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Hymenolepis diminuta-induced fecundity reduction may be caused by changes in hormone binding to Tenebrio molitor ovaries

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, Staffordshire ST5 5BG, UK
H. Hurd
Affiliation:
Centre for Applied Entomology and Parasitology, Department of Biological Sciences, Keele University, Keele, Staffordshire ST5 5BG, UK
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Summary

Aspects of vitellogenesis, known to be controlled by juvenile hormone, are adversely affected by Hymenolepis diminuta infection of Tenebrio molitor, in spite of circulating titres of the hormone remaining unchanged. It has therefore been proposed that juvenile hormone binding is disrupted at the tissue site level. Juvenile hormone III binding sites were located in the nuclear, microsomal and post-microsomal supernatant fractions of the follicle cells of Tenebrio molitor. When JH-III binding was quantified for both control and Hymenolepis diminuta-infected beetles, binding in the nucleus and cytosol were found to be largely unaffected. However, microsomal binding was severely disrupted; on days 3 and 6 post-infection, binding was greatly diminished, on day 9 post-infection, binding was slightly reduced and, by day 15, binding was ‘restored’ to that of control insects. Using follicle cell microsomes at day 3 post-infection, previous Scatchard analysis revealed the presence of at least two JH-III binding sites. The first is of higher affinity, Kd = 5·3 x 10·5 x 10−11 mol/mg protein and the second of lower affinity Kd = 7·7 x 10−7 M, Bmax = 9·75 x 10−11 mol/mg protein. A comparison with microsomal binding parameters of follicle cells from non-infected Tenebrio indicated that although the Bmax values were unchanged, the Kd value of the higher affinity site was increased by approximately 5-fold. These data are indicative of a parasite-induced competitive binding inhibitor.

