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Subcellular localization of Trypanosoma cruzi arginine kinase

Published online by Cambridge University Press:  27 July 2009

MARIANA R. MIRANDA
Affiliation:
Laboratorio de Biología Molecular de Trypanosoma cruzi (LBMTC), Instituto de Investigaciones Médicas (IDIM), CONICET and Universidad de Buenos Aires, Combatientes de Malvinas 3150, Buenos Aires, Argentina
LEÓN A. BOUVIER
Affiliation:
Laboratorio de Biología Molecular de Trypanosoma cruzi (LBMTC), Instituto de Investigaciones Médicas (IDIM), CONICET and Universidad de Buenos Aires, Combatientes de Malvinas 3150, Buenos Aires, Argentina
GASPAR E. CANEPA
Affiliation:
Laboratorio de Biología Molecular de Trypanosoma cruzi (LBMTC), Instituto de Investigaciones Médicas (IDIM), CONICET and Universidad de Buenos Aires, Combatientes de Malvinas 3150, Buenos Aires, Argentina
CLAUDIO A. PEREIRA*
Affiliation:
Laboratorio de Biología Molecular de Trypanosoma cruzi (LBMTC), Instituto de Investigaciones Médicas (IDIM), CONICET and Universidad de Buenos Aires, Combatientes de Malvinas 3150, Buenos Aires, Argentina
*
*Corresponding author: IDIM, Combatientes de Malvinas 3150, (1427) Bs. As., Argentina. Tel: +5411 4514 8701. Fax: +5411 4523 8904. E-mail: cpereira@mail.retina.ar

