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Naturally occurring agglutinins against trypanosomatid flagellates in the haemolymph of insects

Published online by Cambridge University Press:  06 April 2009

G. A. Ingram ,
Janet East  and
D. H. Molyneux
G. A. Ingram
Affiliation:
School of Life Sciences, Department of Biology, University of Salford, Salford M5 4WT
Janet East
Affiliation:
School of Life Sciences, Department of Biology, University of Salford, Salford M5 4WT
D. H. Molyneux
Affiliation:
School of Life Sciences, Department of Biology, University of Salford, Salford M5 4WT
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Summary

In vitro studies of the behaviour of the trypanosomatid flagellates Trypanosoma brucei and Leishmania hertigi in the presence of cell-free haemolymph of locusts, Schistocerca gregaria and cockroaches, Periplaneta americana revealed the presence of parasite agglutinins. The range of normal values of agglutination titres was 2−4 to 2−13. Physico-chemical treatment of haemolymph indicated that these agglutinins are protein or glycoprotein in nature and are only partially affected by heat treatment below 65°C, at which temperature incubation of haemolymph for 30 min abrogated all agglutination. Agglutination was not dependent on the presence of Ca2+ or Mg2+. Prior infection of locusts and cockroaches with T. brucei and L. hertigi significantly increased agglutinin titres between Days 4 and 6 in cockroaches (P < 0·05) and from Days 2 to 4 when L. hertigi was inoculated into locusts. The induced differences in titres observed in locusts infected with T. brucei were not significant. Lysozyme levels were significantly increased after inoculation of T. brucei into cockroaches compared with placebo-inoculated and uninoculated controls. L. hertigi inoculation produced significant increases in lysozyme levels compared with controls between Days 1 and 7 in locusts and 3 to 6 in cockroaches. These studies indicate that, at least in easily manipulated model systems, induced responses to intrahaemocoelic inoculation to trypanosomes and Leishmania can occur. As far as we are aware this is the first report of an induced response of an insect to such important parasites. The possibility that induced responses in natural vectors to these parasites occurs requires investigation.

Type
Research Article
Information
Parasitology , Volume 89 , Issue 3 , December 1984 , pp. 435 - 451
Copyright
Copyright © Cambridge University Press 1984

