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A review of the progress made in recent years on research and understanding of immunity in insect vectors of human and animal diseases

Published online by Cambridge University Press:  19 September 2011

Godwin P. Kaaya
Affiliation:
The International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, Kenya
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Abstract

Different modes of immune reactions of insect vectors of human and animal diseases to nematode and protozoan parasites, fungi, bacteria, viruses and to other biological materials e.g. xenografts are discussed in this paper. Since most of the insect vectors of diseases are adult dipterans with low numbers of circulating haemocytes, their mode of defence against metazoan parasites and fungal pathogens is primarily by means of humoral encapsulation, with little haemocyte participation. Although earlier workers reported that humoral capsules in dipterans were formed without direct participation by haemocytes, this paper reveals increasing evidence of cellular involvement in the formation of humoral capsules, both at the initial and terminal stages of the encapsulation process. The role of phenoloxidase system in non-self recognition and in the process of melanization of haemolymph and capsules formed around parasites and fungal pathogens is also discussed. Immune defence of insect vectors against bacterial invasion by means of haemocytic reactions e.g. phagocytosis and nodule formation and by synthesis and release of humoral antibacterial factors e.g. lysozyme, attacins and cecropins is described and compared with similar reactions reported to occur in other insects. The role of lectins in defence of insect vectors against the parasites they transmit e.g. sandflies against Leishmania, blackflies against Onchocerca and tsetse against Trypanosomes is discussed and the possible mechanisms by which some parasites evade recognition and attack by the vector immune systems are also briefly discussed.

Résumé

Les différents modes de réactions immunisées des insectes vecteurs de maladies humaines et animates centre les nématodes et les protozoaires parasites, les champignons les bactéries, les viruses et autres matériels biologiques par exemple xenogratis sont discutés dans cette publication. Comme plus d' insectes vecteurs de maladies sont des diptères adultes ayant un nombre inférieur d'hemocytes, leur mode de défense centre les métazoaires parasites et les champignons pathogènes est principalement par moyen d'encapsulation humorale, avec une moindre participation d'hemocyte. Bien que des recherches antérieures ont montré que les capsules humorales chez les diptères étaient formées sans participation directe d'hemocytes, cette publication révèle une évidence accrue sur la participation cellulaire dans la formation des capsules humorales, au niveau initial et final du processus d'encapsulation. Le rôle du système phenoloxidase dans le processus de melanisation d'hémolymphe et les capsules formées autour des parasites et des champignons pathogènes est aussi discuté. La défense immunisée des insectes vecteurs centre l'invasion bactérienne par moyen de réactions hémocytaire par exemple la phagocy tose et la formation de nodules et par la synthèse et la liberation des éléments antibactériens humoraux par example lysosomes, attacines et cecropines est décrite et comparée aux réaction apparues chez d'autres insectes. Le rôle de lectines dans la défense des insectes vecteurs contre les parasites qu'ils transmettent par exemple les phlébotomes contre Leishmania, les slmulies contre l'Onchocerca et les mouches tsé-tsé contre Trypanosoma est discuté. Les mecanismes possibles par lesquels certains parasites échappent d'être reconnues et attaqués par les systèmes vecteurs ‘immunises’ sont aussi brièvement discutés.

