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Phenotypic plasticity of male Schistosoma mansoni from the peritoneal cavity and hepatic portal system of laboratory mice and hamsters

Published online by Cambridge University Press:  26 February 2014

V.L.T Mati*
Affiliation:
Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
R.M. Freitas
Affiliation:
Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
R.S. Bicalho
Affiliation:
Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
A.L. Melo
Affiliation:
Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

Abstract

Morphometric analysis of Schistosoma mansoni male worms obtained from AKR/J and Swiss mice was carried out. Rodents infected by the intraperitoneal route with 80 cercariae of the schistosome (LE strain) were killed by cervical dislocation at 45 and 60 days post-infection and both peritoneal lavage and perfusion of the portal system were performed for the recovery of adult worms. Characteristics including total body length, the distance between oral and ventral suckers, extension of testicular mass and the number of testes were considered in the morphological analysis. Changes that occurred in S. mansoni recovered from the peritoneal cavity or from the portal system of AKR/J and Swiss mice included total body length and reproductive characteristics. Significant morphometric alterations were also observed when worms recovered from the portal system of both strains of mice were compared with the schistosomes obtained from hamsters (Mesocricetus auratus), the vertebrate host in which the LE strain had been adapted and maintained by successive passages for more than four decades. The present results reinforce the idea that S. mansoni has high plastic potential and adaptive capacity.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

Amorim, J.P. (1953) Infestação experimental e natural de murídeos pelo Schistosoma mansoni (nota prévia). Revista Brasileira de Malariologia 5, 219222.Google Scholar
Ben-Efraim, S. & Cinader, B. (1964) The role of complement in the passive cutaneous reaction of mice. Journal of Experimental Medicine 120, 925942.Google Scholar
Bicalho, R.S., Melo, A.L. & Pereira, L.H. (1993) Desenvolvimento do Schistosoma mansoni na cavidade peritoneal de camundongos da linhagem AKR/J. Revista do Instituto de Medicina Tropical de São Paulo 35, 411416.CrossRefGoogle ScholarPubMed
Bitner-Mathé, B.C. & Klaczko, L.B. (1999) Plasticity of Drosophila melanogaster wing morphology: effects of sex, temperature and density. Genetica 105, 203210.Google Scholar
Bogéa, T. (2005) Phenotypic plasticity in the cercarial indices of human and rodent samples of Schistosoma mansoni (Digenea: Schistosomatidae). Annals of Tropical Medicine and Parasitology 99, 583592.Google Scholar
Castaneda, L.E., Sabat, P., Gonzalez, S.P. & Nespolo, R.F. (2006) Digestive plasticity in tadpoles of the Chilean giant frog (Caudiverbera caudiverbera): factorial effects of diet and temperature. Physiological and Biochemical Zoology 79, 919926.Google Scholar
Chao, L.P., Jones, J.T. & Kusel, J.R. (1986) An in vivo model for the study of chemotaxis induced by schistosomula of Schistosoma mansoni . Parasitology 92, 117132.CrossRefGoogle Scholar
Cheever, A.W., Lenzi, J.A., Lenzi, H.L. & Andrade, Z.A. (2002) Experimental models of Schistosoma mansoni infection. Memórias do Instituto Oswaldo Cruz 97, 917940.Google Scholar
Cinader, B. & Dubiski, S. (1964) Effect of autologous protein on the specificity of the antibody response: mouse and rabbit antibody to MuBL. Nature 202, 102103.Google Scholar
Coles, G.C. & Thurston, J.P. (1970) Testes number in East African Schistosoma mansoni . Journal of Helminthology 44, 6973.Google Scholar
Curry, A.J., Else, K.J., Jones, F., Bancroft, A., Grencis, R.K. & Dunne, D.W. (1995) Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris . Journal of Experimental Medicine 181, 769774.Google Scholar