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References

REFERENCES

Anderson, R. S., Day, N. K. B. & Good, R. A. (1972). Specific hemagglutinin and a modulator of complement in cockroach haemolymph. Infection and Immunity 5, 55–9.CrossRefGoogle Scholar
Bernheimer, A. W. (1952). Hemagglutinins in caterpillar bloods. Science 115, 150–1.CrossRefGoogle ScholarPubMed
Boman, H. G., Boman, A. & Pigon, A. (1981). Immune and injury responses in Cecropia pupae—RNA isolation and comparison of protein synthesis in vivo and in vitro. Insect Biochemistry 11, 33–42.CrossRefGoogle Scholar
Boman, H. G. & Steiner, H. (1981). Humoral immunity in Cecropia pupae. Current Topics in Microbiology and Immunology 94/95, 75–91.CrossRefGoogle ScholarPubMed
Chadwick, J. M. & Aston, W. P. (1978). An overview of insect immunity. In Animal Models of Comparative and Developmental Aspects of Immunity and Disease (ed. Gershwin, M. E. and Cooper, E. L.), pp. 1–14. Oxford: Pergamon Press.Google Scholar
Chorney, M. J. & Cheng, T. C. (1980). Discrimination of self and non-self in invertebrates. Contemporary Topics in Immunobiology 9, 37–54.CrossRefGoogle ScholarPubMed
Cohen, E. (1974). Biomedical perspectives of agglutinins of invertebrate and plant origins. Annals of the New York Academy of Sciences 234, 1–412.Google Scholar
Cooper, E. L. (1981). Immunity in invertebrates. CRC Critical Reviews in Immunology 2, 1–32.Google Scholar
Croft, S. L., East, J. S. & Molyneux, D. H. (1982). Anti-trypanosomal factor in the haemolymph of Glossina. Acta Tropica 39, 293–302.Google ScholarPubMed
Cunningham, I. (1977). New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. Journal of Protozoology 24, 325–9.CrossRefGoogle ScholarPubMed
Donlon, W. C. & Wemyss, C. T. (1976). Analysis of the hemagglutinin and general protein element of the haemolymph of the West Indian leaf cockroach, Blaberus craniifer. Journal of Invertebrate Pathology 28, 191–4.CrossRefGoogle Scholar
East, J., Molyneux, D. H., Maudlin, I. & Dukes, P. (1983). Effect of Glossina haemolymph on salivarian trypanosomes in vitro. Annals of Tropical Medicine and Parasitology 77, 97–9.CrossRefGoogle ScholarPubMed
Faye, I. & Wyatt, G. R. (1980). The synthesis of antibacterial proteins in isolated fat body from Cecropia silkmoth pupae. Experientia 36, 1325–6.CrossRefGoogle ScholarPubMed
Feir, D. & Walz, M. A. (1964). An agglutinating factor in insect hemolymph. Annals of the Entomological Society of America 57, 388.CrossRefGoogle Scholar
Hapner, K. D. & Jermyn, M. A. (1981). Haemagglutinin activity in the haemolymph of Teleogryllus commodus (Walker). Insect Biochemistry 11, 287–95.CrossRefGoogle Scholar
Hoffmann, D. (1980). Induction of antibacterial activity in the blood of the migratory locust Locusta migratoria. Journal of Insect Physiology 26, 539–49.CrossRefGoogle Scholar
Hoffmann, D. & Brehelin, M. (1976). Sur l'origine et le rôle d'une activité de type lysozyme mise en évidence dans le sang de Locusta migratoria migratorioides. Acrida 5, 181–8.Google Scholar
Ingram, G. A., East, J. & Molyneux, D. H. (1983). Agglutinins of Trypanosoma, Leishmania and Crithidia in insect haemolymph. Developmental and Comparative Immunology 7, 649–52.Google Scholar
Jurenka, R., Manfredi, K. & Hapner, K. D. (1982). Haemagglutinin activity in Acrididae (grasshopper) hemolymph. Journal of Insect Physiology 28, 177–81.CrossRefGoogle Scholar
Kamon, E. & Shulov, A. (1965). Immune response of locusts to venom of the scorpion. Journal of Invertebrate Pathology 7, 192–8.Google Scholar
Karp, R. D. & Rheins, L. A. (1980). Induction of specific humoral immunity to soluble proteins in the American cockroach (Periplaneta americana). II. Nature of the secondary response. Developmental and Comparative Immunology 4, 629–939.CrossRefGoogle ScholarPubMed
Kamano, H., Mizuno, D. & Natori, S. (1980). Purification of lectin induced in the hemolymph of Sarcophaga peregrina larvae on injury. Journal of Biological Chemistry 255, 2919–24.CrossRefGoogle Scholar
Lackie, A. M. (1980). Invertebrate immunity. Parasitology 80, 393–412.CrossRefGoogle ScholarPubMed
Lackie, A. M. (1981 a). The specificity of the serum agglutinins of Periplaneta americana and Schistocerca gregaria and its relationship to the insects' immune response. Journal of Insect Physiology 27, 139–43.Google Scholar
Lackie, A. M. (1981 b). Humoral mechanisms in the immune response of insects to larvae of Hymenolepis diminuta (Cestoda). Parasite Immunology 3, 201–8.CrossRefGoogle ScholarPubMed
