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Heterogeneity in extracellular nucleotide hydrolysis among clinical isolates of Trichomonas vaginalis

Published online by Cambridge University Press:  07 March 2005

T. TASCA ,
C. D. BONAN ,
G. A. DE CARLI ,
J. J. F. SARKIS  and
J. F. ALDERETE
T. TASCA
Affiliation:
Department of Microbiology, MC7758, University of Texas Health Science Center, 7703 Floyd Curl Drive, San Antonio, TX 78229-3900, USA Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos 2600 – Anexo, 90035-003 Porto Alegre, RS, Brazil Laboratório de Parasitologia Clínica, Departamento de Análises Clinicas, Faculdade de Farmácia, Pontificia Universidade Católica do Rio Grande do Sul, Avenida Ipiranga, 6681, Caixa Postal 1429, 90619-900, Porto Alegre, RS, Brazil
C. D. BONAN
Affiliation:
Laboratório de Pesquisa Bioquímica, Departamento de Ciências Fisiológicas, Faculdade de Biociências, Pontificia Universidade Católica do Rio Grande do Sul, Avenida Ipiranga, 6681, Caixa Postal 1429, 90619-900, Porto Alegre, RS, Brazil
G. A. DE CARLI
Affiliation:
Laboratório de Parasitologia Clínica, Departamento de Análises Clinicas, Faculdade de Farmácia, Pontificia Universidade Católica do Rio Grande do Sul, Avenida Ipiranga, 6681, Caixa Postal 1429, 90619-900, Porto Alegre, RS, Brazil
J. J. F. SARKIS
Affiliation:
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos 2600 – Anexo, 90035-003 Porto Alegre, RS, Brazil
J. F. ALDERETE
Affiliation:
Department of Microbiology, MC7758, University of Texas Health Science Center, 7703 Floyd Curl Drive, San Antonio, TX 78229-3900, USA
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Abstract

Trichomonas vaginalis is a parasitic protozoan that causes trichomonosis, a sexually-transmitted disease, with serious sequelae to women and men. As the host–parasite relationship is complex, it is important to investigate biochemical aspects of the parasite that contribute to our understanding of trichomonal biology and pathogenesis. Nucleoside triphosphate diphosphohydrolase 1 (NTPDase 1), which hydrolyses extracellular ATP and ADP, and ecto-5′-nucleotidase, which hyrolyses AMP, have been characterized in laboratory isolates of T. vaginalis. Here we show that the extracellular ATP[ratio ]ADP hydrolysis ratio varies among fresh clinical isolates, which presented higher ATPase and ADPase activities than long-term-grown isolates. Growth of parasites in iron-replete and iron-depleted medium resulted in different, albeit minor, patterns in extracellular ATP and ADP hydrolysis among isolates. Importantly, some isolates had low or absent ecto-5′-nucleotidase activity, regardless of environmental conditions tested. For isolates with ecto-5′-nucleotidase activity, high- and low-iron trichomonads had increased and decreased levels of activity, respectively, compared to organisms grown in normal TYM-serum medium. This suggests a regulation in expression of either the enzyme amounts and/or activity under the control of iron. Finally, we found no correlation between the presence or absence of dsRNA virus infection among trichomonad isolates and NTPDase and ecto-5′-nucleotidase activities.

