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Hymenolepis diminuta: metacestode-induced reduction in the synthesis of the yolk protein, vitellogenin, in the fat body of Tenebrio molitor

Published online by Cambridge University Press:  06 April 2009

T. J. Webb  and
H. Hurd
T. J. Webb*
Affiliation:
Centre for Applied Entomology and Parasitology, Department of Biological Sciences, Keele University, Keele, Staffs ST5 5BG, UK
H. Hurd
Affiliation:
Centre for Applied Entomology and Parasitology, Department of Biological Sciences, Keele University, Keele, Staffs ST5 5BG, UK
*
* Corresponding author Dr Tracey Webb.
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Summary

Vitellogenin synthesis by the fat body has been monitored using in vitro culture and immunoprecipitation. This system was found to be efficient for measuring vitellogenin production in both non-infected Tenebrio molitor and those infected with Hymenolepis diminuta. In fat bodies from infected beetles, vitellogenin production was decreased by up to 75% (day 24 post-infection) and, at all times investigated, vitellogenin synthesis was significantly below control levels (days 3–30 post-infection). Incubating fat bodies from control insects with isolated metacestodes indicated that this may be a direct effect by the parasite which is developmental stage-specific. Stage II, but not stage III–IV, nor heat-killed parasites could bring about this decrease in vitellogenin. In addition, these effects may be density dependent within the range of 2–20 parasites per fat body; only 2 metacestodes were necessary to cause a significant decrease. Since metacestodes do not take up vitellogenin, nor limit the amount of [14C] leucine available to the fat body for vitellogenin production, it is conceivable that the parasite produces a potent inhibitor of vitellogenin synthesis, or a molecule which induces cells within the fat body to do so.

Keywords

Tenebrio molitorHymenolepis diminutaCestodavitellogeninvitellognesisfat body
Type
Research Article
Information
Parasitology , Volume 112 , Issue 4 , April 1996 , pp. 429 - 436
Copyright
Copyright © Cambridge University Press 1996

