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Biochemical surface components of Brugia pahangi microfilariae

Published online by Cambridge University Press:  06 April 2009

G. Sayers ,
C. D. Mackenzie  and
D. A. Denham
G. Sayers
Affiliation:
Wolfson Tropical Pathology Unit and Medical Helminthology, London School of Hygiene and Tropical Medicine, London
C. D. Mackenzie
Affiliation:
Wolfson Tropical Pathology Unit and Medical Helminthology, London School of Hygiene and Tropical Medicine, London
D. A. Denham
Affiliation:
Wolfson Tropical Pathology Unit and Medical Helminthology, London School of Hygiene and Tropical Medicine, London
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Summary

The sheath and cuticle of microfilariae of Brugia pahangi were examined by electron microscopy and the presence of various proteins, carbohydrate and enzymes sought. The epicuticle of microfilariae consists of a pentalaminate structure (24·0 ± 1·4 nm), a cortex (13·7 ± 3·6 nm) and a basal zone (27·8 ±4·8 nm) which is often banded in appearance. The pentalaminate layers are not continuous at the base of the interannular grooves. The sheath and the epicuticle of B. pahangi stained positively with concanavalin A and saccharated iron oxide. The sheath of approximately 50% of microfilariae showed activity for acid phosphatase, 5′ nucleotidase and peroxidase, but not for ATPases, alkaline phosphatase or esterase. No enzymes were detected in the epicuticle although the cortex and basal layers of the cuticle did show enzymic activity. Structures beneath the cuticle in the main body of the worms contained considerable enzymic activity. Microfilariae directly isolated from the blood of infected cats were found by immunochemical means to carry serum proteins on their sheaths but not on their cuticles. These studies extend the definition of the outer structures of microfilariae and confirm that they significantly differ in morphology and enzyme content from typical mammalian cell membranes.

Type
Research Article
Information
Parasitology , Volume 89 , Issue 3 , December 1984 , pp. 425 - 434
Copyright
Copyright © Cambridge University Press 1984