Davies, S.J. & McKerrow, J.H. (2003) Developmental plasticity in schistosomes and other helminths. International Journal for Parasitology 33, 12771284.CrossRefGoogle ScholarPubMed
Fan, P.C. & Pao, K.Y. (2006) Study of the morphological characteristics of Schistosoma mansoni in mice, squirrels, and hamsters. Southeast Asian Journal of Tropical Medicine and Public Health 37, 3339.Google Scholar
Galanti, S.E., Huang, S.C. & Pearce, E.J. (2012) Cell death and reproductive regression in female Schistosoma mansoni . PLoS Neglected Tropical Diseases 6, e1509.Google Scholar
Geyer, K.K., Rodríguez-López, C.M., Chalmers, I.W., Munshi, S.E., Truscott, M., Heald, J., Wilkinson, M.J. & Hoffmann, K.F. (2011) Cytosine methylation regulates oviposition in the pathogenic blood fluke Schistosoma mansoni . Nature Communications 2, 424.CrossRefGoogle ScholarPubMed
Guerassimov, A., Hoshino, Y., Takubo, Y., Turcotte, A., Yamamoto, M., Ghezzo, H., Triantafillopoulos, A., Whittaker, K., Hoidal, J.R. & Cosio, M.G. (2004) The development of emphysema in cigarette smoke-exposed mice is strain dependent. American Journal of Respiratory and Critical Care Medicine 170, 974980.CrossRefGoogle ScholarPubMed
Hernandez, D.C., Lim, K.C., McKerrow, J.H. & Davies, S.J. (2004) Schistosoma mansoni: sex-specific modulation of parasite growth by host immune signals. Experimental Parasitology 106, 5961.Google Scholar
Herrmann, K.K. & Poulin, R. (2012) Geographic variation in life cycle strategies of a progenetic trematode. Journal of Parasitology 98, 103110.CrossRefGoogle ScholarPubMed
Jiang, H., Rummage, J.A., Zhou, A., Chen, Z., Herriot, M.J., Stewart, C.A., Kolosov, M. & Leu, R.W. (1996) IFN-alpha beta reconstitutes the deficiency in lipid A-activated AKR macrophages for nitric oxide synthase. Journal of Immunology 157, 305312.Google Scholar
Kastner, M.R., Kohn, A., Teixeira, E.D. & Pitanga, L.C. (1975) Estudo morfológico de Schistosma mansoni Sambon, 1907 encontrado na espécie humana. Revista da Sociedade Brasileira de Medicina Tropical 9, 247261.Google Scholar
Kiontke, K. & Fitch, D. (2010) Phenotypic plasticity: different teeth for different feasts. Current Biology 20, R710R712.Google Scholar
Kruger, F.J., Hamilton-Attwell, V.L., Tiedt, L., Visser, P.S. & Joubert, P.H. (1988) Notes on the occurrence of tubercular spines in Schistosoma margrebowiei and Schistosoma mattheei . Onderstepoort Journal of Veterinary Research 55, 187189.Google Scholar
Kuntz, R.E. (1952) Natural infection of an Egyptian gerbil with Schistosoma mansoni . Proceedings of the Helminthological Society of Washington 19, 123124.Google Scholar
Kunz, W. (2001) Schistosome male-female interaction: induction of germ-cell differentiation. Trends in Parasitology 17, 227231.Google Scholar
Lefebvre, F. & Poulin, R. (2005) Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology 130, 587605.Google Scholar
Loverde, P.T., Niles, E.G., Osman, A. & Wu, W. (2004) Schistosoma mansoni male-female interactions. Canadian Journal of Zoology 82, 357374.CrossRefGoogle Scholar
Lutz, A. (1919) O Schistosomum mansoni e a schistosomatose segundo observações feitas no Brasil. Memórias do Instituto Oswaldo Cruz 11, 121155.CrossRefGoogle Scholar
Machado-Silva, J.R., Galvão, 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., Galvão, C., Oliveira, R.M., Presgrave, O.A. & Gomes, D.C. (1995) Schistosoma mansoni Sambon, 1907: comparative morphological studies of some Brazilian strains. Revista do Instituto de Medicina Tropical de São Paulo 37, 441447.Google Scholar
Maggi, M.D., Sardella, N.H., Ruffinengo, S.R. & Eguaras, M.J. (2009) Morphotypes of Varroa destructor collected in Apis mellifera colonies from different geographic locations of Argentina. Parasitology Research 105, 16291636.CrossRefGoogle ScholarPubMed
Martinez, E.M., Neves, R.H., Oliveira, R.M., Machado-Silva, J.R. & Rey, L. (2003) Parasitological and morphological characteristics of Brazilian strains of Schistosoma mansoni in Mus musculus . Revista da Sociedade Brasileira de Medicina Tropical 36, 557564.Google Scholar
