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The induction of Trypanosoma cruzi trypomastigote to amastigote transformation by low pH

Published online by Cambridge University Press:  06 April 2009

S. Tomlinson ,
F. Vandekerckhove ,
U. Frevert  and
V. Nussenzweig
S. Tomlinson
Affiliation:
Michael Heidelberger Division of Immunology, Department of Pathology
F. Vandekerckhove
Affiliation:
Michael Heidelberger Division of Immunology, Department of Pathology
U. Frevert
Affiliation:
Department of Parasitology, New York University Medical Center, 550 First Avenue, New York, NY 10016, USA
V. Nussenzweig
Affiliation:
Michael Heidelberger Division of Immunology, Department of Pathology
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Summary

Following cell invasion, Trypanosoma cruzi trypomastigotes transform into amastigotes, which are the mammalian replicative forms of the parasite. Although amastigotes represent a critical stage in the life-cycle of T. cruzi, little is known of the factors controlling trypomastigote to amastigote transformation. Kanbera et al. (1990) observed that exposure of trypomastigotes to acidic pH induced their transformation into rounded forms resembling amastigotes. We confirm their observation and, using two strains of T. cruzi, establish that these transformants are ultrastructurally and biochemically indistinguishable from natural amastigotes. Incubation of trypomastigotes in medium at pH 5·0 for 2 h was sufficient to trigger their transformation into forms resembling amastigotes. Electron microscopical analysis confirmed that the kinetoplast structure, and general morphological features of the acid-induced, extracellular amastigotes were indistinguishable from those of intracellular-derived amastigotes. The extracellular transformation was accompanied by the acquisition of the stage-specific surface antigen of the naturally transformed amastigotes (Ssp-4), and loss of a stagespecific trypomastigote antigen (Ssp-3). Trypomastigotes incubated at neutral pH did not transform into amastigotes, and did not acquire the Ssp-4 epitope or lose the Ssp-3 epitope. Finally, acid-induced amastigotes subsequently incorporated [3H]thymidine into their DNA, indicating that the important replicative property of intracellular amastigotes is also exhibited by these in vitro transformants. This effect of low pH appears to be of physiological relevance, and acid-induced extracellular transformation appears to represent a valid experimental technique for studies of the molecular mechanisms involved in the differentiation process.

