Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-30T20:21:20.015Z Has data issue: false hasContentIssue false
  • English
  • Français

Hatching mechanism of the metacercaria of Plagiorchis species 1 (Trematoda: Plagiorchiidae)

Published online by Cambridge University Press:  05 June 2009

Dieter Bock
Dieter Bock*
Affiliation:
Universität Ulm, Sektion Elektronenmikroskopie, Oberer Eselsberg, D-7900 Ulm, Federal Republic of Germany
*
Tannenweg 55, D-2000 Hamburg 62, Federal Republic of Germany.
Get access Rights & Permissions [Opens in a new window]

Abstract

Metacercariae of Plagiorchis species 1 were observed to hatch by an active mechanism in a medium free of enzymes. A hatching opening in the bilayered cyst wall was formed by the combined action of caecal fluid extruded by the activated larva through the mouth opening and an internal pressure due to the tendency of the cyst wall to contract on hatching, resulting in an explosive expulsion of part of the metacercarial body. The cyst wall was apparently pierced at any place where the larva delivered its caecal fluid. After excystation the hatching medium contained high phosphatase and proteinase activities and was able to dissolve the inner walls of empty cyst envelopes. The phosphatase activity assayed on 4-methylumbelliferyl phosphate was optimal at pH 3–5. The proteolytic activity was demonstrable on photographic film, Azocoll, and synthetic chromogenic and fluorogenic peptides. A preference for peptides was found which are also susceptible to plasmin. The proteolytic activity was optimal at pH 3–9 and 40–45°C and, when assayed on Suc-Ala-Phe-Lys-MCA, was only due to thiol proteinase(s) according to inhibitor studies. It is suggested that the proteinase(s) represent the hatching enzyme(s) of the metacercaria, because (a) only proteolytic activity was detectable in the pH range optimal for excystment, (b) the inner cyst wall is stabilized by proteins, and (c) the inner wall is dissolved by other proteinases such as trypsin. Enzyme histochemical investigations of metacercariae showed that, in the caeca, acid phosphatase was present mainly before hatching and non-specific esterase developed after hatching. Proteolytic activity was not localized with the methods used although it was suggested that it derived from the caecal fluid. A possible relationship of the thiol proteinase(s) detected in the hatching medium to haemoglobin-digesting proteinases from the gut of schistosomes is discussed.