Martinez, E.M., Costa-Silva, M., Neves, R.H., Oliveira, R.M. & Machado-Silva, J.R. (2008) Biological implications of the phenotypic plasticity in the Schistosoma mansoni-Nectomys squamipes model. Revista do Instituto de Medicina Tropical de São Paulo 50, 229232.CrossRefGoogle ScholarPubMed
Matejusová, I., Koubková, B., Gelnar, M. & Cunningham, C.O. (2002) Paradiplozoon homoion Bychowsky & Nagibina, 1959 versus P. gracile Reichenbach-Klinke, 1961 (Monogenea): two species or phenotypic plasticity? Systematic Parasitology 53, 3947.Google Scholar
Mati, V.L. (2009) Efeitos da dexametasona e pentoxifilina na esquistossomose mansoni experimental: Aspectos do parasitismo e histopatologia hepática em camundongos da linhagem AKR/J . MSc dissertation, Universidade Federal de Minas Gerais, Belo Horizonte.Google Scholar
Mati, V.L. & Melo, A.L. (2013) Current applications of oogram methodology in experimental schistosomiasis; fecundity of female Schistosoma mansoni and egg release in the intestine of AKR/J mice following immunomodulatory treatment with pentoxifylline. Journal of Helminthology 87, 115124.Google Scholar
Mati, V.L., Freitas, R.M. & Melo, A.L. (2010) Effects of pentoxifylline during Schistosoma mansoni infection in Swiss mice: an analysis of worm burden, fecundity and liver histopathology. Journal of Helminthology 84, 348354.Google Scholar
Mati, V.L., Pinto, H.A. & Melo, A.L. (2013) Experimental infection of Swiss and AKR/J mice with Centrocestus formosanus (Trematoda: Heterophyidae). Revista do Instituto de Medicina Tropical de São Paulo 55, 133136.CrossRefGoogle ScholarPubMed
Melo, A.L. & Pereira, L.H. (1980) Inhibitory effect of oxamniquine on the detachment of the tail of Schistosoma mansoni . Journal of Parasitology 66, 10671068.Google Scholar
Melo, A.L. & Pereira, L.H. (1985) Kinetics of the cercaria-schistosomulum tranformation in vivo . Revista da Sociedade Brasileira de Medicina Tropical 18, 1721.Google Scholar
Melo, A.L., Pereira, L.H. & Correa, M.C. (1978) In vivo cercaria-schistosomulum transformation: inhibitory effect of oxamniquine. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 158159.CrossRefGoogle ScholarPubMed
Melo, A.L., Pereira, L.H. & Chamone, M. (1980) The effect of a previous Schistosoma mansoni infection on schistosomulum recovery from the peritoneal cavity of laboratory mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 827.Google Scholar
Melo, A.L., Machado, C.R. & Pereira, L.H. (1993a) Host cell adhesion to Schistosoma mansoni larvae in the peritoneal cavity of naive mice: histological and scanning electron microscopic studies. Revista do Instituto de Medicina Tropical de São Paulo 35, 1722.Google Scholar
Melo, A.L., Machado, C.R. & Pereira, L.H. (1993b) Interaction between neutrophils and Schistosoma mansoni larvae in vivo: a transmission electron-microscopic study. Revista do Instituto de Medicina Tropical de São Paulo 35, 2933.Google Scholar
Melo, A.L., Hermeto, M.V., Bicalho, R.S., Vargas, A.P., Favaretto, F.J. & Pereira, L.H. (1994) Schistosoma mansoni: the effect of dexamethasone on the cercaria-schistosomulum transformation in vivo . Revista do Instituto de Medicina Tropical de São Paulo 36, 8993.Google Scholar
Moore, D.V. & Meleney, H.E. (1955) Development of Schistosoma mansoni in the peritoneal cavity of mice. Journal of Parasitology 41, 235245.Google Scholar
Neves, R.H., Oliveira, S.A., Machado-Silva, J.R., Coutinho, E. & Gomes, D.C. (2002) Phenotypic characterization of Schistosoma mansoni adult worms recovered from undernourished mice: a morphometric study focusing on the reproductive system. Revista da Sociedade Brasileira de Medicina Tropical 35, 405407.Google Scholar
Neves, R.H., Costa-Silva, M., Martinez, E.M., Branquinho, T.B., 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., Alencar, A.C., Aguila, M.B., Mandarim-Lacerda, C.A., Machado-Silva, J.R. & Gomes, D.C. (2007) Light and confocal microscopic observations of adult Schistosoma mansoni from mice fed on a high-fat diet. Journal of Helminthology 81, 361368.CrossRefGoogle ScholarPubMed
