Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-29T09:44:31.089Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite development and adaptive specialization

Published online by Cambridge University Press:  06 April 2009

A. E. Bianco  and
R. M. Maizels
A. E. Bianco
Affiliation:
Department of Pure and Applied Biology, Imperial College of Science and Technology, Prince Consort Road, London SW7 2BB
R. M. Maizels
Affiliation:
Department of Pure and Applied Biology, Imperial College of Science and Technology, Prince Consort Road, London SW7 2BB
Get access Rights & Permissions [Opens in a new window]

Summary

The complex life-cycles of parasitic animals are a product of exploiting the process of development to generate organisms with different biological potentials within a species. Successive stages of the parasite adapt to functions such as host invasion and transmission, and to the colonization of a variety of niches, often involving different hosts, tissues or cells. Understanding the molecular basis of adaptive biology among parasities is a major challenge that lies at the heart of research in contemporary parasitology. Differences in scale at the levels of genomic complexity and cell biology exist between most parasitic protozoa and helminths, rendering a cautionary note to making generalized observations. The two principal approaches used to gain insights into adaptive specializations are to start with a biological activity and identify the molecule, or select molecules with particular properties and deduce function. Both have their part to play, with their inherent advantages and limitations, and both are illustrated with examples of studies on adaptive biology among parasitic nematodes.

Keywords

developmentadaptationnematodes
Type
Research Article
Information
Parasitology , Volume 99 , supplement S1: Symposium of the British Society for Parasitoiogy and the Linnean Society Special Issue: Research developments in the study of parasitic infections , January 1989 , pp. S113 - S123
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

