Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-03T01:00:04.716Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunosuppression by larvae of Moniliformis moniliformis (Acanthocephala) in their cockroach host (Periplaneta Americana)

Published online by Cambridge University Press:  06 April 2009

Ann M. Lackie  and
Rohan Holt
Ann M. Lackie
Affiliation:
Department of Zoology, The University, Glasgow G12 8QQ, Scotland
Rohan Holt
Affiliation:
Department of Zoology, The University, Glasgow G12 8QQ, Scotland
Get access Rights & Permissions [Opens in a new window]

Summary

The results of 4 different assays for haemocytic immune responsiveness in the cockroach, Periplaneta americana, have shown that the presence of larvae of Moniliformis moniliformis within the haemocoele depresses the insect's immune reactivity. Thus, the proportion of haemocytes that phagocytose fluorescent latex beads in vivo, the proportion of haemocytes that can be stimulated in vitro by the β1,3-glucan, laminarin, to produce phenoloxidase, and the number of haemocytic aggregates produced in vivo in response to zymosan stimulation, are significantly depressed compared with control, unparasitized cockroaches. Also, when cockroaches are injected intra-haemocoelically with hatched oncospheres of the tapeworm, Hymenolepis diminuta, a higher prevalence and intensity of tapeworm larvae are found in insects already parasitized by M. moniliformis. All of these assays show that depression rather than total suppression of the immune response occurs; in the wild, this may be sufficient to ensure that the cockroach does not succumb to unrelated infections during the long developmental period of the parasite.