Type
Reviews: A Ten Year Perspective of Insect Science 1980–1989
Copyright
Copyright © ICIPE 1989

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References

REFERENCES

Amouriq, L. (1960) Formules hemocytaires de la larve de la nymphe et de l'adulte de Culex hortensis (Dipt. Culicidae). Bull. Soc. Entomol. (France) 65, 135139.CrossRefGoogle Scholar
Andreadis, T.G. and Hall, D.W. (1976) Neoaplectana carpocapsae: Encapsulation in Aedes aegypti and the changes in host hemocyte and hemolymph proteins. Exp. Parasitol. 39, 252261.CrossRefGoogle ScholarPubMed
Bhat, U.K.M. and Singh, K.R.P. (1975) The haemocytes of the mosquito Aedes albopictus and their comparison with larval cells cultured in vitro. Experiential 31, 13311332.CrossRefGoogle Scholar
Bishop, D.H.L. and Beaty, B.J. (1986) Inteference-immunity of mosquitoes to bunyavirus superinfection. In Immune Mechanisms in Invertebrate Vectors(Edited by Lackie, A.M.), pp. 95115, Clarendon Press, Oxford.Google Scholar
Bitkowska, E., Dzbenski, T.H., Szadziewska, M. and Wegner, Z. (1982) Inhibitions of xenograft rejection reaction in the bug Triatoma infestans during infection with a protozoan, Trypanosoma cruzi. J. Invertebr. Pathol. 40, 186189.CrossRefGoogle ScholarPubMed
Boman, H.G. and Hultmark, D. (1987) Cell-free immunity in insects. A. Rev. Microbiol. 41, 103126.CrossRefGoogle ScholarPubMed
Bradley, T.J. and Nayar, J.K. (1985) Intracellular melanization of the larvae of Dirofilaria immitis in the malpighian tubules of the mosquito Aedes sollicitans. J. Invertebr. Pathol. 45, 339345.CrossRefGoogle ScholarPubMed
Brey, P.T., Lebrum, R.A., Papierok, B., Ohayon, H., Vennavalli, S. and Hafez, J. (1988) Defense reactions by larvae of Aedes aegypti during infection by the aquatic fungus Lagenidium giganteum (Oomycete). Cell Tissue Res. 253, 245250.CrossRefGoogle ScholarPubMed
Bronskill, J.F. (1962) Encapsulation of rhabditoid nematodes in mosquitoes. Can. J. Zool. 40, 12691275.CrossRefGoogle Scholar
Cameron, G.R. (1934) Inflammation in the caterpillars of Lepidoptera. J. Pathol. Bacterial. 38, 441466.CrossRefGoogle Scholar
Chaithong, U. and Townson, H. (1989) Immune responses of mosquitoes to filariae and bacteria. Proc. Int. Symp. Mol. Ins. Sci., October 22–27, Tucson, Arizona, USA p. 17.Google Scholar
Chen, C.C. and Laurence, B.R. (1985) An ultrastructural study on the encapsulation of microfilariae of Brugia pahangi in the haemocoel of Anopheles quadrimaculatus. Int. J. Parasitol. 15, 421428.CrossRefGoogle Scholar
Christensen, B.M. and Forton, K.F. (1986) Hemocytemediated melanization of microfilariae in Aedes aegypti. J. Parasitol. 72, 220225.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
Christensen, B.M., Lafond, M.M. and Christensen, L.A. (1986) Defense reactions of mosquitoes to filarial worms: Effect of host age on the immune response to Dirofilaria immitis microfilariae. J. Parasitol. 72, 212215.CrossRefGoogle ScholarPubMed
Christensen, B.M., Sutherland, D.R. and Gleason, L.N. (1984) Defence reactions of mosquitoes to filarial worms: Comparative studies on the response of three different mosquitoes to inoculated Brugia pahangi and Dirofilaria immitis microfilariae. J. Invertebr. Pathol. 44, 267274.CrossRefGoogle ScholarPubMed
Collins, F.H., Sakai, R.K., Vernick, K.D., Paskewitz, S., Seeley, D. C., Miller, L.H., Collins, W.E., Campbell, C.C. and Gwadz, R.W. (1986) Genetic selection of aplasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234, 607609.CrossRefGoogle ScholarPubMed
Croft, S. L., East, J.S. and Molyneux, D.H. (1982) Anti-trypanosomal factor in the haemolymph of Glossina. Acta Trop. (Basel) 39, 293302.Google ScholarPubMed
