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The ultrastructure of taeniid cestode oncospheres and localization of host-protective antigens

Published online by Cambridge University Press:  16 October 2009

A. JABBAR ,
Z. SWIDERSKI ,
D. MLOCICKI ,
I. BEVERIDGE  and
M. W. LIGHTOWLERS
A. JABBAR
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
Z. SWIDERSKI
Affiliation:
Witold Stefanski Institute of Parasitology, Polish Academy of Sciences, 51/55 Twarda Street, 00-818 Warsaw, Poland Medical University of Warsaw, Department of General Biology and Parasitology, 5 Chalubinskiego Street, 02-004 Warsaw, Poland
D. MLOCICKI
Affiliation:
Witold Stefanski Institute of Parasitology, Polish Academy of Sciences, 51/55 Twarda Street, 00-818 Warsaw, Poland Medical University of Warsaw, Department of Medical Biology, 73, Nowogrodzka Street, 02-018 Warsaw, Poland
I. BEVERIDGE
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
M. W. LIGHTOWLERS*
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
*
*Corresponding author. Tel.: +61 3 9731 2284. Fax.: +61 3 9741 5461. E-mail: marshall@unimelb.edu.au
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Summary

Taeniid eggs contain an infective larval form of the parasite, known as the oncosphere, which has been found to be highly susceptible to attack by the host's immune system and this fact has been exploited in the development of highly effective vaccines. Relatively little is known about the structure of taeniid oncospheres and the localization of host-protective antigens within or on the oncosphere. Here, we briefly review the current state of knowledge of the structure of the oncosphere and present preliminary data on the localization of a host-protective antigen within the oncospheres of Taenia ovis. The precise localization of the antigens, in the context of a detailed knowledge of the ultrastructure of the parasite, may reveal the immune mechanisms by which the taeniid parasites are killed by vaccine-induced immune responses, which, in turn, may provide clues about how vaccines could be developed against other parasitic helminths.

Keywords

oncosphereultrastructurevaccine antigenimmuno-localizationTaeniaEchinococcusCestoda
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 521 - 535
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Benitez, L., Garate, T., Harrison, L. J., Kirkham, P., Brookes, S. M. and Parkhouse, R. M. (1996). Cloning and sequencing of the gene encoding the principal 18-kDa secreted antigen of activated oncospheres of Taenia saginata. Molecular and Biochemical Parasitology 78, 265–268.CrossRefGoogle ScholarPubMed
Bogh, H. O., Rickard, M. D. and Lightowlers, M. W. (1988). Studies on stage-specific immunity against Taenia taeniaeformis metacestodes in mice. Parasite Immunology 10, 255–264.CrossRefGoogle ScholarPubMed
Brahic, M. and Haase, A. T. (1978). Detection of viral sequences of low reiteration frequency by in situ hybridization. Proceedings of the National Academy of Sciences, USA 75, 6125–6129.CrossRefGoogle ScholarPubMed
Chow, C., Gauci, C. G., Cowman, A. F. and Lightowlers, M. W. (2004). Echinococcus granulosus: oncosphere-specific transcription of genes encoding a host-protective antigen. Experimental Parasitology 106, 183–186.CrossRefGoogle ScholarPubMed
Conn, D. B. and Swiderski, Z. (2008). A standardised terminology of embryonic envelopes and associated developmental stages of tapeworms (Platyhelminthes, Cestoda). Folia Parasitologica 55, 42–52.CrossRefGoogle ScholarPubMed
Craig, P. and Pawlowski, Z. (2002). Cestode Zoonoses: Echinococcosis and Cysticercosis an Emergent and Global Problem. IOS Press, Amsterdam.Google Scholar
Craig, P. S. and Larrieu, E. (2006). Control of cystic echinococcosis/hydatidosis: 1863–2002. Advances in Parasitology 61, 443–508.CrossRefGoogle ScholarPubMed
Engelkirk, P. G. and Williams, J. F. (1982). Taenia taeniaeformis (Cestoda) in the rat: ultrastructure of the host–parasite interface on days 1 to 7 postinfection. Journal of Parasitology 68, 620–633.CrossRefGoogle ScholarPubMed
