of the parasite. Protein and Peptide Letters 2, 313320.CrossRefGoogle Scholar
Carmona, C., Dowd, A.J., Smith, A.M. & Dalton, J.P. (1993) Cathepsin L proteinase secreted by Fasciola hepatica in vitro prevents antibody-mediated eosinophil attachment to newly excysted juveniles. Molecular and Biochemical Parasitology 62, 918.CrossRefGoogle ScholarPubMed
Chung, Y.B., Kong, Y., Joo, I.J., Cho, S.Y. & Kang, S.Y. (1995) Excystment of Paragonimus westermani metacercariae by endogenous cysteine protease. Journal of Parasitology 81, 137142.CrossRefGoogle ScholarPubMed
Chung, Y.B., Kong, Y., Yang, H.J., Kang, S.Y. & Cho, S.Y. (1997) Cysteine protease activities during maturation stages of Paragonimus westermani . Journal of Parasitology 83, 902907.CrossRefGoogle ScholarPubMed
Dalton, J.P. & Heffernan, M. (1989) Thiol proteases released in vitro by Fasciola hepatica . Molecular and Biochemical Parasitology 35, 161166.CrossRefGoogle ScholarPubMed
Dixon, K.E. (1965) The structure and histochemistry of the cyst wall of the metacercaria of Fasciola hepatica L. Parasitology 55, 215226.CrossRefGoogle ScholarPubMed
Dowd, A.J., Smith, A.M., McGonigle, S. & Dalton, J.P. (1994) Purification and characterization of a second cathepsin L proteinase secreted by the parasitic trematode Fasciola hepatica . European Journal of Biochemistry 223, 9198.CrossRefGoogle ScholarPubMed
El-Mayas, H. & Kearn, G.C. (1995) In vitro excystment of the metacercaria of Cryptocotyle concavum from the common goby Pomatoschistus microps . Journal of Helminthology 69, 285297.CrossRefGoogle Scholar
Fried, B. (1994) Metacercariae excystment of trematodes. Advances in Parasitology 33, 91144.CrossRefGoogle Scholar
Hamajima, F., Yamakami, K. & Fujino, T. (1985) Localization of a thiol protease in metacercarial lung fluke. Japanese Journal of Parasitology 34, 507508.Google Scholar
Heussler, V.T. & Dobbelaere, D.A.E. (1994) Cloning of a protease gene family of Fasciola hepatica by the polymerase chain reaction. Molecular and Biochemical Parasitology 64, 1123.CrossRefGoogle ScholarPubMed
Ikeda, T. & Oikawa, Y. (1991) Paragonimus ohirai: immunobiochemical characterization on the tegumental glycocalyx of excysted juvenile recognized by a monoclonal antibody. Experimental Parasitology 72, 252261.CrossRefGoogle ScholarPubMed
Ikeda, T. (2001a) Effect of ionophores on in vitro excystment of Paragonimus ohirai metacercariae. Parasitology Research 87, 343344.CrossRefGoogle ScholarPubMed
Ikeda, T. (2001b) Protein A immunocapture assay detecting antibodies to fluke cysteine proteinases for immunodiagnosis of human paragonimiasis and fascioliasis. Journal of Helminthology 75, 245249.Google ScholarPubMed
Intapan, P.M. & Maleewong, W. (2001) In vitro excystation of Paragonimus heterotremus metacercariae. Journal of Parasitology 87, 11841186.CrossRefGoogle ScholarPubMed
Klinkert, M-Q., Felleisen, R., Link, G., Ruppel, A. & Beck, E. (1989) Primary structures of Sm31/32 diagnostic proteins of Schistosoma mansoni and their identification as proteases. Molecular and Biochemical Parasitology 33, 113122.CrossRefGoogle ScholarPubMed
Lackie, A.M. (1975) The activation of infective stages of endoparasites of vertebrates. Biological Reviews 50, 285323.CrossRefGoogle ScholarPubMed
Merckelbach, A., Hasse, S., Dell, R., Eschlbeck, A. & Ruppel, A. (1994) cDNA sequences of Schistosoma japonicum coding for two cathepsin B-like proteins and Sj32. Tropical Medicine and Parasitology 45, 193198.Google ScholarPubMed
Oshima, T., Yoshida, Y. & Kihata, M. (1958) Studies on the excystation of the metacercariae of Paragonimus westermani. (1) Especially on the effect of bile salts. Bulletin of the Institute for Public Health (Tokyo) 7, 256269.Google Scholar
Smith, A.M., Dowd, A.J., McGonigle, S., Keegan, P.S., Brennan, G., Trudgett, A. & Dalton, J.P. (1993) Purification of a cathepsin L-like proteinase secreted by adult Fasciola hepatica . Molecular and Biochemical Parasitology 62, 18.CrossRefGoogle ScholarPubMed
Smith, A.M., Dalton, J.P., Clough, K.A., Kilbane, C.L., Harrop, S.A., Hole, N. & Brindley, P.J. (1994) Adult Schistosoma mansoni express cathepsin L proteinase activity. Molecular and Biochemical Parasitology 67, 1119.CrossRefGoogle ScholarPubMed
Sommerville, R.I. & Rogers, W.P. (1987) The nature and action of host signals. Advances in Parasitology 26, 239293.CrossRefGoogle ScholarPubMed
Sukhdeo, M.V.K. & Mettrick, D.F. (1986) The behavior of juvenile Fasciola hepatica . Journal of Parasitology 72, 492497.CrossRefGoogle ScholarPubMed
Yamakami, K. (1986) Purification and properties of a thiol protease from lung fluke adult Paragonimus ohirai . Comparative Biochemistry and Physiology 83B, 501506 Google Scholar
Yamakami, K. & Hamajima, F. (1987) Purification and properties of a neutral thiol protease from larval trematode parasite Paragonimus westermani metacercariae. Comparative Biochemistry and Physiology 87B, 643648.Google Scholar
Yamakami, K. & Hamajima, F. (1988) Proteolytic activity of secretions from newly excysted metacercariae of Paragonimus westermani . Japanese Journal of Parasitology 37, 380384.Google Scholar
Yamakami, K., Hamajima, F., Akao, S. & Tadakuma, T. (1995) Purification and characterization of acid cysteine protease from metacercariae of the mammalian trematode parasite Paragonimus westermani . European Journal of Biochemistry 233, 490497.CrossRefGoogle ScholarPubMed
Yun, D.H., Chung, J.Y., Chung, Y.B., Bahk, Y.Y., Kang, S.Y., Kong, Y. & Cho, S.Y. (2000) Structural and immunological characteristics of a 28-kilodalton cruzipain-like cysteine protease of Paragonimus westermani expressed in the definitive host stage. Clinical and Diagnostic Laboratory Immunology 7, 932939.CrossRefGoogle ScholarPubMed