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Plasmodium-Induced Changes in Haemolymph Polypeptides During Development and Ageing of the Malaria Vector Anopheles stephensi (Diptera: Culicidae)

Published online by Cambridge University Press:  19 September 2011

S. K. Gakhar
Affiliation:
Department of Biosciences, Maharshi Dayanand University Rohtak-124001, Haryana, India
Harish K. Shandilya
Affiliation:
Department of Biosciences, Maharshi Dayanand University Rohtak-124001, Haryana, India
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Abstract

Changes in the pattern of haemolymph polypeptides were studied to map the innate immune response of the malaria vector Anopheles stephensi (Diptera: Culicidae) to infection by the parasite Plasmodium yoelii yoelii. In addition, changes in the ontogenetic pattern due to glucose feeding, age, sex and gonotrophic cycle-related proteins were analysed. Six polypeptides were induced and 22 polypeptides disappeared due to glucose feeding during various stages of the mosquito's adult life. Five polypeptide patterns (91, 100, 108, 133 & 145 KDa) were found exclusively in female haemolymph. The changes in these polypeptide patterns have been correlated with sexual dimorphism in their feeding behaviour.

In total, 18 polypeptides were induced in the haemolymph of parasitised mosquitoes during different stages of development. Most of the polypeptides were induced in the early stages of infection, i.e. immediately after a bloodmeal. One polypeptide (25 KDa) was induced in all the stages. The expression of two polypeptides (32.5 and 70 KDa) on day 9 and one polypeptide (42 KDa) on day 15 was also enhanced following parasitism. The different induced proteins may help mosquitoes of different ages cope with parasite infection. The parasite evidently elicits immune responses in multiple tissues of the mosquito, including two epithelia which the parasite must traverse to complete its development. The mechanism of these responses and their significance in malaria transmission are discussed.

Résumé

Des changements dans la composition des polypeptides de l'hémolymphe ont été étudiés afin de suivre la réponse immunitaire innée chez Anopheles stephensi, un moustique vecteur de la malaria, après que celui-ci aitété infecté par le parasite Plasmodium yoelii yoelii. En plus, on a analysé les changements de la composition ontogénétique découlant de l'alimentation au glucose, de l'âge, du sexe spécifique et des protéines liées aux cycles gonotrophiques. Six polypeptides étaient induits, tandis que 22 autres disparaissaient suite à l'alimentation du moustique sur du glucose, au cours de son existence à l'état imaginal. Cinq polypeptides (91,100,108,133, et 145 KDa) étaient uniquement présents dans l'hémolymphe du mousUque femelle. Des changements observés dans la composition de ces polypeptides ont été corrélés avec le dimorphisme sexuel de l'insecte suite à son comportement alimentaire. Au total, 18 polypeptides étaient induits dans l'hémolymphe des moustiques parasités au cours de leurs différents stades de développement. La grande majorité des polypeptides était induite dans les premières heures suivant l'infection, c'est-à-dire immédiatement après un repas sanguin. Un seul polypeptide (25 KDa) était induit au niveau de tous les stades. L'apparition de deux polypeptides (32.5 et 70 KDa) au 9ème jour et d'un autre polypeptide (42 KDa) au 15ème jour, était aussi renforcée par le parasitisme. Les différentes protéines induites pourraient aider le moustique à endurer l'infection due au parasite, au cours de ses différents stades de développement. Aussi, le parasite puise apparemment les réponses immunitaires des différents tissus du corps du moustique dont les tissus épithéliaux que le parasite doit traverser afin de compléter son développement. L'article discute le mécanisme des différentes réponses et leur rôle dans la transmission de la malaria.