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References

REFERENCES

Axline, S. G. (1970). Functional biochemistry of the macrophage. Seminars in Hematology 7, 142–60.Google ScholarPubMed
Bainton, D. F. & Farquhar, M. G. (1968). Differences in enzyme content of azurophil and specific granules of polymorphonuclear leukocytes. II. Cytochemistry and electron microscopy of bone marrow cells. Journal of Cell Biology 39, 229–317.Google ScholarPubMed
Bird, A. F. (1979). Ultrastructure of the tail region of the second stage preparasitic larva of the root-knot nematode. International Journal for Parasitology 9, 357–70.CrossRefGoogle Scholar
Cherian, P. V., Stromberg, B. E., Weiner, D. J. & Soulsby, E. J. L. (1980). Fine structure and cytochemical evidence for the presence of polysaccharide surface coat of Dirofilaria immitis microfilariae. International Journal for Parasitology 10, 227–33.Google Scholar
Choi, J. (1965). Electron microscopy of absorption of tracer materials by toad urinary bladder epithelium. Journal of Cell Biology 25, 175–92.Google Scholar
Cline, M. J. (1975). The White Cell, pp. 39–70. Harvard University Press, Massachusetts.Google Scholar
Daveney, E. & Howells, R. C. (1979). The exsheathment of Brugia pahangi microfilariae under controlled conditions. Annals of Tropical Medicine and Hygiene 73, 227–33.Google Scholar
Ernst, S. A. (1972 a). Transport of adenosine triphosphate cytochemistry. I. Biochemical characterization of ouabain-sensitive, potassium-dependent phosphatase activity in secretory epithelium of the avian salt gland. Journal of Histochemistry and Cytochemistry 20, 23–38.Google Scholar
Ernst, S. A. (1972 b). Transport of adenosine triphosphatase cytochemistry. 11. Cytochemical localization of ouabain-sensitive, potassium-dependent phosphatase activity in secretory epithelium of the avian salt gland. Journal of Histochemistry and Cytochemistry 20, 23–38.Google Scholar
Furman, A. & Ash, L. R. (1983). Analysis of Brugia pahangi microfilariae surface carbohydrates: comparison of the binding of a panel of fluoresceinated lectins to mature in vivo-derivecl and immature in utero-derived microfilariae. Acta Tropica 40, 45–51.Google ScholarPubMed
Gasic, G. & Berwick, L. (1963). Hale stain for sialic acid containing mucins. Journal of Cell Biology 19, 223–8.Google Scholar
Graham, R. C. & Karnovsky, M. J. (1966). The early stages of absorption of infected horse-radish peroxidase in the proximal tubules of mouse kidney: Ultrastructural cytochemistry by a new technique. Journal of Histochemistry and Cytochemistry 14, 291–302.CrossRefGoogle Scholar
Howells, R. E. & Chen, S. N. (1981). Brugia pahangi: Feeding and nutrient uptake in vitro and in vivo. Experimental Parasitology 51, 42–58.CrossRefGoogle ScholarPubMed
Hugon, J. S. & Borger, M. (1966). A direct lead method for electron microscopic visualization of alkaline phosphatase activity. Journal of Histochemistry and Cytochemistry, 14, 429–31.CrossRefGoogle ScholarPubMed
Jacob, N. O. & Jørgensen, P. L. (1969). A quantitative biochemical and histochemical study of the lead method for localization of ATPase-hydrolysing enzyme. Journal of Histochemistry and Cytochemistry 17, 443–53.Google Scholar
Johnson, P. A., Mackenzie, C. D., Suswillo, R. R. & Denham, D. A. (1981). Serum mediated adherence of feline granulocytes to microfilariae of Brugia pahangi in vitro: variations with parasite maturation. Parasite Immunology 3, 69–80.Google Scholar
Jungery, M., Mackenzie, C. D. & Ogilvie, B. M. (1983). Some properties of the surface of nematode larvae. Journal of Helminthology 57, 291–5.CrossRefGoogle ScholarPubMed
Kasa, P. & Csillik, B. (1966). Electron microscopic localization of choline esterase by a copper-lead thiocholine technique. Journal of Neurochemistry 13, 1345–9.CrossRefGoogle ScholarPubMed
Kellenberger, E., Ryter, A. & Sechaud, J. (1958). Fixation and embedding of bacteria. Journal of Biophysical and Biochemical Cytology 4, 671–5.CrossRefGoogle Scholar
Kozek, W. J. (1971). Ultrastructure of the microfilaria of Dirofilaria immitis. Journal of Parasitology 57, 1052–67.CrossRefGoogle ScholarPubMed
Kozek, W. J. & Raccurt, C. (1983). Ultrastructure of Mansonella ozzardi microfilariae, with a comparison of the South American (Simuliid-transmitted) and the Caribbean (Culicoidtransmitted) forms. Tropenmedizin und Parasitologie 34, 38–53.Google Scholar
Laurence, B. R. & Simpson, M. G. (1974). The ultrastructure of microfilariae of Brugia, Nematoda: Filarioidea. International Journal for Parasitology 4, 523–36.Google Scholar
Luft, J. H. (1966). Electron microscopy of cell extraneous coats as revealed by ruthenium red staining. Federation Proceedings 25, 1773.Google Scholar
Mackenzie, C. D., Preston, P. M. & Ogilvie, B. M. (1978). Immunological properties of the surface of parasitic nematodes. Nature, London 276, 826–8.Google Scholar
Mackenzie, C. D. (1980). Eosinophil leucocytes in filarial infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 74 (Suppl.), 51–8.Google Scholar
Maizels, R. M., Philipp, M. & Ogilvie, B. M. (1982). Molecules on the surfaces of parasitic nematodes as probes of the immune response in infection. Immunological Review 61, 109–36.CrossRefGoogle ScholarPubMed
Martinez-Palomo, A. (1978). Ultrastructure characterization of cuticle of Onchocerca volvulus microfilariae. Journal of Parasitology 64, 127–36.CrossRefGoogle Scholar
McLaren, D. (1972). Ultrastructural studies on microfilariae. Parasitology 65, 317–32.Google Scholar
McLaren, D. (1980). Schistosoma mansoni: The Parasite Surface in Relation to Host Immunity (ed. Brown, K. N.), pp. 11–21. Research Studies Press.Google Scholar
Novikoff, A. B. & Goldfischer, S. (1961). Nucleoside phosphatase activity in the golgi apparatus and its usefulness for cytological studies. Proceedings of the National Academy of Sciences, USA 47, 803–9.Google Scholar
Omar, M. S. (1977). Distribution of acid phosphatase activity in larval stages of Wuchereria bancrofti, Brugia malayi, Brugia pahangi, and Dirofilaria immitis in the mosquito. Tropenmedizin und Parasitologie 28, 100–8.Google Scholar
Omar, M. S. (1978). Histochemical enzyme staining patterns of Onchocerca volvulus microfilariae and their occurrence in different onchocerciasis areas. Tropenmedizin und Parasitologie 29, 462–72.Google Scholar
Omar, M. S. & Nathan, M. B. (1979). The histochemical pattern of acid phosphatase activity in Mansonella ozzardi microfilariae from Trinidad, West Indies. Tropenmedizin und Parasitologie 30, 475–6.Google ScholarPubMed
Philipp, M., Parkhouse, R. M. E. & Ogilvie, B. M. (1980). Changing proteins on the surface of a parasitic nematode. Nature, London, 287, 538–40.CrossRefGoogle ScholarPubMed
Piessens, W. F. & Mackenzie, C. D. (1982). Immunology of lymphatic filariasis and onchocerciasis. In Immunology of Parasitic Infections (ed. Cohn, S. and Warren, K. S.), pp. 622–53. Oxford: Blackwell Scientific Publications.Google Scholar
Revel, J. P. & Karnovsky, M. J. (1967). Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. Journal of Cell Biology 33, C7–12.CrossRefGoogle ScholarPubMed
Reynolds, E. S. (1963). Use of lead citrate at high pH as an electron opaque skin in electron microscopy. Journal of Cell Biology 17, 208–12.CrossRefGoogle Scholar
Rogers, R., Ellis, D. S. & Denham, D. A. (1976). Studies with Brugia pahangi. 14. Intrauterine development of the microfilariae and a comparison with other filarial species. Journal of Helminthology 50, 251–7.Google Scholar
Ryter, A. & De Chastellier, C. (1977). Morphometric and cytochemical studies of Dictyostelium discoideum in vegetative phase. Digestive system and membrane turnover. Journal of Cell Biology 75, 251–7.Google ScholarPubMed
Taylor, A. E. R. (1960). The spermatogenesis and entomology of Litomosoides carinii and Dirofilaria immitis. Journal of Helminthology 34, 3–12.Google Scholar
Van Den Bossche, H. (1981). A look at the mode of action of some old and new antifilarial compounds. Annales de la Société Belge de Médecine Tropicale 61, 287–96.Google Scholar
Watson, M. L. (1958). Staining of tissue sections for electron microscopy with heavy metal. Journal of Biophysical and Biochemical Cytology 4, 475–8.Google Scholar
Yen, P. K. F. & Mak, J. W. (1978). Histochemical differentiation of Brugia, Wuchereria, Dirofilaria and Breinlia microfilariae. Annals of Tropical Medicine and Parasitology 72, 157–62.Google Scholar