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Intermembrane lipid transfer during Trypanosoma cruzi-induced erythrocyte membrane destabilization

Published online by Cambridge University Press:  06 April 2009

H. D. Luján  and
D. H. Bronia
H. D. Luján
Affiliation:
Cátedra de Química Biológica, Facultad de Ciencias Médicos, Universidad Nacional de Córdoba; C.C. 35, suc. 16, C.P. 5000; Córdoba, Argentina
D. H. Bronia
Affiliation:
Cátedra de Química Biológica, Facultad de Ciencias Médicos, Universidad Nacional de Córdoba; C.C. 35, suc. 16, C.P. 5000; Córdoba, Argentina
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Summary

The ability of Trypanosoma cruzi to induce erythrocyte membrane destabilization in vitro was studied. Epimastigote forms adhered to human erythrocytes and caused fusion or lysis of the red cells, depending on the conditions of the interaction. Red cells were fused in the presence of calcium, while haemolysis was induced in the absence of the cation. Dextran 60 C facilitated fusion but delayed lysis. Optimum pH and temperature for fusion were 7·4 and 37 °C, respectively. Lipid alterations were produced in the plasma membrane of the red cell during the interaction with the parasite. A Ca2+-independent increase of lysophospholipids and free fatty acids was common to both the lysis and fusion processes. A relative increase of 1, 2-diacylglycerides was unique to the fusion process and these changes were dependent on Ca2+. The transfer of free fatty acids and lysophospholipids from T. cruzi to erythrocyte membranes was demonstrated using parasites pre-labelled with radioactive phospholipids. Pre-treatment of parasites with exogenous phospholipase A2 abolished the fusogenicity, while lysis was increased. Neither fusion nor haemolysis occurred when the parasites were pre-treated with fatty acid free albumin, phospholipase A2 inhibitors or when these compounds were present in the medium during the parasite-erythrocyte interaction. Our results suggest that T. cruzi induces erythrocyte membrane destabilization in vitro by transfer of lipid material in a calcium independent manner and that this ion is necessary for other membrane alterations that lead to erythrocyte fusion.

Keywords

Trypanosoma cruzierythrocyte membranehaemolysiscell fusionLeishmania spp.calciummembrane lipidsphospholipase A2
Type
Research Article
Information
Parasitology , Volume 108 , Issue 3 , April 1994 , pp. 323 - 334
Copyright
Copyright © Cambridge University Press 1994

