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Do schistosomes grow old? A confocal laser scanning microscopy study

Published online by Cambridge University Press:  27 November 2009

J.R. Machado-Silva*
Affiliation:
Laboratório de Hemintologia Romero Lascasas Porto, Departamento de Microbiologia, Imunologia e Parasitologia, Faculdade de Ciências Médicas, Universidade do Estado do Rio de Janeiro, Rua Prof. Manoel de Abreu, 444, 5° andar, 20511- 070Rio de Janeiro, RJ, Brasil
R.H. Neves
Affiliation:
Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Fiocruz, Av Brasil 4365, Manguinhos21045-900, Rio de Janeiro, Brasil
R. Rodrigues-Silva
Affiliation:
Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Fiocruz, Av Brasil 4365, Manguinhos21045-900, Rio de Janeiro, Brasil
*

Abstract

Infected hosts progressively decrease egg output during the chronic phase of Schistosoma mansoni infection. Ageing may be a factor that results in a progressive decrease in the ability to reproduce. This study was performed to gain insight into the effects of ageing on adult schistosomes, using confocal laser scanning microscopy. Adult worms were recovered from experimentally infected Nectomys squamipes (water rat). Viable eggs were voided in the faeces for 65 weeks and, thereafter, only unviable eggs were eliminated. The rat died after 70 weeks in captivity. Recovered worms (six males and one female) were prepared for confocal microscopy and images were obtained with an LSM 510–ZETA laser confocal microscope. The overall morphology of the adult worms (suckers and tegument) and reproductive organs were the focus of this work. The suckers, ovary, vitellaria and oocytes appeared to be apparently normal. The ootype was formed by flattened cells and unclear nuclei, suggesting that the mechanism for eggshell production by the ootype during organogenesis might have been impaired. Testicular lobes showed empty areas around the germinative cells. Male adult worms showed flaccid musculature of the dorsal surface. Taken together, the present results provided several indications of infertility in older male and female schistosomes.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2010