Engelkirk, P. G. and Williams, J. F. (1983). Taenia taeniaeformis (Cestoda) in the rat: ultrastructure of the host–parasite interface on days 8 to 22 postinfection. Journal of Parasitology 69, 828–837.CrossRefGoogle ScholarPubMed
Fairweather, I. and Threadgold, L. T. (1981). Hymenolepis nana: the fine structure of the ‘penetration gland’ and nerve cells within the oncosphere. Parasitology 82, 445–458.CrossRefGoogle ScholarPubMed
Flisser, A., Gauci, C. G., Zoli, A., Martinez-Ocana, J., Garza-Rodriguez, A., Dominguez-Alpizar, J. L., Maravilla, P., Rodriguez-Canul, R., Avila, G., Aguilar-Vega, L., Kyngdon, C., Geerts, S. and Lightowlers, M. W. (2004). Induction of protection against porcine cysticercosis by vaccination with recombinant oncosphere antigens. Infection and Immunity 72, 5292–5297.CrossRefGoogle ScholarPubMed
Furukawa, T., Miyazato, T., Okamoto, K. and Nakai, Y. (1977). The fine structure of the hatched oncopsheres of Hymenolepis nana. Japanese Journal of Parasitology 26, 49–62.Google Scholar
Furukawa, T., Niwa, A. and Miyazato, T. (1981). Ultrastructural aspects of immune damage to Hymenolepis nana oncospheres in mice. International Journal for Parasitology 11, 287–300.CrossRefGoogle ScholarPubMed
Gauci, C., Merli, M., Muller, V., Chow, C., Yagi, K., Mackenstedt, U. and Lightowlers, M. W. (2002). Molecular cloning of a vaccine antigen against infection with the larval stage of Echinococcus multilocularis. Infection and Immunity 70, 3969–3972.CrossRefGoogle ScholarPubMed
Gauci, C. G., Verastegui, M. R., Gilman, R. H. and Lightowlers, M. W. (2006). Taenia solium and Taenia ovis: stage-specific expression of the vaccine antigen genes, TSOL18, TSOL16, and homologues, in oncospheres. Experimental Parasitology 113, 272–275.CrossRefGoogle ScholarPubMed
Gauci, C., Vural, G., Oncel, T., Varcasia, A., Damian, V., Kyngdon, C. T., Craig, P. S., Anderson, G. A. and Lightowlers, M. W. (2008). Vaccination with recombinant oncosphere antigens reduces the susceptibility of sheep to infection with Taenia multiceps. International Journal for Parasitology 38, 1041–1050.CrossRefGoogle ScholarPubMed
Harris, A., Heath, D. D., Lawrence, S. B. and Shaw, R. J. (1987). Ultrastructure of changes at the surface during the early development phases of Taenia ovis cysticerci in vitro. International Journal for Parasitology 17, 903–910.CrossRefGoogle ScholarPubMed
Harris, A., Heath, D. D., Lawrence, S. B. and Shaw, R. J. (1989). Echinococcus granulosus: ultrastructure of epithelial changes during the first 8 days of metacestode development in vitro. International Journal for Parasitology 19, 621–629.CrossRefGoogle ScholarPubMed
Harrison, G. B., Heath, D. D., Dempster, R. P., Gauci, C., Newton, S. E., Cameron, W. G., Robinson, C. M., Lawrence, S. B., Lightowlers, M. W. and Rickard, M. D. (1996). Identification and cDNA cloning of two novel low molecular weight host-protective antigens from Taenia ovis oncospheres. International Journal for Parasitology 26, 195–204.CrossRefGoogle ScholarPubMed
Harrison, L. J. S. and Parkhouse, R. M. E. (1986). Passive protection against Taenia saginata infection in cattle by a mouse monoclonal antibody reactive with the surface of the invasive oncopshere. Parasite Immunology 8, 319–332.CrossRefGoogle Scholar
Heath, D. D. (1971). The migration of oncospheres of Taenia pisiformis, T. serialis and Echinococcus granulosus within the intermediate host. International Journal for Parasitology 1, 145–152.CrossRefGoogle ScholarPubMed
Heath, D. D. (1973). Resistance to Taenia pisiformis larvae in rabbits: I. Examination of the antigenically protective phase of larval development. International Journal for Parasitology 3, 485–489.CrossRefGoogle ScholarPubMed
Heath, D. D. (1976). Resistance to Taenia pisiformis larvae in rabbits: immunization against infection using non-living antigens from in vitro culture. International Journal for Parasitology 6, 19–24.CrossRefGoogle ScholarPubMed