Keywords

Plagiorchismetacercariaeexcystationhatching mechanismhatching enzymethiol proteinasedigestive enzymecaecal fluidenzyme histochemistryhaemoglobinase
Type
Research Article
Information
Journal of Helminthology , Volume 63 , Issue 2 , June 1989 , pp. 153 - 171
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Asanji, M. F. & Williams, M. O. (1975) Studies on the excystment of trematode metacercariae in vitro. Zeitschrift für Parasitenkunde, 47, 151–163.Google Scholar
Barrett, A. J. (1977a) Introduction to the history and classification of tissue proteinases. In: Proteinases in Mammalian Cells and Tissues (editor, Barrett, A. J.) pp. 1–55. North Holland Publ. Co.: Amsterdam.Google Scholar
Barrett, A. J. (1977b) Cathepsin B and other thiol proteinases. In: Proteinases in Mammalian Cells and Tissues (editor, Barrett, A. J.) pp. 181–208. North Holland Publ. Co.: Amsterdam.Google Scholar
Bass, H. S. & Leflore, W. B. (1984) In vitro excystment of the metacercaria of Acanthoparyphium spinulosum (Trematoda: Echinostomatidae). Proceedings of the Helminthological Society of Washington, 51, 149–153.Google Scholar
Bird, A. F. (1968) Changes associated with parasitism in nematodes. III. Ultrastructure of the egg shell, larval cuticle, and contents of the subventral oesophagus glands in Meloidogyne javanica, with some observations on hatching. Journal of Parasitology, 54, 475–489.Google Scholar
Blair, D. (1976) Observations on the life-cycle of the strigeoid trematode Apatemon (Apatemon) gracilis (Rudolphi, 1819) Szidat, 1928. Journal of Helminthology, 50, 125–131.Google Scholar
Bock, D. (1984) The life cycle of Plagiorchis spec. 1, a species of the Plagiorchis elegans group (Trematoda, Plagiorchiidae). Zeitschrift für Parasitenkunde, 70, 359–373.Google Scholar
Bock, D. (1986) In vitro excystment of the metacercaria of Plagiorchis species 1 (Trematoda, Plagiorchiidae). International Journal for Parasitology, 16, 641–645.Google Scholar
Bock, D. (1988) Formation, histochemistry and ultrastructure of the metacercarial cyst wall of Plagiorchis species 1 (Trematoda, Plagiorchiidae). International Journal for Parasitology, 18, 379–388.Google Scholar
Bogitsh, B. J. (1975) Cytochemical observations on the gastrodermis of digenetic trematodes. Transactions of the American Microscopical Society, 94, 524–528.Google Scholar
Bogitsh, B. J. & Dresden, M. H. (1983) Fluorescent histochemistry of acid proteases in adult Schistosoma mansoni and Schistosoma japonicum. Journal of Parasitology, 69, 106–110.Google Scholar
Bogitsh, B. J. & Shannon, W. A. (1971) Cytochemical and biochemical observations on the digestive tracts of digenetic trematodes. VIII. Acid phosphatase activity in Schistosoma mansoni and Schistosomatium douthitti. Experimental Parasitology, 29, 337–347.Google Scholar
Croll, N. A. (1974) Necator americanus: activity patterns in the egg and the mechanism of hatching. Experimental Parasitology, 35, 80–85.Google Scholar
Crompton, D. W. T. (1973) The sites occupied by some parasitic helminths in the alimentary tract of vertebrates. Biological Reviews, 48, 27–83.Google Scholar
Davis, C. C. (1968) Mechanisms of hatching in aquatic invertebrate eggs. Oceanography and Marine Biology. An Annual Review, 6, 325–376.Google Scholar
Davis, D. A., Bogitsh, B. J. & Nunnally, D. A. (1969) Cytochemical and biochemical observations on the digestive tracts of digenetic trematodes. III. Nonspecific esterase in Haematoloechus medioplexus. Experimental Parasitology, 24, 121–129.Google Scholar
Dawes, B. (1961) On the early stages of Fasciola hepatica penetrating into the liver of an experimental host, the mouse. A histological picture. Journal of Helminthology, Suppl., 41–52.Google Scholar
Dixon, K. E. (1966) The physiology of excystment of the metacercaria of Fasciola hepatica L. Parasitology, 56, 431–456.Google Scholar
Documenta, Geigy (1960) Wissenschaftliche Tabellen (editor, J. R., Geigy, A. G.) Basle.Google Scholar
Dolbeare, F. A. & Smith, R. E. (1977) Flow cytometric measurement of peptidases with use of 5-nitrosalicylaldehyde and 4-methoxy-β-naphthylamine derivatives. Clinical Chemistry, 23, 1485–1491.CrossRefGoogle ScholarPubMed
Dresden, M. H. & Deelder, A. M. (1979) Schistosoma mansoni: Thiol proteinase properties of adult worm “hemoglobinase”. Experimental Parasitology, 48, 190–197.Google Scholar
Erasmus, D. A. & Bennett, L. J. (1965) A study of some of the factors affecting excystation in vitro of the metacercarial stages of Holostephanus lühei Szidat, 1936 and Cyathocotyle bushiensis Khan, 1962 (Strigeida: Trematoda). Journal of Helminthology, 39, 185–196.Google Scholar
Fashuyi, S. A. (1986) Excystment of the metacercaria of the trematode Mesocoelium monodi. International Journal for Parasitology, 16, 237–239.Google Scholar
