Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-22T20:43:51.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Rapid changes in the surface of parasitic nematodes during transition from pre- to post-parasitic forms

Published online by Cambridge University Press:  06 April 2009

L. Proudfoot ,
J. R. Kusel ,
H. V. Smith ,
W. Harnett ,
M. J. Worms  and
M. W. Kennedy
L. Proudfoot
Affiliation:
Department of Biochemistry, University of Glasgow, Glasgow
J. R. Kusel
Affiliation:
Department of Biochemistry, University of Glasgow, Glasgow
H. V. Smith
Affiliation:
Scottish Parasite Diagnostic Laboratory, Stobhill General Hospital, Glasgow
W. Harnett
Affiliation:
Division of Parasitology, National Institute for Medical Research, London
M. J. Worms
Affiliation:
Division of Parasitology, National Institute for Medical Research, London
M. W. Kennedy
Affiliation:
Wellcome Laboratories for Experimental Parasitology, University of Glasgow, Bearsden, Glasgow
Get access Rights & Permissions [Opens in a new window]

Summary

All mammalian-parasitic stages of a range of nematode species investigated (Brugia pahangi, Acanthocheilonema viteae, Strongyloides ratti, Nippostrongylus brasiliensis, Trichinella spiralis and Ostertagia ostertagi) labelled in a surface-restricted manner with the fluorescent lipid analogues 5-N-(octadecanoyl)aminofluorescein (AF18) or nitrobenzoxadiazole-cholesterol (NBD-chol), but failed to bind other similar probes. In contrast, the surfaces of the ‘pre-parasitic’ infective stages of these species had affinity for neither AF18 nor NBD-chol. This exclusion of lipid analogues changed rapidly upon exposure of the larvae to tissue culture conditions which mimic the mammalian tissue environment (e.g. RPMI 1640/37°C) such that the above probes could then insert into the surface layer of the larvae. The dauer larva of Caenorhabditis elegans also excluded the probes, but became permissive to labelling upon stimulation to emerge from the dauer state. The time taken for the surface transformation to occur ranged from less than 10 min in the vector-borne parasites to approximately 5 h in those which enter by the oral route, with direct skin-penetrators occupying an intermediate position. In all cases, the alteration proceeded too rapidly for it to have been associated with a moult. Fluorescence Recovery After Photobleaching (FRAP) studies of A. viteae larvae showed that approximately 50% of the AF18 probe was free to diffuse within the plane of the surface immediately after transformation. This is only a transitory state because AF18 was found to be highly restricted in its lateral diffusion on the surface of adult parasites. In the larvae of S. ratti, the change in affinity for AF18 was accompanied by the rapid shedding of an otherwise stable surface coat of polyanionic material, here visualized by labelling with fluorescein-conjugated cationized ferritin. Incubation of larvae in lipid-rich host serum during the induction of transformation inhibited subsequent labelling with AF 18. This possibly reflects competition for insertion sites and an in vivo propensity towards the acquisition of host lipid by invading parasites.

Keywords

fluorescent lipid probesFluorescence Recovery After PhotobleachingBrugia pahangiAcanthocheilonema viteaeStrongyloides rattiNippostrongylus brasiliensisTrichinella spiralisOstertagia ostertagiCaenorhabditis elegans
Type
Research Article
Information
Parasitology , Volume 107 , Issue 1 , July 1993 , pp. 107 - 117
Copyright
Copyright © Cambridge University Press 1993