Keywords

Hymenolepis diminutaTenebrio molitorjuvenile hormonejuvenile hormone binding proteinsvitellogenesishost fecundity depletionCestodaPlatyhelminthes
Type
Research Article
Information
Parasitology , Volume 110 , Issue 5 , June 1995 , pp. 565 - 571
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Abu-Hakima, R. & Davey, K. G. (1977). The action of juvenile hormone on the follicle cells of Rhodnius prolixus: the importance of volume changes. Journal of Experimental Biology 69, 33–44.Google Scholar
Abu-Hakima, R. & Davey, K. G. (1979). A possible relationship between ouabain-sensitive (Na+-K+) dependent ATPase and the effect of juvenile hormone on the follicle cells of Rhodnius prolixus. Insect Biochemistry 9, 195–8.CrossRefGoogle Scholar
Aronson, N. N. & Touster, O. (1974). Isolation of rat liver plasma membrane fragments in isotonic sucrose. In Methods in Enzymology, Vol. 31 (ed. Fleischer, S. & Packer, L.), pp. 90–102. London: Academic Press.Google Scholar
Bhattacharya, A. K., Ameel, J. J. & Waldbauer, G. P. (1970). A method of sexing living pupal and adult yellow mealworms. Annals of the Entomological Society of America 63B, 1783–5.CrossRefGoogle Scholar
Davey, K. G. (1993). Hormonal integration of egg production in Rhodnius prolixus. American Zoologist 33, 397–402.Google Scholar
Davey, K. G. & Kuster, J. E. (1980). The source of an antigonadotrophin in the female of Rhodnius prolixus Stal. Canadian Journal of Zoology 59, 761–4.CrossRefGoogle Scholar
Davey, K. G., Sevala, V. L. & Gordon, D. R. B. (1993). The action of juvenile hormone and antigonadotrophin on the follicle cells of Locusta migratoria. Invertebrate Reproduction and Development 24, 39–46.CrossRefGoogle Scholar
de Jong-Brink, M., Elsaadany, M. M. & Boer, H. H. (1988 a). Trichobilharzia ocellata: interference with endocrine control of female reproduction of Lymnaea stagnalis. Experimental Parasitology 65, 91–100.CrossRefGoogle ScholarPubMed
de Jong-Brink, M., Elsaadany, M. M. & Boer, H. H. (1988 b). Schistosomin, an antagonist of calfluxin. Experimental Parasitology 65, 109–18.CrossRefGoogle ScholarPubMed
Dowell, F. H. & Jones, A. W. (1966). Establishment of Tribolium confusum populations after stress by parasitism with Hymenolepis microstoma. Experimental Parasitology 18, 99–108.Google Scholar
Engelmann, F. (1984). The regulation of vitellogenesis in insects: the pleiotropic role of juvenile hormones. In Biosynthesis, Metabolism and Mode of Action of Invertebrate Hormones (ed. Hoffmann, J. A. & Porchet, M.), pp. 444–453. Berlin: Springer.Google Scholar
Goodman, W. G. & Chang, E. S. (1985). Juvenile hormone cellular and hemolymph binding proteins. In Comprehensive Insect Biochemistry, Physiology and Pharmacology, vol. 7(ed. Kerkut, G. A. & Gilbert, L. I.), pp. 491–510. Oxford: Pergamon Press.Google Scholar
Hundley, D. F. & Bertzen, A. K. (1969). Collection, sterilization and storage of Hymenolepis diminuta eggs. Journal of Parasitology 55, 1095–6.Google Scholar
Hurd, H. (1990). 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. (1993). Reproductive disturbances induced by parasites and pathogens of insects. In Parasites and Pathogens of Insects, vol. 1 (ed. Beckage, N. E., Thompson, S. N. & Federici, B. A.), pp. 87–105. New York: Academic Press.Google Scholar
Hurd, H. & Arme, C. (1984). Pathophysiology of Hymenolepis diminuta infections in 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.Google Scholar
Hurd, H. & Arme, C. (1987 a). Hymenolepis diminuta: effect of infection upon the patency of the follicular epithelium in the intermediate host, Tenebrio molitor. Journal of Invertebrate Pathology 49, 227–34.CrossRefGoogle ScholarPubMed
Hurd, H. & Arme, C. (1987 b). 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
Hurd, H., Strambi, C. & Beckage, N. E. (1990). Hymenolepis diminuta: an investigation of juvenile hormone litre, degradation and supplementation in the intermediate host, Tenebrio molitor. Parasitology 100, 445–52.CrossRefGoogle Scholar
Hurd, H. & Weaver, R. J. (1987). Evidence against the hypothesis that metacestodes of Hymenolepis diminuta inhibit corpora allata functioning in the intermediate host, Tenebrio molitor. Parasitology 95, 93–6.CrossRefGoogle ScholarPubMed
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
Ilenchuk, T. T. & Davey, K. G. (1987 a). Effects of various compounds on Na/K ATPase activity, JH-I binding capacity and patency response in the follicles of Rhodnius prolixus. Insect Biochemistry 17, 1085–9.Google Scholar
Ilenchuk, T. T. & Davey, K. G. (1987 b). The development of responsiveness to juvenile hormone in the follicle cells of Rhodnius prolixus. Insect Biochemistry 17, 525–9.CrossRefGoogle Scholar
Joosse, J., Elk, Van R., Mosselman, S., Wortelboer, H. & Van Diepen, J. C. E. (1988). Schistosomin: a pronase-sensitive agent in the haemolymph of Trichobilharzia ocellata-infected Lymnaea stagnalis inhibits the activity of the albumen glands in vitro. Parasitology Research 74, 228–34.Google 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
Keymer, A. (1980). The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum. Parasitology 81, 405–21.Google Scholar
Keymer, A. (1981). Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 50, 941–50.Google Scholar
Koeppe, J. K., Hobson, K. & Wellman, S. E. (1980). Juvenile hormone regulation of the structural changes and DNA synthesis in the follicular epithelium of Leucophaea maderae. Journal of Insect Physiology 26, 229–40.Google Scholar
Koeppe, J. K. & Wellman, S. E. (1980). Ovarian maturation in Leucophaea maderae: juvenile hormone regulation of thymidine uptake into follicle cell DNA. Journal of Insect Physiology 26, 219–28.CrossRefGoogle Scholar
Lapointe, M. C. & Koeppe, J. K. (1980). Juvenile hormone stimulation of ovarian thymidine kinase in Leucophaea maderae. American Zoologist 20, 901–10.Google Scholar
Mircheff, A. K. & Wright, E. M. (1976). Analytical isolation of plasma membranes of intestinal epithelial cells: identification of Na, K-ATPase rich membranes and the distribution of enzyme activities. Journal of Membrane Biology 28, 309–33.CrossRefGoogle ScholarPubMed
Rosenthal, H. E. (1967). A graphic method for the determination and presentation of binding parameters in a complex system. Analytical Biochemistry 20, 525–32.CrossRefGoogle ScholarPubMed
Scatchard, G. (1949). The attraction of proteins for small molecules. Annals of the New York Academy of Sciences 51, 660–72.CrossRefGoogle Scholar
Sevala, V. L. & Davey, K. G. (1989). Action of juvenile hormone on the follicle cells of Rhodnius prolixus: evidence for a novel mechanism involving protein kinase C. Experientia 45, 355–6.Google 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.Google Scholar
Sottocasa, G. L., Kuylenstiera, B., Ernst, L. & Bergstrand, A. (1967). An electron transport system associated with the outer membrane of liver mitochondria. Journal of Cell Biology 32, 415–38.CrossRefGoogle ScholarPubMed
Mellaert, Van H., Hendrickx, K., Rans, M., Cardoen, J. & De Loof, 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
Mellaert, Van H., Theunis, S. & De Loof, A. (1985). Juvenile hormone proteins in Sarcophaga bullata haemolymph and vitellogenic ovaries.Google Scholar
Wang, Z. & Davey, K. G. (1992). Characterisation of yolk protein and its receptor on the oocyte membrane in Rhodnius prolixus. Insect Biochemistry 2, 757–67.CrossRefGoogle Scholar
Webb, T. J. & Hurd, H. (1995 a). Microsomal juvenile hormone binding proteins in the follicle cells of Tenebrio molitor. Insect Biochemistry and Molecular Biology (In the Press).Google Scholar
Webb, T. J. & Hurd, H. (1995 b). The use of a monoclonal antibody to detect parasite induced reduction in vitellogenin content in the ovaries of Tenebrio molitor. Journal of Insect Physiology (In the Press).Google Scholar
Weder, H. G., Schildknecht, J., Lutz, R. & Kesselring, P. (1974). Determination of binding parameters from Scatchard plots. European Journal of Biochemistry 42, 475–81.Google Scholar