Olstad, K., Bachmann, L. & Bakke, T.A. (2009) Phenotypic plasticity of taxonomic and diagnostic structures in gyrodactylosis-causing flatworms (Monogenea, Platyhelminthes). Parasitology 136, 13051315.Google Scholar
Pellegrino, J. & Siqueira, A.F. (1956) Técnica de perfusão para colheita de Schistosoma mansoni em cobaias experimentalmente infestadas. Revista Brasileira de Malariología e Doenças Tropicais 8, 589597.Google Scholar
Pereira, L.H., Coelho, P.M., Fonseca, J.J., Bredt, A. & Pellegrino, J. (1972) Migration of Schistosoma mansoni larvae in the albino mouse. Revista do Instituto de Medicina Tropical de São Paulo 14, 306309.Google Scholar
Pereira, L.H., Pellegrino, J., Valadares, T.E., Mello, R.T. & Coelho, P.M. (1974) A new approach for screening prophylactic agents in schistosomiasis. Revista do Instituto de Medicina Tropical de São Paulo 16, 123126.Google Scholar
Pirajá-da-Silva, M.A. (1908) La Schistosomose a Bahia. Archives de Parasitologie 13, 281300.Google Scholar
Poulin, R. (2003) Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 28992903.Google Scholar
Pyrrho, A.S., Ramos, J.A., Neto, R.M., Silva, C.S., Lenzi, H.L., Takiya, C.M. & Gattass, C.R. (2002) Dexamethasone, a drug for attenuation of Schistosoma mansoni infection morbidity. Antimicrobial Agents and Chemotherapy 46, 34903498.Google Scholar
Rey, L. (1993) Non-human vertebrate hosts of Schistosoma mansoni and schistosomiasis transmission in Brazil. Research and Reviews in Parasitology 53, 1325.Google Scholar
Ribeiro-Paes, J.T. & Rodrigues, V. (1997) Sex determination and female reproductive development in the genus Schistosoma . Revista do Instituto de Medicina Tropical de São Paulo 39, 337344.Google Scholar
Saoud, M.F. (1965) Comparative studies on the characteristics of some geographical strains of Schistosoma mansoni in mice and hamsters. Journal of Helminthology 39, 101112.Google Scholar
Saoud, M.F. (1966) On the infra-specific variations of the male sexual glands of Schistosoma mansoni . Journal of Helminthology 40, 385394.Google Scholar
Senft, A.W., Gibler, W.B. & Knopf, P.M. (1978) Scanning electron microscope observations on tegument maturation in Schistosoma mansoni grown in permissive and non-permissive hosts. American Journal of Tropical Medicine and Hygiene 27, 258266.Google Scholar
Silva, L.M., Fernandes, A.L., Barbosa, A. Jr, Oliveira, I.R. & Andrade, Z.A. (2000) Significance of schistosomal granuloma modulation. Memórias do Instituto Oswaldo Cruz 95, 353361.Google Scholar
Stirewalt, M.A., Kuntz, R.E. & Evans, A.S. (1951) The relative susceptibilities of the commonly used laboratory mammals to infection by Schistosoma mansoni . American Journal of Tropical Medicine and Hygiene 31, 5782.CrossRefGoogle ScholarPubMed
Sudati, J.E., Rivas, F. & Fried, B. (1997) Effect of a high protein diet on worm recovery, growth and distribution of Echinostoma caproni in ICR mice. Journal of Helminthology 71, 351354.Google Scholar
Ting-An, W. & Hong-Xiang, Z. (2009) PTK-pathways and TGF-beta signaling pathways in schistosomes. Journal of Basic Microbiology 49, 2531.Google Scholar
Tristão, A.R. (2001) Apoptose em granulomas esquistossomóticos hepáticos e peritoneais de camundongos . MSc dissertation, Universidade Federal de Minas Gerais, Belo Horizonte.Google Scholar
Valero, M.A., Darce, N.A., Panova, M. & Mas-Coma, S. (2001) Relationships between host species and morphometric patterns in Fasciola hepatica adults and eggs from the northern Bolivian Altiplano hyperendemic region. Veterinary Parasitology 102, 85100.Google Scholar
West, D.B., Waguespack, J. & McCollister, S. (1995) Dietary obesity in the mouse: interaction of strain with diet composition. American Journal of Physiology 268, 658665.Google Scholar
Yamaya, H., Basaki, Y., Togawa, M., Kojima, M., Kiniwa, M. & Matsuura, N. (1995) Down-regulation of Th2 cell-mediated murine peritoneal eosinophilia by antiallergic agents. Life Sciences 56, 16471654.Google Scholar