Heath, D. D., Parmeter, S. N., Osborn, P. J. and Lawrence, S. B. (1981). Resistance to Echinococcus granulosus infection in lambs. Journal of Parasitology 67, 797–799.CrossRefGoogle ScholarPubMed
Heath, D. D. and Holcman, B. (1997). Vaccination against echinococcus in perspective. Acta Tropica 67, 37–41.CrossRefGoogle Scholar
Hoberg, E. P. (2002). Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes and Infection 4, 859–866.CrossRefGoogle ScholarPubMed
Holcman, B., Heath, D. D. and Shaw, R. J. (1994). Ultrastructure of oncosphere and early stages of metacestode development of Echinococcus granulosus. International Journal for Parasitology 24, 623–635.CrossRefGoogle ScholarPubMed
Johnson, K. S., Harrison, G. B., Lightowlers, M. W., O'hoy, K. L., Cougle, W. G., Dempster, R. P., Lawrence, S. B., Vinton, J. G., Heath, D. D. and Rickard, M. D. (1989). Vaccination against ovine cysticercosis using a defined recombinant antigen. Nature 338, 585–587.CrossRefGoogle ScholarPubMed
Kyngdon, C. T., Gauci, C. G., Rolfe, R. A., Velasquez Guzman, J. C., Farfan Salazar, M. J., Verastegui Pimentel, M. R., Gonzalez, A. E., Garcia, H. H., Gilmanl, R. H., Strugnell, R. A. and Lightowlers, M. W. (2006). In vitro oncosphere-killing assays to determine immunity to the larvae of Taenia pisiformis, Taenia ovis, Taenia saginata, and Taenia solium. Journal of Parasitology 92, 273–281.CrossRefGoogle Scholar
Laws, G. F. (1968). The hatching of taeniid eggs. Experimental Parasitology 23, 1–10.CrossRefGoogle ScholarPubMed
Lethbridge, R. C. (1971). The hatching of Hymenolepis diminuta eggs and penetration of the hexacanths in Tenebrio molitor beetles. Parasitology 62, 445–456.CrossRefGoogle ScholarPubMed
Lethbridge, R. C. and Gijsbers, M. F. (1974). Penetration gland secretion by hexacanths of Hymenolepis diminuta. Parasitology 68, 303–311.CrossRefGoogle ScholarPubMed
Lightowlers, M. W. (2006). Cestode vaccines: origins, current status and future prospects. Parasitology 133 (Suppl.) S27–S42.CrossRefGoogle ScholarPubMed
Lightowlers, M. W., Flisser, A., Gauci, C. G., Heath, D. D., Jensen, O. and Rolfe, R. (2000). Vaccination against cysticercosis and hydatid disease. Parasitology Today 16, 191–196.CrossRefGoogle ScholarPubMed
Lightowlers, M. W., Gauci, C. G., Chow, C., Drew, D. R., Gauci, S. M., Heath, D. D., Jackson, D. C., Dadley-Moore, D. L. and Read, A. J. (2003). Molecular and genetic characterisation of the host-protective oncosphere antigens of taeniid cestode parasites. International Journal for Parasitology 33, 1207–1217.CrossRefGoogle ScholarPubMed
Lightowlers, M. W., Gemmell, M. A., Harrison, G. B. L., Heath, D. D., Rickard, M. D. and Roberts, M. G. (1992). Control of tissue parasites II. Cestodes. In Animal Parasite Control Utilizing Biotechnology, (ed. Yong, W. K.), pp. 171–198. CRC Press, Boca Raton.Google Scholar
Lightowlers, M. W., Lawrence, S. B., Gauci, C. G., Young, J., Ralston, M. J., Maas, D. and Health, D. D. (1996 a). Vaccination against hydatidosis using a defined recombinant antigen. Parasite Immunology 18, 457–462.CrossRefGoogle ScholarPubMed
Lightowlers, M. W., Rolfe, R. and Gauci, C. G. (1996 b). Taenia saginata: vaccination against cysticercosis in cattle with recombinant oncosphere antigens. Experimental Parasitology 84, 330–338.CrossRefGoogle ScholarPubMed
Lightowlers, M. W., Waterkeyn, J. G., Rothel, J. S., Gauci, C. G. and Harrison, G. B. (1996 c). Host-protective fragments and antibody binding epitopes of the Taenia ovis 45 W recombinant antigen. Parasite Immunology 18, 507–513.CrossRefGoogle Scholar
Mayta, H., Hancock, K., Levine, M. Z., Gilman, R. H., Farfan, M. J., Verastegui, M., Lane, W. S., Garcia, H. H., Gonzalez, A. E. and Tsang, V. C. (2007). Characterization of a novel Taenia solium oncosphere antigen. Molecular and Biochemical Parasitology 156, 154–161.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Goding, J. W. and Rickard, M. D. (1977). Studies on immune responses to larval cestodes in mice. Increased susceptibility of certain mouse strains and hypothymic mice to Taenia taeniaeformis and analysis of passive transfer of resistance with serum. Australian Journal of Experimental Biology and Medical Science 55, 165–186.CrossRefGoogle ScholarPubMed