Dalhammar, G. and Steiner, H. (1984) Characterization of inhibitor A—A protease from Bacillus thuringiensis which degrades attacins and cecropins, two classes of antibacterial proteins in insects. Eur. J. Biochem. 139, 247252.CrossRefGoogle Scholar
Dimarcq, J.L., Keppi, E., Dunbar, B., Lambert, J., Reichmart, J.M., Hoffmann, D., Rankine, S.M., Fothergill, J.E. and Hoffmann, J.A. (1988) Insect immunity: Purification and characterization of a family of novel inducible antibacterial proteins from immunized larvae of the dipteran Phormia terranovae and complete amino-acid sequence of the predominant member, diptericin A. Eur. J. Biochem. 171, 1722.CrossRefGoogle ScholarPubMed
Dimarcq, J.L., Reichhart, J. M., Lambert, J., Wicker, C., Hoffmann, J. and Hoffmann, D. (1989) Insect immunity: Molecular characterization of Diptericins and insect defensins, two families of induced antibacterial peptides from the dipteran Phormia terranovae. Int. Symp. Molec. Ins. Sci. October 22–27, Tucson, Arizona, USA, p. 28.Google Scholar
Distelmans, W., D'Haeseleer, F., Kaufman, L. and Rousseeuw, P. (1982) The susceptibility of Glossina palpalis palpalis at different ages to infection with Trypanosoma congolense. Ann. Soc. Belg. Med. Trop. 62, 4147.Google ScholarPubMed
Drif, L. and Brehelin, M. (1983) The circulating hemocytes of Culex pipiens and Aedes aegypti: Cytology, histochemistry, hemograms and functions. Dev. Comp. Immunol. 7, 687690.CrossRefGoogle Scholar
Dunn, P.E. (1986) Biochemical aspects of insect immunology. Annu. Rev. Entomol. 31, 321339.CrossRefGoogle Scholar
East, J., Molyneux, D.H. and Hillen, N. (1980) Haemocytes of Glossina. Ann. Trop. Med. Parasitol. 74, 471474.CrossRefGoogle ScholarPubMed
East, J., Molyneux, D.H., Maudlin, I. and Dukes, P. (1983) Effect of Glossina haemolymph on salivarian trypanosomes in vitro. Ann. Trop. Med. Parasitol. 77, 9799.CrossRefGoogle ScholarPubMed
Elce, B.J. (1971) The transmission of Trypanosoma congolense through Glossina morsitans and the white mouse. Trans. R. Soc. Trop. Med. Hyg. 65, 239.CrossRefGoogle Scholar
Elce, B.J. (1974) The development of salivarian trypanosomes in Glossina morsitans and small laboratory animals. Trans. R. Soc. Trop. Med. Hyg. 68, 162.Google Scholar
Esslinger, J.H. (1962) Behaviour of microfilariae of Brugia pahangi in Anopheles quadrimaculatus. Am. J. Trop. Med. Hyg. 1, 749758.CrossRefGoogle Scholar
Foley, D.A. (1978) Innate cellular defence by mosquito hemocytes. In Comparative Pathobiology (Edited by Bulla, A.L. Jr and Cheng, T.C.), pp. 113144, New York, Plenum Press 4.Google Scholar
Forton, K.F., Christensen, B.M. and Sutherland, D.R. (1985) Ultrastructure of the melanization response of Aedes trivittatus against inoculated Dirofilaria immitis microfilariae. J. Parasitol. 71, 331341.CrossRefGoogle ScholarPubMed
Gagen, S.J. and Ratcliffe, N.A. (1976) Studies on the in vivo cellular reactions and fate of injected bacteria in Galleria mellonella and Pieris brassicae larvae. J. Invertebr. Pathol. 28, 1724.CrossRefGoogle Scholar
Gooding, L.G., Green, D.G., Guy, M.W. and Voller, A. (1972) Immunosuppression during trypanosomiasis. Br. J. Exp. Pathol. 53, 4043.Google Scholar
Götz, P. (1986) Mechanisms of encapsulation in dipteran hosts. In Immune Mechanisms in Invertebrate Vectors (Edited by Lackie, A.M.), pp. 119, Clarendon Press, Oxford.Google Scholar
Götz, P., Roettgen, I. and Lingg, W. (1977) Encapsulement humoralen tant que reaction de defense chez les Dipteres. Ann. Parasitol. Hum. Comp. 52, 9597.CrossRefGoogle Scholar
Götz, P. and Vey, A. (1974) Humoral encapsulation in Diptera (Insecta): Defence reaction of Chironomus larvae against fungi. Parasitol. 68, 113.CrossRefGoogle ScholarPubMed
Greenwood, B.M., Whittle, H.C. and Molyneux, D.H. (1973) Immunosuppression in Gambian trypanosomiasis. Trans. R. Soc. Trop. Med. Hyg. 67, 846850.CrossRefGoogle ScholarPubMed
Grimstone, A.V., Rotheram, S. and Salt, G. (1967) An electron microscope study of capsule formation by insect blood cells. J. Cell Sci. 2, 281292.CrossRefGoogle ScholarPubMed
Ham, P.J. and Garms, R. (1988) The relationship between innate susceptibility to Onchocerca and haemolymph attenuation of microfilarial motility in vitro using British and West African blackflies. Trop. Med. Parasitol. 39, 230234.Google ScholarPubMed
Ham, P.J., Zulu, M.B. and Zahedi, M. (1988) In vitro haemagglutination and attenuation of microfilarial motility by haemolymph from individual blackflies (Simulium ornatum) infected with Onchocerca lienalis. Med. Vet. Entomol. 2, 718.CrossRefGoogle ScholarPubMed
Harley, J. (1971) The influence of the age of the fly at the time of the infecting feed on infecting of Glossina fuscipes with Trypanosoma rhodesiense. Ann. Trop. Med. Parasitol. 65, 191196.CrossRefGoogle ScholarPubMed
Harley, J.M.B. and Wilson, A.J. (1968) Comparison between Glossina morsitans, G. pallidipes and G. fuscipes as vectors of trypanosomes of the Trypanosoma congolense group: The proportions infected experimentally and the number of the infective organisms extruded during feeding. Ann. Trop. Med. Parasitol. 62, 178187.CrossRefGoogle Scholar
Harmsen, R. (1973) The nature of the establishment barrier for Trypanosoma brucei in the gut of Glossina pallidipes. Trans. R. Soc. Trop. Med. Hyg. 67, 364373.CrossRefGoogle ScholarPubMed
Harris, K.L., Christensen, B.M. and Miranpuri, G.S. (1986) Comparative studies on the melanization response of male and female mosquitoes against microfilariae. Dev. Comp. Immunol. 10, 305310.CrossRefGoogle ScholarPubMed
Ho, B.C., Yap, E.H. and Singh, M. (1982) Melanization and encapsulation in Aedes aegypti and Aedes togoi in response to parasitization by a filarioid nematode (Breinlia booliati). Parasitol. 85, 567575.CrossRefGoogle ScholarPubMed
Ibrahim, E.A.R., Ingram, G.A. and Molyneux, D.H. (1984) Haemagglutinins and parasite agglutinins in haemolymph and gut of Glossina. Tropenmed. Parasitol. 35, 151156.Google ScholarPubMed
Ingram, G.A., East, J. and Molyneux, D. H. (1983) Agglutinins of Trypanosoma, Leishmania and Crithidia in insect haemolymph. Dev. Comp. Immunol. 7, 649652.CrossRefGoogle Scholar
Ingram, G.A., East, J. and Molyneux, D.H. (1984) Naturally occurring agglutinins against trypanosomatid flagellates in the haemolymph of insects. Parasitol. 89, 435451.CrossRefGoogle ScholarPubMed
Jones, J.C. (1953) On the heart in relation to circulation of hemocytes in insects. Ann. Entomol. Soc. Am. 46, 366372.CrossRefGoogle Scholar
Jones, J.C. (1958) Heat fixation and the blood cells of Aedes aegypti larvae. Anat. Rec. 132, 461.Google Scholar
Kaaya, G.P., Boman, H.G. and Flyg, C. (1987) Insect immunity: Induction of cecropin and attacin-like antibacterial factors in the haemolymph of Glossina morsitans morsitans. Insect Biochem. 17, 309315.CrossRefGoogle Scholar
Kaaya, G.P. and Darji, N. (1988) The humoral defence system in tsetse: Differences in response due to age, sex and antigen types. Dev. Comp. Immunol. 12, 255268.CrossRefGoogle ScholarPubMed
Kaaya, G.P. and Otieno, L.H. (1981) Haemocytes of Glossina: I. Morphological classification and the pattern of change with age of the flies. Insect Sci. Applic. 2, 175180.Google Scholar
Kaaya, G.P. and Ratcliffe, N.A. (1982) Comparative study of haemocytes and the associated cells of some medically important Dipterans. J. Morphol. 173, 351365.CrossRefGoogle Scholar
Kaaya, G.P., Ratcliffe, N.A. and Alemu, P. (1986a) Cellular and humoral defenses of Glossina (Diptera: Glossinidae): Reactions against bacteria, trypanosomes and experimental implants. J. Med. Entomol. 23, 3043.CrossRefGoogle ScholarPubMed