Type
Research Articles
Copyright
Copyright © ICIPE 2000

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References

REFERENCES

Asgari, S., Theopold, U., Craig, W. and Schmidt, O. (1998) A protein with protective properties against the cellular defense reactions in insects. Proc. Natl. Acad. Sci. USA 95, 36903695.CrossRefGoogle ScholarPubMed
Boman, H. G. and Hultmark, D. (1987) Cell free immunity in insects. Annu. Rev. Microbiol. 41, 103126.CrossRefGoogle ScholarPubMed
Christensen, B. M. and LaFond, M. M. (1986) Parasite-induced suppression of the immune response in Aedes aegypti by Brugia pahangi. J. Parasitol. 72, 216219.CrossRefGoogle ScholarPubMed
Dimopoulos, G., Richman, A., Muller, H.-M. and Kafatos, F. C. (1997) Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc. Natl. Acad. Sci., USA 94, 1150811513.CrossRefGoogle ScholarPubMed
Dimopoulos, G., Seeley, D., Wolf, A. and Kafatos, F. C. (1998) Malaria infection of the mosquito Anopheles gambiae activates immuno-responsive genes during critical transition stages of the parasite life cycle. The EMBO J. 17, 61156123.CrossRefGoogle Scholar
Dinamarca, M. and Levenbook, L. (1966) Oxidation, utilisation and incorporation into protein of alanine and lysine during metamorphosis of blowfly Phormia regina (Meigen.). With an appendix by Jhon Z. Hearon. Arch. Biochem. 117, 110119.CrossRefGoogle Scholar
Gakhar, S. K. and Maleyvar, R. P. (1984a) Age and sex related free tera. Proc. Indian Nail. Sci. Acad. B50, 362364.Google Scholar
Gakhar, S. K. and Maleyvar, R. P. (1984b) Quantitative changes in free amino-acids during metamorphosis of Trabala vishnou (Lepidoptera: Insecta) and sex specific differences. Proc. Natl. Sci. Acad. B50, 277285.Google Scholar
Gakhar, S. K. and Singh, S. (1998) Protein pattern in ageing malaria vector mosquito, Anopheles stephensi. J. Cytol. Genet. 33, 6167.Google Scholar
Gakhar, S. K., Singh, S. and Shandilya, H. (1997) Changes in soluble proteins during the development of malaria vector Anopheles stephensi (Diptera: Insecta). Proc. Indian Natl. Sci. Acad. B63, 289298.Google Scholar
Gakhar, S. K., and Vandana, (1989) Rearing technique and life cycle of Anopheles stephensi. Jeevanti. 7, 3540.Google Scholar
Gakhar, S. K. and Vandana, (1993) Developmental expression of alkaline phosphates in A. stephensi (Diptera: Culicidae). Proc. Indian Natl. Sci. Acad. 59, 531536.Google Scholar
Gakhar, S. K., Vandana, , Shandilya, H. K. and Singh, S. (1999) Expression of small heat shock proteins (HSPs) during insect development. In Recent Trends in Developmental Biology (Edited by Gakhar, S. K. and Mishra, S. N.). Himalaya Press, Delhi.Google Scholar
Golenda, C. F., Starkweather, W. H. and Wirtz, R. A. (1990) The distribution of circumsporozoites protein (CS) in Anopheles stephensi mosquitoes infected with Plasmodium falciparaum malaria. J. Histochem. Cytochem. 38, 475481.CrossRefGoogle Scholar
Gooding, R. H. (1975) Digestive enzymes and their control in hematophagous insects. Acta Tropica 32, 96111.Google Scholar
Gupta, U. S. and Banerjee, S. (1988) Sexual dimorphism in the haemolymph proteins of insects. Proc. Indian Natl. Sci. Acad. B58, 1721.Google Scholar
Ham, P. J., Albuquerque, C., Smithies, B., Chalk, R., Klager, S. and Hagen, H. (1994) Antibacterial peptides in insect vectors of tropical parasitic disease. Ciba Found. Symp. 186, 140151.Google ScholarPubMed
Hoffmann, J. A. (1995) Innate immunity of insects. Curr. Opin. Immunol. 7, 410.CrossRefGoogle ScholarPubMed
Hoffmann, J. A., Reichhart, J. M. and Hetru, C. (1996) Innate immunity of higher insects. Curr. Opin. Immunol. 8, 813.CrossRefGoogle ScholarPubMed
Hogg, J. C., Carwardine, S. and Hurd, H. (1997) The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi. Parasitol. Res. 83, 374379.CrossRefGoogle ScholarPubMed
Izumi, S., Yano, K., Yamamoto, Y. and Takahashi, S. Y. (1994) Yolk proteins from insect eggs: Structure, biosynthesis and programmed degradation during embryogenesis—Review. J. Insect Physiol. 40, 735.CrossRefGoogle Scholar
James, A. A., Blackmer, K. and Racioppi, J. V. (1989) A salivary gland-specific, maltase-like gene of the vector mosquito, Aedes aegypti. Gene. 75, 7383.CrossRefGoogle ScholarPubMed