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References

Ahkong, Q. F., Fischer, D., Tampion, W. & Lucy, J. A. (1973). The fusion of erythrocytes by fatty acids, esters, retinol and α-tocopherol. The Biochemical Journal 136, 147–55.Google Scholar
Allan, D., Billah, M. M., Finean, J. B. & Michell, R. H. (1976). Release of diacylglycerol-enriched vesicles from erythrocytes with increased intracellular [Ca2+]. Nature, London 261, 58–60.CrossRefGoogle ScholarPubMed
Allan, D. & Michell, R. H. (1975). Accumulation of 1, 2-diacylglycerol in the plasma membrane may lead to echinocyte transformation of erythrocytes. Nature, London 258, 348–9.CrossRefGoogle ScholarPubMed
Allan, D. & Thomas, P. (1978). A calcium-activated polyphosphoinositide phosphodiesterase in the plasma membrane of human and rabbit erythrocytes. Biochimica et Biophysica Acta 508, 277–86.CrossRefGoogle ScholarPubMed
Allan, D. & Thomas, P. (1981). Ca2+-induced biochemical changes in human erythrocytes and their relation to microvesiculation. The Biochemical Journal 198, 433–40.CrossRefGoogle ScholarPubMed
Andrews, N. W. (1990). The acid-active hemolysin of Trypanosoma cruzi. Experimental Parasitology 71, 241–4.CrossRefGoogle ScholarPubMed
Andrews, N. W. & Whitlow, M. B. (1989). Secretion by Trypanosoma cruzi of a hemolysin active at low pH. Molecular and Biochemical Parasitology 33, 249–56.CrossRefGoogle ScholarPubMed
Andrews, N. W., Abrahams, C. K., Slatin, S. T. & Griffiths, G. (1990). A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 61, 1277–87.Google Scholar
Bartlett, G. R. (1959). Phosphorus assay in column chromatography. Journal of Biological Chemistry 234, 466–8.CrossRefGoogle ScholarPubMed
Bianco, I. D., Fidelio, G. D. & Maggio, B. (1989). Modulation of phospholipase A2 activity by neutral and anionic glycosphingilipids in monolayers. The Biochemical Journal 258, 95–9.CrossRefGoogle ScholarPubMed
Bianco, I. D., Fidelio, G. D. & Maggio, B. (1990). Effect of sulfatide and gangliosides on phospholipase C and phospholipase A2 A monolayer study. Biochimca et Biophysica Acta 1026, 179–85.CrossRefGoogle ScholarPubMed
Blow, A. M. J., Botham, G. M. & Lucy, J. A. (1979). Calcium ions and cell fusion. Effect of chemical fusogens on the permeability of erythrocytes to calcium and other ions. The Biochemical Journal 182, 555–63.Google Scholar
Boveris, A., Docampo, R., Turrens, J. F. & Stoppani, A. O. M. (1978). Effect of β-lapachone on superoxide anion and hydrogen peroxide production in Trypanosoma cruzi. The Biochemical Journal 175, 431–9.CrossRefGoogle ScholarPubMed
Budzko, D. B. & Kierszenbaum, F. (1974). Isolation of Trypanosoma cruzi from blood. Journal of Parasitology 60, 1037–8.CrossRefGoogle ScholarPubMed
Burger, K. N. & Verkleij, A. J. (1990). Membrane fusion. Experientia 15, 631–44.Google Scholar
Calderón, R. O., Aguerri, A. M. & Bronia, D. H. (1986). Trypanosoma cruzi: variable fusogenic ability by different growth phases of the epimastigote form. Experimental Parasitology 62, 45 3–5.Google Scholar
Calderón, R. O. & Fabro, S. P. (1983). Trypanosoma cruzi: fusogenic ability of membranes from cultured epimastigotes in interaction with human syncytiotrophoblast. Experimental Parasitology 56, 169–79.Google Scholar
Calderón, R. O., Luján, H. D., Aguerri, A. M. & Bronia, D. H. (1989). Trypanosoma cruzi: involvement of proteolytic activity during cell fusion induced by epimastigote form. Molecular and Cellular Biochemistry 86, 189–200.CrossRefGoogle ScholarPubMed
Castanys, S., Gammarro, F., Ruiz-Perez, L. M. & Osuna, A. (1990). Purification of a glycoprotein excreted by Trypanosoma cruzi to increase the permeability of the host-cell membrane. Biochemical and Biophysical Research Communications 166, 736–42.CrossRefGoogle ScholarPubMed
Connelly, M. C. & Kierszenbaum, F. (1984). Modulation of macrophage interaction with Trypanosoma cruzi by phospholipase A2-sensitive components of the parasite membrane. Biochemical and Biophysical Research Communications 121, 931–9.Google Scholar
Correa, S. G., Bianco, I. D., Riera, C. M. & Fidelio, G. D. (1991). Anti-inflammatory effect of gangliosides in the rat hindpaw edema test. European Journal of Pharmacology 199, 93–8.Google Scholar
Creutz, C. E. (1981). Cis-unsaturated fatty acids induce the fusion of chromaffin granules aggregated by synexin. Journal of Cell Biology 91, 247–56.CrossRefGoogle ScholarPubMed
Dimitrov, D. S. & Jain, R. K. (1984). Membrane stability. Biochimica et Biophysica Acta 779, 437–68.CrossRefGoogle ScholarPubMed
Folch, J., Lees, N. & Sloane-Stanley, F. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–509.CrossRefGoogle ScholarPubMed
Freeman, C. P. & West, D. (1966). Complete separation of lipid classes on a single thin-layer plate. Journal of Lipid Research 7, 324–7.Google Scholar
Golan, D. E., Brown, C. S., Cianci, C. M., Furlong, S. T. & Caulfield, J. P. (1986). Schistosomula of Schistosoma mansoni use lysophosphatidylcholine to lyse adherent human red blood cells and immobilize red cell membrane components. Journal of Cell Biology 103, 819–28.CrossRefGoogle ScholarPubMed
