Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T07:26:05.221Z Has data issue: false hasContentIssue false
  • English
  • Français

Electron Microscopy Analysis of the Nucleolus of Trypanosoma cruzi

Published online by Cambridge University Press:  07 July 2005

Gabriel López-Velázquez ,
Roberto Hernández ,
Imelda López-Villaseñor ,
Horacio Reyes-Vivas ,
María de L. Segura-Valdez  and
Luis F. Jiménez-García
Gabriel López-Velázquez
Affiliation:
Department of Cell Biology, Faculty of Sciences, National Autonomous University of Mexico, México D.F., 04510, México Biochemistry and Genetics Laboratory, National Institute of Pediatrics, S.S., D.F., 04530, México
Roberto Hernández
Affiliation:
Department of Molecular Biology and Biotechnology, Biomedical Research Institute, National Autonomous University of Mexico, México D.F., 04510, México
Imelda López-Villaseñor
Affiliation:
Department of Molecular Biology and Biotechnology, Biomedical Research Institute, National Autonomous University of Mexico, México D.F., 04510, México
Horacio Reyes-Vivas
Affiliation:
Biochemistry and Genetics Laboratory, National Institute of Pediatrics, S.S., D.F., 04530, México
María de L. Segura-Valdez
Affiliation:
Department of Cell Biology, Faculty of Sciences, National Autonomous University of Mexico, México D.F., 04510, México
Luis F. Jiménez-García
Affiliation:
Department of Cell Biology, Faculty of Sciences, National Autonomous University of Mexico, México D.F., 04510, México
Get access

Abstract

The nucleolus is the main site for synthesis and processing of ribosomal RNA in eukaryotes. In mammals, plants, and yeast the nucleolus has been extensively characterized by electron microscopy, but in the majority of the unicellular eukaryotes no such studies have been performed. Here we used ultrastructural cytochemical and immunocytochemical techniques as well as three-dimensional reconstruction to analyze the nucleolus of Trypanosoma cruzi, which is an early divergent eukaryote of medical importance. In T. cruzi epimastigotes the nucleolus is a spherical intranuclear ribonucleoprotein organelle localized in a relatively central position within the nucleus. Dense fibrillar and granular components but not fibrillar centers were observed. In addition, nuclear bodies resembling Cajal bodies were observed associated to the nucleolus in the surrounding nucleoplasm. Our results provide additional morphological data to better understand the synthesis and processing of the ribosomal RNA in kinetoplastids.

Keywords

Cajal bodiesnucleolusnucleusribosomal RNATrypanosoma cruzi
Type
BIOLOGICAL APPLICATIONS
Information
Microscopy and Microanalysis , Volume 11 , Issue 4 , August 2005 , pp. 293 - 299
Copyright
© 2005 Microscopy Society of America

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

REFERENCES

Agabian, N. (1990). Trans-splicing of nuclear pre-mRNAs. Cell 61, 1157–1160.Google Scholar
Bernhard, W. (1969). A new staining procedure for electron microscopical cytology. J Ultrastruct Res 27, 250–258.Google Scholar
Busch, H. & Smetana, K. (1970). The Nucleolus. New York: Academic Press.
Castro, C., Hernández, R., & Castañeda, M. (1981). Trypanosoma cruzi ribosomal RNA: Internal break in the large molecular mass species and number of genes. Mol Biochem Parasitol 2, 219–233.Google Scholar
Chung, H.M., Shea, C., Fields, S., Taub, R.N., Van der Ploeg, L.H., & Tse, D.B. (1990). Architectural organization in the interphase nucleus of the protozoan Trypanosoma brucei: Location of telomeres and mini-chromosomes. EMBO J 9, 2611–2619.Google Scholar
Djikeng, A., Ferreira, L., D'Angelo, M., Dolezal, P., Lambl, T., Murta, S., Triggs, V., Ulbert, S., Villarino, A., Renzi, S., Ullu, E., & Tschudi, C. (2001). Characterization of a candidate Trypanosoma brucei U1 small nuclear RNA gene. Mol Biochem Parasitol 113, 109–115.Google Scholar
Dunbar, D.A., Wormsley, S., Lowe, T.M., & Baserga, S.J. (2000). Fibrillarin-associated box C/D small nucleolar RNAs in Trypanosoma brucei. Sequence conservation and implications for 2′-O-ribose methylation of rRNA. J Biol Chem 275, 14767–14776.Google Scholar
Elias, M.C.O.B., Marques-Porto, R., Freymüller, E., & Schenkman, S. (2001). Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Mol Biochem Parasitol 112, 79–90.Google Scholar
Enright, C. & Sollner-Webb, B. (1994). Ribosomal RNA processing in vertebrates. In RNA Processing. A Practical Approach, Higgins, S.J. & Hames, B.D. (Eds.), pp. 135–171. New York: Oxford University Press.
Esponda, P., Souto-Padrón, T., & De Souza, W. (1983). Fine structure and cytochemistry of the nucleus and the kinetoplast of epimastigotes of Trypanosoma cruzi. J Protozool 30, 105–110.Google Scholar
Gall, J.G. (2000). Cajal bodies: The first 100 years. Annu Rev Cell Dev Biol 16, 273–300.Google Scholar
Goodpasture, C. & Bloom, S.E. (1975). Visualization of nucleolus organizer regions in mammalian chromosomes using silver stain. Chromosoma 53, 37–50.Google Scholar
Hartshorne, T. & Agabian, T. (1993). RNA B is the major nucleolar trimethylguanosine-capped small nuclear RNA associated with fibrillarin and pre-rRNAs in Trypanosoma brucei. Mol Cell Biol 13, 144–154.Google Scholar
Hernández, R., Díaz-de León, F., & Castañeda, M. (1988). Molecular cloning and partial characterization of ribosomal RNA genes from Trypanosoma cruzi. Mol Biochem Parasitol 27, 275–280.Google Scholar
Herwaldt, B.L. (1999). Leishmaniasis. Lancet 2, 1191–1199.Google Scholar
Huang, S. (2002). Building an efficient factory: Where is pre-rRNA synthesized in the nucleolus? J Cell Biol 157, 739–741.Google Scholar
Ismaili, N., Pérez-Morga, D., Walsh, P., Mayeda, A., Pays, A., Tebabi, P., Krainer, A.R., & Pays, E. (1999). Characterization of a SR protein from Trypanosoma brucei with homology to RNA-binding cis-splicing proteins. Mol Biochem Parasitol 102, 103–115.Google Scholar
Jess, W., Hammer, A., & Cornelissen, A.W. (1989). Complete sequence of the gene encoding the largest subunit of RNA polymerase I of Trypanosoma brucei. FEBS Lett 249, 123–128.Google Scholar
Jiménez-García, L.F., Elizundia, J.M., Lopez-Zamorano, B., Maciel, A., Zavala, G., Echeverría, O.M., & Vázquez-Nin, G.H. (1989). Implications for evolution of nuclear structures of animals, plants, fungi and protoctists. Biosystems 22, 103–116.Google Scholar
Jiménez-García, L.F., Segura-Valdez, M. de L., Ochs, R.L., Rothblum, L.I., Hannan, R., & Spector, D.L. (1994). Nucleologenesis: U3snRNA-containing prenucleolar bodies moves to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell 5, 955–966.Google Scholar
Jordan, E.G. & Cullis, C.A. (1982). The nucleolus. New York: Cambridge University Press.
Lamond, A.I. & Earnshaw, W.C. (1998). Structure and function in the nucleus. Science 280, 547–587.Google Scholar
López-Velázquez, G., Márquez, J., Ubaldo, E., Corkidi, G., Echeverría, O.M., & Vázquez-Nin, G.H. (1996). Three dimensional analyses of the arrangement of compact chromatin in the nucleus of G0 rat lymphocytes. Histochem Cell Biol 105, 153–161.Google Scholar
Martin, M., Moreno Díaz de la Espina, S., & Medina, F.J. (1998). Immunolocalization of DNA at nucleolar structural components in onion cells. Chromosoma 98, 368.Google Scholar
Misteli, T. (2001). Protein dynamics: Implications for nuclear architecture and gene expression. Science 291, 843–847.Google Scholar
Ogbadoyi, E., Ersfeld, K., Robinson, D., Sherwin, T., & Gull, K. (2000). Architecture of the Trypanosoma brucei nucleus during interphase and mitosis. Chromosoma 108, 501–513.Google Scholar
Risueño, M.C. & Medina, F.J. (1986). The Nucleolar Structure in Plant Cells. Vizcaya, Spain: Universidad del País Vasco.
Roth, J. (1986). Post-embedding cytochemistry with gold-labeled reagents. A review. J Microsc 143, 125–137.Google Scholar
Scheer, U. & Hock, R. (1999). Structure and function of the nucleolus. Curr Opin Cell Biol 11, 385–390.Google Scholar
Schwarzacher, H.G. & Mosgoller, W. (2000). Ribosome biogenesis in man: Current views on nucleolar structures and function. Cytogen Cell Genet 91, 243–254.Google Scholar
Shaw, P. & Jordan, G.E. (1995). The nucleolus. Annu Rev Cell Dev Biol 11, 93–121.Google Scholar
Sogin, M., Gunderson, J.H., Elwood, H.J., Alonso, R., & Peattie, D.A. (1989). Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science 243, 75–77.Google Scholar
Spector, D.L. (1993). Macromolecular domains within the cell nucleus. Annu Rev Cell Biol 9, 265–315.Google Scholar
Spector, D.L. (2001). Nuclear domains. J Cell Sci 114, 2891–2893.Google Scholar
Spector, D.L., Goldman, R.D., & Leinwand, L.A. (1998). Cells: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Thiry, M. & Goessens, G. (1996). Nucleolar functional organization. In The Nucleolus during the Cell Cycle, pp. 101–127. New York: Chapman & Hall Press.
Vázquez-Nin, G.H. & Echeverría, O.M. (2000). Introducción a la Microscopía Electrónica Aplicada a las Ciencias Biológicas. Mexico City: Universidad Nacional Autónoma de México-Fondo de Cultura Económica.
Wagner, W. & So, M. (1990). Genomic variation of Trypanosoma cruzi: Involvement of multicopy genes. Infect Immun 58, 3217–3224.Google Scholar
Wettstein, R. & Graver, A. (1973). Film-supporting frames for mounting section grids. J Ultrastruct Res 43, 436–447.Google Scholar
World Health Organization. (1997). Progress 1995–1996, Thirteenth Program Report of the UNDP/World Bank/WHO Special Program for Research and Training in Tropical Diseases. pp. 112–123. Geneva: World Health Organization.