Luther, P., Otto, D., Köhler, W. & Fischer, G. (1975). Immunisierungsversuche zur Erzeugung von antikörperähnlichen Substanzen bei Raupen von Mamestra brassicae L. (Insecta, Lepid., Noct.). Acta biologica et medica germanica 34, 1421–7.Google Scholar
Malke, H. (1964). Wirkung von Lysozym auf die Symbionten der Blatiiden. Zeitschrift für allgemeine Mikrobiologie 4, 88–91.CrossRefGoogle Scholar
Malke, H. (1965). Über das Vorkommen von Lysozym in Insekten. Zeitschrift für allgemeine Mikrobiologie 5, 42–7.CrossRefGoogle Scholar
Mohrig, W. & Messner, B. (1968 a). Immunreaktionen bei Insekten. I. Lysozym als grundlegender antibakterieller Faktor im humoralen Abwehrmechanisma der Insekten. Biologisches Zentraiblatt 87, 439–70.Google Scholar
Mohrig, W. & Messner, B. (1968 b). Immunreaktionen bei Insekten. II. Lysozym als antimikrobielles Agans im Darmtrakt von Insekten. Biologisches Zentralblatt 87, 705–18.Google Scholar
Molyneux, D. H. (1977). Vector relationships in the Trypanosomatidae. Advances in Parasitology 15, 1–82.CrossRefGoogle ScholarPubMed
Molyneux, D. H. (1980). Host-trypanosome interactions in Glossina. Insect Science and its Applications 1, 39–46.Google Scholar
Nogge, G. & Gerresheim, A. (1982). Experiments on the elimination of symbionts from the tsetse fly, Glossina morsitans morsitans (Diptera: Glossinidae), by antibiotics and lysozyme. Journal of Invertebrate Pathology 40, 166–79.Google Scholar
Osserman, E. F. & Lawlor, D. P. (1966). Serum and urinary lysozyme (muramidase) in monocytic and monomyelocytic leukemia. Journal of Experimental Medicine 124, 921–51.CrossRefGoogle ScholarPubMed
Pereira, M. E. A., Andrade, A. F. & Ribeiro, J. M. C. (1981). Lectins of distinct specificity in Rhodnius prolixus interact selectively with Trypanosoma cruzi. Science 211, 597–600.CrossRefGoogle ScholarPubMed
Peters, W., Kolb, H. & Kolb-Bachofen, V. (1983). Evidence for a sugar receptor (lectin) in the peritrophic membrane of the blowfly larva, Calliphora erythrocephala Mg. (Diptera). Journal of Insect Physiology 29, 275–80.CrossRefGoogle Scholar
Ratcliffe, N. A. & Rowley, A. F. (1982). Recognition factors in insect haemolymph. Developmental and Comparative Immunology. ISDCI Invertebrate Immunology Conference,August 31st–September 3rd,Swansea. Abstract p. 24.Google Scholar
Rheins, L. A. & Karp, R. D. (1982). An inducible humoral factor in the American cockroach (Periplaneta americana): precipitin activity that is sensitive to a proteolytic enzyme. Journal of Invertebrate Pathology 40, 190–6.Google Scholar
Rheins, L. A., Karp, R. D. & Butz, A. (1980). Induction of specific humoral immunity to soluble proteins in the American cockroach (Periplaneta americana). I. Nature of the primary response. Developmental and Comparative Immunology 4, 447–58.CrossRefGoogle ScholarPubMed
Schottelius, J. (1982). Lectin binding strain-specific carbohydrates on the cell surface of Leishmania strains from the Old World. Zeitschrift für Parasitenkunde 66, 237–47.Google Scholar
Scott, M. T. (1971). A naturally occurring hemagglutinin in the hemolymph of the American cockroach. Archives de Zoologie Experimentale Generale 112, 73–80.Google Scholar
Scott, M. T. (1972). Partial characterization of the hemagglutinating activity in the hemolymph of the American cockroach (Periplaneta americana). Journal of Invertebrate Pathoiogy 19, 66–71.Google Scholar
Seaman, R. & Robert, N. L. (1968). Immunological response of male cockroaches to injection of Tetrahymena pyriformis. Science 161, 1359–61.CrossRefGoogle ScholarPubMed
Stein, E. A. & Cooper, E. L. (1982). Agglutinins as receptor molecules: a phylogenetic approach. In Developmental Immunology: Clinical Problems and Ageing (ed. Cooper, E. L. and Brazier, M. A. B.), pp. 85–98. London: Academic Press.Google Scholar
Warr, G. W. (1981 a). Immunity in invertebrates. Journal of Invertebrate Pathology 38, 311–14.Google Scholar
Warr, G. W. (1981 b). Evolution of the lymphocyte. Immunology Today 2, 64–8.CrossRefGoogle ScholarPubMed
Wright, R. W. & Cooper, E. L. (1982). Origins of lymphocytes, cellular immunity and the major histocompatibility system. In Developmental Immunology: Clinical Problems and Ageing (ed. Cooper, E. L. and Brazier, M. A. B.), pp. 13–26. London: Academic Press.Google Scholar
Yeaton, R. W. (1981). Invertebrate lectins: 1. Occurrence. Developmental and Comparative Immunology 5, 391–402.CrossRefGoogle Scholar