Miyazato, T., Furukawa, M., Inoque, M., Niwa, A., Inoque, T. and Shimoda, K. (1977 a). Electron microscopic observations on the penetration of oncosphers of Hymenolepis nana in to the intestine of mouse. Acta Medica Kinki University 2, 1–18.Google Scholar
Miyazato, T., Furukawa, M., Inoque, M., Niwa, A., Inoque, T. and Shimoda, K. (1977 b). Fine structure and the mode of secretory function of the penetration glands of Hymenolepis nana oncospheres. Acta Medica Kinki University 2, 177–188.Google Scholar
Mlocicki, D. (2006). Embryonic development of the anoplocephalid cestode Mosgovoyia ctenoides (Railliet, 1890) Beveridge, 1978. PhD Thesis, Institute of Parasitology PAS, Warsaw, Poland, 122 pp.Google Scholar
Mlocicki, D., Swiderski, Z., Conn, D. B., Eira, C., Miquel, J. and Baranowska-Korczyc, A. (2005). Ultrastructure of oncospheral hook formation in the cestode Mosgovoyia ctenoides (Railliet, 1890) Beveridge, 1978 (Cyclophyllidea, Anoplocephaliae). Acta Parasitologica 59, 124–131.Google Scholar
Mlocicki, D., Swiderski, Z., Miquel, J., Eira, C. and Conn, D. B. (2006). Cellular organization of the oncosphere of Mosgovoyia ctenoides (Cestoda: Anoplocephalidae). Journal of Parasitology 92, 953–961.CrossRefGoogle ScholarPubMed
Moczon, T. (1996). A serine proteinase in the penetration glands of hexacanths of Hymenolepis diminuta (Cestoda, Cyclophyllidea). Parasitology Research 82, 67–71.CrossRefGoogle ScholarPubMed
Morseth, D. J. (1965). Ultrastructure of developing taeniid embryophores and associated structures. Experimental Parasitology 16, 207–216.CrossRefGoogle ScholarPubMed
Morseth, D. J. (1966). Chemical composition of embryophoric blocks of Taenia hydatigena, Taenia ovis, and Taenia pisiformis eggs. Experimental Parasitology 18, 347–354.CrossRefGoogle ScholarPubMed
Nieland, M. L. (1968). Electron microscope observations on the egg of Taenia taeniaeformis. Journal of Parasitology 54, 957–969.CrossRefGoogle ScholarPubMed
Ogren, R. E. (1971). Criteria for anterior polarity and symmetry in tapeworm hexacanth embryos. Proceedings of the Pennsylvania Academy of Science 45, 40–41.Google Scholar
Patak, K. M. L. and Gaur, S. N. S. (1990). Immunization of pigs with culture antigens of Taenia solium. Veterinary Parasitology 34, 353–357.CrossRefGoogle Scholar
Pence, D. B. (1970). Electron microscope and histochemical studies on the eggs of Hymenolepis diminuta. Journal of Parasitology 56, 84–97.CrossRefGoogle ScholarPubMed
Rajasekariah, G. R., Mitchell, G. F. and Rickard, M. D. (1980 a). Taenia taeniaeformis in mice: protective immunization with oncospheres and their products. International Journal for Parasitology 10, 155–160.CrossRefGoogle ScholarPubMed
Rajasekariah, G. R., Rickard, M. D. and Mitchell, G. F. (1980 b). Immunization of mice against infection with Taenia taeniaeformis using various antigens prepared from eggs, oncospheres, developing larvae and strobilocerci. International Journal for Parasitology 10, 315–324.CrossRefGoogle ScholarPubMed
Reid, W. M. (1948). Penetration glands in cyclophyllidean onchospheres. Transactions of the American Microscopical Society 67, 177–182.CrossRefGoogle Scholar
Rickard, M. D. and Adolph, A. J. (1976). Vaccination of calves against Taenia saginata infection using a ‘‘parasite-free’' vaccine. Veterinary Parasitology 1, 389–392.CrossRefGoogle Scholar
Rickard, M. D. and Adolph, A. J. (1977). Vaccination of lambs against infection with Taenia ovis using antigens collected during short-term in vitro incubation of activated T. ovis oncospheres. Parasitology 75, 183–188.CrossRefGoogle ScholarPubMed
Rickard, M. D. and Bell, K. J. (1971). Successful vaccination of lambs against infection with Taenia ovis using antigens produced during in vitro cultivation of the larval stages. Research in Veterinary Science 12, 401–402.CrossRefGoogle ScholarPubMed
