Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-27T23:41:56.407Z Has data issue: false hasContentIssue false

Nucleologenesis in Trypanosoma cruzi

Published online by Cambridge University Press:  29 April 2016

Tomás Nepomuceno-Mejía
Affiliation:
Laboratory of Electron Microscopy, Faculty of Science, National Autonomous University of Mexico, México Cd. Mx. 04510, México
Reyna Lara-Martínez
Affiliation:
Laboratory of Electron Microscopy, Faculty of Science, National Autonomous University of Mexico, México Cd. Mx. 04510, México
Roberto Hernández
Affiliation:
Department of Molecular Biology and Biotechnology, Biomedical Research Institute, National Autonomous University of Mexico, México Cd. Mx. 04510, México
María de Lourdes Segura-Valdez
Affiliation:
Laboratory of Electron Microscopy, Faculty of Science, National Autonomous University of Mexico, México Cd. Mx. 04510, México
Luis F. Jiménez-García*
Affiliation:
Laboratory of Electron Microscopy, Faculty of Science, National Autonomous University of Mexico, México Cd. Mx. 04510, México
*
*Corresponding author. [email protected]
Get access

Abstract

Nucleolar assembly is a cellular event that requires the synthesis and processing of ribosomal RNA, in addition to the participation of pre-nucleolar bodies (PNBs) at the end of mitosis. In mammals and plants, nucleolar biogenesis has been described in detail, but in unicellular eukaryotes it is a poorly understood process. In this study, we used light and electron microscopy cytochemical techniques to investigate the distribution of nucleolar components in the pathway of nucleolus rebuilding during closed cell division in epimastigotes of Trypanosoma cruzi, the etiologic agent of American trypanosomiasis. Silver impregnation specific for nucleolar organizer regions and an ethylenediaminetetraacetic acid regressive procedure to preferentially stain ribonucleoprotein revealed the conservation and dispersion of nucleolar material throughout the nucleoplasm during cell division. Furthermore, at the end of mitosis, the argyrophilic proteins were concentrated in the nucleolar organizer region. Unexpectedly, accumulation of nucleolar material in the form of PNBs was not visualized. We suggest that formation of the nucleolus in epimastigotes of T. cruzi occurs by a process that does not require the concentration of nucleolar material within intermediate nuclear bodies such as mammalian and plant PNBs.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2016

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.)

Footnotes

Current address: CONACYT Research Fellow, Regional Center for Public Health Research, Tapachula, Chiapas, México.

References

Angelier, N., Tramier, M., Louvet, E., Coppey-Moisan, M., Savino, T.M., De Mey, J.R. & Hernandez-Verdun, D. (2005). Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Mol Biol Cell 16, 28622871.Google Scholar
Benavente, R. (1991). Postmitotic nuclear reorganization events analyzed in living cells. Chromosoma 100, 215220.10.1007/BF00344154Google Scholar
Bernhard, W. (1969). A new staining procedure for electron microscopical cytology. J Ultrastruct Res 27, 250265.10.1016/S0022-5320(69)80016-XGoogle Scholar
Boisvert, F.M., Van-Koningsbruggen, S., Navascues, J. & Lamond, A.I. (2007). The multifunctional nucleolus. Nat Rev Mol Cell Biol 8, 574585.10.1038/nrm2184Google Scholar
Camargo, E.P. (1964). Growth and differentiation in Trypanosoma cruzi I. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop Sao Paulo 6, 93100.Google Scholar
Carron, C., Balor, S., Delavoie, F., Plisson-Chastang, C., Faubladier, M., Gleizes, P.E. & O’Donohue, M.F. (2012). Post-mitotic dynamics of pre-nucleolar bodies is driven by pre-rRNA processing. J Cell Sci 125, 45324542.10.1242/jcs.106419Google Scholar
De Souza, W. (2002). Basic cell biology of Trypanosoma cruzi. Curr Pharm Des 8, 269285.10.2174/1381612023396276Google Scholar
Dimario, P.J. (2004). Cell and molecular biology of nucleolar assembly and disassembly. Int Rev Cytol 239, 99178.10.1016/S0074-7696(04)39003-0Google Scholar
Dundr, M., Misteli, T. & Olson, M.O. (2000). The dynamics of postmitotic reassembly of the nucleolus. J Cell Biol 150, 433446.10.1083/jcb.150.3.433Google Scholar
Elias, M.C., Da Cunha, J.P., De Faria, F.P., Mortara, R.A., Freymüller, E. & Schenkman, S. (2007). Morphological events during the Trypanosoma cruzi cell cycle. Protist 158, 147157.10.1016/j.protis.2006.10.002Google Scholar
Elias, M.C., 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, 7990.10.1016/S0166-6851(00)00349-2Google Scholar
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, 105110.Google Scholar
Fomproix, N., Gébrane-Younès, J. & Hernandez-Verdun, D. (1998). Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis. J Cell Sci 111, 359372.Google Scholar
Goodpasture, C. & Bloom, S.E. (1975). Visualization of nucleolus organizer regions in mammalian chromosomes using silver stain. Chromosoma 53, 3750.10.1007/BF00329389Google Scholar
Henras, A.K., Plisson-Chastang, C., O’Donohue, M.F., Chakraborty, A. & Gleizes, P.E. (2015). An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip Rev RNA 6, 225242.10.1002/wrna.1269Google Scholar
Hernández, R., Cevallos, A.M., Nepomuceno-Mejía, T. & López-Villaseñor, I. (2012). Stationary phase in Trypanosoma cruzi epimastigotes as a preadaptative stage for metacyclogenesis. Parasitol Res 111, 509514.10.1007/s00436-012-2974-yGoogle Scholar
Hernandez-Verdun, D. (2006). Nucleolus: From structure to dynamics. Histochem Cell Biol 125, 127137.Google Scholar
Hernandez-Verdun, D. (2011). Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2, 189194.10.4161/nucl.2.3.16246Google Scholar
Hernandez-Verdun, D., Roussel, P. & Gébrane-Younès, J. (2002). Emerging concepts of nucleolar assembly. J Cell Sci 115, 22652270.Google Scholar
Jiménez-García, L.F., Rothblum, L.I., Busch, H. & Ochs, R.L. (1989). Nucleologenesis: Use of non-isotopic in situ hybridization and immunocytochemistry to compare the localization of rDNA and nucleolar proteins during mitosis. Biol Cell 65, 239246.10.1111/j.1768-322X.1989.tb00795.xGoogle Scholar
Jiménez-García, L.F, Segura-Valdez, M.L., Ochs, R.L., Rothblum, L.I., Hannan, R. & Spector, D.L. (1994). Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell 5, 955966.Google Scholar
López-Velázquez, G., Hernández, R., López-Villaseñor, I., Reyes-Vivas, H., Segura-Valdez, M.L. & Jiménez-García, L.F. (2005). Electron microscopy analysis of the nucleolus of Trypanosoma cruzi. Microsc Microanal 11, 293299.Google Scholar
McClintock, B. (1934). The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z Zellforsch Mikrosk Anat 21, 294328.Google Scholar
Muro, E., Gébrane-Younés, J., Jobart-Malfait, A., Louvet, E., Roussel, P. & Hernandez-Verdun, D. (2010). The traffic of proteins between nucleolar organizer regions and prenucleolar bodies governs the assembly of the nucleolus at exit of mitosis. Nucleus 1, 202211.10.4161/nucl.11334Google Scholar
Nepomuceno-Mejía, T., Lara-Martínez, R., Cevallos, A.M., López-Villaseñor, I., Jiménez-García, L.F. & Hernández, R. (2010). The Trypanosoma cruzi nucleolus: A morphometrical analysis of cultured epimastigotes in the exponential and stationary phases. FEMS Microbiol Lett 313, 4146.10.1111/j.1574-6968.2010.02117.xGoogle Scholar
Ochs, R.L., Lischwe, M.A., Shen, E., Caroll, R.E. & Busch, H. (1985). Nucleologenesis: Composition and fate of prenucleolar bodies. Chromosoma 92, 330336.10.1007/BF00327463Google Scholar
Savino, T.M., Gébrane-Younès, J., De Mey, J., Sibarita, J.B. & Hernandez-Verdun, D. (2001). Nucleolar assembly of the rRNA processing machinery in living cells. J Cell Biol 153, 10971110.10.1083/jcb.153.5.1097Google Scholar
Spector, D.L., Goldman, R.D. & Leinwand, L.A. (1998). Cells: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press.Google Scholar
Stevens, B.J. (1965). The fine structure of the nucleolus during mitosis in the grasshopper neuroblast cell. J Cell Biol 24, 349368.10.1083/jcb.24.3.349Google Scholar
Teixeira, D.E., Benchimol, M., Crepaldi, P.H. & De Souza, W. (2012). Interactive multimedia to teach the life cycle of Trypanosoma cruzi, the causative agent of Chagas disease. PLoS Negl Trop Dis 6, e1749.10.1371/journal.pntd.0001749Google Scholar
Testillano, P.S., Sanchez-Pina, M.A., Olmedilla, A., Ollacarizqueta, M.A., Tandler, C.J. & Risueño, M.C. (1991). A specific ultrastructural method to reveals DNA: The NAMA-Ur. J Histochem Cytochem 39, 14271438.10.1177/39.10.1719069Google Scholar
Toro, G.C. & Galanti, N. (1988). H1 histone and histone variants in Trypanosoma cruzi. Exp Cell Res 174, 1624.Google Scholar
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.Google Scholar