Anders, R. F., Coppel, R. L., Brown, G. V., Saint, R. B., Cowman, A. F., Lingelbach, K. R., Mitchell, G. F. & Kemp, D. J. (1984). Plasmodium falciparum complementary DNA clones expressed in Escherichia coli encode many distinct antigens. Molecular Biology and Medicine 2, 177–91.Google ScholarPubMed
Anders, R. F., Murray, L. J., Thomas, L. M., Davern, K. M., Brown, G. v. & Kemp, D. J. (1987). Structure and function of candidate vaccine antigens in Plasmodium falciparum. Biochemical Society Symposia 53, 103–14.Google ScholarPubMed
Bain, O. (1969). Morphology of larval stages and microfilariae of Onchocerca volvulus in Simulium damnosum and redescription of the microfilaria. Annals de Parasitologic Humaine et Comparée 44, 69–81.CrossRefGoogle ScholarPubMed
Bianco, A. E., Crewther, P. E., Coppel, R. L., Stahl, H. D., Kemp, D. J., Anders, R. F. & Brown, G. V. (1988). Patterns of antigen expression in asexual blood stages and gametocytes of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 38, 258–67.CrossRefGoogle ScholarPubMed
Bianco, A. E. & Muller, R. (1982). Experimental transmission of Onchocerca lienalis to calves. In Parasites – Their World and Ours. Proceedings of the Fifth International Congress of Parasitology, August 7–14, Toronto, 1982. Molecular and Biochemical Parasitology, Suppl. p. 349.Google Scholar
Blackwell, J. M., Ezekowitz, R. A. B., Roberts, M. B., Channon, J. Y., Sim, R. B. & Gordon, S. (1985). Macrophage complement and lectin-like receptors bind Leishmania in the absence of serum. Journal of Experimental Medicine 4, 705–15.Google Scholar
Brown, G. V., Culvenor, J. G., Crewther, P. E., Bianco, A. E., Coppel, R. L., Saint, R. B., Stahl, H. D., Kemp, D. J. & Anders, R. F. (1985). Localization of the ring-infected erythrocyte surface antigen of Plasmodium falciparum in merozoites and ring-infected erythrocytes. Journal of Experimental Medicine 162, 774–9.CrossRefGoogle ScholarPubMed
Camus, D. & Hadley, T. J. (1985). A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 230, 553–6.CrossRefGoogle ScholarPubMed
Carter, R. & Miller, L. H. (1979). Evidence for environmental modulation of gametocytogenesis Plasmodium falciparum in continuous culture. Bulletin of the World Health Organization 57, Suppl 1, 37–52.Google ScholarPubMed
Coppel, R. L., Brown, G. V., Langford, C. J., Bianco, A. E., Stahl, H. D., McIntyre, P., Corcoran, L. M., Woodrow, G., Favaloro, J. M., Crewther, P. E., Mitchell, G. F., Anders, R. F. & Kemp, D. J. (1985). Production of asexual blood stage antigens. In Proceedings of the First Asia and Pacific Conference on Malaria; Practical Considerations on Malaria Vaccines and Clinical Trials, Hawaii.Google Scholar
Coppel, R. L., Cowman, A. F., Anders, R. F., Bianco, A. E., Saint, R. B., Lingelbach, K. R., Kemp, D. J. & Brown, G. V. (1984). Immune sera recognize on erythrocytes a Plasmodium falciparum antigen composed of repeated amino acid sequences. Nature, London 310, 789–91.CrossRefGoogle ScholarPubMed
De Savigny, D. H. (1975). In vitro maintenance of Toxocara canis larvae and a simple method for the production of Toxocara ES antigen for the use in serodiagnostic tests for visceral larva migrans. Journal of Parasitology 61, 781–2.CrossRefGoogle Scholar
Doenhoff, M. J., Hassounah, O. A. & Lucas, S. B. (1985). Does the immunopathology induced by schistosome eggs potentiate parasite survival? Immunology Today 6, 203–6.CrossRefGoogle ScholarPubMed
Duke, B. O. L. (1980). Observations on Onchocerca volvulus in experimentally infected chimpanzees. Tropenmedizin und Parasitologie 31, 41–5.Google ScholarPubMed
Eichler, D. A. (1971). Studies on Onchocerca gutturosa (Newmann 1910) and its development in Simulium ornatum. 2. Behaviour of S. ornatum in relation to the transmission of O. gutturosa. Journal of Helminthology 45, 259–70.CrossRefGoogle Scholar
Eichler, D. A. & Nelson, G. S. (1971). Studies on Onchocerca gutturosa (Newmann 1910) and its development in Simulium ornatum. 1. Observations on O. gutturosa in cattle in south-east England. Journal of Helminthology 45, 245–58.CrossRefGoogle Scholar
Epstein, H. F., Waterston, R. H. & Brenner, S. (1974). A mutant affecting the heavy chain of myosin in Caenorhabditis elegans. Journal of Molecular Biology 90, 291–300.CrossRefGoogle ScholarPubMed
Glickman, L. T. & Schantz, P. M. (1981). Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiological Reviews 3, 230–50.CrossRefGoogle ScholarPubMed
Harris, H. E. & Epstein, H. F. (1977). Myosin and paramyosin of Caenorhabditis elegans: biochemical and structural properties of wild-type and mutant proteins. Cell 10, 709–19.CrossRefGoogle ScholarPubMed
Hawking, F. (1967). The twenty-four hour periodicity of microfilariae: Biological mechanisms responsible for its production and control. Proceedings of the Royal Society, B 169, 59–76.Google Scholar