Flegg, J. J. M. (1968) Embryogenic studies of some Xiphinema and Longidorus species. Nematologica, 14, 137–145.Google Scholar
Fried, B. & Butler, M. S. (1978) Infectivity, excystation, and development on the chick chorioallantois of the metacercaria of Echinostoma revolutum (Trematoda). Journal of Parasitology, 64, 175–177.Google Scholar
Fried, B., Leflore, W. B. & Bass, H. S. (1984) Histochemical localization of hydrolytic enzymes in the cercaria and excysted metacercaria of Echinostoma revolutum (Trematoda). Proceedings of the Helminthological Society of Washington, 51, 140–143.Google Scholar
Fried, B., Robbins, S. H. & Nelson, P. D. (1978) In vivo and in vitro excystation of Zygocotyle lunata (Trematoda) metacercariae and histochemical observations on the cyst. Journal of Parasitology, 64, 395–397.Google Scholar
Fripp, P. J. (1967) Histochemical localization of esterase activity in schistosomes. Experimental Parasitology, 21, 380–390.Google Scholar
Hagenmaier, H. E. (1974) The hatching process in fish embryos. V. Characterization of the hatching protease (chorionase) from the perivitelline fluid of the rainbow trout, Salmo gairdneri Rich, as a metalloenzyme. Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen, 175, 157–162.Google Scholar
Hamajima, F., Yamakami, K. & Fujino, T. (1985) Localization of a thiol protease in metacercarial lung fluke. Japanese Journal of Parasitology, 34, 507–508.Google Scholar
Hemenway, M. (1948) Studies on excystment of Clinostomum metacercariae by use of artificial digestion. Proceedings of the Iowa Academy of Science, 55, 375–381.Google Scholar
Hinck, L. W. & Ivey, M. H. (1976) Proteinase activity in Ascaris suum eggs, hatching fluid, and excretions-secretions. Journal of Parasitology, 62, 771–774.Google Scholar
Howell, M. J. (1970) Excystment of the metacercariae of Echinoparyphium serratum (Trematoda: Echinostomatidae). Journal of Helminthology, 44, 35–56.Google Scholar
Irwin, S. W. B. (1983) In vitro excystment of the metacercaria of Maritrema arenaria (Digenea: Microphallidae). International Journal for Parasitology, 13, 191–196.Google Scholar
Irwin, S. W. B., Mckerr, G., Judge, B. C. & Moran, J. (1984) Studies on metacercarial excystment in Himasthla leptosoma (Trematoda: Echinostomatidae) and newly emerged metacercariae. International Journal for Parasitology, 14, 415–421.Google Scholar
Iwanaga, S., Morita, T., Kato, H., Harada, T., Adachi, N., Sugo, T., Maruyama, I., Takada, K., Kimura, T. & Sakakibara, S. (1979) Fluorogenic peptide substrates for proteases in blood coagulation, kallikrein-kinin and fibrinolysis systems. In: Kinins II. Biochemistry, Pathophysiology, and Clinical Aspects (editors, Fujii, S., Moriya, H. & Suzuki, T.) pp. 147–163. Plenum Press: New York, London.Google Scholar
Jennings, J. B. & Leflore, W. B. (1972) The histochemical demonstration of certain aspects of cercarial morphology. Transactions of the American Microscopical Society, 91, 56–62.Google Scholar
Johnston, B. R. & Halton, D. W. (1981) Excystation in vitro of Bucephaloides gracilescens metacefcaria (Trematoda: Bucephalidae). Zeitschrift für Parasitenkunde, 65, 71–78.Google Scholar
Kafatos, F. C., Law, J. H. & Tartakoff, A. M. (1967) Cocoonase II. Substrate specificity, inhibitors and classification of the enzyme. Journal of Biological Chemistry, 242, 1488–1494.Google Scholar
Kirschner, K. & Bacha, W. J. (1980) Excystment of Himasthla quissetensis (Trematoda: Echinostomatidae) metacercariae in vitro. Journal of Parasitology, 66, 263–267.Google Scholar
Kojima, K., Kinoshita, H., Kato, T., Nagatsu, T., Takada, K. & Sakakibara, S. (1979) A new and highly sensitive fluorescence assay for collagenase-like peptidase activity. Analytical Biochemistry, 100, 43–50.Google Scholar
Lackie, A. M. (1975) The activation of infective stages of endoparasites of vertebrates. Biological Reviews, 50, 285–323.Google Scholar
Leflore, W. B. & Bass, H. S. (1983a) Observations on morphology and hydrolytic enzyme histochemistry of excysted metacercariae of Himasthla rhigedana (Trematoda: Echinostomatidae). International Journal for Parasitology, 13, 179–183.Google Scholar
Leflore, W. B. & Bass, H. S. (1983b) In vitro excystment of the metacercaria of Cloacitrema michiganensis (Trematoda, Philophthalmidae). Journal of Parasitology, 69, 200–204.Google Scholar
Lojda, Z., Gossrau, R. & Schiebler, T. H. (1976) Enzymhistochemische Methoden. Springer-Verlag: Berlin, Heidelberg, New York.Google Scholar
Mattler, L. E. & Bang, N. U. (1977) Serine protease specificity for peptide chromogenic substrates. Thrombosis and Haemostasis, 38, 776–792.Google Scholar