Haest, C. W. M., Plasa, G. & Deuticke, B. (1981). Selective removal of lipids from the outer membrane layer of human erythrocytes without hemolysis. Biochimica et Biophysica Acta 649, 701–8.Google Scholar
Hazlett, T. L., Deems, R. A. & Dennis, E. A. (1989). Activation, aggregation, inhibition and the mechanism of phospholipase A2. Advances in Experimental Medicine and Biology 279, 49–64.Google Scholar
Herrmann, A., Zachowsky, A., Devaux, P. F. & Blumenthal, R. (1991). Control of fusion of biological membranes by phospholipid asymmetry. In Cell and Model Membrane Interaction (ed. Ohki, S.), pp. 89–113. New York: Plenum Press.CrossRefGoogle Scholar
Kaneda, Y., Nagakura, K. & Goutsu, T. (1986). Lipid composition of three morphological stages of Trypanosoma cruzi. Comparative Biochemistry and Physiology 83B, 533–6.Google Scholar
Karnovski, M. J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. Journal of Cell Biology 27, 137A.Google Scholar
Kipnis, T. L., Calich, V. L. G. & Dias Da Silva, W. (1979). Active entry of bloodstream forms of Trypanosoma cruzi into macrophages. Parasitology 78, 89–98.CrossRefGoogle ScholarPubMed
Lang, R. D. A., Wickenden, C., Wynne, J. & Lucy, J. A. (1984). Proteolysis of ankyrin and of band 3 protein in chemically induced cell fusion. Ca2+ is not mandatory for fusion. The Biochemical Journal 218, 295–305.Google Scholar
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.Google Scholar
Lucy, J. A. (1984). Do hydrophobic sequences cleaved from cellular polypeptides induce membrane fusion reactions in vivo: FEBS Letters 166, 223–31.CrossRefGoogle ScholarPubMed
Lucy, J. A. & Ahkong, Q. F. (1986). An osmotic model for the fusion of biological membranes. FEBS Letters 199, 1–11.CrossRefGoogle ScholarPubMed
Macala, L. J., Yu, R. K. & Ando, S. (1983). Analysis of brain lipids by high performance thin-layer chromatography and densitometry. Journal of Lipid Research 24, 1243–50.Google Scholar
Maeda, T., Asano, A., Okada, Y. & Ohnishi, S. I. (1977). Transmembrane phospholipid motions induced by F glycoprotein in hemagglutinating virus Japens. Journal of Virology 21, 232–41.CrossRefGoogle Scholar
Morris, S. A., Hatcher, V., Tanowitz, H. B. & Wittner, M. (1988). Alterations in intracellular calcium following infection of endothelial cells with Trypanosoma cruzi. Molecular and Biochemical Parasitology 29, 213–21.Google Scholar
Osuna, A., Castanys, S., Rodriguez Cabezas, M. N. & Gamarro, F. (1990). Trypanosoma cruzi: calcium ion movement during internalization in host HeLa cells. International Journal for Parasitology 20, 673–6.CrossRefGoogle ScholarPubMed
Papahadjopoulos, D., Poste, G. & Vail, W. J. (1979). Studies on membrane fusion with natural and model membranes. In Methods in Membrane Biology, vol. 10. (ed. Korn, E. D.), pp. 1–121. New York: Plenum Press.Google Scholar
Ponder, E. (1971). Hemolysis and Related Phenomena. New York: Grune and Stratton, Inc.Google Scholar
Poste, G. & Pasternak, C. A. (1978). Virus induced cell fusion. In Membrane Fusion, Cell Surface Reviews 15, 306–67.Google Scholar
Rollofsen, B. & Zwahl, R. F. A. (1976). The use of phospholipases in the determination of asymmetric phospholipid distribution in membranes. In Methods in Membrane Biology, vol. 7 (ed. Korn, E. D.), pp. 147–77. New York: Plenum Press.Google Scholar
Schenkman, S. & Mortara, R. A. (1992). HeLa cells extend and internalize pseudopodia during active invasion by Trypanosoma cruzi. Journal of Cell Science 101, 895–905.Google Scholar
Schenkman, S., Robbins, E. S. & Nussenzweig, V. (1991). Attachment of Trypanosoma cruzi to mammalian cells requires parasite energy, and invasion can be independent of the target cell cytoskeleton. Infection and Immunity 59, 645–54.Google Scholar
Searsey, R. L., Bergquist, L. M. & Jung, R. C. (1960). Rapid ultramicroestimation of serum total cholesterol. Journal of Lipid Research 1, 349–51.CrossRefGoogle Scholar
Skipski, V. P. & Barclay, M. (1969). Thin layer Chromatography of lipids. In Methods in Enzymology (ed. Colowick, S. P. & Kaplan, N. O.), pp. 530–598. New York and London: Academic Press.Google Scholar
Spector, A. A. (1975). Fatty acid binding to plasma albumin. Journal of Lipid Research 16, 165–79.Google Scholar
Stoch, J. & Kleinfeld, A. M. (1985). The lipid structure of biological membranes. Trends in Biochemical Sciences 10, 418–21.CrossRefGoogle Scholar
Struck, D. K. & Pagano, R. E. (1980). Insertion of fluorescent phospholipids into the plasma membrane of a mammalian cell. Journal of Biological Chemistry 255, 5404–10.CrossRefGoogle ScholarPubMed
Stubbs, C. D. & Smith, A. D. (1984). The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochimica et Biophysica Acta 779, 89–137.Google Scholar
White, J. M. (1992). Membrane fusion. Science 258, 917–24.Google Scholar
Young, J. D. & Cohn, Z. A. (1987). Cellular and humoral mechanisms of cytotoxicity: structural and functional analogies. Advances in Immunology 41, 169–332.Google ScholarPubMed
Zimmermann, V. (1982). Electric field-mediated fusion and related electrical phenomena. Biochimica et Biophysica Acta 694, 227–77.CrossRefGoogle ScholarPubMed