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Cytochemical localization of cytochrome c oxidase activity in mitochondria in the tegument and tegumental and parenchymal cells of the trematodes Echinostoma trivolvis, Zygocotyle lunata, Schistosoma mansoni, Fasciola gigantica and Paragonimus ohirai

Published online by Cambridge University Press:  05 June 2009

T. Fujino
Affiliation:
Department of Parasitology, Faculty of Medicine, Kyushu University, 812 Fukuoka, Japan
B. Fried
Affiliation:
Department of Biology, Lafayette College, Easton, Pennsylvania 18042, USA
S. Takamiya
Affiliation:
Department of Parasitology, Juntendo University School of Medicine, 113 Tokyo, Japan

Abstract

Cytochrome c oxidase in the mitochondria of the tegument and tegumental and parenchymal cells was examined cytochemically in Echinostoma trivolvis, Zygocotyle lunata, Schistosoma mansoni, Fasciola gigantica and Paragonimus ohirai, trematodes that inhabit different sites in their vertebrate hosts. Clear differences in enzyme activity occurred in the mitochondria of these species, probably reflecting the different energy metabolisms of these worms. Marked aerobic metabolism occurred in S. mansoni and P. ohirai adults that inhabit the host mesenteric veins and the lungs, respectively. The tegument and parenchymal cells of S. mansoni possess relatively few, small mitochondria with tubular cristae which are heavily reactive for cytochrome c oxidase. In P. ohirai, the activity for cytochrome c oxidase in tegumental mitochondria increased gradually from juveniles to adults, reflecting that the respiratory activity increased with growth and the aerobic metabolism is activated when the worms reach the lung. P. ohirai juveniles and adults had two types of mitochondria with different shapes and enzyme activities that were located in two different types of parenchymal cells. The intestinal species, E. trivolvis had mitochondria in the basal aspect of the tegument, and some variations in enzyme activity of their mitochondria in the tegumental and parenchymal cells were observed, suggesting that they possess both aerobic and anaerobic metabolic systems. Z. lunata that live in rodent caeca are devoid of mitochondria in the tegument and have many characteristic mitochondria with undeveloped cristae in the parenchymal cells. Mitochondria of F. gigantica showed weak or no activity for cytochrome c oxidase, suggesting that the worm is well-adapted to an anaerobic environment in the host bile duct.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 1995

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References

Foster, L.A., Chen, G.-Z., VandeWaa, E.A.Pax, R.A. & Bennett, J.L. (1989) Glutamine- vs glucose-supported motor activity in Schistosoma mansoni: physiological relevance of aerobic metabolism. Experimental Parasitology 69, 4453.CrossRefGoogle ScholarPubMed
Fry, M. & Beesley, J.E. (1985) Cytochemical localization of cytochrome oxidase in tissues of parasitic nematodes. Parasitology 90, 145156.CrossRefGoogle Scholar
Fujino, T. & Fried, B. (1993) Expulsion of Echinostoma trivolvis (Cort, 1914) Kanev, 1985 and retention of E. caproni Richard, 1964 (Trematoda: Echinostomatidae) in C3H mice: pathological, ultrastructural, and cytochemical effects on the host intestine. Parasitology Research 79, 286292.CrossRefGoogle ScholarPubMed
Fukuda, K. (1986) Differentiation and degeneration of tegumental cells in adult lung flukes, Paragonimus species (Trematoda: Troglotrematidae). International Journal for Parasitology 16, 147156.Google ScholarPubMed
Hamajima, F., Fujino, T., Yamagami, K. & Fukuda, K. (1982) Mitochondria in the body wall of life cycle stages of lung flukes of the genus Paragonimus, and mitochondrial cytochrome components of the adult worm. Comparative Biochemistry and Physiology 71A, 149156.Google Scholar
Irwin, S.W.B., McCloughlin, T.J.J. & Fried, B. (1991) Scanning and transmission electron microscopical observations on the tegument of excysted metacercariae and adults of Zygocotyle lunata. Journal of Helminthology 65, 270274.CrossRefGoogle ScholarPubMed
Robinson, R.D. & Halton, D.W. (1983) Functional morphology of the tegument of Corrigia vitta (Trematoda: Dicroceoliidae). Zeitschrift für Parasitenkunde 69, 319333.CrossRefGoogle Scholar
Takamiya, S., Wang, H., Hiraishi, A., Yu, Y., Hamajima, E & Aoki, T. (1994) Respiratory chain of the lung fluke Paragonimus westermani: facultative anaerobic mitochondria. Archives of Biochemistry and Biophysics 312, 142150.CrossRefGoogle ScholarPubMed
Tielens, A.G.M. (1994) Energy generation in parasitic helminths. Parasitology Today 10, 346352.CrossRefGoogle ScholarPubMed
Tielens, A.G.M., van der Meer, P. & van den Bergh, S.G. (1981) The aerobic energy metabolism of the juvenile Fasciola hepatica. Molecular and Biochemical Parasitology 3, 205214.CrossRefGoogle ScholarPubMed
Tielens, A.G.M., van der Heuvel, J.M. & van den Bergh, S.C. (1984) The energy metabolism of Fasciola hepatica during its development in the final host. Molecular and Biochemical Parasitology 13, 301307.CrossRefGoogle ScholarPubMed
Tielens, A.G.M., van der Heuvel, J.M. & van den Bergh, S.G. (1987) Differences in intermediary energy metabolism between juvenile and adult Fasciola hepatica. Molecular and Biochemical Parasitology 24, 273281.CrossRefGoogle ScholarPubMed
Tielens, A.C.M. & van den Bergh, S.G. (1993) Aerobic and anaerobic energy metabolism in the life cycle of parasitic helminths. pp. 1940in Hochachka, P.W., Lutz, P.L., Sick, T., Rosenthal, M. & van den Thillart, C. (Eds) Surviving hypoxia. Mechanisms of control and adaptation. CRC Press.Google Scholar
Van Oordt, B.E.P., van den Heuvel, J.M., Tielens, A.G.M. & van den Bergh, S.G. (1985) The energy production of the adult Schistosoma mansoni is for a large part aerobic. Molecular and Biochemical Parasitology 16, 117126.CrossRefGoogle ScholarPubMed
Van Oordt, B.E.P., Tielens, A.G.M. & van den Bergh, S.G. (1988) The energy metabolism of Schistosoma mansoni during its development in the hamster. Parasitology Research 75, 3135.CrossRefGoogle ScholarPubMed