Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-26T05:35:34.658Z Has data issue: false hasContentIssue false

Phospholipase A1 from Trypanosoma cruzi infective stages generates lipid messengers that activate host cell protein kinase c

Published online by Cambridge University Press:  23 November 2006

M. L. BELAUNZARÁN
Affiliation:
Department of Microbiology, School of Medicine, University of Buenos Aires, Paraguay 2155, C1121ABG, Buenos Aires, Argentina
M. J. WAINSZELBAUM
Affiliation:
Department of Cell Biology and Physiology, Washington University, School of Medicine, 660 S. Euclid Avenue, Box 8228, St Louis, MO 63110 USA
E. M. LAMMEL
Affiliation:
Department of Cell Biology and Physiology, Washington University, School of Medicine, 660 S. Euclid Avenue, Box 8228, St Louis, MO 63110 USA
G. GIMENEZ
Affiliation:
Department of Microbiology, School of Medicine, University of Buenos Aires, Paraguay 2155, C1121ABG, Buenos Aires, Argentina
M. M. ALOISE
Affiliation:
Department of Microbiology, School of Medicine, University of Buenos Aires, Paraguay 2155, C1121ABG, Buenos Aires, Argentina
J. FLORIN-CHRISTENSEN
Affiliation:
Department of Microbiology, School of Medicine, University of Buenos Aires, Paraguay 2155, C1121ABG, Buenos Aires, Argentina
E. L. D. ISOLA
Affiliation:
Department of Microbiology, School of Medicine, University of Buenos Aires, Paraguay 2155, C1121ABG, Buenos Aires, Argentina

Abstract

Here we have studied phospholipase A1 (Plase A1) from Trypanosoma cruzi infective stages and it's possible role regarding the interaction with mammalian host cells. Plase A1 was mainly detected as a membrane-bound activity in the infective amastigote and trypomastigote stages, being remarkably higher with respect to the non-infective epimastigotes. It is noteworthy that only the infective stages secreted Plase A1. Moreover, along the differentiation process from epimastigotes into metacyclic trypomastigotes, the secreted enzyme activity increased simultaneously with the appearance of metacyclic forms, as expected. Since this enzyme is predominantly membrane-associated and secreted by the infective stages, Vero cell lipid profile modifications were analysed after interaction with either intact infective parasites or purified T. cruzi Plase A1. Significant changes in Vero cell lipid composition were observed, with the appearance of free fatty acids, diacylglycerol and lysophosphatidylcholine. Concomitantly with the generation of second lipid messengers, host cell protein kinase C activation was demonstrated. These results indicate that T. cruzi Plase A1 could play a critical role in the early events of parasite-host cell interaction that precede invasion.

Type
Research Article
Copyright
© 2006 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