Rickard, M. D. and Outteridge, P. M. (1974). Antibody and cell-mediated immunity in rabbits infected with the larval stages of Taenia pisiformis. Zeitschrift für Parasitenkunde 44, 187–201.CrossRefGoogle ScholarPubMed
Rickard, M. D. and Williams, J. F. (1982). Hydatidosis/cysticercosis: immune mechanisms and immunization against infection. Advances in Parasitology 21, 229–296.CrossRefGoogle ScholarPubMed
Rybicka, K. (1966). Embryogenesis in cestodes. Advances in Parasitology 4, 107–186.CrossRefGoogle ScholarPubMed
Schramlova, J. and Blazek, K. (1982). Ultrastructure of the hatched and unhatched oncospheres of Taenia saginata. Folia Parasitologica 29, 45–50.Google ScholarPubMed
Schramlova, J., Blazek, K., Marhoul, Z. and Singhvi, A. (1984). Ultrastructure of Taenia saginata oncospheres cultivated in artificial media. Folia Parasitologica 31, 247–251.Google ScholarPubMed
Silverman, P. H. (1954). Studies on the biology of some tapeworms of the genus Taenia. I. Factors affecting hatching and activation of taeniid ova, and some criteria of their viability. Annals of Tropical Medicine and Parasitology 48, 207–215.CrossRefGoogle Scholar
Silverman, P. H. (1955). A technique for studying the in vitro effect of serum on activated taeniid hexacanth embryos. Nature 176, 598–599.CrossRefGoogle ScholarPubMed
Silverman, P. H. and Maneely, R. B. (1955). Studies on the biology of some tapeworms of the genus Taenia. III. The role of the secreting gland of the hexacanth embryo in the penetration of the intestinal mucosa of the intermediate host, and some of its histochemical reactions. Annals of Tropical Medicine and Parasitology 49, 326–330.CrossRefGoogle ScholarPubMed
Stevenson, P. (1983). Observations on the hatching and activation of fresh Taenia saginata eggs. Annals of Tropical Medicine and Parasitology 77, 399–404.CrossRefGoogle ScholarPubMed
Swiderski, Z. (1972). La structure fine de l'oncosphère du cestode Catenotaenia pusilla (Goeze, 1782) (Cyclophyllidea, Catenotaeniidae). La Cellule 69, 207–237.Google Scholar
Swiderski, Z. (1976). Oncospheral hook morphogenesis in the davaineid cestode cestode Inermicapsifer madagascariensis (Davaine, 1870) Baer, 1956. International Journal for Parasitology 6, 495–504.CrossRefGoogle ScholarPubMed
Swiderski, Z. (1981). Reproductive and developmental biology of the cestodes. In Advances in Invertebrate Reproduction (ed. Clark, W. H. and Adams, T. S.), pp. 365–366. Elsevier, North Holland.Google Scholar
Swiderski, Z. (1983). Echinococcus granulosus: hook-muscle systems and cellular organisation of infective oncospheres. International Journal for Parasitology 13, 289–299.CrossRefGoogle ScholarPubMed
Swiderski, Z., Miquel, J., Młocicki, D., Georgiev, B. B., Eira, C., Grytner-Ziecina, B. and Feliu, C. (2007). Post-embryonic development and ultrastructural characteristics of the polycephalic larvae of Taenia parva Baer, 1926 (Cyclophyllidea, Taeniidae). Acta Parasitologica 52, 31–50.CrossRefGoogle Scholar
Swiderski, Z., Ndiaye, P. I., Miquel, J., Tkach, V., Marchand, B., Chomicz, L., Grytner-Ziecina, B. and Sereda, M. J. (2002). Ultrastructural study of the embryonic development of the anoplocephalid cestode Anoplocephaloides dentata, an intestinal parasite of Arvicolidae rodents. II Differentiation and cellular organisation of the oncosphere. Acta Parasitologica 46, 280–292.Google Scholar
Swiderski, Z. and Tkach, V. V. (1997). Ultrastructural studies on the cellular organisation of the oncospheres of the nematotaeniid cestode Nematotaenia dispar (Goeze, 1782). Acta Parasitologica 42, 158–167.Google Scholar
Swiderski, Z. and Tkach, V. V. (2002). Ultrastructure of embryonic development of Inermicapsifer madagascariensis (Cestoda, Anoplocephalidae) with emphasis on the cellular organisation of the infective eggs. Acta Parasitologica 47, 105–120.Google Scholar
Waterkeyn, J., Gauci, C., Cowman, A. and Lightowlers, M. (1997). Sequence analysis of a gene family encoding Taenia ovis vaccine antigens expressed during embryogenesis of eggs. Molecular and Biochemical Parasitology 86, 75–84.Google ScholarPubMed