Kaaya, G.P., Otieno, L.H., Darji, N. and Alemu, P. (1986b) Defense reactions of Glossina morsitans morsitans against different species of bacteria and Trypanosoma brucei brucei. Ada Trop. 43, 3142.Google ScholarPubMed
Keppi, E., Zachary, D., Robertson, M., Hoffmann, D. and Hoffmann, J.A. (1986) Inducible antibacterial proteins in the haemolymph of Phormia terranovae (Diptera). Purification and possible origin of one protein. Insect Biochem. 16, 395402.CrossRefGoogle Scholar
Kirschbaum, J.B. (1985) Potential implication of genetic engineering and other biotechnologies to insect control. Annu. Rev. Entomol. 30, 5170.CrossRefGoogle ScholarPubMed
Kockum, K., Faye, I., Hofsten, P.V., Lee, J.Y., Xanthopoulos, K.G. and Boman, H.G. (1984) Insect immunity: Isolation and sequence of two cDNA clones corresponding to acidic and basic attacins from Hyalophora cecropia. EMBO J. 3, 20712075.CrossRefGoogle ScholarPubMed
Komano, H. and Natori, S. (1985) Participation of Sarcophaga peregrina humoral lectin in the lysis of sheep red blood cells injected into the abdominal cavity of larvae. Dev. Comp. Immunol. 9, 3140.CrossRefGoogle ScholarPubMed
Lafond, M.M., Christensen, B.M. and Lasee, B.A. (1985) Defense reactions of mosquitoes to filarial worms: Potential mechanism for avoidance of the response by Brugia pahangi microfilariae. J. Invertebr. Pathol. 46, 2630.CrossRefGoogle ScholarPubMed
Lee, J.Y., Edlund, T., Ny, T., Faye, I. and Boman, H.G. (1983) Insect immunity: Isolation of cDNA clones corresponding to attacins and immune protein P4 from Hyalophora cecropia. EMBO J. 2, 577581.CrossRefGoogle ScholarPubMed
Matsumoto, N., Okada, M., Takahashi, H., Ming, Q. X., Nakajima, Y. (1986) Molecular cloning of a cDNA and assignment of the C-terminal of sarcotoxin 1A, a potent antibacterial protein of Sarcophaga peregrina. Biochem. J. 239, 717722.CrossRefGoogle Scholar
Maudlin, I. and Ellis, D.S. (1985) Association between intracellular rickettsial-like infections of midgut cells and susceptibility to trypanosome infection in Glossina spp. Z. Parasiten. 71, 683687.CrossRefGoogle Scholar
Maudlin, I., Kabayo, J.P., Flood, M.E.T. and Evans, D.A. (1984) Serum factors and the maturation of Trypanosoma congolense infections in Glossina morsitans. Z. Parasiten. 70, 1119.CrossRefGoogle ScholarPubMed
Maudlin, I. and Welburn, S.C. (1987) Lectin mediated establishment of midgut infections of Trypanosoma congolense and Trypanosoma brucei in Glossina morsitans. Trop. Med. Parasitol. 38, 167170.Google ScholarPubMed
Maudlin, I. and Welburn, S.C. (1988a) The role of lectins and trypanosome genotype in the maturation of midgut infections in Glossina morsitans. Trop. Med. Parasitol. 39, 5658.Google ScholarPubMed
Maudlin, I. and Welburn, S.C. (1988b) Tsetse immunity and the transmission of trypanosomiasis. Parasitol. Today 4, 109111.CrossRefGoogle ScholarPubMed
Moloo, S.K. and Shaw, M.K. (1989) Rickettsial infections of midgut cells are not associated with susceptibility of Glossina morsitans centralis to Trypanosoma congolense infection. Acta Trop. 46, 223227.CrossRefGoogle Scholar
Molyneux, D.H., Takle, G., Ibrahim, E.A. and Ingram, G.A. (1986) Insect immunity to trypanosomatidae. In Immune Mechanisms in Invertebrate Vectors (Edited by Lackie, A.M.), pp. 117144, Clarendon Press, Oxford.Google Scholar
Mshelbwala, A.S. (1972) Trypanosoma brucei in the haemocoele of tsetse flies. Trans. R. Soc. Trop. Med. Hyg. 66, 637643.CrossRefGoogle ScholarPubMed
Natori, S. (1977) Bactericidal substance induced in the haemolymph of Sarcophaga peregrina larvae. J. Insect Physiol. 23, 11691173.CrossRefGoogle Scholar
Okada, M. and Natori, S. (1985a) Ionophore activity of Sarcotoxin I, a bactericidal protein of Sarcophaga peregrina. Biochem J. 229, 453458.CrossRefGoogle Scholar
