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Bloodmeal digestion by strains of Anopheles stephensi Liston (Diptera: Culicidae) of differing susceptibility to Plasmodium falciparum

Published online by Cambridge University Press:  06 April 2009

A. M. Feldmann
Affiliation:
Research Institute Ital., P.O. Box 48, 6700 AA, Wageningen, The Netherlands
P. F. Billingsley
Affiliation:
Swiss Tropical Institute, Postfach 4002, Basel, Switzerland
E. Savelkoul
Affiliation:
Research Institute Ital., P.O. Box 48, 6700 AA, Wageningen, The Netherlands

Extract

Blood digestion was studied in strains of Anopheles stephensi which had been genetically selected for either refractoriness or susceptibility to infection by Plasmodium falciparum. Females of the refractory Pb3—9a strain ingested more blood than selected (Sda-500) and unselected (Punjab) susceptible females and began to degrade the haemoglobin soon after feeding. In susceptible females, haemoglobin degradation started only after a significant post-feeding lag period. Total protein content of the midgut after the bloodmeal was correspondingly higher for refractory than for susceptible females, but absolute and relative rates of protein degradation were not significantly different between the different mosquito strains. Bloodmeal induction of midgut trypsin activity and the maximal trypsin activity were the same for the different strains. The residual aminopeptidase activity and its relative post-feeding activity (enzyme units per midgut) were significantly higher in refractory females. However, when converting to specific aminopeptidase activity, no differences between strains were evident. The results indicate that both the early initiation of haemoglobin degradation and higher aminopeptidase activity in the Pb3—9a refractory strain are important in the limitation of parasite development within the mosquito midgut, whereas trypsin plays no role in this process.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

Azambuja, P. D., Guimaraes, J. & Garcia, E. S. (1983). Hemolytic factor from the crop of Rhodnius prolixus: evidence and partial characterization. Journal of Insect Physiology 29, 833–7.CrossRefGoogle Scholar
Behin, R. (1968). The influence of chicken serum proteins on the infection of Aedes aegypti with Plasmodium gallinaceum. American Journal of Tropical Medicine and Hygiene 17, 457–60.CrossRefGoogle ScholarPubMed
Berner, R., Rudin, W. & Hecker, H. (1983). Peritrophic membranes and protease activity in the midgut of the malaria mosquito, Anopheles stephensi (Liston) (Insecta: Diptera) under normal and experimental conditions. Journal of Ultrastructural Research 83, 195204.CrossRefGoogle ScholarPubMed
Billingsley, P. F. (1989). Blood digestion in the mosquito, Anopheles stephensi Liston (Diptera: Culicidae): partial characterisation and post-feeding activity of midgut aminopeptidases. Archives of Insect Biochemical Physiology. (In the Press).Google Scholar
Briegel, H. (1983). Manipulation of age-dependent kinetics of the induction of intestinal trypsin in the mosquito Aedes aegypti (Diptera: Culicidae). Entomologia Generalis 8, 217–23.CrossRefGoogle Scholar
Briegel, H. & Lea, A. O. (1975). Relationship between protein and proteolytic activity in the midgut of mosquitoes. Journal of Insect Physiology 21, 15971604.CrossRefGoogle ScholarPubMed
Briegel, H., Lea, A. O. & Klowden, M. J. (1979). Hemoglobinometry as a method for measuring blood meal sizes of mosquitoes. Journal of Medical Entomology 15, 235–8.CrossRefGoogle Scholar
Campbell, R. C. (1974). Statistics for Biologists. Cambridge: Cambridge University Press.Google Scholar
Collins, F. H., Sakai, R. K., Vernick, K. D., Paskewitz, S., Seeley, D. C., Miller, L. H., Collins, W. E., Campbell, C. C. & Gwadz, R. W. (1986). Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234, 607–10.CrossRefGoogle ScholarPubMed
Coluzzi, M., Concetti, A. & Ascoli, F. (1982). Effect of cibarial armature of mosquitoes (Diptera, Culicidae) on blood-meal hemolysis. Journal of Insect Physiology 28, 885–8.CrossRefGoogle Scholar
Curtis, C. F. (1968). Possible use of translocations to fix desirable genes in insect populations. Nature, London 218, 368.CrossRefGoogle Scholar
Downe, A. E. R. & Archer, J. A. (1975). The effects of different blood-meal sources on digestion and egg production in Culex tarsalis Coq. (Diptera: Culicidae). Journal of Medical Entomology 12, 431–7.CrossRefGoogle ScholarPubMed
Erlanger, B. F., Kokowsky, N. & Cohen, W. (1969). The preparation of two new chromogenic substrates of trypsin. Archives of Biochemical Biophysiology 95, 271–8.CrossRefGoogle Scholar
Feldmann, A. & Ponnudurai, T. (1989). Selection of Anopheles stephensi for refractoriness and susceptibility to Plasmodium falciparum. Medical and Veterinary Entomology 3, 4152.CrossRefGoogle ScholarPubMed
Felix, C., Betschart, B., Billingsley, P. F. & Freyvogel, T. A. (1989). Post-feeding induction of trypsin in the midgut of Aedes aegypti (Diptera: Culicidae) is separable into two cellular phases. Insect Biochemistry (in the Press).Google Scholar
Frizzi, G. A., Rinaldi, A. & Bianchi, U. (1975). Genetic studies on mechanisms influencing the susceptibility of Anopheles mosquitoes to plasmodial infection. Mosquito News 35, 505–8.Google Scholar
Gass, R. F. (1977). Influences of blood digestion on the development of Plasmodium gallinaceum (Brumpt) in the midgut of Aedes aegypti (L.). Acta Tropica 34, 127–40.Google ScholarPubMed
Gass, R. F. & Yeates, R. A. (1979). In vitro damage of cultured ookinetes of Plasmodium gallinaceum by digestive proteinases from susceptible Aedes aegypti. Acta Tropica 36, 243–52.Google ScholarPubMed
Gooding, R. H. (1973). The digestive processes of haematophagous insects. IV. Secretion of trypsin by Aedes aegypti (Diptera: Culcidae). Canadian Entomologist 105, 599603.CrossRefGoogle Scholar
Graf, R. & Briegel, H. (1982). Comparison between aminopeptidase and trypsin activity in blood-fed females of Aedes aegypti. Revue Suisse Zoologique 89, 845–50.CrossRefGoogle Scholar
Hayes, R. O. (1953). Determination of a physiological saline solution for Aedes aegypti L. Journal of Economical Entomology 46, 624–7.CrossRefGoogle Scholar
Houseman, J. G. & Downe, A. E. R. (1986). Methods of measuring blood meal size and proteinase activity for determining effects of mated state on digestive processes of female Aedes aegypti (L.) (Diptera: Culicidae). Canadian Entomology 118, 241–8.CrossRefGoogle Scholar
Hovanitz, W. (1947). Physiological factors which influence the infection of Aedes aegypti with Plasmodium falciparum. American Journal of Hygiene 45, 6781.Google Scholar
Huang, C. T. (1971). Vertebrate serum inhibitors of Aedes aegypti trypsin. Insect Biochemistry 1, 207–27.CrossRefGoogle Scholar
Huff, C. G. (1930). Individual immunity and susceptibility of Culex pipiens to various species of bird malaria as studied by means of double infections feedings. American Journal of Hygiene 12, 424–41.Google Scholar
Janse, C. J., Rouwenhorst, R. J., Van Der Klooser, P. F. J., Van Der Kaay, H. J. & Overdulve, J. P. (1985). Development of plasmodium berghei ookinetes in the midgut of Anopheles atroparvus mosquitoes and in vitro. Parasitology 91, 219–25.CrossRefGoogle ScholarPubMed
Kilama, W. L. & Craig, G. B. (1969). Monofactorial inheritance of susceptibility to Plasmodium gallinaceum in Aedes aegypti. Annals of Tropical Medicine and Parasitology 63, 419–32.CrossRefGoogle ScholarPubMed
Kunz, P. A. (1978). Resolution and properties of the proteinases in adult Aedes aegypti (L). Insect Biochemistry 8, 169–75.CrossRefGoogle Scholar
Nijhout, M. M. (1979). Plasmodium gallinaceum: exflagellation stimulated by a mosquito factor. Experimental Parasitology 48, 7580.CrossRefGoogle ScholarPubMed
Peterson, G. L. (1977). A simplification of the protein assay method of Lowry et.al. which is more generally applicable. Analytical Biochemistry 83, 246–56.CrossRefGoogle ScholarPubMed
Ponnudurai, T., Meuwissen, J., Leeuwenberg, A. D. E. M., Verhave, J. P. & Lensen, A. H. W. (1982). The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Transactions of the Royal Society for Tropical Medicine and Hygiene 76, 242–50.CrossRefGoogle ScholarPubMed
Reid, G. D. F. & Boid, R. (1984). Assessment of temporal changes in haem and protein levels in ixodid tickes following blood engorgement, and their use as age-grading parameters. Journal of Insect Physiology 30, 975–8.CrossRefGoogle Scholar
Rosenberg, R., Koontz, L. C., Alston, K. & Friedman, F. K. (1984). Plasmodium gallinaceum: erythrocyte factor essential for zygote infection of Aedes aegypti. Experimental Parasitology 57, 158–64.CrossRefGoogle ScholarPubMed
Rutledge, L. C., Ward, R. A. & Buckwalter, R. M. (1973). Plasmodium ssp.: dispersion of malarial oocyst populations in Anophelene and Culicine mosquitoes. Experimental Parasitology 34, 132–41.CrossRefGoogle Scholar
Sinden, R. E. (1984). The biology of Plasmodium in the mosquito. Experientia 40, 1330–43.CrossRefGoogle ScholarPubMed
Whitten, M. J. (1971). Insect control by genetic manipulation of natural populations. Science 171, 612–18.CrossRefGoogle ScholarPubMed
Van Der Kaay, H. J. & Boorsma, L. (1977). A susceptible and refractive strain of Anopheles atroparvus to infection with Plasmodium berghei. Acta Leidensiae 45, 1319.Google ScholarPubMed
Yang, Y. J. & Davies, D. M. (1971). Trypsin and chymotrypsin during metamorphosis in Aedes aegypti and properties of the chymotrypsin. Journal of Insect Physiology 17, 117–31.CrossRefGoogle ScholarPubMed
Yeates, R. A. & Steiger, S. (1981). Ultrastructural damage of in vitro cultured ookinetes of Plasmodium gallinaceum (Brumpt) by purified proteinases of susceptible Aedes aegypti (L.). Zeitschrift für Parasitenkunde 66, 93–7.CrossRefGoogle ScholarPubMed
Ward, R. A. (1963). Genetic aspects of the susceptibility of mosquitoes to malarial infection. Experimental Parasitology 13, 328–41.CrossRefGoogle ScholarPubMed
Wigglesworth, V. B. (1943). The fate of haemoglobin in Rhodnius prolixus (Hemiptera) and other arthropods. Proceedings of the Royal Society London, B131, 313–39.Google Scholar