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

Abraham, D., Grieve, R. B. & Mika-Grieve, M. (1988). Dirofilaria immitis: surface properties of third- and fourth-stage larvae. Experimental Parasitology 65, 157–67.CrossRefGoogle ScholarPubMed
Badley, J. E., Grieve, R. B., Rockey, J. H. & Glickman, L. T. (1987). Immune-mediated adherence of eosino-phils to Toxocara canis infective larvae: the role of excretory-secretory antigens. Parasite Immunology 9, 133–43.CrossRefGoogle Scholar
Bird, A. F. (1980). The nematode cuticle and its surface. In Nematodes as Biological Models (ed. Zuckerman, B. M.), pp. 213–236. New York: Academic Press.Google Scholar
Clegg, J. A. (1969). Skin penetration by cercariae of the bird schistosome Austrobilharzia terrigalensis: the stimulatory effect of cholesterol. Parasitology 59, 973–89.CrossRefGoogle ScholarPubMed
Devaney, E. & Jecock, R. M. (1991). The expression of the Mr 30000 antigen in the third stage larvae of Brugia pahangi. Parasite Immunology 13, 75–87.CrossRefGoogle Scholar
Foley, M., Macgregor, A. N., Kusel, J. H., Garland, P. B., Downie, T. & Moore, I. (1986). The lateral diffusion of lipid probes in the surface membrane of Schistosoma mansoni. Journal of Cell Biology 103, 807–18.CrossRefGoogle ScholarPubMed
Grove, D. I., Wharton, A., Northern, C. & Papadimitriou, J. M. (1987). Electron microscopical studies of Strongyloides ratti infective larvae: loss of the surface coat during skin penetration. Journal of Parasitology 73, 1030–4.CrossRefGoogle ScholarPubMed
Gruner, S. M., Cullis, P. R., Hope, M. J. & Tilcock, C. P. S. (1985). Lipid polymorphism: the molecular basis of non-bilayer phases. Annual Review of Biophysics and Biophysical Chemistry 14, 211–38.CrossRefGoogle Scholar
Himmelhoch, S. & Zuckerman, B. M. (1978). Caenorhabditis briggsae: ageing and the structural turnover of the outer cuticle surface and the intestine. Experimental Parasitology 45, 208–14.CrossRefGoogle ScholarPubMed
Kennedy, M. W., Foley, M., Knox, K., Birmingham, J., Harnett, W., Worms, M. J., Kusel, J. R. & Garland, P. B. (1987 a). Are the biophysical properties of the surface of filarial parasites different from other nematodes? In Molecular Paradigms for Eradicating Helminthic Parasites (ed. MacInnis, A. J.), pp. 289–300. New York: NY: Alan R. Liss, Inc.Google Scholar
Kennedy, M. W., Foley, M., Kuo, Y.-M., Kusel, J. R. & Garland, P. B. (1987 b). Biophysical properties of the surface lipid of parasitic nematodes. Molecular and Biochemical Parasitology 22, 233–40.CrossRefGoogle ScholarPubMed
King, C. A. & Preston, T. M. (1977). Fluoresceinated cationised ferritin as a membrane probe for anionic sites at the cell surface. FEBS Letters 73, 59–63.Google ScholarPubMed
Lee, D. L., Wright, K. A. & Shivers, R. R. (1984). A freeze-fracture study of the surface of the infective-stage larva of the nematode Trichinella. Tissue and Cell 16, 819–28.CrossRefGoogle ScholarPubMed
Lee, D. L., Wright, K. A. & Shivers, R. R. (1984). A freeze-fracture study of the body wall of adult in utero larvae and infective-stage larvae of Trichinella (Nematoda). Tissue and Cell 18, 219–30.CrossRefGoogle Scholar
Murrell, K. D. & Graham, C. E. (1983). Shedding of antibody complexes by Strongyloides ratti (Nematoda) larvae. Journal of Parasitology 69, 70–3.CrossRefGoogle ScholarPubMed
Peters, R. (1981). Translational diffusion in the plasma membrane of single cells as studied by fluorescence microphotolysis. Cell Biology International Reports 5, 733–60.CrossRefGoogle ScholarPubMed
Philipp, M. & Rumjanek, F. D. (1984). Antigenic and dynamic properties of helminth surface Structures. Molecular and Biochemical Parasitology 10, 245–68.CrossRefGoogle ScholarPubMed
Proudfoot, L., Kusel, J. R., Smith, H. V. & Kennedy, M. W. (1991). Biophysical properties of the nematode surface. In Parasitic Nematodes Antigens, Membranes and Genes (ed. Kennedy, M. W.), pp. 1–26. London and Philadelphia: Taylor & Francis.Google Scholar
Stewart, G. L., Despommier, D. D., Burnham, J. & Raines, K. M. (1987). Trichinella spiralis; Behaviour, structure and biochemistry of larvae following exposure to components of the host enteric environment. Experimental Parasitology 63, 195–204.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1971). Penetration stimuli for schistosome cercariae. In Aspects of the Biology of Symbiosis (ed. Cheng, T. C.), pp. 1–23. Baltimore: University Park Press.Google Scholar
Storey, N. & Philipp, M. (1992). Brugia malayi; Patterns of expression of surface-associated antigens. Experimental Parasitology 74, 57–68.CrossRefGoogle ScholarPubMed
Stryer, L. (1978). Fluorescence energy transfer as a spectroscopic ruler. Annual Reviews of Biochemistry 47, 819–46.CrossRefGoogle ScholarPubMed
Wagner, A. (1959). Stimulation of Schistosomatium douthitti cercariae to penetrate their host. Journal of Parasitology 45, 16–18.Google Scholar
Wolf, D. E. (1988). Probing the lateral organization and dynamics of membranes. In CRC Critical Reviews: Spectroscopic Membrane Probes (ed. Loew, L.), pp. 194–216. Boca Raton, Florida: CRC Press, Inc.Google Scholar
Wright, K. A. (1987). The nematode's cuticle - its surface and the epidermis; function, homology, analogy. Journal of Parasitology 73, 1077–83.CrossRefGoogle ScholarPubMed
Wright, K. A. & Hong, H. (1988). Characterization of the accessory layer of the cuticle of muscle larvae of Trichinella spiralis. Journal of Parasitology 74, 440–51.CrossRefGoogle ScholarPubMed