Keywords

immunosuppressionhaemocytic responsePeriplaneta americanaMoniliformis moniliformisHymenolepis diminuta
Type
Research Article
Information
Parasitology , Volume 98 , Issue 2 , April 1989 , pp. 307 - 314
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Chain, B. M. & Anderson, R. S. (1983). Inflammation in insects. The release of a plasmatocyte depletion factor following interaction between bacteria and haemocytes. Journal of Insect Physiology 29, 1–4.CrossRefGoogle Scholar
Crompton, D. W. T., Keymer, A. E. & Arnold, S. E. (1984). Investigating over-dispersion: Moniliformis (Acanthocephala) and rats. Parasitology 88, 317–31.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. & Lassière, O. (1987).Acanthocephala. In In Vitro Cultivation of Parasites, 2nd edn (ed. Taylor, A. E. R. and Baker, J. R.), pp. 394–413. London: Academic Press.Google Scholar
Davies, D. H., Strand, M. R. & Vinson, S. B. (1987). Changes in differential haemocyte count and in vitro behaviour of plasmatocytes from host Heliothis virescens caused by Campoletis sonorensis polydnavirus. Journal of Insect Physiology 33, 143–53.CrossRefGoogle Scholar
Dikkeboom, R., Tijnagel, J. M. G. H., Mulder, E. C., Van Der Knaap, W. P. W. (1987). Hemocytes of the pond snail Lymnaea stagnalis generate reactive forms of oxygen. Journal of Invertebrate Pathology 49, 321–31.CrossRefGoogle ScholarPubMed
Dularay, B. & Lackie, A. M. (1987). The effect of biotic and abiotic implants on the recongnition of Blatta orientalis cuticular transplants by the cockroach Periplaneta americana. Developmental and Comparative Immunology 11, 69–77.CrossRefGoogle Scholar
Götz, P., Boman, A. & Boman, H. G. (1981). Interactions between insect immunity and an insect-pathogenic nematode with symbiotic bacteria. Proceedings of the Royal Society of London, B212, 333–50.Google Scholar
Gunnarsson, S. G. S. (1988). Effects in vivo of β1,3-glucans from fungal cell walls on the circulating haemocytes of the desert locust Schistocerca gregaria. Journal of Insect Physiology 34, 47–51.CrossRefGoogle Scholar
Gunnarsson, S. G. S. & Lackie, A. M. (1985). Hemocytic aggregation in Schistocerca gregaria and Periplaneta americana as a response to injected substances of microbial origin. Journal of Invertebrate Pathology 46, 312–19.CrossRefGoogle Scholar
Gunnarsson, S. G. S., Lackie, A. M. & Huxham, I. M.(1988). Infection of Schistocerca gregaria by the fungus Metarhizium anisopliae: Effects on the circulating haemocytes. Journal of Experimental Zoology (in the Press).Google Scholar
Hoffmann, D., Brehélin, M. & Hoffmann, J. A. (1974). Modifications of the hemogram and of the hemocytopoietic tissue of male adults of Locusta migratoria (Orthoptera) after injection of Bacillus thuringiensis. Journal of Invertebrate Pathology 24, 238–47.CrossRefGoogle ScholarPubMed
Holt, R. (1988). Hymenolepis diminuta utilises the envelope surrounding Moniliformis moniliformis in order to survive in the cockroach host. Journal of Parasitology (in the Press).Google Scholar
Huxham, I. M. & Lackie, A. M. (1986). A simple visual method of assessing the activation and inhibition of phenoloxidase production by insect haemocytes in vitro. Journal of Immunological Methods 94, 271–7.CrossRefGoogle Scholar
Huxham, I. M. & Lackie, A. M. (1988). Behaviour in vitro of separated fractions of haemocytes of the locust Schistocerca gregaria. Cell and Tissue Research 251, 677–84.CrossRefGoogle Scholar
Huxham, I. M., Lackie, A. M. & McCorkindale, N. J. (1988). Inhibitory effects of cyclodepsipeptides, destruxins, from the fungus Metarhizium anisopliae on cellular immunity in insects. Journal of Insect Physiology (in the Press).Google Scholar
King, D. & Robinson, E. S. (1967). Aspects of the development of Moniliformis dubius. Journal of Parasitology 53, 142–9.CrossRefGoogle ScholarPubMed
Lackie, A. M. (1976). Evasion of the haemocytic defence reaction of certain insects by larvae of Hymenolepis diminuta (Cestoda). Parasitology 73, 97–107.CrossRefGoogle ScholarPubMed
Lackie, A. M. (1986 a). Evasion of insect immunity by helminth larvae. In Immune Mechanisms in Invertebrate Vectors. Symposia of the Zoological Society of London, vol. 56 (ed. Lackie, A. M.), pp. 161–178. Oxford: Oxford University Press.Google Scholar
Lackie, A. M. (1986 b). Transplantation. The limits of recognition. In Hemocytic and Humoral Immunity in Arthropods (ed. Gupta, A. P.), pp. 191–223. New York: John Wiley & Sons.Google Scholar
Lackie, A. M. (1988 a). Immune mechanisms in insects. Parasitology Today 4, 98–105.CrossRefGoogle ScholarPubMed
Lackie, A. M. (1988 b). Haemocyte behaviour. Advances in Insect Physiology 21 (in the Press).CrossRefGoogle Scholar
Lackie, A. M. & Lackie, J. M. (1979). Evasion of the insect immune response by Moniliformis dubius(Acanthocephala): further observations on the origin of the envelope. Parasitology 79, 297–301.CrossRefGoogle ScholarPubMed
Lackie, A. M. & Vasta, G. R. (1988). The role of galactosyl-binding lectin in the cellular immune response of the cockroach Periplaneta americana (Dictyoptera). Immunology 64, 353–7.Google ScholarPubMed
Lackie, J. M. (1972). The course of infection and growth of Moniliformis dubius (Acanthocephala) in the intermediate host Periplaneta americana. Parasitology 64, 95–106.CrossRefGoogle ScholarPubMed
Lackie, J. M. (1975). The host specificity of Moniliformis dubius (Acanthocephala), a parasite of cockroaches. International Journal for Parasitology 5, 301–7.CrossRefGoogle ScholarPubMed
Lackie, J. M. & Rotheram, S. (1972). Observations on the envelope surrounding Moniliformis dubius (Acanthocephala) in the intermediate host, Periplaneta americana. Parasitology 65, 303–8.CrossRefGoogle ScholarPubMed
O'Brien, V. (1988). The role of the envelope of Moniliformis moniliformis in immune evasion. Ph.D. thesis, University of Glasgow.Google Scholar
Peake, P. W. (1979). Isolation and characterization of the haemocytes of Calliphora vicina on density gradients of Ficoll. Journal of Insect Physiology 25, 795–803.CrossRefGoogle Scholar
Ratcliffe, N. A. (1986). Insect cellular immunity and the recognition of foreign-ness. In Immune Mechanisms in Invertebrate Vectors. Symposia of the Zoological Society of London 56 (ed. Lackie, A. M.), pp. 21–58. Oxford: Oxford University Press.Google Scholar
Rizki, R. M. & Rizki, T. M. (1984). Selective destruction of a host blood cell type by a parasitoid wasp. Proceedings of the National Academy of Sciences, USA 81, 6154–8.CrossRefGoogle ScholarPubMed
Rotheram, S. & Crompton, D. W. T. (1972). Observations on the early relationship between Moniliformis dubius (Acanthocephala) and the haemocytes of the intermediate host, Periplaneta americana. Parasitology 64, 15–21.CrossRefGoogle Scholar
Smith, V. J. & Söderhäll, K. (1986). Cellular immune mechanisms in crustacea. In Immune Mechanisms in Invertebrate Vectors, Symposia of the Zoological Society of London 56 (ed. Lackie, A. M.), pp. 59–80. Oxford: Oxford University Press.Google Scholar
Smith, V. J., SöderhäLL, K. & Hamilton, M. (1984). β1,3-glucan induced cellular defence reactions in the shore crab, Carcinus maenas. Comparative Biochemistry and Physiology 77A, 635–9.CrossRefGoogle Scholar
Stoltz, D. B. & Guzo, D. (1986). Apparent haemocytic transformations associated with parasitoid-induced inhibition of immunity in Malacosoma disstria larvae. Journal of Insect Physiology 32, 377–88.CrossRefGoogle Scholar