Keywords

Trypanosoma cruziamastigotetransformationdifferentiationpHlysosome
Type
Research Article
Information
Parasitology , Volume 110 , Issue 5 , June 1995 , pp. 547 - 554
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Andrews, N. W., Hong, K. S., Robbins, E. S. & Nussenzweig, V. (1987). Stage-specific surface antigens expressed during the morphogenesis of vertebrate forms of Trypanosoma cruzi. Experimental Parasitology 64, 474–84.CrossRefGoogle ScholarPubMed
Andrews, N. W., Robbins, E. S., Ley, V., Hong, K. S. & Nussenzweig, V. (1988). Developmentally regulated phospholipase C-mediated release of the major surface glycoprotein of amastigotes of Trypanosoma cruzi. Journal of Experimental Medicine 167, 300–14.CrossRefGoogle ScholarPubMed
Andrews, N. W. & Whitlow, M. B. (1989). Secretion of Trypanosoma cruzi of a hemolysin active at low pH. Molecular and Biochemical Parasitology 33, 249–56.CrossRefGoogle ScholarPubMed
Brack, C. (1968). Elektronmikroskopische Untersuchungen zum Lebenszyklus von Trypanosoma cruzi. Acta Tropica 25, 289–356.Google Scholar
Castellani, O., Ribiero, L. V. & Fernandes, J. F. (1967). Differentiation of Trypanosoma cruzi in culture. Journal of Protozoology 14, 447–51.CrossRefGoogle ScholarPubMed
de Souza, W. (1984). Cell biology of Trypanosoma cruzi. International Review of Cytology 86, 197–283.CrossRefGoogle ScholarPubMed
Glauert, A. M., Baker, J. R. & Selden, L. F. (1982). Mechanism of entry and development of Trypanosoma dionisii in non-phagocytic cells. Journal of Cell Science 56, 371–87.CrossRefGoogle ScholarPubMed
Hall, B. F. (1993). Trypanosoma cruzi: mechanisms for entry into host cells. Seminars in Cell Biology 4, 323–33.CrossRefGoogle ScholarPubMed
Harth, G., Andrews, N. W., Mills, A. A., Engel, J. C., Smith, R. & McKerrow, J. H. (1993). Peptide-fluoromethyl ketones arrest intracellular replication and intercellular transmission of Trypanosoma cruzi. Molecular and Biochemical Parasitology 58, 17–24.CrossRefGoogle ScholarPubMed
Howard, P. K., Sefton, B. M. & Firtel, R. A. (1993). Tyrosine phosphorylation of actin in Dictyostelium associated with cell-shape changes. Science 259, 241–4.CrossRefGoogle ScholarPubMed
Kanbara, H., Uemura, H., Nakazawa, S. & Fukama, T. (1990). Effect of low pH on transformation of Trypanosoma cruzi trypomastigote to amastigote. Japanese Journal of Parasitology 39, 226–8.Google Scholar
Ley, V., Andrews, N. W., Robbins, E. S. & Nussenzweig, V. (1988). Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. Journal of Experimental Medicine 168, 649–59.CrossRefGoogle ScholarPubMed
Ley, V., Robbins, E. S., Nussenzweig, V. & Andrews, N. W. (1990). The exit of Trypanosoma cruzi from the phagosome is inhibited by raising the pH of acidic compartments. Journal of Experimental Medicine 171, 401–13.CrossRefGoogle Scholar
Lima, A. P., Scharfstein, J., Storer, A. C. & Menard, R. (1992). Temperature-dependent substrate inhibition of the cysteine proteinase (GP57/51) from Trypanosoma cruzi. Molecular and Biochemical Parasitology 56, 335–8.CrossRefGoogle ScholarPubMed
Meyer, H. (1958). The fine structure of the flagellum and the kinetoplast-chondriome of Trypanosoma (Schizotrypanum) cruzi in tissue culture. Journal of Protozoology 15, 614–21.CrossRefGoogle Scholar
Meyer, H. (1969). Further studies on the fine structure of the kinetoplast-chondriome of Trypanosoma (Schizotrypanum) cruzi in thin sections of infected tissue cultures. Revista do Institute de Medicina Tropical de São Paulo 11, 48–56.Google ScholarPubMed
Ouaissi, A., Cornette, J., Schoeneck, R., Plumas-Marty, B., Taibi, A., Loyens, M. & Capron, A. (1992).Fibronectin cleavage fragments provide a growth factor-like activity for the differentiation of Trypanosoma cruzi trypomastigotes to amastigotes. European Journal of Cell Biology 59, 68–79.Google ScholarPubMed
Ribeiro, Dos Santos R., Rossi, M. A., Laus, J. L., Silva, J. S., Savino, W. & Mengel, J. (1992). Anti-CD4 abrogates rejection and reestablishes long-term tolerance to syngeneic newborn hearts grafted in mice chronically infected with Trypanosoma cruzi. Journal of Experimental Medicine 175, 29–39.Google Scholar
Rojas, M. V. & Galanti, N. (1991). Relationship between DNA methylation and cell proliferation in Trypanosoma cruzi. FEBS Letters 295, 31–4.CrossRefGoogle ScholarPubMed
Sanabria, A. (1971). Ultrastructure of Trypanosoma cruzi in mouse liver. Experimental Parasitology 30, 187–98.CrossRefGoogle ScholarPubMed
Schenkman, S., Jiang, M.-S., Hart, G. W. & Nussenzweig, V. (1991). A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell 65, 1117–25.CrossRefGoogle ScholarPubMed
Shariff, A. & Luna, E. J. (1992). Diacylglycerol-stimulated formation of actin nucleation sites at plasma membranes. Science 256, 245–7.CrossRefGoogle ScholarPubMed
Silva, L. H. P. & Nussenzweig, V. (1953). Sobre uma cepa de Trypanosoma cruzi altamente virulenta para o camundongo branco. Folia Clinica Biologica 20, 191–203.Google Scholar
Simpson, L. (1972). The kinetoplast of the hemoflagellates. International Review of Cytology 32, 139–207.CrossRefGoogle Scholar
Tardieux, I., Webster, P., Ravesloot, J., Boron, W., Lunn, J. A., Heuser, J. E. & Andrews, N. W. (1992).Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell 71, 1117–30.CrossRefGoogle ScholarPubMed
Zilberstein, D., Blumenfeld, N., Liveanu, V., Gepstein, A. & Jaffe, C. L. (1991). Growth at acidic pH induces an amastigote stage-specific protein in Leishmania promastigotes. Molecular and Biochemical Parasitology 45, 175–8.CrossRefGoogle ScholarPubMed