Skip to main content Accessibility help
×
Home

Light and confocal microscopic observations of adult Schistosoma mansoni from mice fed on a high-fat diet

  • Renata H. Neves (a1) (a2), Alba C.M.B. Alencar (a1), Marcia B. Águila (a3), Carlos A. Mandarim-de-Lacerda (a3), José R. Machado- Silva (a1) and Delir C. Gomes (a2)...

Abstract

The morphological aspects of Schistosoma mansoni adult worms recovered from albino mice fed on a cholesterol-rich diet compared to mice fed on a standard chow were investigated. After feeding on their respective diets for over a period of 5 months, mice were subcutaneously infected with c. 50 S. mansoni cercariae/mouse. Blood samples were obtained 1 day prior to experimental infections and 63 days later, when mice were euthanized by jugular section (hypovolaemic shock). Total cholesterol (TC) levels were determined. Recovered worms were stained with hydrochloric carmine, and preserved as whole-mounts for examination by bright-field and laser confocal microscopy. The infected mice fed on high-fat chow showed higher levels of serum lipoproteins than the infected mice fed on standard chow, except for very-low-density lipoprotein cholesterol (VLDL-c) and triglycerides (TG). In this experiment, worms from mice fed on a high-fat chow showed a greater percentage of morphological differentiation regarding supernumerary testes, seminal vesicle, and seminal receptacle. In mice of this group, the rate of oocyte laying in the ovary was much higher than in control females. The present results suggest that cholesterol could be actively involved in the modulation of cell signalling and reproduction, because the lobes contained fully developed oocytes in variable amounts, different from control males. The data presented here are the first to report the role of a cholesterol-rich diet affecting the development of S. mansoni worms.