Altin, J. G. and Pagler, E. B. ( 1995). A one-step procedure for biotinylation and chemical cross-linking of lymphocyte surface and intracellular membrane-associated molecules. Analytical Biochemistry 224, 382389.CrossRefGoogle Scholar
Aparicio, I. M., Scharfstein, J. and Lima, A. P. ( 2004). A new cruzipain-mediated pathway of human cell invasion by Trypanosoma cruzi requires trypomastigote membranes. Infection and Immunity 72, 58925902.CrossRefGoogle Scholar
Asahi, H., Kawabata, M., Moribayashi, A. and Okumura, H. ( 1986). Cytotoxic factors toward neuroblastoma cells in trypomastigotes of Trypanosoma cruzi. Canadian Journal of Microbiology 32, 711718.CrossRefGoogle Scholar
Barderi, P., Campetella, O., Frasch, A. C., Santomé, J. A., Hellman, U., Pettersson, U. and Cazzulo, J. J. ( 1998). The NADP+-linked glutamate dehydrogenase from Trypanosoma cruzi: sequence, genomic organization and expression. The Biochemical Journal 330, 951958.CrossRefGoogle Scholar
Baron, C. B., Cunningham, M., Strauss, J. F. and Coburn, R. F. ( 1984). Pharmacomechanical coupling in smooth muscle may involve phosphatidylinositol metabolism. Proceedings of the National Academy of Sciences, USA 81, 68996903.CrossRefGoogle Scholar
Bertello, L. E., Alves, M. J., Colli, W. and Lederkremer, R. M. ( 2000). Evidence for phospholipases from Trypanosoma cruzi active on phosphatidylinositol and inositolphosphoceramide. The Biochemical Journal 345, 7784.CrossRefGoogle Scholar
Bligh, E. G. and Dyer, W. J. ( 1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemical Physiology 37, 911917.CrossRefGoogle Scholar
Brattsand, G., Friedrich, B. and Gullberg, M. ( 1989). A rapid separation procedure to analyze phosphorylation of two putative protein kinase C substrates in intact lymphocytes. Scandinavian Journal of Immunology 30, 233240.CrossRefGoogle Scholar
Burleigh, B. A. and Woolsey, A. M. ( 2002). Cell signalling and Trypanosoma cruzi invasion. Cell Microbiology 4, 701711.CrossRefGoogle Scholar
De Souza, W. ( 2000). O parasito e sua interaçao com os hospedeiros in Guanabara Koogan S. A. (Eds.), Trypanosoma cruzi e Doença de Chagas 2a ediço, Brener, Z., Andrade, Z. A. and Barral-Netto, M., Brazil, pp. 88126.
Florin-Christensen, M., Florin-Christensen, J., Isola, E. L. D., Lammel, E., Meinardi, E., Brenner, R. R. and Rasmussen, L. ( 1997). Temperature acclimation of Trypanosoma cruzi epimastigote and metacyclic trypomastigote lipids. Molecular and Biochemical Parasitology 88, 2533.CrossRefGoogle Scholar
Gonçalves, M. F., Umezawa, E. S., Katzin, A. M., de Souza, W., Alves, M. J. M., Zingales, B. and Colli, W. ( 1991). Trypanosoma cruzi: Shedding of surface antigens as membrane vesicles. Experimental Parasitology 72, 4353.CrossRefGoogle Scholar
González Cappa, S. M., Bijovsky, A. T., Freilij, H., Muller, L. A. and Katzin, M. A. ( 1981). Aislamiento de una cepa de Trypanosoma cruzi a predominio de formas delgadas en la Argentina. Medicina Buenos Aires 41, 119120.Google Scholar
Goodall, H. and Johnson, M. H. ( 1982). Use of carboxyfluorescein diacetate to study formation of permeable channels between mouse blastomeres. Nature, London 295, 524526.CrossRefGoogle Scholar
Gruppi, A., Cerban, F. M. and Vottero-Cima, E. ( 1997). Exoantigens from Trypanosoma cruzi contain cruzipain. Acta Tropica 63, 141149.CrossRefGoogle Scholar
Hambrey, P. N., Mellors, A. and Tizard, I. R. ( 1981). The phospholipases of pathogenic and non-pathogenic Trypanosoma species. Molecular and Biochemical Parasitology 2, 177186.CrossRefGoogle Scholar
Hansra, G., Garcia-Paramio, P., Prevostel, C., Whelan, R. D., Bornancin, F. and Parker, P. J. ( 1999). Multisite dephosphorylation and desensitization of conventional protein kinase C isotypes. The Biochemical Journal 342, 337344.CrossRefGoogle Scholar
Hostetler, K. Y., Yazaki, P. J. and van den Bosch, H. ( 1982). Purification of lysosomal phospholipase A. Evidence for multiple isoenzymes in rat liver. Journal of Biological Chemistry 257, 1336713373.Google Scholar
Isola, E. L. D., Lammel, E. M. and González Cappa, S. M. ( 1986). Trypanosoma cruzi: Differentiation after interaction of epimastigotes and Triatoma infestans intestinal homogenate. Experimental Parasitology 62, 329335.CrossRefGoogle Scholar
Junker, C. E., Vaughn, J. and Cory, J. ( 1967). Adaptation of an insect cell line (Grace's Antheraea cells) to medium free of insect hemolymph. Science 155, 15651566.Google Scholar
Laemmli, U. K. ( 1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T. Nature, London 227, 680684.CrossRefGoogle Scholar