Laemli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of Bacteriphage T4. Nature 227, 680685.CrossRefGoogle Scholar
Locke, J., McDermid, H., Brae, T. and Atkinson, B. G. (1982) Developmental changes in the synthesis of haemolymph polypeptides and their sequestration by the prepupal fat body in Calpodes ethlius Stoll (Lepidoptera: Hesperiidae). Insect Biochem. 12, 430440.CrossRefGoogle Scholar
Lowenberger, C., Bulet, P., Charlet, M., Hetru, C., Hodgeman, B., Christensen, B. M. and Hoffmann, J. A. (1995) Insect immunity: Isolation of three novel inducible antibacterial defensins from the vector mosquito, Aedes aegypti. Insect Mol. Biochem. 25, 867873.CrossRefGoogle ScholarPubMed
Mack, S. R. and Vanderberg, J. P. (1978) Haemolymph of A. stephensi from uninfected and Plasmodium berghei infected mosquitoes. 1. Control procedure and physical characteristics. J. Parasitol. 64, 918923.CrossRefGoogle Scholar
Mack, S. R., Samuels, S. and Vanderberg, J. P. (1979) Haemolymph of A. stephensi from uninfectedand Plasmodium bergei-infected mosquitoes. 2. Free amino acids. J. Parasitol. 65, 130136.CrossRefGoogle ScholarPubMed
Meis, J. F. G. M., Pool, G., Van Gemert, G. J., Lensen, A. H. W., Ponnudurai, T. and Meuwissen, J. H. E. T. (1989) Plasmodium falciparum ookinetes migrate intercellularly through Anopheles stephensi midgut epithelium. Parasitol. Res. 76, 1319.CrossRefGoogle ScholarPubMed
Patel, N. and Schneiderman, H. (1969) The effect of perfusion on the synthesis and release of blood proteins by diapause pupae of the Ceropia silkworm. J. Insect Physiol. 15, 643660.CrossRefGoogle Scholar
Rembold, B. and Graf, H. (1972) Isolierung und Charkakterisierung eines kastenspezifischen Proteins aus der Honigbiene. Z. Physiol. Chem. 353, 16151624.CrossRefGoogle Scholar
Richman, A. and Kafatos, F. C. (1996) Immunity to eukaryotic parasites in vector insects. Curr. Opin. Immunol. 8, 1419.CrossRefGoogle ScholarPubMed
Richman, A. M., Bulet, P., Barillas-Mury, C., Hoffman, J. A. and Kafatos, F. C. (1996) Inducible immune factors of the vector mosquito to Anopheles gambiae: Biochemical purification of a defensin antibacterial peptide and molecular cloning of preprodefensin cDNA. Insect Mol. Biol. 5, 203210.CrossRefGoogle ScholarPubMed
Richman, A. M., Dimopoulos, G., Seeley, D. and Kafatos, F. C. (1997) Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. EMBO J. 16, 61146119.CrossRefGoogle ScholarPubMed
Rizki, R. M. and Rizki, T. M. (1984) Selective destruction of a host blood cell type by a parasitoid wasp. Proc. Natl. Acad. Sci. USA 81, 61546158.CrossRefGoogle ScholarPubMed
Schmidt, G. H. and Schwankl, W. (1975) Changes in haemolyph proteins during the metamorphosis of both sexes and castes of polygynous Formica rufa L. (Ins. Hym.). Comp. Biochem. Physiol. 52B, 365380.Google Scholar
Schoenle, E. J., Adams, L. D. and Sammons, D. W. (1984) Insulin induced rapid decrease of a major protein in fat cell plasma membranes. J. Biol. Chem, 259, 12112.CrossRefGoogle Scholar
Shandilya, H. (1998) Developmental changes in Anopheles mosquitoes due to Plasmodium infection. PhD thesis, M. D. University, Rohtak, India. 160 pp.Google Scholar
Shandilya, H., Gakhar, S. K. and Adak, T. (1999) Plasmodium infection-induced changes in salivary gland proteins of malaria vector Anopheles stephensi (Diptera: Culicidae). Japanese J. Infect. Dis. 52, 214216.Google ScholarPubMed
Snyder, M. and Davidson, N. (1983) Two gene families clustered in a small region of the Drosophila genome. J. Mol. Biol. 166, 101118.CrossRefGoogle Scholar
Sroka, P. and Vinson, S. B. (1978) Phenoloxidase activity in the haemolymph of parasitized and unparasitized Heliothis virescens. Insect Biochem. 8, 399402.CrossRefGoogle Scholar
Stoltz, D. B. and Cook, D. I. (1983) Inhibition of host phenoloxidase activity by parasitoid Hymenoptera. Experientia 39, 10221024.CrossRefGoogle Scholar
Subbarao, S. K., Sharma, V. P., Vasantha, K. and Adak, T. (1984) Effect of malathion spraying on four Anopheline species and the development of resistance in A. stephensi in Mandora, Haryana. Indian J. Malariol. 21, 109114.Google Scholar
World Health Organisation (1982) Basic information on mosquito vectors and diseases. In Manual on Environment Management for Mosquito Control. Annx. 1, WHO, Geneva, Switzerland.Google Scholar