Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-23T01:36:11.717Z Has data issue: false hasContentIssue false

External stimuli and intracellular signalling in the modification of the nematode surface during transition to the mammalian host environment

Published online by Cambridge University Press:  06 April 2009

L. Proudfoot
Affiliation:
1Department of Biochemistry, University of Glasgow, Glasgow
J. R. Kusel
Affiliation:
1Department of Biochemistry, University of Glasgow, Glasgow
H. V. Smith
Affiliation:
2Scottish Parasite Diagnostic Laboratory, Stobhill General Hospital, Glasgow
M. W. Kennedy
Affiliation:
3Wellcome Laboratories for Experimental Parasitology, University of Glasgow, Bearsden, Glasgow, UK

Summary

Previous work has shown that the surface of infective larvae of parasitic nematodes will not bind the fluorescent lipid analogue 5-N(octadecanoyl)aminofluorescein (AF18) until after exposure of the parasite to mammalian tissue-culture conditions. In this study, culture media which are permissive or non-permissive for the acquisition of lipophilicity for AF18 were altered in order to examine possible stimuli involved. This showed that external alkaline pH and high sodium ion concentration were highly stimulatory. The internal signalling pathways which may be involved in the surface alteration were then examined using agents which are known to affect intracellular signalling in mammalian cells. The results indicated that elevation of cGMP levels was stimulatory whereas inhibition of a putative Na+/H+ antiporter or calcium mobilization was inhibitory, and it is argued that high intracellular levels of cAMP may be inhibitory. Whilst the precise effects of the agents used on nematode cells remain to be established, these results provide a framework for the examination of the processes involved in the modification of the nematode surface which takes place immediately after the infection event.

Type
Research Article
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

REFERENCES

Campbell, A. K. (1983). Intracellular Calcium-Its Universal Role as Regulator. New York: John Wiley & Sons.Google Scholar
Foley, M., MacGregor, A. N., Kusel, J. R., Garland, P. B., Downie, T. & Moore, I. (1986). The lateral diffusion of lipid probes in the surface membranes of Schistosoma mansoni. Journal of Cell Biology 103, 807–18.CrossRefGoogle ScholarPubMed
Frelin, C., Vigne, P., Ladoux, A. & Lazdunski, M. (1988). The regulation of the intracellular pH in cells from vertebrates. European Journal of Biochemistry 174, 314.CrossRefGoogle ScholarPubMed
Garbers, D. L. (1989). Cyclic GMP and the second messenger hypothesis. Trends in Neurobiological Sciences 11/12, 64–7.CrossRefGoogle Scholar
Heyworth, C. M., Wallace, A. V., Wilson, S. R. & Houslay, M. D. (1984). An assessment of the ability of insulin-stimulated cyclic AMP phosphodiesterase to decrease hepatocyte intracellular cyclic AMP concentrations. Biochemical Journal 222, 183–7.CrossRefGoogle ScholarPubMed
Katsuki, S., Arnold, W., Mittal, C. & Murad, F. (1977). Stimulation of guanylate cyclase by sodium nitroprusside, nitroglycerin and nitric oxide in various tissue preparations and comparison to the effects of sodium azide and hydroxylamine. Journal of Cyclic Nucleotide Research 3, 23–5.Google Scholar
Kawamoto, F., Alejo-Blanco, R., Fleck, S. L., Kawamoto, Y. & Sinden, R. E. (1990). Possible roles of Ca2+ and cGMP as mediators of the exflagellation of Plasmodium berghei and P. falciparum. Molecular and Biochemical Parasitology 42, 101–8.CrossRefGoogle Scholar
Kawamoto, F., Shozawa, A., Kumada, N. & Kojima, K. (1989). Possible roles of cAMP and Ca2+ in the regulation of miracidial transformation in Schistosoma mansoni. Parasitology Research 75, 368–74.CrossRefGoogle ScholarPubMed
Kennedy, M. W., Foley, M., Kuo, Y.-M., Kusel, J. R. & Garland, P. B. (1987). Biophysical properties of the surface lipid of parasitic nematodes. Molecular and Biochemical Parasitology 22, 233–40.CrossRefGoogle ScholarPubMed
Madshus, I. H. (1988). Regulation of intracellular pH in eukaryotic cells. Biochemical Journal 250, 18.CrossRefGoogle ScholarPubMed
Moolenaar, W. H. (1986). Effects of growth factors on intracellular pH regulation. Annual Review of Physiology 48, 363–76.CrossRefGoogle ScholarPubMed
Moolenaar, W. H., Tsien, R. Y., Van Der Saag, P. T. & De Laat, S. W. (1983). Na+/H+ exchange and cytoplasmic pH in the action of growth factors in human fibroblasts. Nature, London 304, 645–8.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1984 a). Turnover of inositol phospholipids and signal transduction. Science 225, 1365–70.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1984 b). The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature, London 308, 693–7.CrossRefGoogle ScholarPubMed
Petronijevic, T. & Rogers, W. P. (1987). The physiology of infection with nematodes: the role of intracellular pH in the development of the early parasitic stage. Comparative Biochemistry and Physiology 88A, 207–12.CrossRefGoogle ScholarPubMed
Petronijevic, T., Rogers, W. P. & Sommerville, R. I. (1986). Organic and inorganic acids as the stimulus for exsheathment of infective juveniles of nematodes. International Journal for Parasitology 16, 163–8.CrossRefGoogle ScholarPubMed
Proudfoot, L., Kusel, J. R., Smith, H. V., Harnett, W., Worms, M. J. & Kennedy, M. W. (1993). Rapid changes in the surface of parasitic nematodes during transition from pre- to post-parasitic forms. Parasitology 107, 107–17.CrossRefGoogle ScholarPubMed
Schultz, K. D., Schultz, K. & Schultz, G. (1977). Sodium nitroprusside and other smooth muscle- relaxants increase cyclic GMP levels in rat ductus deferens. Nature, London 265, 750–1.CrossRefGoogle ScholarPubMed
Siffert, W. & Akkerman, J. W. N. (1987). Activation of sodium—proton exchange is a prerequisite for Ca++ mobilization in human platelets. Nature, London 325, 456–8.CrossRefGoogle Scholar
Skou, J. C. (1965). Enzymatic basis for active transport of Na+ and K+ across cell membrane. Physiological Reviews 45, 596617.CrossRefGoogle Scholar
Tanabe, K. (1984). Inhibitory effect of rhodamine 123 on the growth of rodent malaria parasites, Plasmodium yoelii. Journal of Protozoology 31, 310–13.CrossRefGoogle Scholar
Thomas, R. C. (1984). Experimental displacement of intracellular pH and the mechanism of its subsequent recovery. Journal of Physiology 354, 322.CrossRefGoogle ScholarPubMed