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Induction of the prophenoloxidase-activating system of Simulium (Diptera: Simuliidae) following Onchocerca (Nematoda: Filarioidea) infection

Published online by Cambridge University Press:  06 April 2009

H.-E. Hagen ,
J. Grunewald  and
P. J. Ham
H.-E. Hagen
Affiliation:
Centre for Applied Entomology and Parasitology, Department of Biological Sciences, Keele University, Staffs ST5 5BG, UK
J. Grunewald
Affiliation:
Institute of Tropical Medicine, University of Tübingen, Wilhelmstrasse 27, D-72074 Tübingen 1, Germany
P. J. Ham
Affiliation:
Centre for Applied Entomology and Parasitology, Department of Biological Sciences, Keele University, Staffs ST5 5BG, UK
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Extract

Trials were carried out to study the humoral immune response of blackflies to filariae following infection using the intrathoracic injection technique. An induced 66 kDa protein was abundant in the haemolymph of the European species Simulium ornatum following infection with bovine Onchocerca lienalis. This protein was apparently at higher concentrations in the haemolymph of sham-inoculated flies, i.e. flies that received sterile medium without the parasites. A molecule of the same size was also observed in the haemolymph of infected S. damnosum s.l. following infection with human O. volvulus or bovine O. ochengi. However, the level of this protein was lower in blackflies injected with microfilariae of bovine O. dukei. Unlike O. volvulus and O. ochengi this species is not transmitted by S. damnosum s.l. under natural conditions. No such reaction was observed if the African blackflies had received a sham inoculation. Feeding experiments with wild-caught nulliparous S. damnosum sl. on Onchocerca-infected cattle supported the results of the injection trials. The 66 kDa protein could only be found in the haemolymph of specimens infected via a blood meal. This 66 kDa molecule was identified as phenoloxidase. It appeared in the haemolymph due to the activation of the prophenoloxidase system following the filarial infection and we hypothesize that it may be sequestered by the parasites, as part of a non-self recognition system.