Okada, M. and Natori, S. (1985b) Primary structure of Sarcotoxin I, an antibacterial protein induced in the haemolymph of Sarcophaga peregrina (Flesh fly) larvae. J. Biol. Chem. 260, 71747177.CrossRefGoogle ScholarPubMed
Orihel, T.C. (1975) The peritrophic membrane: Its role as a barrier to infection of the arthropod host. In Invertebrate Immunity (Edited by Maramorosch, K. and Shope, R.E.), pp. 6573, Academic Press, Inc., New York, San Francisco, London.CrossRefGoogle Scholar
Otieno, L.H. (1973) Trypanosoma (Trypanozoon) brucei in the haemolymph of experimentally infected young Glossina morsitans. Trans. R. Soc. Trop. Med. Hyg. 67, 886887.CrossRefGoogle ScholarPubMed
Otieno, L.H., Darji, N. and Onyango, P. (1976) Development of Trypanosoma (Trypanozoon) brucei in Glossina morsitans inoculated into the tsetse haemocoele. Acta Trop. (Basel) 33, 143150.Google Scholar
Pendland, J.C., Heath, M.A. and Boucias, D.G. (1988) Function of a galactose-binding lectin from Spodoptera exigua larval haemolymph: Opsonization of blastospores from entomogenous hyphomycetes. J. Insect Physiol. 34, 533540.CrossRefGoogle Scholar
Pereira, M.E.A., Andrade, A.F.B. and Ribeiro, J.M.C. (1981) Lectins of distinct specificity inRhodnius prolixus interact selectively with Trypanosoma cruzi. Science N.Y. 211, 597600.CrossRefGoogle ScholarPubMed
Pereira, M.E., Loures, M.A., Villalta, F. and Andrade, A.F.B. (1980) Lectin receptors as markers for Trypanosoma cruzi: Developmental stages and a study of the interaction of wheat germ agglutinin with sialic acid residue on epimastigote cells. J. Exp. Med. 152, 13751392.CrossRefGoogle Scholar
Peters, W., Kolb, H. and Kolb-Bachofen, V. (1983) Evidence for a sugar receptor (lectin) in the peritrophic membrane of the blowfly larva, Calliphora erythrocephala Mg. (Diptera). J. Insect Physiol. 29, 275280.CrossRefGoogle Scholar
Poinar, G.O. Jr, Hess, R.T., Hansen, E. and Hansen, J.W. (1979) Laboratory infection of blackflies (Simuliidae) and midges (Chironomidae) by the mosquito mermithid, Romanomermis culicivorax. J. Parasitol. 64, 613615.CrossRefGoogle Scholar
Poinar, G.O. Jr and Leutenegger, R. (1971) Ultrastructural investigation of the melanization process in Culex pipiens (Culicidae) in response to a nematode. J. Ultrastruc. Res. 36, 149158.CrossRefGoogle ScholarPubMed
Ratcliffe, N.A. (1986) Insect cellular immunity and the recognition of foreignness. In Immune Mechanisms in Invertebrate Vectors (Edited by Lackie, A.M.), pp. 2143, Clarendon Press, Oxford.Google Scholar
Ratcliffe, N.A. and Gagen, S.J. (1976) Cellular defense reactions of insect hemocytes in vivo: Nodule formation and development in Galleria mellonella and Pieris brassicae larvae. J. Invertebr. Pathol. 28, 373382.CrossRefGoogle Scholar
Ratcliffe, N.A. and Gagen, S.J. (1977) Studies on the in vivo cellular reactions of insects: An ultrastructural analysis of nodule formation in Galleria mellonella. Tissue Cell 9, 7385.CrossRefGoogle ScholarPubMed
Ratcliffe, N.A., Leonard, C. and Rowley, A.F. (1984) Prophenoloxidase activation: Nonself recognition and cell cooperation in insect immunity. Science 226, 557559.CrossRefGoogle ScholarPubMed
Ratcliffe, N.A. and Rowley, A.F. (1979) Role of hemocytes in defence against biological agents. In Insect Hemocytes, Development, Forms, Functions and Techniques (Edited by Gupta, A.P.), pp. 331414, Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Ratcliffe, N.A., Rowley, A.F., Fitzgerald, S.W. and Rhodes, C. (1985) Invertebrate immunity: Basic concepts and recent advances. Int. Rev. Cytol. 97, 183350.CrossRefGoogle Scholar
