Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T07:01:08.837Z Has data issue: false hasContentIssue false
  • English
  • Français

Reservosome: an endocytic compartment in epimastigote forms of the protozoan Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae). Correlation between endocytosis of nutrients and cell differentiation

Published online by Cambridge University Press:  14 September 2004

R. C. B. Q. FIGUEIREDO ,
D. S. ROSA ,
Y. M. GOMES ,
M. NAKASAWA  and
M. J. SOARES
R. C. B. Q. FIGUEIREDO
Affiliation:
Departamento de Biologia Celular Ultrastructura, Centro de Pesquisas Aggeu Megalhães/FIOCRUZ, Av. Moraes Rego s/n°, 50670-420 Recife, PE, Brazil
D. S. ROSA
Affiliation:
Universidade Federal de São Paulo, Departamento de Microbiologia Imunobiologia e Parasitologia – UNIFESP, Rua Botucatu 862/6° andar, Vila Clementino, 04023-062 São Paulo, SP, Brazil
Y. M. GOMES
Affiliation:
Departamento de Imunologia, Centro de Pesquisas Aggeu Magalhães/FIOCRUZ, Av. Moraes Rego s/n°, 50670-420 Recife, PE, Brazil
M. NAKASAWA
Affiliation:
Departamento de Imunologia, Centro de Pesquisas Aggeu Magalhães/FIOCRUZ, Av. Moraes Rego s/n°, 50670-420 Recife, PE, Brazil
M. J. SOARES
Affiliation:
Departamento de Ultra-estrutura e Biologia Celular, Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brazil
Get access Rights & Permissions [Opens in a new window]

Abstract

Reservosomes are large membrane-bound organelles found at the posterior end of epimastigote forms of Trypanosoma cruzi, but absent in amastigotes and trypomastigotes. We have transferred bloodstream trypomastigotes to LIT medium supplemented with gold-labelled transferrin in order to analyse, at the ultrastructural level, the occurrence of reservosomes and endocytosis during the trypomastigote to epimastigote differentiation. After 24 h, the trypomastigotes differentiated into amastigotes, which adhered to each other forming large clusters. Electron-dense vesicles were detected close to the Golgi complex in cells with intermediary characteristics between amastigotes and epimastigotes, but typical reservosomes at the posterior cell tip were still absent. Transferrin–gold complexes were observed only bound to the surface of clustered cells. After 72 h, epimastigotes were observed being released from the clusters and free-swimming epimastigotes appeared, containing electron-dense vesicles at their posterior region. Typical reservosomes, labelled with transferrin–gold, were observed only in free-swimming epimastigotes. When fully differentiated epimastigotes were incubated with transferrin–gold complexes and then processed for the immunocytochemical detection of cysteine proteinase, all reservosomes were positive for the enzyme, but co-localization of both markers did not occur in all organelles. Our data demonstrate that in T. cruzi epimastigotes endocytosis is strongly related to reservosome biogenesis during the trypomastigote to epimastigote differentiation process.

Keywords

endocytosisKinetoplastidareservosomesTrypanosoma cruzi
Type
Research Article
Information
Parasitology , Volume 129 , Issue 4 , October 2004 , pp. 431 - 438
Copyright
2004 Cambridge University Press