Summary

Phosphoarginine is a cell energy buffer molecule synthesized by the enzyme arginine kinase. In Trypanosoma cruzi, the aetiological agent of Chagas' disease, 2 different isoforms were identified by data mining, but only 1 was expressed during the parasite life cycle. The digitonin extraction pattern of arginine kinase differed from those obtained for reservosomes, glycosomes and mitochondrial markers, and similar to the cytosolic marker. Immunofluorescence analysis revealed that although arginine kinase is localized mainly in unknown punctuated structures and also in the cytosol, it did not co-localize with any of the subcelular markers. This punctuated pattern has previously been observed in many cytosolic proteins of trypanosomatids. The knowledge of the subcellular localization of phosphagen kinases is a crucial issue to understand their physiological role in protozoan parasites.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Aranda, A., Maugeri, D., Uttaro, A. D., Opperdoes, F., Cazzulo, J. J. and Nowicki, C. (2006). The malate dehydrogenase isoforms from Trypanosoma brucei: subcellular localization and differential expression in bloodstream and procyclic forms. International Journal for Parasitology 36, 295307.CrossRefGoogle ScholarPubMed
Barderi, P., Campetella, O., Frasch, A. C., Santome, 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 ScholarPubMed
Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D. C., Lennard, N. J., Caler, E., Hamlin, N. E., Haas, B., Böhme, U., Hannick, L., Aslett, M. A., Shallom, J., Marcello, L., Hou, L., Wickstead, B., Alsmark, U. C., Arrowsmith, C., Atkin, R. J., Barron, A. J., Bringaud, F., Brooks, K., Carrington, M., Cherevach, I., Chillingworth, T. J., Churcher, C., Clark, L. N., Corton, C. H., Cronin, A., Davies, R. M., Doggett, J., Djikeng, A., Feldblyum, T., Field, M. C., Fraser, A., Goodhead, I., Hance, Z., Harper, D., Harris, B. R., Hauser, H., Hostetler, J., Ivens, A., Jagels, K., Johnson, D., Johnson, J., Jones, K., Kerhornou, A. X., Koo, H., Larke, N., Landfear, S., Larkin, C., Leech, V., Line, A., Lord, A., Macleod, A., Mooney, P. J., Moule, S., Martin, D. M., Morgan, G. W., Mungall, K., Norbertczak, H., Ormond, D., Pai, G., Peacock, C. S., Peterson, J., Quail, M. A., Rabbinowitsch, E., Rajandream, M. A., Reitter, C., Salzberg, S. L., Sanders, M., Schobel, S., Sharp, S., Simmonds, M., Simpson, A. J., Tallon, L., Turner, C. M., Tait, A., Tivey, A. R., Van Aken, S., Walker, D., Wanless, D., Wang, S., White, B., White, O., Whitehead, S., Woodward, J., Wortman, J., Adams, M. D., Embley, T. M., Gull, K., Ullu, E., Barry, J. D., Fairlamb, A. H., Opperdoes, F., Barrell, B. G., Donelson, J. E., Hall, N., Fraser, C. M., Melville, S. E. and El-Sayed, N. M. (2005). The genome of the African trypanosome Trypanosoma brucei. Science 309, 416422.CrossRefGoogle ScholarPubMed
Bouvier, L. A., Miranda, M. R., Canepa, G. E., Alves, M. J. and Pereira, C. A. (2006). An expanded adenylate kinase gene family in the protozoan parasite Trypanosoma cruzi. Biochimica et Biophysica Acta 1760, 913921.CrossRefGoogle ScholarPubMed
Caceres, A. J., Portillo, R., Acosta, H., Rosales, D., Quinones, W., Avilan, L., Salazar, L., Dubourdieu, M., Michels, P. A. and Concepcion, J. L. (2003). Molecular and biochemical characterization of hexokinase from Trypanosoma cruzi. Molecular and Biochemical Parasitology 126, 251262.CrossRefGoogle ScholarPubMed
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 São Paulo 12, 93100.Google Scholar
Canonaco, F., Schlattner, U., Pruett, P. S., Wallimann, T. and Sauer, U. (2002). Functional expression of phosphagen kinase systems confers resistance to transient stresses in Saccharomyces cerevisiae by buffering the ATP pool. The Journal of Biological Chemistry 277, 3130331309.CrossRefGoogle ScholarPubMed
Canonaco, F., Schlattner, U., Wallimann, T. and Sauer, U. (2003). Functional expression of arginine kinase improves recovery from pH stress of Escherichia coli. Biotechnology Letters 25, 10131017.CrossRefGoogle ScholarPubMed
Cazzulo, J. J. (1994). Intermediate metabolism in Trypanosoma cruzi. Journal of Bioenergetics and Biomembranes 26, 157165.CrossRefGoogle ScholarPubMed
Cazzulo, J. J., Cazzulo Franke, M. C. and Franke de Cazzulo, B. M. (1989). On the regulatory properties of the pyruvate kinase from Trypanosoma cruzi epimastigotes. FEMS Microbiology Letters 50, 259263.CrossRefGoogle ScholarPubMed
De Melo, L. D., Sant'Anna, C., Reis, S. A., Lourenço, D., De Souza, W., Lopes, U. G. and Cunha-e-Silva, N. L. (2008). Evolutionary conservation of actin-binding proteins in Trypanosoma cruzi and unusual subcellular localization of the actin homologue. Parasitology 135, 955965.CrossRefGoogle ScholarPubMed
de Souza, W., Carreiro, I. P., Miranda, K. and Silva, N. L. (2000). Two special organelles found in Trypanosoma cruzi. Anais da Academia Brasileira de Ciências 72, 421432.CrossRefGoogle ScholarPubMed
Denicola, A., Rubbo, H., Haden, L. and Turrens, J. F. (2002). Extramitochondrial localization of NADH-fumarate reductase in trypanosomatids. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 133, 2327.CrossRefGoogle Scholar
Dzeja, P. P., Bortolon, R., Perez-Terzic, C., Holmuhamedov, E. L. and Terzic, A. (2002). Energetic communication between mitochondria and nucleus directed by catalyzed phosphotransfer. Proceedings of the National Academy of Sciences, USA 99, 1015610161.CrossRefGoogle ScholarPubMed
Dzeja, P. P. and Terzic, A. (2003). Phosphotransfer networks and cellular energetics. The Journal of Experimental Biology 206, 20392047.CrossRefGoogle ScholarPubMed
Ellington, W. R. (2001). Evolution and physiological roles of phosphagen systems. Annual Review of Physiology 63, 289325.CrossRefGoogle ScholarPubMed
Ferella, M., Li, Z. H., Andersson, B. and Docampo, R. (2008). Farnesyl diphosphate synthase localizes to the cytoplasm of Trypanosoma cruzi and T. brucei. Experimental Parasitology 119, 308312.CrossRefGoogle Scholar
Leroux, A., Fleming-Canepa, X., Aranda, A., Maugeri, D., Cazzulo, J. J., Sánchez, M. A. and Nowicki, C. (2006). Functional characterization and subcellular localization of the three malate dehydrogenase isozymes in Leishmania spp. Molecular and Biochemical Parasitology 149, 7485.CrossRefGoogle ScholarPubMed
Marciano, D., Llorentea, C., Maugeri, D., Fuentea, C., Opperdoes, F., Cazzulo, J. J. and Nowicki, C. (2008). Biochemical characterization of stage-specific isoforms of aspartate aminotransferases from Trypanosoma cruzi and Trypanosoma brucei. Molecular and Biochemical Parasitology 161, 1220.CrossRefGoogle ScholarPubMed
Miranda, M. R., Canepa, G. E., Bouvier, L. A. and Pereira, C. A. (2006). Trypanosoma cruzi: Oxidative stress induces arginine kinase expression. Experimental Parasitology 114, 341344.CrossRefGoogle ScholarPubMed
Miranda, M. R., Canepa, G. E., Bouvier, L. A. and Pereira, C. A. (2008). Trypanosoma cruzi: multiple nucleoside diphosphate kinase isoforms in a single cell. Experimental Parasitology 120, 103107.CrossRefGoogle Scholar
Pereira, C. A., Alonso, G., Ivaldi, S., Bouvier, L., Torres, H. and Flawiá, M. (2003 a). Screening of substrate analogs as potential enzyme Inhibitors for the arginine kinase of Trypanosoma cruzi. The Journal of Eukaryotic Microbiology 50, 132134.CrossRefGoogle ScholarPubMed
Pereira, C. A., Alonso, G. D., Ivaldi, S., Silber, A. M., Alves, M. J., Torres, H. N. and Flawia, M. M. (2003 b). Arginine kinase overexpression improves Trypanosoma cruzi survival capability. FEBS Letters 554, 201205.CrossRefGoogle ScholarPubMed
Pereira, C. A., Alonso, G. D., Paveto, M. C., Flawia, M. M. and Torres, H. N. (1999). L-arginine uptake and L-phosphoarginine synthesis in Trypanosoma cruzi. The Journal of Eukaryotic Microbiology 46, 566570.CrossRefGoogle ScholarPubMed
Pereira, C. A., Alonso, G. D., Paveto, M. C., Iribarren, A., Cabanas, M. L., Torres, H. N. and Flawia, M. M. (2000). Trypanosoma cruzi arginine kinase characterization and cloning. A novel energetic pathway in protozoan parasites. The Journal of Biological Chemistry 275, 14951501.CrossRefGoogle ScholarPubMed
Pereira, C. A., Alonso, G. D., Torres, H. N. and Flawia, M. M. (2002). Arginine kinase: a common feature for management of energy reserves in African and American flagellated trypanosomatids. The Journal of Eukaryotic Microbiology 49, 8285.CrossRefGoogle ScholarPubMed