Hermentin, P. (1987). Malaria invasion of human erythrocytes. Parasitology Today 3, 52–5.CrossRefGoogle ScholarPubMed
Hinck, L. W. & Ivey, M. H. (1976). Proteinase activity in Ascaris suum eggs, hatching fluid and excretions/secretions. Journal of Parasitology 62, 771–4.CrossRefGoogle ScholarPubMed
Hotez, P. J., Le Trang, N., McKerrow, J. H. & Cerami, A. (1985). Isolation and characterization of a proteolytic enzyme from the adult hook worm Ancylostoma caninum. Journal of Biological Chemistry 260, 7343–8.CrossRefGoogle Scholar
Howard, R. J. (1988). Plasmodium falciparum proteins at the host erythrocyte membrane: their biological and immunological significance and novel parasite organelles which deliver them to the cell surface. In The Biology of Parasitism: A Molecular and Immunological Approach: (ed. Englund, P. T. & Sher, A.), pp. 111–145. New York: Alan R. Liss Inc.Google Scholar
Jans, C. & Mons, B. (1987). DNA synthesis and genome structure of Plasmodium: a review. Acta Leidensia 56, 1–13.Google Scholar
Johnson, C. D., Duckett, J. G., Culotti, J. G., Herman, R. K., Meneely, P. M. & Russell, R. L. (1981). An acetylcholinesterase-deficient mutant of the nematode Caenorhabditis elegans. Genetics 97, 261–79.CrossRefGoogle ScholarPubMed
Joiner, K. A. (1988). Molecular basis for interactions between parasites and the complement cascade. In The Biology of Parasitism: A Molecular and Immunological Approach (ed. Englund, P. T. & Sher, A.), pp. 309–328. New York: Alan R. Liss Inc.Google Scholar
Lok, J. B., Pollack, R. J., Cupp, E. W., Bernardo, M. J., Donnelly, J. J. & Albiez, E. J. (1984). Development of Onchocerca lienalis and O. volvulus from the third to fourth larval stage in vitro. Tropenmedizin und Parasitologie 35, 209–11.Google Scholar
Lee, D. L. (1970). The fine structure of the excretory system in adult Nippostrongylus braziliensis (Nematoda) and a suggested function for the excretory glands. Tissue and Cell 2, 225–31.CrossRefGoogle Scholar
Maina, C. V., Grandea, A. G., Tuyen, A. T. K., Asikin, N., Williams, S. A. & McReynolds, L. A. (1987). Dirofilaria immitis: Genomic complexity and characterization of a structural gene. In Molecular Paradigms for Eradicating Helminthic Parasites, pp. 193–204. New York: A. R. Liss.Google Scholar
Maizels, R. M., De Savigny, D. & Ogilvie, B. M. (1984). Characterization of surface and excretory-secretory antigens of Toxocara canis infective larvae. Parasite Immunology 6, 23–37.CrossRefGoogle ScholarPubMed
Maizels, R. M., Kennedy, M. W., Meghji, M., Robertson, B. D. & Smith, H. v. (1987). Shared carbohydrate epitopes on distinct surface and secreted antigens of the parasitic nematode Toxocara canis. Journal of Immunology 139, 207–14.CrossRefGoogle ScholarPubMed
McLaren, D. J. (1974). The anterior glands of Necator americanus (Nematoda: Strongyloidea) I. Ultra-structural studies. International Journal for Parasitology 4, 25–37.CrossRefGoogle Scholar
McKerrow, J. H., Keene, W. E., Jeong, K. H. & Werb, Z. (1983), Degradation of extracellular matrix by larvae of Schistosoma mansoni. 1. Degradation by cercariae as a model for initial parasite invasion of host. Laboratory Investigation 49, 195–200.Google Scholar
McKerrow, J. H., Pino-Heiss, S., Lindquist, R. & Werb, Z. (1985). Purification and characterization of an elastinolytic proteinase secreted by cercariae of Schistosoma mansoni. Journal of Biological Chemistry 260, 3703–7.CrossRefGoogle ScholarPubMed
Meghji, M. & Maizels, R. M. (1986). Biochemical properties of larval excretory-secretory glycoproteins of the parasitic nematode Toxocara canis. Molecular and Biochemical Parasitology 18, 155–70.CrossRefGoogle ScholarPubMed
Miller, L. H., Haynes, J. D., McAuliffe, F. M., Shiroishi, T., Durocher, J. R. & McGinniss, M. H. (1977). Evidence for differences in erythrocyte surface receptors for the malaria parasites Plasmodium falciparum and Plasmodium knowlesi. Journal of Experimental Medicine 146, 277–81.CrossRefGoogle Scholar
Miller, L. H., Mason, S. J., Clyde, D. F. & McGinniss, M. H. (1976). The resistance factor to Plasmodium vivax in blacks: the Duffy-Blood-Group Genotype FyFy. New England Journal of Medicine 295, 302–4.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Beall, J. A., Cruise, K. M., Tui, W. U. & Garcia, E. G. (1985). Antibody responses to the antigen Sj26 of Schistosoma japonicum worms that is recognised by genetically resistant 129/J mice. Parasite Immunology 7, 165–78.CrossRefGoogle Scholar
Muniz, J. & Borriello, A. (1945). Estudo sobre a acao litica de diferentes soros sobre as formas de cultura e sanguicolas do Schizotrypanum cruzi. Revista Brasileira de Biologia 5, 563–76.Google ScholarPubMed
Nardin, E., Gwadz, R. W. & Nussenzweig, R. S. (1979). Characterisation of sporozoite surface antigens by indirect immunofluorescence: detection of stage- and species-specific antimalarial antibodies. Bulletin of the World Health Organization 57, 211–17.Google ScholarPubMed