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

BONALDO, M. C., SOUTO-PADRÓN, T., DE SOUZA, W. & GOLDENBERG, S. (1998). Cell-substrate adhesion during Trypanosoma cruzi differentiation. Journal of Cell Biology 106, 1349–1358.Google Scholar
BRITIGAN, B. E., LEWIS, T. S., McCORMICK, M. L. & WILSON, M. E. (1998). Evidence for the existence of a surface receptor for ferriclactoferrin and ferrictransferrin associated with the plasma membrane of the protozoan parasite Leishmania donovani. Advances in Experimental Medicine and Biology 443, 135–140.CrossRefGoogle Scholar
CAMARGO, E. P. (1964). Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid medium. Revista do Instituto de Medicina Tropical de São Paulo 6, 93–100.Google Scholar
CHAGAS, C. (1909). Nova tripanosomiase humana. Estudo sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen. n. sp. ajente etiolojico de nova entidade morbida no homen. Memórias do Instituto Oswaldo Cruz 1, 159–218.Google Scholar
CONTRERAS, V. T., SALLES, J. M., THOMAZ, N., MOREL, C. M. & GOLDENBERG, S. (1985). In vitro differentiation of Trypanosoma cruzi under chemically defined conditions. Molecular and Biochemical Parasitology 16, 315–327.CrossRefGoogle Scholar
CORRÊA, A. F., ANDRADE, L. R. & SOARES, M. J. (2002). Elemental composition of acidocalcisomes of Trypanosoma cruzi bloodstream trypomastigote forms. Parasitology Research 88, 875–880.CrossRefGoogle Scholar
CUNHA-E-SILVA, N. L., ATELLA, G. C., PORTO-CARREIRO, I., MORGADO-DIAZ, J., PEREIRA, M. G. & DE SOUZA, W. (2002). Isolation and characterization of a reservosome fraction from Trypanosoma cruzi. FEMS Microbiology Letters 214, 7–12.CrossRefGoogle Scholar
DE SOUZA, W. (2002). Special organelles of some pathogenic protozoa. Parasitology Research 88, 1013–1025.CrossRefGoogle Scholar
DE SOUZA, W., CARVALHO, T. C., BENCHIMOL, M. & CHIARI, E. (1978). Trypanosoma cruzi: Ultrastructural, cytochemical and freeze-fracture studies of protein uptake. Experimental Parasitology 45, 101–115.CrossRefGoogle Scholar
DE SOUZA, W., CARREIRO, I. P., MIRANDA, K. & SILVA, N. L. (2000). Two special organelles found in Trypanosoma cruzi. Anais da Academia Brasileira de Ciências 72, 421–432.CrossRefGoogle Scholar
ENGEL, J. C., COYLE, P. S., PALMER, J., HSIEH, I., BAINTON, D. F. & McKERROW, J. H. (1998). Cysteine protease inhibitors alter Golgi complex ultrastructure and function in Trypanosoma cruzi. Journal of Cell Science 11, 597–606.Google Scholar
FIGUEIREDO, R. C. B. Q., STEINDEL, M. & SOARES, M. J. (1994). The reservosomes of epimastigote forms of Trypanosoma cruzi: occurrence during in vitro cultivation. Parasitology Research 80, 517–522.CrossRefGoogle Scholar
FIGUEIREDO, R. C. B. Q., ROSA, D. S. & 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 Scholar
KOLLIEN, A. H., SCHMID, T. J. & SCHAUB, G. A. (1998). Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans. Acta Tropica 70, 127–141.CrossRefGoogle Scholar
LANDFEAR, S. M. & IGNATUSHCHENKO, M. (2001). The flagellum and flagellar pocket of trypanosomatids. Molecular Biochemical Parasitology 115, 1–17.CrossRefGoogle Scholar
LIMA, M. F. & VILLALTA, F. (1990). Trypanosoma cruzi receptors for human transferrin and their role. Molecular and Biochemical Parasitology 38, 245–252.CrossRefGoogle Scholar
MEIRELLES, M. N. L., SOUTO-PADARÓN, T. & DE SOUZA, W. (1984). Participation of cell surface anionic sites in the interaction between Trypanosoma cruzi and macrophages. Journal of Submicroscopy, Cytology and Pathology 16, 533–545.Google Scholar
MENDONÇA, M. S. M., SILVA, J. L. N., CUNHA-E-SILVA, N. L., DE SOUZA, W. & LOPES, U. G. (2000). Characterization of a Rab11 homologue in Trypanosoma cruzi. Gene 243, 179–185.CrossRefGoogle Scholar
MORGAN, G. W., HALL, B. S., DENNY, P. W., CARRINGTON, M. & FIELD, M. C. (2002). The Kinetoplastida endocytic apparatus. Part I: a dynamic system for nutrition and evasion of host defences. Trends in Parasitology 18, 491–496.Google Scholar
PORTO-CARREIRO, I., ATTIAS, M., MIRANDA, K., DE SOUZA, W. & CUNHA-E-SILVA, N. L. (2000). Trypanosoma cruzi epimastigote endocytic pathway: cargo enters the cytostome and passes through an early endosomal network before storage in reservosomes. European Journal of Cell Biology 79, 858–869.CrossRefGoogle Scholar
SCHELL, D., BOROWY, N. K. & OVERATH, P. (1991). Transferrin is a growth factor for the bloodstream form of Trypanosoma brucei. Parasitology Research 77, 558–560.CrossRefGoogle Scholar
SHEFF, D. R., DARO, E. A., HULL, M. & MELLMAN, I. (1999). The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. Journal of Cell Biology 145, 123–139.CrossRefGoogle Scholar
SLOT, J. W. & GEUZE, H. J. (1985). A new method of preparing gold probes for multiple labeling cytochemistry. European Journal of Cell Biology 38, 87–93.Google Scholar
SOARES, M. J. (1999). The reservosome of Trypanosoma cruzi epimastigotes: an organelle of the endocytic pathway with role in metacyclogenesis. Memórias do Instituto Oswaldo Cruz 94, 139–141.CrossRefGoogle Scholar
SOARES, M. J. & DE SOUZA, W. (1988). Cytoplasmic organelles of trypanosomatids: a cytochemical and stereological study. Journal of Submicroscopy, Cytology and Pathology 20, 349–361.Google Scholar
SOARES, M. J. & DE SOUZA, W. (1991). Endocytosis of gold-labeled proteins and LDL by Trypanosoma cruzi. Parasitology Research 77, 461–468.CrossRefGoogle Scholar
SOARES, M. J., SOUTO-PADRÓN, T., BONALDO, M. C., GOLDENBERG, S. & DE SOUZA, W. (1989). A stereological study of the differentiation process in Trypanosoma cruzi. Parasitology Research 75, 522–527.CrossRefGoogle Scholar
SOARES, M. J., SOUTO-PADRÓN, T. & DE SOUZA, W. (1992). Indentification of a large pre-lysosomal compartment in the pathogenic protozoon Trypanosoma cruzi. Journal of Cell Science 102, 157–167.Google Scholar
SOUTO-PADRÓN, T., CAMPETELLA, O. E., CAZZULO, J. J. & DE SOUZA, W. (1990). Cysteine proteinase in Trypanosoma cruzi: immunocytochemical localization and involvement in parasite–host cell interaction. Journal of Cell Science 96, 485–490.Google Scholar
STEVERDING, D. (2000). The transferrin receptor of Trypanosoma brucei. Parasitology International 48, 191–198.CrossRefGoogle Scholar
URBINA, J. A. (1994). Intermediary metabolism of Trypanosoma cruzi. Parasitology Today 10, 107–110.CrossRefGoogle Scholar
WILSON, M. E., LEWIS, T. S., MILLER, M. A., McCORMICK, M. L. & BRITIGAN, B. E. (2002). Leishmania chagasi: uptake of iron bound to lactoferrin or transferrin requires an iron reductase. Experimental Parasitology 100, 196–207.CrossRefGoogle Scholar
WILSON, M. E., VORHIES, R. W., ANDERSEN, K. A. & BRITIGAN, B. E. (1994). Acquisition of iron from transferrin and lactoferrin by the protozoan Leishmania chagasi. Infection and Immunology 62, 3262–3269.Google Scholar