Keywords

insect immunityhaemolymphOnchocercaSimuliumAedesphenoloxidaseriver blindness
Type
Research Article
Information
Parasitology , Volume 109 , Issue 5 , December 1994 , pp. 649 - 655
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Ashida, M., Kinoshita, K. & Brey, P. T. (1990). Studies on prophenoloxidase activation in the mosquito Aedes aegypti L. European Journal of Biochemistry 188, 507–15.CrossRefGoogle ScholarPubMed
Aspan, A. & Söderhäll, K. (1991). Purification of prophenoloxidase from the crayfish blood cells, and its activation by an endogenous serine protease. Insect Biochemistry 21, 363–73.CrossRefGoogle Scholar
Bain, O., Denke, A. M., Amegee, Y. & Chabaud, A. G. (1971). Les onchocercques des bovins au Togo: les microfilaires et leurs distributions. Annales de l' Université Bénin 3, 117–23.Google Scholar
Bianco, A. E., Ham, P. J., Townson, S., Mustafa, M. B. & Nelson, G. S. (1989). A semi-automated system of intrathoracic injection for the large-scale production of Onchocerca lienalis infective larvae. Annals of Tropical Medicine and Parasitology 38, 57–64.Google Scholar
Bidochka, M. J., Gillespie, J. P. & Khachatourians, G. G. (1989). Phenoloxidase activity of acriid grasshoppers from the subfamily Melanplinae and Oedipodinae. Comparative Biochemistry and Physiology 94B, 117–24.Google Scholar
Blacklock, D. B. (1926). The development of Onchocerca volvulus in Simulium damnosum. Annals of Tropical Medicine and Parasitology 20, 1–48.CrossRefGoogle Scholar
Brookmann, J. L., Ratcliffe, N. A. & Rowley, A. F. (1988). Optimisation of a monoloayer phagocytosis assay and its application for studying the role of the phenoloxidase system of the wax moth, Galleria mellonella. Insect Physiology 34, 337–45.CrossRefGoogle Scholar
Denke, A. M. & Bain, O. (1978). Données sur le cycle d'Onchocerca ochengi chez Simulium damnosum s.l. au Togo. Annales de Parasitologie Humaine et Comparée 53, 757–60.CrossRefGoogle Scholar
Duke, B. O. L., Lewis, D. J. & Moore, P. J. (1966). Onchocerca-Simulium complexes I. Transmission of forest and Sudan-savannah strains of Onchocerca volvulus, from Cameroon, by Simulium damnosum from various West African bioclimatic zones. Annals of Tropical Medicine and Parasitology 60, 318–36.CrossRefGoogle Scholar
Ham, P. J. (1992). Immunity in haematophagous insect vectors of parasitic infection. Advances in Disease Vector Research 9, 101–49.CrossRefGoogle Scholar
Ham, P. J., Albuquerque, C. M., Baxter, A. J., Chalk, R. & Hagen, H. E. (1994 a). Approaches to vector control: New and trusted. 1. Humoral immune responses in blackfly and mosquito vectors of filariae. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 132–5.CrossRefGoogle ScholarPubMed
Ham, P. J., Albuquerque, C. M., Smithies, B., Chalk, R., Klager, S. & Hagen, H. E. (1994 b). Antibacterial peptides in insect vectors of tropical parasitic disease. Ciba Foundation Symposia Proceedings (in the Press).Google ScholarPubMed
Ham, P. J. & Banya, A. J. (1984). The effect of experimental Onchocerca infections on the fecundity and oviposition of laboratory reared Simulium sp. (Diptera, Simuliidae). Tropenmedizin und Parasitologie 35, 61–6.Google ScholarPubMed
Ham, P. J. & Bianco, A. E. (1983). Screening of some British simuliids for susceptibility to experimental Onchocerca lienalis infection. Zeitschrift für Parasitenkunde 69, 765–72.CrossRefGoogle ScholarPubMed
Ham, P. J. & Gale, C. L. (1984). Blood meal enhanced Onchocerca development and its correlation with fecundity in laboratory reared blackflies (Diptera, Simuliidae). Tropenmedizin und Parasitologie 35, 212–16.Google ScholarPubMed
Ham, P. J., Townson, S., James, E. R. & Bianco, A. E. (1981). An improved technique for the cryopreservation of Onchocerca microfilariae. Parasitology 83, 139–46.CrossRefGoogle ScholarPubMed
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680–5.CrossRefGoogle ScholarPubMed
Lorenz, R. J. (1984). Biometrie, Grundbegriffe der Biometrie. Stuttgart: G. Fischer Verlag.Google Scholar
Nellaiappan, K. & Vinayagam, A. (1986). A rapid method for detection of tyrosinase activity in electrophoresis. Stain Technology 61, 269–72.CrossRefGoogle ScholarPubMed
Nelson, G. S. (1962). Observation on the development of Setaria labiatopapillosa using new techniques for infecting Aedes aegypti. Journal of Helminthology 36, 281–96.CrossRefGoogle ScholarPubMed
Omar, M. S., Denke, A. M. & Raybould, J. N. (1979). The development of Onchocerca ochengi (Nematoda: Filarioidea) to the infective stage in Simulium damnosum s.l. with a note on the histochemical staining of the parasite. Tropenmedizin und Parasitologie 30, 157–62.Google Scholar
Schägger, H. & Von Jagow, G. (1987). Tricine-sodium dodecyl sulfate polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Analytical Biochemistry 166, 368–79.CrossRefGoogle ScholarPubMed
Shih, C. M. & Chen, C. C. (1991). Haemolymph monophenoloxidase activity in Armigeres subalbatus infected with Brugia pahangi. International Journal for Parasitology 21, 357–9.CrossRefGoogle Scholar
Smail, A. J. & Ham, P. J. (1988). Onchocerca induced haemolymph lectins in blackflies: confirmation by sugar inhibition of erythrocyte agglutination. Tropical Medicine and Parasitology 39, 82–3.Google Scholar
Söderhäll, K. & Smith, V. J. (1986). Pro-phenoloxidase-activating cascade as a recognition and defense system in arthropods. In Hemocytic and Humoral Immunity in Arthropods (ed. Gupta, A. P.), pp. 251–285. London: Wiley & Sons.Google Scholar
Wahl, G., Ekale, D., Enyong, P. & Renz, R. (1991). The development of Onchocerca dukei and O. ochengi microfilariae to the infective stage larvae in Simulium damnosum s.l. and in members of the S. medusiforme group, following intrathoracic injection. Annals of Tropical Medicine and Parasitology 85, 329–37.CrossRefGoogle Scholar
Wahl, G. & Renz, A. (1991). Transmission of Onchocerca dukei by Simulium bovis in North-Cameroon. Tropical Medicine and Parasitology 42, 368–70.Google ScholarPubMed
Wenk, P. & Raybould, J. N. (1972). Mating, blood feeding and oviposition of Simulium damnosum Theobald in the laboratory. Bulletin of the World Health Organization 47, 627–34.Google ScholarPubMed
Wirtz, H. P. (1983). Nahrungsaufnahme und Natalität bei palaearktischen und afrikanischen Simuliiden (Diptera). Dissertation der Fakultät für Biologie, Universität Tübingen.Google Scholar