Newport, G., McKerrow, J., Barr, P. & Agabian, N. (1987). Stage-specific expression of schistosome proteases. Molecular Strategies of Parasitic Invasion. UCLA Symposia on Molecular and Cellular Biology, New Series 42, 121–31.Google Scholar
Nogueria, N., Bianco, C. & Cohn, Z. (1975). Studies on the selective lysis and purification of Trypanosoma cruzi. Journal of Experimental Medicine 142, 224–9.CrossRefGoogle Scholar
Ogilvie, B. M., Rothwell, T. L. W., Bremner, K. C., Schnitzerling, H. J., Nolan, J. & Keith, R. K. (1973). Acetylcholinesterase secretion by parasitic nematodes – I. Evidence for secretion by a number of species. International Journal for Parasitology 3, 589–97.CrossRefGoogle ScholarPubMed
Pasvol, G., Wainscoat, J. S. A. & Weatherall, D. J. (1982). Erythrocytes deficient in glycophorin resist invasion by the malaria parasite Plasmodium falciparum. Nature, London 297, 64–6.CrossRefGoogle Scholar
Perlmann, H., Berzins, K., Wahlgren, M., Carlsson, J., Bjorkman, A., Patarroyo, M. E. & Perlmann, P. (1984). Antibodies in malaria sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum. Journal of Experimental Medicine 159, 1686–1704.CrossRefGoogle ScholarPubMed
Philipp, M. (1984). Acetylcholinesterase secreted by intestinal nematodes: a reinterpretation of its putative role of ‘biochemical holdfast’. Transactions of the Royal Society for Tropical Medicine and Hygiene 78, 138–9.CrossRefGoogle ScholarPubMed
Purkeson, J. & Despommier, D. D. (1974). Fine structure of the muscle phase of Trichinella spiralis in the mouse. In Trichinellosis (ed. Kim, C.). New York: Intext Editions, pp. 7–23.Google Scholar
Rathaur, S., Robertson, B. D., Selkirk, M. E. & Maizels, R. M. (1987). Secretory acetylcholinesterases from Brugia malayi adult and microfilarial parasites. Molecular and Biochemical Parasitology 26, 257–65.CrossRefGoogle ScholarPubMed
Ravetch, J. V., Kochan, J. & Perkins, M. (1985). Isolation of the gene for a glycophorin-binding protein implicated in erythrocyte invasion by a malaria parasite. Science 227, 1593–7.CrossRefGoogle ScholarPubMed
Rhoads, M. L. (1983). Trichinella spiralis: identification and purification of superoxide dismutase. Experimental Parasitology 56, 41–54.CrossRefGoogle ScholarPubMed
Rhoads, M. L. (1984). Secretory cholinesterases of nematodes: Possible functions in the host–parasite relationship. Tropical Veterinarian 2, 3–10.Google Scholar
Roberts, J. M. D., Neumann, E., Goeckel, C. W. & Highton, R. B. (1967). Onchocerciasis in Kenya, 9, 11 and 18 years after elimination of the vector. World Health Organization Bulletin 37, 195–212.Google ScholarPubMed
Robertson, B. D., Bianco, A. E., McKerrow, J. & Maizels, R. M. (1989). Toxocara canis: proteolytic enzymes secreted by the infective larvae in vitro. Experimental Parasitology (in the Press).CrossRefGoogle ScholarPubMed
Robertson, B. D., Kwan-Lim, G-E. & Maizels, R. M. (1988). A sensitive microplate assay for the detection of proteolytic enzymes using radiolabeled gelatin. Analytical Biochemistry 172, 284–7.CrossRefGoogle ScholarPubMed
Sacks, D. (1988). Developmental biology of Leishmania promastigotes. In The Biology of Parasitism: A Molecular and Immunological Approach (ed. Englund, P. T. & Sher, A.), pp. 93–103. New York: Alan R. Liss Inc.Google Scholar
Scothorn, M. W., Koutz, F. R. & Groves, H. F. (1965). Prenatal Toxocara canis infection in pups. Journal of the American Veterinary Medical Association 146, 45–8.Google ScholarPubMed
Selkirk, M. E., Rutherford, P. J., Denham, D. A., Partono, F. & Maizels, R. M. (1987). Cloned antigen genes of Brugia filarial parasites. Biochemical Society Symposia 53, 91–102.Google ScholarPubMed
Smith, D. M., Davern, K. M., Board, P. G., Tui, W. U., Garcia, E. G. & Mitchell, G. F. (1986). M 26000 antigen of Schistosoma japonicum recognized by resistant WEHI 129/J mice is a parasite gluthathione S-transferase. Proceedings of the National Academy of Sciences, USA 83, 8703–7.CrossRefGoogle Scholar
Stewart, G. L. & Giannini, S. H. (1982). Striated muscle parasites: a review. Experimental Parasitology 53, 406–47.CrossRefGoogle ScholarPubMed
Van Schravendijk, M. R., Wilson, R. J. M. & Newbold, C. I. (1987). Possible pitfalls in the identification of glycophorin-binding proteins of Plasmodium falciparum. Journal of Experimental Medicine 166, 376–90.CrossRefGoogle ScholarPubMed
Wakelin, D. (1984). Immunity to Parasites: How Animals Control Parasitic Infections. London: Edward Arnold Publishers Ltd.Google Scholar
Wilson, M. E. & Pearson, R. D. (1986). Evidence that Leishmania donovani utilizes a mannose receptor on human mononuclear phagocytes to establish intracellular parasitism. Journal of Immunology 136, 4681–8.CrossRefGoogle ScholarPubMed