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

  • JULIANA C. VIDAL (a1) (a2), CAROLINA DE L. ALCANTARA (a1) (a2), WANDERLEY DE SOUZA (a1) (a2) and NARCISA L. CUNHA-E-SILVA (a1) (a2)

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.

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Corresponding author

*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

References

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Adade, C. M., de Castro, S. L. and Soares, M. J. (2007). Ultrastructural localization of Trypanosoma cruzi lysosomes by aryl sulphatase cytochemistry. Micron 38, 252256.
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, 883897.
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, 93100.
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, 941951.
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, 315327.
De Souza, W. (2002). Basic cell biology of Trypanosoma cruzi . Current Pharmaceutical Design 8, 269285.
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, 67124.
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, 775784.
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, 663670.
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, 12131218.
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, 8186.
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, 285304.
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.
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, 18391847.
Marks, M. S., Heijnen, H. F. and Raposo, G. (2013). Lysosome-related organelles: unusual compartments become mainstream. Current Opinion in Cell Biology 25, 495505.
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, 815817.
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.
Roth, J. (1983). Application of lectin–gold complexes for electron microscopic localization of glycoconjugates on thin sections. Journal of Histochemistry and Cytochemistry 31, 987999.
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, 11871198.
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, 599605.
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, 17821794.
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, 8793.
Soares, M. J. and De Souza, W. (1988). Cytoplasmic organelles of trypanosomatids: a cytochemical and stereological study. Journal of Submicroscopic Cytology and Pathology 20, 349361.
Soares, M. J. and de Souza, W. (1991). Endocytosis of gold-labeled proteins and LDL by Trypanosoma cruzi . Parasitology Research 77, 461468.
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, 522527.
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, 157167.
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, 2939.
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, 319328.
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, 467474.

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

  • JULIANA C. VIDAL (a1) (a2), CAROLINA DE L. ALCANTARA (a1) (a2), WANDERLEY DE SOUZA (a1) (a2) and NARCISA L. CUNHA-E-SILVA (a1) (a2)

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