Meyer, M., Aurin, H. & RummelfÄnger, H. (1969) Die Schlüpfdrüse der Geburtshelferkröte Alytes o. obstericans und anderer Froschlurche. Ergebnisse der Anatomie und Entwicklungs-geschichte, 41, 1–64.Google Scholar
Mohandas, A. & Nadakal, A. M. (1978) In vivo development of Echinostoma malayanum Leiper, 1911 with notes on effects of population density, chemical composition and pathogenicity and in vitro excystment of the metacercaria (Trematoda: Echinostomatidae). Zeitschrift für Parasitenkunde, 55, 139–151.Google Scholar
Needham, J. (1963) Chemical Embryology. Vol. III. Hafner Publishing Co.: New York, London.Google Scholar
Nieuwenhuizen, W., WIJNGAARDS, G. & GROENEVELD, E. (1977) Fluorogenic peptide amide substrates for the estimation of plasminogen activators and plasmin. Analytical Biochemistry, 83, 143–148.Google Scholar
Pearse, A. G. E. (1972) Histochemistry Theoretical and Applied. Vol. 2. Churchill Livingstone: Edinburgh, London.Google Scholar
Perry, R. N. & Clarke, A. J. (1981) Hatching mechanisms of nematodes. Parasitology, 83, 435–449.Google Scholar
Pierzchala, P. A., Dorn, C. P. & Zimmerman, M. (1979) A new fluorogenic substrate for plasmin. Biochemical Journal, 183, 555–559.CrossRefGoogle ScholarPubMed
Pike, A. W. & Erasmus, D. A. (1967) The formation, structure and histochemistry of the metacercarial cyst of three species of digenetic trematodes. Parasitology, 57, 683–694.Google Scholar
Rees, G. (1967) The histochemistry of the cystogenous gland and cyst wall of Parorchis acanthus Nicoll, and some details of the morphology and fine structure of the cercaria. Parasitology, 57, 87–110.Google Scholar
Robbins, K. C. & Summaria, L. (1976) Plasminogen and plasmin. In: Methods in Enzymology, Vol. 45 (editor, Lorand, L.) pp. 257–273. Academic Press: New York, San Francisco, London.Google Scholar
Rogers, W. P. (1982) Enzymes in the exsheathing fluid of nematodes and their biological significance. International Journal for Parasitology, 12, 495–502.Google Scholar
Sullivan, C. H. & Bonar, D. B. (1984) Biochemical characterization of the hatching process of Ilyanassa obsoleta. The Journal of Experimental Zoology, 229, 223–234.Google Scholar
Taylor, D. P. (1962) Effect of temperature on hatching of Aphelenchus avenae eggs. Proceedings of the Helminthological Society of Washington, 29, 52–54.Google Scholar
Thompson, M. & Halton, D. W. (1982) Observations on excystment in vitro of Cotylurus variegatus metacercariae (Trematoda: Strigeidae). Zeitschrift für Parasitenkunde, 68, 201–209.Google Scholar
Tverdokhlebov, P. T. (1984) Morfologiya stenki tsisty i mekhanizm ekstsistirovaniya metatser-karii Dicrocoelium lanceatum [Morphology of the cyst wall and excystment mechanisms of Dicrocoelium lanceatum metacercariae]. In: Gel'minty sel'skokhozyaistvennykh i okhotnich'e-promyslovykh zhivotnykh (editor, Sonin, M. D.) pp. 189–198. Nauka: Moscow.Google Scholar
Urch, U. A. & Hedrick, J. L. (1981) Isolation and characterization of the hatching enzyme from the amphibian Xenopus laevis. Archives of Biochemistry and Biophysics, 206, 424–431.Google Scholar
Wilson, R. A. (1968) The hatching mechanism of the egg of Fasciola hepatica L. Parasitology, 58, 79–89.Google Scholar
Yamakami, K. (1986) Purification and properties of a thiol protease from lung fluke adult Paragonimus ohirai. Comparative Biochemistry and Physiology B, 83, 501–506.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 B, 87, 643–648.Google Scholar
ŽDÁrskÁ, Z. (1970) The gland cells of the cercaria of Notocotylus attenuatus (Rudolphi, 1809) and the cyst wall of its adolescaria. Folia Parasitologica, 17, 31–47.Google Scholar
ŽDÁrskÁ, Z. & Soboleva, T. N. (1981a) Morphology and histochemistry of the cercaria and metacercaria of Hasstilesia ovis (Orloff, Erschoff et Badanin, 1914). Folia Parasitologica, 28, 288.Google Scholar
ŽDÁrskÁ, Z. & Soboleva, T. N. (1981b) Histochemistry of the sporocyst and metacercaria of Leucochloridium paradoxum Carus, 1833. Folia Parasitologica, 28, 221–226.Google Scholar
Ždárská, Z., Soboleva, T. N. & Osipovskaya, L. L. (1984) Histochemical and morphological studies on the metacercaria and sporocyst sacs of Leucochloridium perturbatum. Folia Parasitologica, 31, 29–36.Google Scholar
Zimmerman, M., Ashe, B., Yurewicz, E. C. & Patel, G. (1977) Sensitive assays for trypsin, elastase, and chymotrypsin using new fluorogenic substrates. Analytical Biochemistry, 78, 47–51.Google Scholar
Zimmerman, M., Quigley, J. P., Ashe, B., Dorn, C., Goldfarb, R. & Troll, W. (1978) Direct fluorescent assay of urokinase and plasminogen activators of normal and malignant cells: kinetics and inhibitor profiles. Proceedings of the National Academy of Sciences of the USA, 75, 750–753.Google Scholar