Renwrantz, L. (1986) Lectins in molluscs and arthropods: Their occurrence, origin and roles in immunity. In Immune Mechanisms in Invertebrate Vectors (Edited by Lackie, A.M.), pp. 8193, Clarendon Press, Oxford.Google Scholar
Renwrantz, L. and Stahmer, A. (1983) Opsonising properties of an isolated hemolymph agglutinin and demonstration of lectin-like recognition molecules at the surface of hemocytes from Mytilusedulis. J. Comp. Physiol. 149B, 535546.CrossRefGoogle Scholar
Salt, G. (1968) The resistance of insect parasitoids to the defence reactions of their hosts. Biol. Rev. (Cambridge). 43, 200232.CrossRefGoogle Scholar
Salt, G. (1973) Experimental studies in insect parasitism XVI: The mechanism of the resistance of Nemeritis to defence reactions. Proc. R. Soc. Lond. 183, 337350.Google Scholar
Schmit, A.R. and Ratcliffe, N.A. (1977) The encapsulation of foreign tissue implants in Galleria mellonella larvae. J. Insect Physiol. 23, 175184.CrossRefGoogle ScholarPubMed
Schmittner, S.M. and McGhee, R.B. (1970) Host specificity of various species of Crithidia Leger. J. Parasitol. 56, 684693.CrossRefGoogle Scholar
Sutherland, D.R., Christensen, B.M. and Forton, K.F. (1984) Defence reactions of mosquitoes to filarial worms: Role of the microfilarial sheath in the response of mosquitoes to inoculated Brugia pahangi microfilariae. J. Invertebr. Pathol. 44, 275281.CrossRefGoogle ScholarPubMed
Takahashi, H., Komano, H., Kawaguchi, N., Kitamura, N. and Nakanishi, S. (1985) Cloning and sequencing of cDNA of Sarcophaga peregrina humoral lectin induced on injury of the body wall. J. Biol. Chem. 260, 1222812233.CrossRefGoogle ScholarPubMed
Von Hofsten, P., Faye, I., Kockum, K., Lee, J.Y., Xanthopoulos, K.G. (1985) Molecular cloning, cDNA sequencing and chemical synthesis of cecropin B from Hyalophora cecropia. Proc. Natl. Acad. Sci, USA 82, 22402243.CrossRefGoogle Scholar
Wallbanks, K.R., Ingram, G.A. and Molyneux, D.H. (1986) The agglutination of erythrocytes and Leishmania parasites by sandfly gut extracts: Evidence for lectin activity. Trop. Med. Parasitol. 37, 409413.Google ScholarPubMed
Walters, J.B. and Ratcliffe, N.A. (1983) Studies on the in vitro cellular reactions of insects: Fate of pathogenic and non-pathogenic bacteria in Galleria mellonella nodule. J. Insect Physiol. 29, 417424.CrossRefGoogle Scholar
Weathersby, A.B. and McCall, J.W. (1968) The development of Plasmodium gallinaceum Brumpt in the haemocoels of refractory Culex pipiens pipiens Linn. and susceptible Aedes aegypti (Linn.). J. Parasitol. 54, 10171022.CrossRefGoogle Scholar
Welburn, S.C., Maudlin, I. and Ellis, D.S. (1989) Rate of trypanosome killing by lectins in midguts of different species and strains of Glossina. Med. Vet. Entomol. 3, 7782.CrossRefGoogle ScholarPubMed
Wijers, D. (1958) Factors that may influence the infection rate of Glossina palpis with Trypanosoma gambiense. I. The age at the time of the infected feed. Ann. Trop. Med. Parasitol. 52, 385390.CrossRefGoogle ScholarPubMed
Wittig, G. (1965) Phagocytosis by blood cells in healthy and diseased caterpillars. I—Phagocytosis of Bacillus thuringiensis Berliner in Pseudaletia unipuncta (Haworth). J. Invertebr. Pathol. 7, 474488.CrossRefGoogle Scholar
Yeaton, R.N. (1981) Invertebrate lectins: I—Occurrence. Dev. Comp. Immunol. 5, 391402.CrossRefGoogle ScholarPubMed
Zachary, D. and Hoffmann, J.A. (1973) The haemocytes of Calliphora erythrocephala (Meig) Diptera. Z. Zellforsch. Mikrosk. Anat. 141, 5573.CrossRefGoogle Scholar
Zachary, D. and Hoffmann, D. (1984) Lysozyme is stored in the granules of certain haemocyte types in Locusta. J. Insect Physiol. 30, 405411.CrossRefGoogle Scholar
Zeledon, R. and Monge, E. (1966) Natural immunity of the bug, Triatoma infestans to the protozoan, Trypanosoma rangeli. J. Invertebr. Pathol. 8, 420424.CrossRefGoogle Scholar