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References

Abath, F.G. & Werkhauser, R.C. (1996) The tegument of Schistosoma mansoni: functional and immunological features. Parasite Immunology 18, 1520.CrossRefGoogle ScholarPubMed
Barth, L.R., Fernandes, A.P. & Rodrigues, V. (1996) Oviposition by Schistosoma mansoni during in vitro cultivation. Revista do Instituto de Medicina Tropical de Sao Paulo 38, 423426.CrossRefGoogle ScholarPubMed
Braschi, S., Curwen, R.S., Ashton, P.D., Verjovski-Almeida, S. & Wilson, A. (2006) The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6, 14711482.CrossRefGoogle ScholarPubMed
Cheever, A.W., Mosimann, J.E., Deb, S., Cheever, E.A. & Duvall, R.H. (1994) Natural history of Schistosoma mansoni infection in mice: egg production, egg passage in the feces, and contribution of host and parasite death to changes in worm numbers. American Journal of Tropical Medicine and Hygiene 50, 269280.Google Scholar
Ellery, A.W. (1985) Guidelines for specification of animals and husbandry methods when reporting the results of animal experiments. Working Committee for the Biological Characterization of Laboratory Animals/GV–SOLAS. Laboratory Animals 19, 106108.Google ScholarPubMed
Farah, I.O., Mola, P.W., Kariuki, T.M., Nyindo, M., Blanton, R.E. & King, C.L. (2000) Repeated exposure induces periportal fibrosis in Schistosoma mansoni-infected baboons: role of TGF-beta and IL-4. Journal of Immunology 164, 53375343.CrossRefGoogle ScholarPubMed
Fulford, A.J., Butterworth, A.E., Ouma, J.H. & Sturrock, R.F. (1995) A statistical approach to schistosome population dynamics and estimation of the life-span of Schistosoma mansoni in man. Parasitology 110, 307316.CrossRefGoogle ScholarPubMed
Harman, D. (2006) Free radical theory of aging an update: increasing the functional life span. Annals of the New York Academy Sciences 1067, 1021.CrossRefGoogle ScholarPubMed
Harris, A.R., Russell, R.J. & Charters, A.D. (1984) A review of schistosomiasis in immigrants in Western Australia, demonstrating the unusual longevity of Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 385388.Google Scholar
Hughes, S.E., Evason, K., Xiong, C. & Kornfeld, K. (2007) Genetic and pharmacological factors that influence reproductive ageing in nematodes. PLoS Genetics 3, 25.CrossRefGoogle ScholarPubMed
Irie, Y., Basch, P.F. & Beach, N. (1983) Reproductive ultrastructure of adult Schistosoma mansoni grown in vitro. Journal of Parasitology 69, 559566.Google Scholar
Kastner, M.R.Q., Kohn, A., Teixeira, E.D. & Pitanga, L.C. (1975) Estudo morfológico do Schistosoma mansoni Sambon, 1907 encontrado na espécie humana. Revista da Sociedade Brasileira de Medicina Tropical 9, 247261.Google Scholar
Katz, N., Chaves, A. & Pellegrino, J. (1972) A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de São Paulo 14, 397400.Google Scholar
Kusel, J.R., Al-Adhami, B.H. & Doenhoff, M.J. (2007) The schistosome in the mammalian host: understanding the mechanisms of adaptation. Parasitology 134, 14771526.CrossRefGoogle ScholarPubMed
Longo, V.D. & Fabrizio, P. (2002) Regulation of longevity and stress resistance: a molecular strategy conserved from yeast to humans? Cellular and Molecular Life Sciences 59, 903908.CrossRefGoogle ScholarPubMed
Lutz, A.V. (1919) Schistosoma mansoni e a schistosomose, segundo observações feitas no Brasil. Memórias do Instituto Oswaldo Cruz 11, 121125.CrossRefGoogle Scholar
Machado-Silva, J.R., Galvao, C., Presgrave, O.A., Rey, L. & Gomes, D.C. (1994) Host-induced morphological changes of Schistosoma mansoni Sambon, 1907 male worms. Memórias do Instituto Oswaldo Cruz 89, 411416.Google Scholar
Machado-Silva, J.R., Lanfredi, R.M. & Gomes, D.C. (1997) Morphological study of adult male worms of Schistosoma mansoni Sambon, 1907 by scanning electron microscopy. Memórias do Instituto Oswaldo Cruz 92, 647653.CrossRefGoogle ScholarPubMed
Modena, C.M., dos Santos Lima, W. & Coelho, P.M. (2008) Wild and domesticated animals as reservoirs of Schistosomiasis mansoni in Brazil. Acta Tropica 108, 242244.CrossRefGoogle ScholarPubMed
Moreels, T.G., De Man, J.G., Bogers, J.J., De Winter, B.Y., Vrolix, G., Herman, A.G., Van Marck, E.A. & Pelckmans, P.A. (2001) Effect of Schistosoma mansoni-induced granulomatous inflammation on murine gastrointestinal motility. American Journal of Physiology Gastrointestinal and Liver Physiology 280, 10301042.Google Scholar
Neves, R.H., Pereira, M.J., de Oliveira, R.M., Gomes, D.C. & Machado-Silva, J.R. (1998) Schistosoma mansoni Sambon, 1907: morphometric differences between adult worms from sympatric rodent and human isolates. Memórias do Instituto Oswaldo Cruz 93, 309312.Google Scholar
Neves, R.H., Costa-Silva, M., Martinez, E.M., Biolchini Cde, L., Lenzi, H.L., Gomes, D.C. & Machado-Silva, J.R. (2003) Reproductive system abnormalities in Schistosoma mansoni adult worms isolated from Nectomys squamipes (Muridae: Sigmodontinae): brightfield and confocal laser scanning microscopy analysis. Memórias do Instituto Oswaldo Cruz 98, 361365.CrossRefGoogle ScholarPubMed
Neves, R.H., Costa-Silva, M., Martinez, E.M., Branquinho, T.B., de Oliveira, R.M., Lenzi, H.L., Gomes, D.C. & Machado-Silva, J.R. (2004) Phenotypic plasticity in adult worms of Schistosoma mansoni (Trematoda: Schistosomatidae) evidenced by brightfield and confocal laser scanning microscopies. Memórias do Instituto Oswaldo Cruz 99, 131136.Google Scholar
Neves, R.H., de Lamare Biolchini, C., Machado-Silva, J.R., Carvalho, J.J., Branquinho, T.B., Lenzi, H.L., Hulstijn, M. & Gomes, D.C. (2005) A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitology Research 95, 4349.CrossRefGoogle ScholarPubMed
Rocha, R.L., Rocha, M.O., Pedroso, E.R., Colosimo, E.A. & Coelho, P.M. (1995) Egg excretion in the initial phase of experimental murine schistosomiasis mansoni: stability and association with worm burden. Revista do Instituto de Medicina Tropical de São Paulo 37, 325329.CrossRefGoogle ScholarPubMed
Rodrigues e Silva, R., Machado e Silva, J.R., Faerstein, N.F., Lenzi, H.L. & Rey, L. (1992) Natural infection of wild rodents by Schistosoma mansoni. Parasitological aspects. Memórias do Instituto Oswaldo Cruz 87, 271276.Google Scholar
Smithers, S.R. & Terry, R.J. (1965) The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695700.Google Scholar
Southgate, V.R. & Agrawal, M.C. (1990) Human schistosomiasis in India? Parasitology Today 6, 166168.CrossRefGoogle ScholarPubMed
Wilson, R.A., Langermans, J.A., van Dam, G.J., Vervenne, R.A., Hall, S.L., Borges, W.C., Dillon, G.P., Thomas, A.W. & Coulson, P.S. (2008) Elimination of Schistosoma mansoni adult worms by rhesus macaques: basis for a therapeutic vaccine? PLoS Neglected Tropical Diseases 2, 290.Google Scholar