Lira, R., Contreras, L. M., Rita, R. M. and Urbina, J. A. ( 2001). Mechanism of action of anti-proliferative lysophospholipid analogues against the protozoan parasite Trypanosoma cruzi: potentiation of in vitro activity by the sterol biosynthesis inhibitor ketoconazole. Journal of Antimicrobial Chemotherapy 47, 537546.CrossRefGoogle Scholar
Liu, W. S. and Heckman, C. A. ( 1998). The sevenfold way of PKC regulation. Cell Signal 10, 529542.CrossRefGoogle Scholar
Lowry, O. H., Roseborough, N. J., Farr, A. L. and Randall, R. J. ( 1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265275.Google Scholar
Moreno, S. N., Silva, J., Vercesi, A. E. and Docampo, R. ( 1994). Cytisolic-free calcium elevation in Trypanosoma cruzi is required for cell invasion. Journal of Experimental Medicine 180, 15351540.CrossRefGoogle Scholar
Nishizuka, Y. ( 1995). Protein kinase C and lipid signaling for sustained cellular responses. FASEB Journal 9, 484496.CrossRefGoogle Scholar
Opperdoes, F. R. and van Roy, J. ( 1982). The phospholipases of Trypanosoma brucei bloodstream forms and cultured procyclics, Molecular and Biochemical Parasitology 5, 309319.Google Scholar
Parussini, F., Duschak, V. G. and Cazzulo, J. J. ( 1998). Membrane-bound cysteine proteinase isoforms in different developmental stages of Trypanosoma cruzi. Cellular and Molecular Biology 44, 513519.Google Scholar
Pete, M. J., Ross, A. H. and Exton, J. H. ( 1994). Purification and properties of phospholipase A1 from bovine brain. Journal of Biological Chemistry 269, 1949419500.Google Scholar
Prokazova, N. V., Zvezdina, N. D. and Korotaeva, A. A. ( 1998). Effect of lysophosphatidylcholine on transmembrane signal transduction. Cellular and Molecular Biology 63, 3137.Google Scholar
Salto, M. L., Bertello, L. E., Vieira, M., Docampo, R., Moreno, S. N. J. and de Lederkremer, R. M. ( 2003). Formation and remodelling of Inositolphosphoceramide during differentiation of Trypanosoma cruzi from trypomastigote to amastigote. Eukaryotic Cell 2, 756768.CrossRefGoogle Scholar
Souto-Padron, T., Campetella, O. E., Cazullo, J. J. and de Souza, W. ( 1990). Cysteine proteinase in Trypanosoma cruzi: immunocytochemical localization and involvement in parasite-host cell interaction. Journal of Cell Science 96 485490.Google Scholar
Suzuki, Y. and Matsumoto, M. ( 1978). Acid phospholipase A1 requiring phospholipids or Triton X-100 in the cytosil of cultured cells. Journal of Biochemistry (Tokio) 84, 14111422.CrossRefGoogle Scholar
Tardieux, I., Nathanson, M. H. and Andrews, N. W. ( 1994). Role in host cell invasion of Trypanosoma cruzi-induced cytosolic-free Ca2+ transients. The Journal of Experimental Medicine 179, 10171022.CrossRefGoogle Scholar
Tizard, I. R., Mellors, A., Holmes, W. L. and Nielsen, K. ( 1978). The generation of phospholipase A and hemolytic fatty acids by autolysing suspensions of Trypanosoma congolense. Tropenmedizin und Parasitologie 29, 127133.Google Scholar
Tsao, S. C., Iga, T., Sugiyama, Y. and Hanano, M. ( 1982). Effect of chlorpromazine on isolated rat hepatocytes, Biochemical Pharmacology 31, 491497.Google Scholar
Van den Bosch, H. ( 1974). Phosphoglyceride metabolism, Annual Review of Biochemistry 43, 243277.Google Scholar
Villalta, F., Zhang, Y., Bibb, K. E., Pratap, S., Burns, J. M. Jr. and Lima, M. F. ( 1999). Signal transduction in human macrophages by gp83 ligand of Trypanosoma cruzi: trypomastigote gp83 ligand up-regulates trypanosome entry through protein kinase C activation. Molecular and Cellular Biological Research Communication 2, 6470.CrossRefGoogle Scholar
Wainszelbaum, M., Isola, E., Wilkowsky, S., Cannata, J. J., Florin-Christensen, J. and Florin-Christensen, M. ( 2001). Lysosomal phospholipase A1 in Trypanosoma cruzi: an enzyme with a possible role in the pathogenesis of Chagas' disease. The Biochemical Journal 355, 765770.CrossRefGoogle Scholar
Wilkowsky, S. E., Wainszelbaum, M. J. and Isola, E. L. D. ( 1996). Trypanosoma cruzi: Participation of intracellular Ca2+ during metacyclic trypomastigote-macrophage interaction. Biochemical and Biophysical Research Communications 222, 386389.CrossRefGoogle Scholar
Wilkowsky, S. E., Barbieri, M. A., Stahl, P. and Isola, E. L. D. ( 2001). Trypanosoma cruzi: Phosphatidylinositol 3-Kinase and Protein Kinase B activation is associated with parasite invasion. Experimental Cell Research 264, 211218.CrossRefGoogle Scholar
Yu, H. Y., Inoguchi, T., Kakimoto, M., Nakashima, N., Imamura, N., Hashimoto, T., Umeda, F. and Nawata, H. ( 2001). Saturated non-esterified fatty acids stimulate de novo diacylcglycerol síntesis and protein kinase C activity in cultured aortic smooth muscle cells. Diabetología 44, 614620.CrossRefGoogle Scholar