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References

Chalaye, D. (1979). Étude immunochimique des protéines hémolymphatiques et ovocytaires de Rhodnius prolixus. Canadian Journal of Zoology 57, 329–36.CrossRefGoogle Scholar
Engelmann, F. (1979). Insect vitellogenin: identity, biosynthesis and role in vitellogenesis. Advances in Insect Physiology 14, 49–108.CrossRefGoogle Scholar
Engelmann, F. (1983). Vitellogenesis controlled by juvenile hormone. In Endocrinology of Insects, (ed. Downer, R. G. H. & Laufer, H.), pp. 259–270. New York: Alan R. Liss Inc.Google Scholar
Hagedorn, H. H. & Kunkel, J. G. (1979). Vitellogenin and vitellin in insects. Annual Review of Entomology 24, 475–505.CrossRefGoogle Scholar
Harnish, D. G. & White, B. N. (1982). Insect vitellins: identification, purification and characterization from eight orders. Journal of Experimental Zoology 220, 1–10.CrossRefGoogle Scholar
Hurd, H. (1990 a). Parasite induced modulation of insect reproduction. In Advances in Invertebrate Reproduction Vol. 5 (ed. Hoshi, M. & Yamashita, O.), pp. 163–168. Amsterdam: Elsevier Publishers, B.V.Google Scholar
Hurd, H. (1990 b). Physiological and behavioural interactions between parasite and invertebrate hosts. Advances in Parasitology 29, 271–318.CrossRefGoogle ScholarPubMed
Hurd, H. (1993). Reproductive disturbances induced by parasites and pathogens of insects. In Parasites and Pathogens of Insects. Vol. 1: Parasites (ed. Beckage, N. E., Thompson, S. N. & Federici, B. A.), pp. 87–105. London: Academic Press.CrossRefGoogle Scholar
Hurd, H. & Arme, C. (1984 a). Tenebrio molitor (Coleoptera): effect of metacestodes of Hymenolepis diminuta (Cestoda) on haemolymph amino acids. Parasitology 89, 245–51.CrossRefGoogle Scholar
Hurd, H. & Arme, C. (1984 b). Pathophysiology of Hymenolepis diminuta infections of Tenebrio molitor: effect of parasitism on haemolymph proteins. Parasitology 89, 253–62.CrossRefGoogle Scholar
Hurd, H. & Arme, C. (1986 a). Hymenolepis diminuta: effect of metacestodes on production and viability of eggs in the intermediate host, Tenebrio molitor. Journal of Invertebrate Pathology 47, 225–30.CrossRefGoogle ScholarPubMed
Hurd, H. & Arme, C. (1986 b). Hymenolepis diminuta: influence of metacestodes on synthesis and secretion of fat body protein and its ovarian sequestration in the intermediate host, Tenebrio molitor. Parasitology 93, 111–20.CrossRefGoogle ScholarPubMed
Hurd, H. & Arme, C. (1987). Hymenolepis diminuta (Cestoda): the role of intermediate host sex in the establishment, growth and development of metacestodes in Tenebrio molitor (Coleoptera). Helminthologia 24, 23–31.Google Scholar
Ilenchuk, T. T. & Davey, K. G. (1983). Some properties of Na+-K+ ATPase in the follicle cells of Rhodnius prolixus. Insect Biochemistry 12, 675–9.CrossRefGoogle Scholar
Ilenchuk, T. T. & Davey, K. G. (1985). The binding of juvenile hormone to membranes of follicle cells in the insect Rhodnius prolixus. Canadian Journal of Biochemistry and Cell Biology 63, 102–6.CrossRefGoogle Scholar
Kearns, J. Y., Hurd, H. & Pullin, A. S. (1994). Effect of metacestodes of Hymenolepis diminuta on storage and circulating carbohydrates in the intermediate host Tenebrio molitor. Parasitology 108, 473–8.CrossRefGoogle ScholarPubMed
Kunkel, J. G. & Nordin, J. H. (1985). Yolk proteins. In Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 1 (ed. Kerkut, G. A. & Gilbert, L. I.), pp. 84–110. Oxford: Pergamon Press.Google Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature, London 227, 680–5.CrossRefGoogle ScholarPubMed
Maema, M. (1986). Experimental infection of Tribolium confusum (Coleoptera) by Hymenolepis diminuta (Cestoda): host fecundity during infection. Parasitology 92, 405–12.CrossRefGoogle ScholarPubMed
Raikhel, A. S. & Dhadialla, T. S. (1992). Accumulation of yolk proteins in insect oocytes. Annual Review of Entomology 37, 217–51.CrossRefGoogle ScholarPubMed
Renshaw, M. & Hurd, H. (1994 a). The effects of Onchocerca lienalis infection on vitellogenesis in the British blackfly, Simulium ornatum. Parasitology 109, 337–43.CrossRefGoogle ScholarPubMed
Renshaw, M. & Hurd, H. (1994 b). Vitellogenin sequestration by Simulium oocytes: effect of Onchocerca infection. Physiological Entomology 19, 70–4CrossRefGoogle Scholar
Sevala, V. L. & Davey, K. G. (1989). Action of juvenile hormone on the follicle cells of Rhodnius prolixus: evidence for a novel regulatory mechanism involving protein kinase C. Experientia 45, 355–6.CrossRefGoogle Scholar
Sevala, V. L. & Davey, K. G. (1993). Juvenile hormone dependent phosphorylation of a 100 kDa polypeptide is mediated by protein kinase C in the follicle cells of Rhodnius prolixus. Invertebrate Reproduction and Development 23, 189–93.CrossRefGoogle Scholar
Telfer, W. H., Huebner, E. & Smith, D. S. (1982). The cell biology of vitellogenic follicles in Hylaphora and Rhodnius. In Insect Ultrastructure (ed. King, R. C. & Akai, H.) pp. 118–149. New York: Plenum.CrossRefGoogle Scholar
Van Mellaert, H., Hendrickx, K., Rans, M., Cardoen, J. & De Loop, A. (1989). Characterization of a juvenile hormone binding site in the microsomal fraction of Sarcophaga bullata vitellogenic ovaries by means of a filter assay. Comparative Biochemistry and Physiology 92B, 123–7.Google Scholar
Voge, M. & Heyneman, D. (1957). Development of Hymenolepis nana and Hymenolepis diminuta (Cestoda: Hymenolepidae) in the intermediate host, Tribolium confusum. University of California Publications in Zoology 59, 549–80.Google Scholar
Webb, T. J. & Hurd, H. (1995 a). The use of a monoclonal antibody to detect parasite induced reduction in vitellin content in the ovaries of Tenebrio molitor. Journal of Insect Physiology 41, 745–51.CrossRefGoogle Scholar
Webb, T. J. & Hurd, H.` (1995 b). Hymenolepis diminuta- induced fecundity reduction may be caused by changes in hormone binding to the ovaries of Tenebrio molitor. Parasitology 110, 565–71.CrossRefGoogle Scholar
Webb, T. J. & Hurd, H. (1995 c). Microsomal juvenile hormone binding proteins in the follicle cells of Tenebrio molitor. Insect Biochemistry and Molecular Biology 25, 631–7.CrossRefGoogle ScholarPubMed
Wyatt, G. R. & Pan, M. L. (1978). Insect plasma proteins. Annual Review of Biochemistry 47, 779–817.CrossRefGoogle ScholarPubMed