Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T05:03:27.409Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  01 December 2007

Renata H. Neves
Affiliation:
Laboratory of Helminthology Romero Lascasas Porto, Department of Microbiology, Immunology and Parasitology, Faculty of Medical Sciences, Biomedical Center, Rua Prof. Manuel de Abreu 444/50 andar, Vila Isabel, 20511-070, Rio de Janeiro, Brazil Laboratory of Helminth Parasites of Vertebrates, Department of Helminthology, Oswaldo Cruz Institute, Av. Brasil 4365, Manguinhos, 21045-900, Rio de Janeiro, Brazil
Alba C.M.B. Alencar
Affiliation:
Laboratory of Helminthology Romero Lascasas Porto, Department of Microbiology, Immunology and Parasitology, Faculty of Medical Sciences, Biomedical Center, Rua Prof. Manuel de Abreu 444/50 andar, Vila Isabel, 20511-070, Rio de Janeiro, Brazil
Marcia B. Águila
Affiliation:
Laboratory of Morphometry and Cardiovascular Morphology, Institute of Biology, Biomedical Center, State University of Rio de Janeiro, Av. 28 de Setembro 87, Vila Isabel, 20551-030, Rio de Janeiro, Brazil
Carlos A. Mandarim-de-Lacerda
Affiliation:
Laboratory of Morphometry and Cardiovascular Morphology, Institute of Biology, Biomedical Center, State University of Rio de Janeiro, Av. 28 de Setembro 87, Vila Isabel, 20551-030, Rio de Janeiro, Brazil
José R. Machado- Silva
Affiliation:
Laboratory of Helminthology Romero Lascasas Porto, Department of Microbiology, Immunology and Parasitology, Faculty of Medical Sciences, Biomedical Center, Rua Prof. Manuel de Abreu 444/50 andar, Vila Isabel, 20511-070, Rio de Janeiro, Brazil
Delir C. Gomes*
Affiliation:
Laboratory of Helminth Parasites of Vertebrates, Department of Helminthology, Oswaldo Cruz Institute, Av. Brasil 4365, Manguinhos, 21045-900, Rio de Janeiro, Brazil
*
*Tel/Fax: +55 21 25984363, E-mail: [email protected]

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.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2007

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

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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Bansal, D., Bhatti, H.S. & Sehgal, R. (2005) Role of cholesterol in parasitic infections. Lipids in Health and Disease 4, 10.CrossRefGoogle ScholarPubMed
Bica, I., Hamer, D.H. & Stadecker, M.J. (2000) Hepatic schistosomiasis. Infectious Disease Clinics of North America 14, 583604.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
Brindley, P.J. (2005) The molecular biology of schistosomes. Trends in Parasitology 21, 533536.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.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.CrossRefGoogle ScholarPubMed
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
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Popiel, I. & Basch, P.F. (1986) Schistosoma mansoni: cholesterol uptake by paired and unpaired worms. Experimental Parasitology 61, 343347.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Rogers, M.V. & McLaren, D.J. (1987) Analysis of total and surface membrane lipids of Schistosoma mansoni. Molecular and Biochemical Parasitology 22, 273288.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Simons, K. & Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569572.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed