Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-19T15:25:26.301Z Has data issue: false hasContentIssue false
  • English
  • Français

Lysosome-like compartments of Trypanosoma cruzi trypomastigotes may originate directly from epimastigote reservosomes

Published online by Cambridge University Press:  12 January 2017

JULIANA C. VIDAL ,
CAROLINA DE L. ALCANTARA ,
WANDERLEY DE SOUZA  and
NARCISA L. CUNHA-E-SILVA
JULIANA C. VIDAL*
Affiliation:
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Rio de Janeiro, Brazil
CAROLINA DE L. ALCANTARA
Affiliation:
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Rio de Janeiro, Brazil
WANDERLEY DE SOUZA
Affiliation:
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Rio de Janeiro, Brazil
NARCISA L. CUNHA-E-SILVA
Affiliation:
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Rio de Janeiro, Brazil
*
*Corresponding author: Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil and Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Rio de Janeiro, Brazil. E-mail: vidal.ju@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Trypanosoma cruzi epimastigote reservosomes store nutrients taken up during the intense endocytic activity exhibited by this developmental form. Reservosomes were classified as pre-lysosomal compartments. In contrast, trypomastigote forms are not able to take up nutrients from the medium. Interestingly, trypomastigotes also have acidic organelles with the same proteases contained in epimastigote reservosomes. Nevertheless, the origin and function of these organelles have not been disclosed so far. Given the similarities between the compartments of epimastigotes and trypomastigotes, the present study aimed to investigate the origin of metacyclic trypomastigote protease-containing organelles by tracking fluorospheres or colloidal gold particles previously stored in epimastigotes’ reservosomes throughout metacyclogenesis. Using three-dimensional reconstruction of serial electron microscopy images, it was possible to find trypomastigote compartments containing the tracer. Our observations demonstrate that the protease-containing compartments from metacyclic trypomastigotes may originate directly from the reservosomes of epimastigotes.

Keywords

Trypanosoma cruzimetacyclogenesistrypomastigoteslysosome-like organellesreservosomes
Type
Research Article
Information
Parasitology , Volume 144 , Issue 6 , May 2017 , pp. 841 - 850
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Adade, C. M., de Castro, S. L. and Soares, M. J. (2007). Ultrastructural localization of Trypanosoma cruzi lysosomes by aryl sulphatase cytochemistry. Micron 38, 252–256.Google Scholar
Bayer-Santos, E., Aguilar-Bonavides, C., Rodrigues, S. P., Cordero, E. M., Marques, A. F., Varela-Ramirez, A., Choi, H., Yoshida, N., da Silveira, J. F. and Almeida, I. C. (2013). Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. Journal of Proteome Research 12, 883–897.Google Scholar
Camargo, E. P. (1964). Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Revista do Instituto de Medicina Tropical de Sao Paulo 6, 93–100.Google ScholarPubMed
Cardoso, J., Soares, M. J., Menna-Barreto, R. F., Le Bloas, R., Sotomaior, V., Goldenberg, S. and Krieger, M. A. (2008). Inhibition of proteasome activity blocks Trypanosoma cruzi growth and metacyclogenesis. Parasitology Research 103, 941–951.Google Scholar
Contreras, V. T., Salles, J. M., Thomas, N., Morel, C. M. and Goldenberg, S. (1985). In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Molecular & Biochemical Parasitology 16, 315–327.Google Scholar
De Souza, W. (2002). Basic cell biology of Trypanosoma cruzi . Current Pharmaceutical Design 8, 269–285.Google Scholar
de Souza, W., Sant'Anna, C. and Cunha-e-Silva, N. L. (2009). Electron microscopy and cytochemistry analysis of the endocytic pathway of pathogenic protozoa. Progress in Histochemistry and Cytochemistry 44, 67–124.Google Scholar
Docampo, R., Ulrich, P. and Moreno, S. N. (2010). Evolution of acidocalcisomes and their role in polyphosphate storage and osmoregulation in eukaryotic microbes. Philosophical Transactions of the Royal Society of London B, Biological Sciences 365, 775–784.CrossRefGoogle ScholarPubMed
Drobne, D., Milani, M., Leser, V., Tatti, F., Zrimec, A., Znidarsic, N., Kostanjsek, R. and Strus, J. (2008). Imaging of intracellular spherical lamellar structures and tissue gross morphology by a focused ion beam/scanning electron microscope (FIB/SEM). Ultramicroscopy 108, 663–670.Google Scholar
Figueiredo, R. C., Rosa, D. S. and Soares, M. J. (2000). Differentiation of Trypanosoma cruzi epimastigotes: metacyclogenesis and adhesion to substrate are triggered by nutritional stress. Journal of Parasitology 86, 1213–1218.CrossRefGoogle ScholarPubMed
Franke de Cazzulo, B. M., Martinez, J., North, M. J., Coombs, G. H. and Cazzulo, J. J. (1994). Effects of proteinase inhibitors on the growth and differentiation of Trypanosoma cruzi . FEMS Microbiology Letters 124, 81–86.Google Scholar
Garcia-Silva, M. R., das Neves, R. F., Cabrera-Cabrera, F., Sanguinetti, J., Medeiros, L. C., Robello, C., Naya, H., Fernandez-Calero, T., Souto-Padron, T., de Souza, W. and Cayota, A. (2014). Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells. Parasitology Research 113, 285–304.Google Scholar
Kessler, R. L., Gradia, D. F., Pontello Rampazzo Rde, C., Lourenco, E. E., Fidencio, N. J., Manhaes, L., Probst, C. M., Avila, A. R. and Fragoso, S. P. (2013). Stage-regulated GFP Expression in Trypanosoma cruzi: applications from host–parasite interactions to drug screening. PLoS ONE 8, e67441.CrossRefGoogle ScholarPubMed
Lewis, V., Green, S. A., Marsh, M., Vihko, P., Helenius, A. and Mellman, I. (1985). Glycoproteins of the lysosomal membrane. Journal of Cell Biology 100, 1839–1847.Google Scholar
Marks, M. S., Heijnen, H. F. and Raposo, G. (2013). Lysosome-related organelles: unusual compartments become mainstream. Current Opinion in Cell Biology 25, 495–505.Google Scholar
Nagakura, K., Tachibana, H. and Kaneda, Y. (1985). Alteration of the cell surface acid phosphatase concomitant with the morphological transformation in Trypanosoma cruzi . Comparative Biochemistry and Physiology B 81, 815–817.Google Scholar
Reynolds, E. S. (1963). Use of lead citrate at high Ph as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208.Google Scholar
Roth, J. (1983). Application of lectin–gold complexes for electron microscopic localization of glycoconjugates on thin sections. Journal of Histochemistry and Cytochemistry 31, 987–999.CrossRefGoogle ScholarPubMed
Sant'Anna, C., Parussini, F., Lourenco, D., de Souza, W., Cazzulo, J. J. and Cunha-e-Silva, N. L. (2008 a). All Trypanosoma cruzi developmental forms present lysosome-related organelles. Histochemistry and Cell Biology 130, 1187–1198.CrossRefGoogle ScholarPubMed
Sant'Anna, C., Pereira, M. G., Lemgruber, L., de Souza, W. and Cunha e Silva, N. L. (2008 b). New insights into the morphology of Trypanosoma cruzi reservosome. Microscopy Research and Technique 71, 599–605.Google Scholar
Sant'Anna, C., Nakayasu, E. S., Pereira, M. G., Lourenco, D., de Souza, W., Almeida, I. C. and Cunha, E. S. N. L. (2009). Subcellular proteomics of Trypanosoma cruzi reservosomes. Proteomics 9, 1782–1794.CrossRefGoogle ScholarPubMed
Slot, J. W. and Geuze, H. J. (1985). A new method of preparing gold probes for multiple-labeling cytochemistry. European Journal of Cell Biology 38, 87–93.Google ScholarPubMed
Soares, M. J. and De Souza, W. (1988). Cytoplasmic organelles of trypanosomatids: a cytochemical and stereological study. Journal of Submicroscopic Cytology and Pathology 20, 349–361.Google Scholar
Soares, M. J. and de Souza, W. (1991). Endocytosis of gold-labeled proteins and LDL by Trypanosoma cruzi . Parasitology Research 77, 461–468.Google Scholar
Soares, M. J., Souto-Padron, T., Bonaldo, M. C., Goldenberg, S. and de Souza, W. (1989). A stereological study of the differentiation process in Trypanosoma cruzi . Parasitology Research 75, 522–527.Google Scholar
Soares, M. J., Souto-Padron, T. and De Souza, W. (1992). Identification of a large pre-lysosomal compartment in the pathogenic protozoon Trypanosoma cruzi . Journal of Cell Science 102, 157–167.Google Scholar
Trocoli Torrecilhas, A. C., Tonelli, R. R., Pavanelli, W. R., da Silva, J. S., Schumacher, R. I., de Souza, W., NC, E. S., de Almeida Abrahamsohn, I., Colli, W. and Manso Alves, M. J. (2009). Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes and Infection 11, 29–39.Google Scholar
Vidal, J. C., Alcantara, C. L., de Souza, W. and Cunha, E. S. N. L. (2016). Loss of the cytostome–cytopharynx and endocytic ability are late events in Trypanosoma cruzi metacyclogenesis. Journal of Structural Biology 196, 319–328.Google Scholar
Vieira, M., Rohloff, P., Luo, S., Cunha-e-Silva, N. L., de Souza, W. and Docampo, R. (2005). Role for a P-type H+-ATPase in the acidification of the endocytic pathway of Trypanosoma cruzi . Biochemical Journal 392, 467–474.Google Scholar

Vidal supplementary material

Movie 1

Download Vidal supplementary material(Video)
Video 7.7 MB