Keywords

Trichomonas vaginalisnucleoside triphosphate diphosphohydrolaseecto-5′-nucleotidasefresh isolatesheterogeneity
Type
Research Article
Information
Parasitology , Volume 131 , Issue 1 , July 2005 , pp. 71 - 78
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

AIRAS, L., HELLMAN, J., SALMI, M., BONO, P., PUURUNEN, T., SMITH, D. J. & JALKANEN, S. ( 1995). CD73 is involved in lymphocyte binding to the endothelium: characterization of lymphocyte-vascular adhesion protein 2 identifies it as CD73. Journal of Experimental Medicine 182, 1603–1608.CrossRefGoogle Scholar
ALDERETE, J. F. ( 1999). Trichomonas vaginalis, a model mucosal parasite. Reviews in Medical Microbiology 10, 165–173.Google Scholar
ALDERETE, J. F., NGUYEN, J., MUNDODI, V. & LEHKER, M. W. ( 2004). Heme-iron increases levels of AP65-mediated adherence by Trichomonas vaginalis. Microbial Pathogenesis 36, 263–271.CrossRefGoogle Scholar
ALDERETE, J. F., PROVENZANO, D. & LEHKER, M. W. ( 1995). Iron mediates Trichomonas vaginalis resistance to complement lysis. Microbial Pathogenesis 19, 93–103.CrossRefGoogle Scholar
ASAI, T., MIURA, S., SIBLEY, L. D., OKABAYASHI, H. & TAKEUCHI, T. ( 1995). Biochemical and molecular characterization of nucleoside triphosphate hydrolase isozymes from the parasitic protozoan Toxoplasma gondii. The Journal of Biological Chemistry 270, 11391–11397.CrossRefGoogle Scholar
BARROS, F. S., DE MENEZES, L. F., PINHEIRO, A. A. S., SILVA, E. F., LOPES, A. H. C. S., DE SOUZA, W. & MEYER-FERNANDES, J. R. ( 2000). Ectonucleotide diphosphohydrolase activities in Entamoeba histolytica. Archives of Biochemistry and Biophysics 375, 304–314.CrossRefGoogle Scholar
BATTASTINI, A. M., DA ROCHA, J. B., BARCELLOS, C. K., DIAS, R. D. & SARKIS, J. J. ( 1991). Characterization of an ATP diphosphohydrolase (EC 3.6.1.5) in synaptosomes from cerebral cortex of adult rats. Neurochemistry Research 16, 1303–1310.Google Scholar
BIGONNESSE, F., LEVESQUE, S. A., KUKULSKI, F., LECKA, J., ROBSON, S. C., FERNANDES, M. J. & SÉVIGNY, J. ( 2004). Cloning and characterization of mouse nucleoside triphosphate diphosphohydrolase-8. Biochemistry 43, 5511–5519.CrossRefGoogle Scholar
BOUMA, M. G., JEUNHOMME, T. M. M. A., BOYLE, D. L., DENTENER, M. A., VOITENOK, N. N., VAN DEN WILDENBERG, F. A. J. M. & BUURMAN, W. A. ( 1997). Adenosine inhibits neutrophil degranulation in activated human whole blood: involvement of adenosine A2 and A3 receptors. Journal of Immunology 158, 5400–5408.Google Scholar
BRADFORD, M. M. ( 1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 218–254.CrossRefGoogle Scholar
CHAN, K., DELFERT, D. & JUNGER, K. D. ( 1986). A direct colorimetric assay for Ca2+-ATPase activity. Analytical Biochemistry 157, 375–380.CrossRefGoogle Scholar
COIMBRA, E. S., GONÇALVES-DA-COSTA, S. C., CORTE-REAL, S., DE FREITAS, F. G. R., DURÃO, A. C., SOUZA, C. S. F., SILVA-SANTOS, M. I. & VASCONCELOS, E. G. ( 2002). Characterization and cytochemical localization of an ATP diphosphohydrolase from Leishmania amazonensis promastigotes. Parasitology 124, 137–143.CrossRefGoogle Scholar
COSTA E SILVA FILHO, F., DE SOUZA, W. & LOPES, J. D. ( 1988). Presence of laminin-binding proteins in trichomonads and their role in adhesion. Proceedings of the National Academy of Sciences, USA 85, 8042–8046.CrossRefGoogle Scholar
COTCH, M. F., PASTOREK II, J. G., NUGENT, R. P., HILLIER, S. L., GIBBS, R. S., MARTIN, D. H., ESCHENBACH, D. A., EDELMAN, R., CAREY, J. C., REGAN, J. A., KROHN, M. A., KLEBANOFF, M. A., RAO, A. V. & RHOADS, G. G. ( 1997). Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sexually Transmitted Diseases 24, 353–360.CrossRefGoogle Scholar
CRONSTEIN, B. N., LEVIN, R. I., PHILIPS, M., HIRSCHHORN, R., ABRAMSON, S. B. & WEISSMAN, G. ( 1992). Neutrophil adherence to endothelium is enhanced via adenosine A1 receptors and inhibited via adenosine A2 receptors. Journal of Immunology 148, 2201–2206.Google Scholar
CROUCH, M.-L. V. & ALDERETE, J. F. ( 1999). Trichomonas vaginalis interactions with fibronectin and laminin. Microbiology 145, 2835–2843.CrossRefGoogle Scholar
CROUCH, M.-L. V., BENCHIMOL, M. & ALDERETE, J. F. ( 2001). Binding of fibronectin by Trichomonas vaginalis is influenced by iron and calcium. Microbial Pathogenesis 31, 131–144.CrossRefGoogle Scholar
DIAMOND, L. S. ( 1957). The establishment of various trichomonads of animals and man in axenic cultures. Journal of Parasitology 43, 488–490.CrossRefGoogle Scholar
FIETTO, J. L., DE MARCO, R., NASCIMENTO, I. P., CASTRO, I. M., CARVALHO, T. M., DE SOUZA, W., BAHIA, M. T., ALVES, M. J. & VERJOVSKI-ALMEIDA, S. ( 2004). Characterization and immunolocalization of an NTP diphosphohydrolase of Trypanosoma cruzi. Biochemical and Biophysical Research Communication 316, 454–460.CrossRefGoogle Scholar
HEYWORTH, P. G., GUTTERIDGE, W. E. & GINGER, C. D. ( 1982). Purine metabolism in Trichomonas vaginalis. FEBS Letters 141, 106–110.CrossRefGoogle Scholar
HEYWORTH, P. G., GUTTERIDGE, W. E. & GINGER, C. D. ( 1984). Pyrimidine metabolism in Trichomonas vaginalis. FEBS Letters 176, 55–60.CrossRefGoogle Scholar
HOBBS, M. M., KZEMBE, P., REED, A. W., MILLER, W. C., NKATA, E., ZIMBA, D., DALY, C. C., CHAKRABORTY, H., COHEN, M. S. & HOFFMAN, I. ( 1999). Trichomonas vaginalis as a cause of urethritis in Malawian men. Sexually Transmitted Diseases 26, 381–387.CrossRefGoogle Scholar
KANSAS, G. S., WOOD, G. S. & TEDDER, T. F. ( 1991). Expression, distribution, and biochemistry of human CD39. Role in activation-associated homotypic adhesion of lymphocytes. Journal of Immunology 146, 2235–2244.Google Scholar
KASSAI, T., CORDERO DEL CAMPILLO, M., EUZEBY, J., GAAFAR, S., HIEPE, T. & HIMONAS, C. A. ( 1988). Standardized nomenclature of animal parasitic diseases (SNOAPAD). Veterinary Parasitology 29, 299–326.CrossRefGoogle Scholar
KHOSHNAN, A. & ALDERETE, J. F. ( 1994). Trichomonas vaginalis with a double-stranded RNA virus has upregulated levels of phenotypically variable immunogen mRNA. Journal of Virology 68, 4035–4038.Google Scholar
LEHKER, M. W., ARROYO, R. & ALDERETE, J. F. ( 1991). The regulation by iron of the synthesis of adhesins and cytoadherence levels in the protozoan Trichomonas vaginalis. Journal of Experimental Medicine 174, 311–318.CrossRefGoogle Scholar
MALISZEWSKI, C. R., DELESPESSE, G. J., SCHOENBORN, M. A., ARMITAGE, R. J., FANSLOW, W. C., NAKAJIMA, T., BAKER, E., SUTHERLAND, G. R., POINDEXTER, K., BIRKS, C., ALPERT, A., FRIEND, D., GIMPEL, S. D. & GAYLE III, R. B. ( 1994). The CD39 lymphoid cell activation antigen. Molecular cloning and structural characterization. Journal of Immunology 153, 3574–3583.Google Scholar
MATOS, J. A. A., BORGES, F. P., TASCA, T., BOGO, M. R., DE CARLI, G. A., FAUTH, M. G., DIAS, R. D. & BONAN, C. D. ( 2001). Characterisation of an ATP diphosphohydrolase (Apyrase, EC 3.6.1.5) activity in Trichomonas vaginalis. International Journal for Parasitology 31, 770–775.Google Scholar
MÉHUL, B., AUBERY, M., MANHERZ, H.-G. & CODOGNO, P. ( 1993). Dual mechanism of laminin modulation of ecto-5′-nucleotidase activity. Journal of Cellular Biochemistry 52, 266–274.CrossRefGoogle Scholar
MEYER-FERNANDES, J. R., DUTRA, P. M. L., RODRIGUES, C. O., SAADNEHME, J. & LOPES, A. H. C. S. ( 1997). Mg-dependent ecto-ATPase activity in Leishmania tropica. Archives of Biochemistry and Biophysics 341, 40–46.CrossRefGoogle Scholar
MUNAGALA, N. R. & WANG, C. C. ( 2003). Adenosine is the primary precursor of all purine nucleotides in Trichomonas vaginalis. Molecular and Biochemical Parasitology 127, 143–149.CrossRefGoogle Scholar
RESTA, R., HOOKER, S. W., HANSEN, K. R., LAURENT, A. B., PARK, J. L., BLACKBURN, M. R., KNUDSEN, T. B. & THOMPSON, L. F. ( 1993). Murine ecto-5′-nucleotidase (CD73): cDNA cloning and tissue distribution. Gene 133, 171–177.CrossRefGoogle Scholar
SARKIS, J. J. F., BATTASTINI, A. M. O., OLIVEIRA, E. M., FRASSETTO, S. S. & DIAS, R. D. ( 1995). ATP diphosphohydrolases: an overview. Journal of Brazilian Association for the Advancement of Science 47, 131–136.Google Scholar
SORVILLO, F. & KERNDT, P. ( 1998). Trichomonas vaginalis and amplification of HIV-1 transmission. Lancet 351, 213–214.CrossRefGoogle Scholar
STOCHAJ, U., DIECKHOFF, J. M., CRAMER, M. & MANNHERZ, H. G. ( 1989). Evidence for the direct interaction of chicken gizzard 5′-nucleotidase with laminin and fibronectin. Biochimica et Biophysica Acta 992, 385–392.CrossRefGoogle Scholar
TASCA, T., BONAN, C. D., DE CARLI, G. A., BATTASTINI, A. M. & SARKIS, J. J. ( 2003 a). Characterization of an ecto-5′-nucleotidase (EC 3.1.3.5) activity from intact cells of Trichomonas vaginalis. Experimental Parasitology 105, 167–173.Google Scholar
TASCA, T., BORGES, F. P., BONAN, C. D., DE CARLI, G. A., BATTASTINI, A. M. & SARKIS, J. J. ( 2003 b). Effects of metronidazole and tinidazole on NTPDase1 and ecto-5′-nucleotidase from intact cells of Trichomonas vaginalis. FEMS Microbiology Letters 226, 379–384.Google Scholar
VASCONCELOS, E. G., NASCIMENTO, P. S., MEIRELLES, M. N. L., VERJOVSKI-ALEMIDA, S. & FERREIRA, S. T. ( 1993). Characterization and localization of an ATP diphosphohydrolase on the external surface of tegument of Schistosoma mansoni. Molecular and Biochemical Parasitology 58, 205–214.CrossRefGoogle Scholar
VASCONCELOS, E. G., FERREIRA, S. T., CARVALHO, T. M. U., DE SOUZA, W., KETTLUN, A. M., MANCILLA, M., VALENZUELA, M. A. & VERJOVSKI-ALMEDA, S. ( 1996). Partial purification and immunohistochemical localization of ATP diphosphohydrolase from Schistosoma mansoni. The Journal of Biological Chemistry 36, 22139–22145.CrossRefGoogle Scholar
VIIKKI, M., PUKKALA, E., NIEMINEN, P. & HAKAMA, M. ( 2000). Gynaecological infections as risk determinants of subsequent cervical neoplasia. Acta Oncologica 39, 71–75.CrossRefGoogle Scholar
WANG, A. L., WANG, C. C. & ALDERETE, J. F. ( 1987). Trichomonas vaginalis phenotypic variation occurs only among trichomonads with double-stranded RNA virus. Journal of Experimental Medicine 166, 142–150.CrossRefGoogle Scholar
WANG, T. F. & GUIDOTTI, G. ( 1996). CD39 is an ecto-(Ca2+, Mg2+)-apyrase. The Journal of Biological Chemistry 271, 9898–9901.CrossRefGoogle Scholar
WEINSTOCK, H., BERMAN, S. & CATES, W. Jr. ( 2004). Sexually transmitted diseases among American youth: incidence and prevalence estimates, 2000. Perspectives on Sexual and Reproductive Health 36, 6–10.CrossRefGoogle Scholar
WENDEL, K. A., ROMPALO, A. M., ERBELDING, E. J., CHANG, T.-H. & ALDERETE, J. F. ( 2002). Double-stranded RNA viral infection of Trichomonas vaginalis infecting patients attending a sexually transmitted diseases clinic. Journal of Infectious Diseases 186, 558–561.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION ( 2001). Global Prevalence and Incidence of Selected Curable Sexually Transmitted Infections. Overview and Estimates. WHO, Geneva.
ZIMMERMANN, H. ( 1999). Two novel families of ecto-nucleotidases: molecular structures, catalytic properties, and a search for function. Trends in Pharmacological Sciences 20, 231–236.CrossRefGoogle Scholar
ZIMMERMANN, H. ( 2001). Ectonucleotidases: some recent developments and a note on nomenclature. Drug Development Research 52, 44–56.CrossRefGoogle Scholar