Copyright

Corresponding author

*Tel/Fax: +55 21 25984363, E-mail: dcgomes@ioc.fiocruz.br

References

Hide All
Aguila, M.B., Rodrigues-Apfel, M.I. & Mandarim-de-Lacerda, C.A. (1998) Stereology of the myocardium and blood biochemistry in aged rats fed with a cholesterol-rich and canola oil diet (n-3 fatty acid rich). Basic Research in Cardiology 93, 182191.
Aguila, M.B., Loureiro, C.C., Pinheiro Ada, R. & Mandarim-de-Lacerda, C.A. (2002) Lipid metabolism in rats fed diets containing different types of lipids. Arquivos Brasileiros de Cardiologia 78, 2538.
Bansal, D., Bhatti, H.S. & Sehgal, R. (2005) Role of cholesterol in parasitic infections. Lipids in Health and Disease 4, 10.
Bica, I., Hamer, D.H. & Stadecker, M.J. (2000) Hepatic schistosomiasis. Infectious Disease Clinics of North America 14, 583604.
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.
Brindley, P.J. (2005) The molecular biology of schistosomes. Trends in Parasitology 21, 533536.
Choi, B.K., Chitwood, D.J. & Paik, Y.K. (2003) Proteomic changes during disturbance of cholesterol metabolism by azacoprostane treatment in Caenorhabditis elegans. Molecular and Cellular Proteomics 2, 10861095.
Coutinho, E.M., Barros, A.F., Barbosa, A. Jr, Oliveira, S.A., Silva, L.M., Araujo, R.E. & Andrade, Z.A. (2003) Host nutritional status as a contributory factor to the remodelling of schistosomal hepatic fibrosis. Memórias do Instituto Oswaldo Cruz 98, 919925.
Doenhoff, M.J., Stanley, R.G., Griffiths, K. & Jackson, C.L. (2002) An anti-atherogenic effect of Schistosoma mansoni infections in mice associated with a parasite-induced lowering of blood total cholesterol. Parasitology 125, 415421.
el-Marzouki, Z.M. & Amin, A.M. (1997) Changes in serum lipids of mice experimentally infected with Schistosoma mansoni. Journal of the Egyptian Society of Parasitology 27, 419429.
El Ridi, R., Tallima, H., Mohamed, S.H. & Montash, M. (2004) Depletion of Schistosoma mansoni lung-stage schistosomula cholesterol by methyl-beta-cyclodextrin dramatically increases specific antibody binding to surface membrane antigens. Journal of Parasitology 90, 727732.
Fernandez, M.L. & Volek, J.S. (2006) Guinea pigs: A suitable animal model to study lipoprotein metabolism, atherosclerosis and inflammation. Nutrition and Metabolism 3, 17.
Frazer, B.A., Reddy, A., Fried, B. & Sherma, J. (1997) Effects of diet on the lipid composition of Echinostoma caproni (Trematoda) in ICR mice. Parasitology Research 83, 642645.
Friedwald, W.T., Levy, R.I. & Friedrickson, D.S. (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clinical Chemistry 18, 499502.
Furlong, S.T., Thibault, K.S., Morbelli, L.M., Quinn, J.J. & Rogers, R.A. (1995) Uptake and compartmentalization of fluorescent lipid analogs in larval Schistosoma mansoni. Journal of Lipid Research 36, 112.
Haseeb, M.A., Eveland, L.K. & Fried, B. (1985) The uptake, localization and transfer of [4-14C]cholesterol in Schistosoma mansoni males and females maintained in vitro. Comparative Biochemistry and Physiology – Part A 82, 421423.
Hulstijn, M., Barros, L.A., Neves, R.H., Moura, E.G. & Machado-Silva, J.R. (2003) Morphological changes in the reproductive organs of male and female Schistosoma mansoni worms caused by streptozotocin, a drug used to induce diabetes mellitus. Parasitology 126, 5361.
Hulstijn, M., Barros, L.A., Neves, R.H., Moura, E.G., Gomes, D.C. & Machado-Silva, J.R. (2006) Hermaphrodites and supernumerary testicular lobes in Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by brightfield and confocal microscopy. Journal of Parasitology 92, 454458.
Khovidhunkit, W., Kim, M.S., Memon, R.A., Shigenaga, J.K., Moser, A.H., Feingold, K.R. & Grunfeld, C. (2004) Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. Journal of Lipid Research 45, 11691196.
Lima, V.L., Sena, V.L., Stewart, B., Owen, J.S. & Dolphin, P.J. (1998) An evaluation of the marmoset Callithrix jacchus (sagui) as an experimental model for the dyslipoproteinemia of human Schistosomiasis mansoni. Biochimica et Biophysica Acta 1393, 235243.
Martinez, E.M., Neves, R.H., de 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.
Matyash, V., Geier, C., Henske, A., Mukherjee, S., Hirsh, D., Thiele, C., Grant, B., Maxfield, F.R. & Kurzchalia, T.V. (2001) Distribution and transport of cholesterol in Caenorhabditis elegans. Molecular Biology of the Cell 12, 17251736.
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.
Neves, R.H., Machado-Silva, J.R., Pelajo-Machado, M., Oliveira, S.A., Coutinho, E.M., Lenzi, H.L. & Gomes, D.C. (2001) Morphological aspects of Schistosoma mansoni adult worms isolated from nourished and undernourished mice: a comparative analysis by confocal laser scanning microscopy. Memórias do Instituto Oswaldo Cruz 96, 10131016.
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.
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.
Neves, R.H., Alencar, A.C.B., Costa-Silva, M., Águila, M.B., Mandarim-de-Lacerda, C.A., Machado-Silva, J.R. & Gomes, D.C. (2007) Long-term feeding a high-fat diet causes histological and parasitological effects on murine schistosomiasis mansoni outcome. Experimental Parasitology 115(4), 324332.
Oliveira, S.A., Barbosa, A.A. Jr, Gomes, D.C., Machado-Silva, J.R., Barros, A.F., Neves, R.H. & Coutinho, E.M. (2003) Morphometric study of Schistosoma mansoni adult worms recovered from undernourished infected mice. Memórias do Instituto Oswaldo Cruz 98, 623627.
Oliveira, S.A., Silva, L.M., Barbosa, A.A. Jr, Ribeiro-Dos-Santos, R., Coutinho, E.M., Andrade, Z.A. & Soares, M.B. (2004) Decreased humoral and pathologic responses in undernourished mice infected with Schistosoma mansoni. Parasitology Research 93, 3035.
Popiel, I. & Basch, P.F. (1986) Schistosoma mansoni: cholesterol uptake by paired and unpaired worms. Experimental Parasitology 61, 343347.
Racoosin, E.L., Davies, S.J. & Pearce, E.J. (1999) Caveolae-like structures in the surface membrane of Schistosoma mansoni. Molecular and Biochemical Parasitology 104, 285297.
Ramos, T.M., de Vasconcelos, A.S., de Carvalho, V.C. & Lima, V.L. (2004) Alterations in cholesterol, triglyceride and total phospholipid levels in plasma of Callithrix jacchus (sagui) reinfected by Schistosoma mansoni. Revista da Sociedade Brasileira de Medicina Tropical 37, 3740.
Rogers, M.V. & McLaren, D.J. (1987) Analysis of total and surface membrane lipids of Schistosoma mansoni. Molecular and Biochemical Parasitology 22, 273288.
Rosario, C. & Fried, B. (1999) Effects of a protein-free diet on worm recovery, growth, and distribution of Echinostoma caproni in ICR mice. Journal of Helminthology 73, 167169.
Rumjanek, F.D. & Simpson, A.J. (1980) The incorporation and utilization of radiolabelled lipids by adult Schistosoma mansoni in vitro. Molecular and Biochemical Parasitology 1, 3144.
Sato, S.B., Ishii, K., Makino, A., Iwabuchi, K., Yamaji-Hasegawa, A., Senoh, Y., Nagaoka, I., Sakuraba, H. & Kobayashi, T. (2004) Distribution and transport of cholesterol-rich membrane domains monitored by a membrane-impermeant fluorescent polyethylene glycol-derivatized cholesterol. Journal of Biological Chemistry 279, 2379023796.
Simons, K. & Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569572.
Simpkins, H.L. & Fried, B. (1999) Effects of a diet deficient in vitamins A, D, and E on infectivity, growth, and development of Echinostoma trivolvis in domestic chicks. Parasitology Research 85, 873875.
Simpkins, H.L. & Fried, B. (2001) Effects of a diet deficient in the B complex vitamins on infectivity, growth and distribution of Echinostoma caproni in ICR mice. Journal of Helminthology 75, 7780.
Tallima, H. & El Ridi, R. (2005) Methyl-beta-Cyclodextrin treatment and filipin staining reveal the role of cholesterol in surface membrane antigen sequestration of Schistosoma mansoni and S. haematobium lung-stage larvae. Journal of Parasitology 91, 720725.
Wuhrer, M., Dennis, R.D., Doenhoff, M.J. & Geyer, R. (2000) Stage-associated expression of ceramide structures in glycosphingolipids from the human trematode parasite Schistosoma mansoni. Biochimica et Biophysica Acta 1524, 155161.

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed