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The role of the NTPDase enzyme family in parasites: what do we know, and where to from here?

Published online by Cambridge University Press:  12 March 2012

FIONA M. SANSOM
FIONA M. SANSOM*
Affiliation:
Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Parkville, VIC 3010, Australia
*
*Corresponding author: Tel: +61 3 8344 2351. Fax: +61 3 9348 1421. E-mail: fsansom@unimelb.edu.au
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Summary

Nucleoside triphosphate diphosphohydrolases (NTPDases, GDA1_CD39 protein superfamily) play a diverse range of roles in a number of eukaryotic organisms. In humans NTPDases function in regulating the inflammatory and immune responses, control of vascular haemostasis and purine salvage. In yeast NTPDases are thought to function primarily in the Golgi, crucially involved in nucleotide sugar transport into the Golgi apparatus and subsequent protein glycosylation. Although rare in bacteria, in Legionella pneumophila secreted NTPDases function as virulence factors. In the last 2 decades it has become clear that a large number of parasites encode putative NTPDases, and the functions of a number of these have been investigated. In this review, the available evidence for NTPDases in parasites and the role of these NTPDases is summarized and discussed. Furthermore, the processes by which NTPDases could function in pathogenesis, purine salvage, thromboregulation, inflammation and glycoconjugate formation are considered, and the data supporting such putative roles reviewed. Potential future research directions to further clarify the role and importance of NTPDases in parasites are proposed. An attempt is also made to clarify the nomenclature used in the parasite field for the GDA1_CD39 protein superfamily, and a uniform system suggested.

Keywords

nucleoside triphosphate diphosphohydrolasesNTPDasesnomenclatureenzyme
Type
Review Article
Information
Parasitology , Volume 139 , Issue 8 , July 2012 , pp. 963 - 980
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Abeijon, C., Yanagisawa, K., Mandon, E. C., Hausler, A., Moremen, K., Hirschberg, C. B. and Robbins, P. W. (1993). Guanosine diphosphatase is required for protein and sphingolipid glycosylation in the Golgi lumen of Saccharomyces cerevisiae. The Journal of Cell Biology 122, 307–323.CrossRefGoogle ScholarPubMed
Asai, T., Howe, D. K., Nakajima, K., Nozaki, T., Takeuchi, T. and Sibley, L. D. (1998). Neospora caninum: tachyzoites express a potent type-I nucleoside triphosphate hydrolase. Experimental Parasitology 90, 277–285.CrossRefGoogle ScholarPubMed
Asai, T., Miura, S., Sibley, L. D., Okabayashi, H. and 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 ScholarPubMed
Atkinson, B., Dwyer, K., Enjyoji, K. and Robson, S. C. (2006). Ecto-nucleotidases of the CD39/NTPDase family modulate platelet activation and thrombus formation: Potential as therapeutic targets. Blood Cells, Molecules, and Diseases 36, 217–222.CrossRefGoogle ScholarPubMed
Balana-Fouce, R. and Reguera, R. M. (2007). RNA interference in Trypanosoma brucei: a high-throughput engine for functional genomics in trypanosomatids? Trends in Parasitology 23, 348–351. doi: 10.1016/j.pt.2007.06.008.CrossRefGoogle ScholarPubMed
Barros, F. S., De Menezes, L. F., Pinheiro, A. A., Silva, E. F., Lopes, A. H., De Souza, W. and Meyer-Fernandes, J. R. (2000). Ectonucleotide diphosphohydrolase activities in Entamoeba histolytica. Archives of Biochemistry and Biophysics 375, 304–314.CrossRefGoogle ScholarPubMed
Bastida-Corcuera, F. D., Okumura, C. Y., Colocoussi, A. and Johnson, P. J. (2005). Trichomonas vaginalis lipophosphoglycan mutants have reduced adherence and cytotoxicity to human ectocervical cells. Eukaryotic Cell, 4(11), 1951–1958. doi: 10.1128/EC.4.11.1951-1958.2005.CrossRefGoogle ScholarPubMed
Bermudes, D., Peck, K. R., Afifi, M. A., Beckers, C. J. and Joiner, K. A. (1994). Tandemly repeated genes encode nucleoside triphosphate hydrolase isoforms secreted into the parasitophorous vacuole of Toxoplasma gondii. The Journal of Biological Chemistry 269, 29252–29260.CrossRefGoogle ScholarPubMed
Bernardes, C. F., Meyer-Fernandes, J. R., Saad-Nehme, J., Vannier-Santos, M. A., Peres-Sampaio, C. E. and Vercesi, A. E. (2000). Effects of 4,4′-diisothyocyanatostilbene-2,2′-disulfonic acid on Trypanosoma cruzi proliferation and Ca(2+) homeostasis. The International Journal of Biochemistry and Cell Biology 32, 519–527.Google Scholar
Berninsone, P., Miret, J. J. and Hirschberg, C. B. (1994). The Golgi guanosine diphosphatase is required for transport of GDP-mannose into the lumen of Saccharomyces cerevisiae Golgi vesicles. The Journal of Biological Chemistry 269, 207–211.CrossRefGoogle ScholarPubMed
Berredo-Pinho, M., Peres-Sampaio, C. E., Chrispim, P. P., Belmont-Firpo, R., Lemos, A. P., Martiny, A., Vannier-Santos, M. A. and Meyer-Fernandes, J. R. (2001). A Mg-dependent ecto-ATPase in Leishmania amazonensis and its possible role in adenosine acquisition and virulence. Archives of Biochemistry and Biophysics 391, 16–24. doi:10.1006/abbi.2001.2384S0003-9861(01)92384-7 [pii].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., Bohme, 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, 416–422. doi: 10.1126/science.1112642.CrossRefGoogle ScholarPubMed
Bhardwaj, R., Krautz-Peterson, G. and Skelly, P. J. (2011). Using RNA interference in Schistosoma mansoni. Methods in Molecular Biology 764, 223–239. doi: 10.1007/978-1-61779-188-8_15.CrossRefGoogle ScholarPubMed
Bhardwaj, R. and Skelly, P. J. (2009). Purinergic signaling and immune modulation at the schistosome surface? Trends in Parasitology 25, 256–260. doi: 10.1016/j.pt.2009.03.004.CrossRefGoogle ScholarPubMed
Bisaggio, D. F., Peres-Sampaio, C. E., Meyer-Fernandes, J. R. and Souto-Padron, T. (2003). Ecto-ATPase activity on the surface of Trypanosoma cruzi and its possible role in the parasite-host cell interaction. Parasitology Research 91, 273–282. doi: 10.1007/s00436-003-0965-8.CrossRefGoogle ScholarPubMed
Borsellino, G., Kleinewietfeld, M., Di Mitri, D., Sternjak, A., Diamantini, A., Giometto, R., Hopner, S., Centonze, D., Bernardi, G., Dell'Acqua, M. L., Rossini, P. M., Battistini, L., Rotzschke, O. and Falk, K. (2007). Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 110, 1225–1232.CrossRefGoogle ScholarPubMed
Bours, M. J., Swennen, E. L., Di Virgilio, F., Cronstein, B. N. and Dagnelie, P. C. (2006). Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacology and Therapeutics, 112, 358–404.CrossRefGoogle ScholarPubMed
Burnstock, G. (1972). Purinergic nerves. Pharmacological Reviews 24, 509–581.Google ScholarPubMed
Burnstock, G. (2007). Purine and pyrimidine receptors. Cellular and Molecular Life sciences 64, 1471–1483.CrossRefGoogle ScholarPubMed
Butler, G., Rasmussen, M. D., Lin, M. F., Santos, M. A., Sakthikumar, S., Munro, C. A., Rheinbay, E., Grabherr, M., Forche, A., Reedy, J. L., Agrafioti, I., Arnaud, M. B., Bates, S., Brown, A. J., Brunke, S., Costanzo, M. C., Fitzpatrick, D. A., de Groot, P. W., Harris, D., Hoyer, L. L., Hube, B., Klis, F. M., Kodira, C., Lennard, N., Logue, M. E., Martin, R., Neiman, A. M., Nikolaou, E., Quail, M. A., Quinn, J., Santos, M. C., Schmitzberger, F. F., Sherlock, G., Shah, P., Silverstein, K. A., Skrzypek, M. S., Soll, D., Staggs, R., Stansfield, I., Stumpf, M. P., Sudbery, P. E., Srikantha, T., Zeng, Q., Berman, J., Berriman, M., Heitman, J., Gow, N. A., Lorenz, M. C., Birren, B. W., Kellis, M. and Cuomo, C. A. (2009). Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature, London 459, 657–662. doi: 10.1038/nature08064.CrossRefGoogle ScholarPubMed
Carlton, J. M., Hirt, R. P., Silva, J. C., Delcher, A. L., Schatz, M., Zhao, Q., Wortman, J. R., Bidwell, S. L., Alsmark, U. C., Besteiro, S., Sicheritz-Ponten, T., Noel, C. J., Dacks, J. B., Foster, P. G., Simillion, C., Van de Peer, Y., Miranda-Saavedra, D., Barton, G. J., Westrop, G. D., Muller, S., Dessi, D., Fiori, P. L., Ren, Q., Paulsen, I., Zhang, H., Bastida-Corcuera, F. D., Simoes-Barbosa, A., Brown, M. T., Hayes, R. D., Mukherjee, M., Okumura, C. Y., Schneider, R., Smith, A. J., Vanacova, S., Villalvazo, M., Haas, B. J., Pertea, M., Feldblyum, T. V., Utterback, T. R., Shu, C. L., Osoegawa, K., de Jong, P. J., Hrdy, I., Horvathova, L., Zubacova, Z., Dolezal, P., Malik, S. B., Logsdon, J. M. Jr., Henze, K., Gupta, A., Wang, C. C., Dunne, R. L., Upcroft, J. A., Upcroft, P., White, O., Salzberg, S. L., Tang, P., Chiu, C. H., Lee, Y. S., Embley, T. M., Coombs, G. H., Mottram, J. C., Tachezy, J., Fraser-Liggett, C. M. and Johnson, P. J. (2007). Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315, 207–212.CrossRefGoogle ScholarPubMed
Chaves, S. P., Torres-Santos, E. C., Marques, C., Figliuolo, V. R., Persechini, P. M., Coutinho-Silva, R. and Rossi-Bergmann, B. (2009). Modulation of P2X(7) purinergic receptor in macrophages by Leishmania amazonensis and its role in parasite elimination. Microbes and Infection/Institut Pasteur 11, 842–849. doi: 10.1016/j.micinf.2009.05.001.CrossRefGoogle ScholarPubMed
Chien, M., Morozova, I., Shi, S., Sheng, H., Chen, J., Gomez, S. M., Asamani, G., Hill, K., Nuara, J., Feder, M., Rineer, J., Greenberg, J. J., Steshenko, V., Park, S. H., Zhao, B., Teplitskaya, E., Edwards, J. R., Pampou, S., Georghiou, A., Chou, I. C., Iannuccilli, W., Ulz, M. E., Kim, D. H., Geringer-Sameth, A., Goldsberry, C., Morozov, P., Fischer, S. G., Segal, G., Qu, X., Rzhetsky, A., Zhang, P., Cayanis, E., De Jong, P. J., Ju, J., Kalachikov, S., Shuman, H. A. and Russo, J. J. (2004). The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305, 1966–1968.CrossRefGoogle ScholarPubMed
Collopy-Junior, I., Kneipp, L. F., da Silva, F. C., Rodrigues, M. L., Alviano, C. S. and Meyer-Fernandes, J. R. (2006). Characterization of an ecto-ATPase activity in Fonsecaea pedrosoi. Archives of Microbiology 185, 355–362.CrossRefGoogle ScholarPubMed
Cox, M. A., Gomes, B., Palmer, K., Du, K., Wiekowski, M., Wilburn, B., Petro, M., Chou, C. C., Desquitado, C., Schwarz, M., Lunn, C., Lundell, D., Narula, S. K., Zavodny, P. J. and Jenh, C. H. (2005). The pyrimidinergic P2Y6 receptor mediates a novel release of proinflammatory cytokines and chemokines in monocytic cells stimulated with UDP. Biochemical and Biophysical Research Communications 330, 467–473.CrossRefGoogle ScholarPubMed
Cruz, A., Coburn, C. M. and Beverley, S. M. (1991). Double targeted gene replacement for creating null mutants. Proceedings of the National Academy of Sciences, USA 88, 7170–7174.CrossRefGoogle ScholarPubMed
de Aguiar Matos, J. A., Borges, F. P., Tasca, T., Bogo, M. R., De Carli, G. A., da Graca Fauth, M., Dias, R. D. and 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.CrossRefGoogle ScholarPubMed
de Almeida Marques-da-Silva, E., de Oliveira, J. C., Figueiredo, A. B., de Souza Lima Junior, D., Carneiro, C. M., Rangel Fietto, J. L. and Crocco Afonso, L. C. (2008). Extracellular nucleotide metabolism in Leishmania: influence of adenosine in the establishment of infection. Microbes and Infection/Institut Pasteur 10, 850–857. doi: 10.1016/j.micinf.2008.04.016.CrossRefGoogle ScholarPubMed
de Jesus, J. B., de Sa Pinheiro, A. A., Lopes, A. H. and Meyer-Fernandes, J. R. (2002). An ectonucleotide ATP-diphosphohydrolase activity in Trichomonas vaginalis stimulated by galactose and its possible role in virulence. Zeitschrift für Naturforschung C 57, 890–896.CrossRefGoogle ScholarPubMed
de Sa Pinheiro, A. A., Cosentino-Gomes, D., Lanfredi-Rangel, A., Ferraro, R. B., De Souza, W. and Meyer-Fernandes, J. R. (2008). Giardia lamblia: biochemical characterization of an ecto-ATPase activity. Experimental Parasitology 119, 279–284. doi: S0014-4894(08)00055-6 [pii]10.1016/j.exppara.2008.02.006.CrossRefGoogle ScholarPubMed
de Souza Leite, M., Thomaz, R., Fonseca, F. V., Panizzutti, R., Vercesi, A. E. and Meyer-Fernandes, J. R. (2007). Trypanosoma brucei brucei: Biochemical characterization of ecto-nucleoside triphosphate diphosphohydrolase activities. Experimental Parasitology 115, 315–323.CrossRefGoogle ScholarPubMed
Deaglio, S., Dwyer, K. M., Gao, W., Friedman, D., Usheva, A., Erat, A., Chen, J. F., Enjyoji, K., Linden, J., Oukka, M., Kuchroo, V. K., Strom, T. B. and Robson, S. C. (2007). Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. The Journal of Experimental Medicine 204, 1257–1265.Google Scholar
Deaglio, S. and Robson, S. C. (2011). Ectonucleotidases as regulators of purinergic signaling in thrombosis, inflammation, and immunity. Advances in Pharmacology 61, 301–332. doi: 10.1016/B978-0-12-385526-8.00010-2.CrossRefGoogle ScholarPubMed
dos Passos Lemos, A., de Sa Pinheiro, A. A., de Berredo-Pinho, M., Fonseca de Souza, L., Motta, C. M., de Souza, W. and Meyer-Fernandes, R. (2002). Ectonucleotide diphosphohydrolase activity in Crithidia deanei. Parasitology Research 88, 905–911. doi: 10.1007/s00436-002-0671-y.CrossRefGoogle ScholarPubMed
Douillet, C. D., Robinson, W. P. 3rd, Milano, P. M., Boucher, R. C. and Rich, P. B. (2006). Nucleotides induce IL-6 release from human airway epithelia via P2Y2 and p38 MAPK-dependent pathways. American Journal of Physiology. Lung Cellular and Molecular Physiology 291, L734–746.CrossRefGoogle ScholarPubMed
Downing, T., Imamura, H., Decuypere, S., Clark, T. G., Coombs, G. H., Cotton, J. A., Hilley, J. D., de Doncker, S., Maes, I., Mottram, J. C., Quail, M. A., Rijal, S., Sanders, M., Schonian, G., Stark, O., Sundar, S., Vanaerschot, M., Hertz-Fowler, C., Dujardin, J. C. and Berriman, M. (2011). Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome Research 21, 2143–2156. doi: 10.1101/gr.123430.111.CrossRefGoogle ScholarPubMed
Dwyer, K. M., Robson, S. C., Nandurkar, H. H., Campbell, D. J., Gock, H., Murray-Segal, L. J., Fisicaro, N., Mysore, T. B., Kaczmarek, E., Cowan, P. J. and d'Apice, A. J. (2004). Thromboregulatory manifestations in human CD39 transgenic mice and the implications for thrombotic disease and transplantation. The Journal of Clinical Investigation 113, 1440–1446.CrossRefGoogle Scholar
Enjyoji, K., Sevigny, J., Lin, Y., Frenette, P. S., Christie, P. D., Esch, J. S. 2nd, Imai, M., Edelberg, J. M., Rayburn, H., Lech, M., Beeler, D. L., Csizmadia, E., Wagner, D. D., Robson, S. C. and Rosenberg, R. D. (1999). Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nature Medicine 5, 1010–1017.CrossRefGoogle ScholarPubMed
Ennes-Vidal, V., Castro, R. O., Britto, C., Barrabin, H., D'Avila-Levy, C. M. and Moreira, O. C. (2011). CrATP interferes in the promastigote-macrophage interaction in Leishmania amazonensis infection. Parasitology 138, 960–968. doi: 10.1017/S0031182011000710.CrossRefGoogle ScholarPubMed
Fietto, J. L., DeMarco, R., Nascimento, I. P., Castro, I. M., Carvalho, T. M., de Souza, W., Bahia, M. T., Alves, M. J. and Verjovski-Almeida, S. (2004). Characterization and immunolocalization of an NTP diphosphohydrolase of Trypanosoma cruzi. Biochemical and Biophysical Research Communications 316, 454–460.Google Scholar
Fonseca, F. V., Fonseca de Souza, A. L., Mariano, A. C., Entringer, P. F., Gondim, K. C. and Meyer-Fernandes, J. R. (2006). Trypanosoma rangeli: characterization of a Mg-dependent ecto ATP-diphosphohydrolase activity. Experimental Parasitology 112, 76–84.Google Scholar
Gachet, C. (2006). Regulation of platelet functions by P2 receptors. Annual Review of Pharmacology and Toxicology 46, 277–300.CrossRefGoogle ScholarPubMed
Gao, X. D., Kaigorodov, V. and Jigami, Y. (1999). YND1, a homologue of GDA1, encodes membrane-bound apyrase required for Golgi N- and O-glycosylation in Saccharomyces cerevisiae. The Journal of Biological Chemistry 274, 21450–21456.CrossRefGoogle ScholarPubMed
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, J. C., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. and Barrell, B. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, London 419, 498–511.CrossRefGoogle ScholarPubMed
Giordani, R. B., Weizenmann, M., Rosemberg, D. B., De Carli, G. A., Bogo, M. R., Zuanazzi, J. A. and Tasca, T. (2010). Trichomonas vaginalis nucleoside triphosphate diphosphohydrolase and ecto-5′-nucleotidase activities are inhibited by lycorine and candimine. Parasitology International 59, 226–231. doi: 10.1016/j.parint.2010.02.004.CrossRefGoogle ScholarPubMed
Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J. and Lopez, R. (2010). A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Research 38 (Web Server issue), W695–699. doi: 10.1093/nar/gkq313.CrossRefGoogle ScholarPubMed
Guha-Niyogi, A., Sullivan, D. and Turco, S. (2011). Glycoconjugate structures of parasitic protozoa. Glycobiology 11, 45R–59R.CrossRefGoogle Scholar
Ha, D. S., Schwarz, J. K., Turco, S. J. and Beverley, S. M. (1996). Use of the green fluorescent protein as a marker in transfected Leishmania. Molecular and Biochemical Parasitology 77, 57–64.Google ScholarPubMed
Handa, M. and Guidotti, G. (1996). Purification and cloning of a soluble ATP-diphosphohydrolase (apyrase) from potato tubers (Solanum tuberosum). Biochemical and Biophysical Research Communications 218, 916–923.Google Scholar
Herrero, A. B., Uccelletti, D., Hirschberg, C. B., Dominguez, A. and Abeijon, C. (2002). The Golgi GDPase of the fungal pathogen Candida albicans affects morphogenesis, glycosylation, and cell wall properties. Eukaryotic Cell 1, 420–431.CrossRefGoogle ScholarPubMed
Herwaldt, B. L. (1999). Leishmaniasis. Lancet 354, 1191–1199.CrossRefGoogle ScholarPubMed
Heussler, V. T., Kuenzi, P. and Rottenberg, S. (2001). Inhibition of apoptosis by intracellular protozoan parasites. International Journal for Parasitology 31, 1166–1176.CrossRefGoogle ScholarPubMed
Hirschberg, C. B., Robbins, P. W. and Abeijon, C. (1998). Transporters of nucleotide sugars, ATP, and nucleotide sulfate in the endoplasmic reticulum and Golgi apparatus. Annual Review of Biochemistry 67, 49–69. doi: 10.1146/annurev.biochem.67.1.49.CrossRefGoogle ScholarPubMed
Ivens, A. C., Peacock, C. S., Worthey, E. A., Murphy, L., Aggarwal, G., Berriman, M., Sisk, E., Rajandream, M. A., Adlem, E., Aert, R., Anupama, A., Apostolou, Z., Attipoe, P., Bason, N., Bauser, C., Beck, A., Beverley, S. M., Bianchettin, G., Borzym, K., Bothe, G., Bruschi, C. V., Collins, M., Cadag, E., Ciarloni, L., Clayton, C., Coulson, R. M., Cronin, A., Cruz, A. K., Davies, R. M., De Gaudenzi, J., Dobson, D. E., Duesterhoeft, A., Fazelina, G., Fosker, N., Frasch, A. C., Fraser, A., Fuchs, M., Gabel, C., Goble, A., Goffeau, A., Harris, D., Hertz-Fowler, C., Hilbert, H., Horn, D., Huang, Y., Klages, S., Knights, A., Kube, M., Larke, N., Litvin, L., Lord, A., Louie, T., Marra, M., Masuy, D., Matthews, K., Michaeli, S., Mottram, J. C., Muller-Auer, S., Munden, H., Nelson, S., Norbertczak, H., Oliver, K., O'Neil, S., Pentony, M., Pohl, T. M., Price, C., Purnelle, B., Quail, M. A., Rabbinowitsch, E., Reinhardt, R., Rieger, M., Rinta, J., Robben, J., Robertson, L., Ruiz, J. C., Rutter, S., Saunders, D., Schafer, M., Schein, J., Schwartz, D. C., Seeger, K., Seyler, A., Sharp, S., Shin, H., Sivam, D., Squares, R., Squares, S., Tosato, V., Vogt, C., Volckaert, G., Wambutt, R., Warren, T., Wedler, H., Woodward, J., Zhou, S., Zimmermann, W., Smith, D. F., Blackwell, J. M., Stuart, K. D., Barrell, B. and Myler, P. J. (2005). The genome of the kinetoplastid parasite, Leishmania major. Science 309, 436–442.Google Scholar
Jesus, J. B., Lopes, A. H. and Meyer-Fernandes, J. R. (2002). Characterization of an ecto-ATPase of Tritrichomonas foetus. Veterinary Parasitology 103, 29–42.CrossRefGoogle ScholarPubMed
Johnson, M. S., Broady, K. W. and Johnson, A. M. (1999). Differential recognition of Toxoplasma gondii recombinant nucleoside triphosphate hydrolase isoforms by naturally infected human sera. International Journal for Parasitology 29, 1893–1905.CrossRefGoogle ScholarPubMed
Jones, T., Federspiel, N. A., Chibana, H., Dungan, J., Kalman, S., Magee, B. B., Newport, G., Thorstenson, Y. R., Agabian, N., Magee, P. T., Davis, R. W. and Scherer, S. (2004). The diploid genome sequence of Candida albicans. Proceedings of the National Academy of Sciences, USA 101, 7329–7334. doi: 10.1073/pnas.0401648101.CrossRefGoogle ScholarPubMed
Junior, I. C., Rodrigues, M. L., Alviano, C. S., Travassos, L. R. and Meyer-Fernandes, J. R. (2005). Characterization of an ecto-ATPase activity in Cryptococcus neoformans. FEMS Yeast Research 5, 899–907.CrossRefGoogle ScholarPubMed
Kiffer-Moreira, T., Fernandes Sampaio, M. E., Alviano, D. S., Axelband, F., Cesar, G. V., Cosentino-Gomes, D., Rodrigues, M. L., Nimrichter, L., Vieyra, A., Alviano, C. S. and Meyer-Fernandes, J. R. (2010). Biochemical characterization of an ecto-ATP diphosphohydrolase activity in Candida parapsilosis and its possible role in adenosine acquisition and pathogenesis. FEMS Yeast Research 10, 735–746. doi: 10.1111/j.1567-1364.2010.00641.x.Google Scholar
Kikuchi, T., Furuta, T. and Kojima, S. (2001). Membrane localization and demonstration of isoforms of nucleoside triphosphate hydrolase from Toxoplasma gondii. Parasitology 122, 15–23.CrossRefGoogle ScholarPubMed
Knowles, A. F. (2011). The GDA1_CD39 superfamily: NTPDases with diverse functions. Purinergic Signal 7, 21–45. doi: 10.1007/s11302-010-9214-7.CrossRefGoogle ScholarPubMed
Kukulski, F., Bahrami, F., Ben Yebdri, F., Lecka, J., Martin-Satue, M., Levesque, S. A. and Sevigny, J. (2011). NTPDase1 controls IL-8 production by human neutrophils. Journal of Immunology 187, 644–653. doi: 10.4049/jimmunol.1002680.CrossRefGoogle ScholarPubMed
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948. doi: 10.1093/bioinformatics/btm404.CrossRefGoogle ScholarPubMed
Leite, M. S., Thomaz, R., Oliveira, J. H., Oliveira, P. L. and Meyer-Fernandes, J. R. (2009). Trypanosoma brucei brucei: effects of ferrous iron and heme on ecto-nucleoside triphosphate diphosphohydrolase activity. Experimental Parasitology 121, 137–143. doi: 10.1016/j.exppara.2008.10.018.CrossRefGoogle ScholarPubMed
Letunic, I. and Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128. doi: 10.1093/bioinformatics/btl529.CrossRefGoogle ScholarPubMed
Letunic, I. and Bork, P. (2011). Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Research 39 (Web Server issue), W475–478. doi: 10.1093/nar/gkr201.CrossRefGoogle ScholarPubMed
Levano-Garcia, J., Mortara, R. A., Verjovski-Almeida, S. and DeMarco, R. (2007). Characterization of Schistosoma mansoni ATPDase2 gene, a novel apyrase family member. Biochemical and Biophysical Research Communications 352, 384–389.CrossRefGoogle ScholarPubMed
Levesque, S. A., Kukulski, F., Enjyoji, K., Robson, S. C. and Sevigny, J. (2010). NTPDase1 governs P2X7-dependent functions in murine macrophages. European Journal of Immunology 40, 1473–1485. doi: 10.1002/eji.200939741.Google Scholar
Loftus, B. J., Fung, E., Roncaglia, P., Rowley, D., Amedeo, P., Bruno, D., Vamathevan, J., Miranda, M., Anderson, I. J., Fraser, J. A., Allen, J. E., Bosdet, I. E., Brent, M. R., Chiu, R., Doering, T. L., Donlin, M. J., D'Souza, C. A., Fox, D. S., Grinberg, V., Fu, J., Fukushima, M., Haas, B. J., Huang, J. C., Janbon, G., Jones, S. J., Koo, H. L., Krzywinski, M. I., Kwon-Chung, J. K., Lengeler, K. B., Maiti, R., Marra, M. A., Marra, R. E., Mathewson, C. A., Mitchell, T. G., Pertea, M., Riggs, F. R., Salzberg, S. L., Schein, J. E., Shvartsbeyn, A., Shin, H., Shumway, M., Specht, C. A., Suh, B. B., Tenney, A., Utterback, T. R., Wickes, B. L., Wortman, J. R., Wye, N. H., Kronstad, J. W., Lodge, J. K., Heitman, J., Davis, R. W., Fraser, C. M. and Hyman, R. W. (2005). The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307, 1321–1324. doi: 10.1126/science.1103773.CrossRefGoogle ScholarPubMed
Lopez-Avalos, M. D., Uccelletti, D., Abeijon, C. and Hirschberg, C. B. (2001). The UDPase activity of the Kluyveromyces lactis Golgi GDPase has a role in uridine nucleotide sugar transport into Golgi vesicles. Glycobiology 11, 413–422.CrossRefGoogle Scholar
Luiz Oliveira Penido, M., Resende, D. M., Vianello, M. A., Humberto da Silveira Bordin, F., Jacinto, A. A., Dias, W. D., Montesano, M. A., Nelson, D. L., Marcos Zech Coelho, P. and Vasconcelos, E. G. (2007). A new series of schistosomicide drugs, the alkylaminoalkanethiosulfuric acids, partially inhibit the activity of Schistosoma mansoni ATP diphosphohydrolase. European Journal of Pharmacology 570, 10–17.CrossRefGoogle ScholarPubMed
Marcus, A. J., Broekman, M. J., Drosopoulos, J. H., Islam, N., Alyonycheva, T. N., Safier, L. B., Hajjar, K. A., Posnett, D. N., Schoenborn, M. A., Schooley, K. A., Gayle, R. B. and Maliszewski, C. R. (1997). The endothelial cell ecto-ADPase responsible for inhibition of platelet function is CD39. The Journal of Clinical Investigation 99, 1351–1360.CrossRefGoogle ScholarPubMed
Marques-da-Silva, C., Chaves, M. M., Chaves, S. P., Figliuolo, V. R., Meyer-Fernandes, J. R., Corte-Real, S., Lameu, C., Ulrich, H., Ojcius, D. M., Rossi-Bergmann, B. and Coutinho-Silva, R. (2011). Infection with Leishmania amazonensis upregulates purinergic receptor expression and induces host-cell susceptibility to UTP-mediated apoptosis. Cellular Microbiology 13, 1410–1428. doi: 10.1111/j.1462-5822.2011.01630.x.CrossRefGoogle ScholarPubMed
Matin, A. and Khan, N. A. (2008). Demonstration and partial characterization of ecto-ATPase in Balamuthia mandrillaris and its possible role in the host-cell interactions. Letters in Applied Microbiology 47, 348–354. doi: 10.1111/j.1472-765X.2008.02414.x.CrossRefGoogle ScholarPubMed
Matthews, K. R. (2005). The developmental cell biology of Trypanosoma brucei. Journal of Cell Science 118, 283–290.Google Scholar
McMorran, B. J., Marshall, V. M., de Graaf, C., Drysdale, K. E., Shabbar, M., Smyth, G. K., Corbin, J. E., Alexander, W. S. and Foote, S. J. (2009). Platelets kill intraerythrocytic malarial parasites and mediate survival to infection. Science 323, 797–800. doi: 10.1126/science.1166296.CrossRefGoogle ScholarPubMed
Meyer-Fernandes, J. R. (2002). Ecto-ATPases in protozoa parasites: looking for a function. Parasitology International 51, 299–303.Google Scholar
Meyer-Fernandes, J. R., Cosentino-Gomes, D., Vieira, D. P. and Lopes, A. H. (2010). Ecto-Nucleoside Triphosphate Diphosphohydrolase Activities in Trypanosomatids: Possible Roles in Infection, Virulence and Purine Recycling. The Open Parasitology Journal, 4, 116–119.CrossRefGoogle Scholar
Meyer-Fernandes, J. R., Dutra, P. M., Rodrigues, C. O., Saad-Nehme, J. and Lopes, A. H. (1997). Mg-dependent ecto-ATPase activity in Leishmania tropica. Archives of Biochemistry and Biophysics 341, 40–46.CrossRefGoogle ScholarPubMed
Meyer-Fernandes, J. R., Saad-Nehme, J., Peres-Sampaio, C. E., Belmont-Firpo, R., Bisaggio, D. F., Do Couto, L. C., Fonseca De Souza, A. L., Lopes, A. H. and Souto-Padron, T. (2004). A Mg-dependent ecto-ATPase is increased in the infective stages of Trypanosoma cruzi. Parasitology Research 93, 41–50.CrossRefGoogle ScholarPubMed
Nakaar, V., Beckers, C. J., Polotsky, V. and Joiner, K. A. (1998 a). Basis for substrate specificity of the Toxoplasma gondii nucleoside triphosphate hydrolase. Molecular and Biochemical Parasitology 97, 209–220.Google Scholar
Nakaar, V., Bermudes, D., Peck, K. R. and Joiner, K. A. (1998 b). Upstream elements required for expression of nucleoside triphosphate hydrolase genes of Toxoplasma gondii. Molecular and Biochemical Parasitology 92, 229–239.CrossRefGoogle ScholarPubMed
Nakaar, V., Samuel, B. U., Ngo, E. O. and Joiner, K. A. (1999). Targeted reduction of nucleoside triphosphate hydrolase by antisense RNA inhibits Toxoplasma gondii proliferation. The Journal of Biological Chemistry 274, 5083–5087.CrossRefGoogle ScholarPubMed
Okenu, D. M., Opara, K. N., Nwuba, R. I. and Nwagwu, M. (1999). Purification and characterisation of an extracellularly released protease of Trypanosoma brucei. Parasitology Research 85, 424–428.CrossRefGoogle ScholarPubMed
Paletta-Silva, R. and Meyer-Fernandes, J. R. (2012). Adenosine and immune imbalance in visceral leishmaniasis: the possible role of ectonucleotidases. Journal of Tropical Medicine 2012, 650874. doi: 10.1155/2012/650874.CrossRefGoogle ScholarPubMed
Peacock, C. S., Seeger, K., Harris, D., Murphy, L., Ruiz, J. C., Quail, M. A., Peters, N., Adlem, E., Tivey, A., Aslett, M., Kerhornou, A., Ivens, A., Fraser, A., Rajandream, M. A., Carver, T., Norbertczak, H., Chillingworth, T., Hance, Z., Jagels, K., Moule, S., Ormond, D., Rutter, S., Squares, R., Whitehead, S., Rabbinowitsch, E., Arrowsmith, C., White, B., Thurston, S., Bringaud, F., Baldauf, S. L., Faulconbridge, A., Jeffares, D., Depledge, D. P., Oyola, S. O., Hilley, J. D., Brito, L. O., Tosi, L. R., Barrell, B., Cruz, A. K., Mottram, J. C., Smith, D. F. and Berriman, M. (2007). Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nature Genetics 39, 839–847.Google Scholar
Peres-Sampaio, C. E., de Almeida-Amaral, E. E., Giarola, N. L. and Meyer-Fernandes, J. R. (2008). Leishmania amazonensis: effects of heat shock on ecto-ATPase activity. Experimental Parasitology 119, 135–143. doi: S0014-4894(08)00008-8 [pii] 10.1016/j.exppara.2008.01.003.CrossRefGoogle ScholarPubMed
Peres-Sampaio, C. E., Palumbo, S. T. and Meyer-Fernandes, J. R. (2001). An ecto-ATPase activity present in Leishmania tropica stimulated by dextran sulfate. Zeitschrift für Naturforschung, C 56, 820–825.CrossRefGoogle ScholarPubMed
Pinheiro, C. M., Martins-Duarte, E. S., Ferraro, R. B., Fonseca de Souza, A. L., Gomes, M. T., Lopes, A. H., Vannier-Santos, M. A., Santos, A. L. and Meyer-Fernandes, J. R. (2006). Leishmania amazonensis: Biological and biochemical characterization of ecto-nucleoside triphosphate diphosphohydrolase activities. Experimental Parasitology 114, 16–25.CrossRefGoogle ScholarPubMed
Pizzirani, C., Ferrari, D., Chiozzi, P., Adinolfi, E., Sandona, D., Savaglio, E. and Di Virgilio, F. (2007). Stimulation of P2 receptors causes release of IL-1{beta}-loaded microvesicles from human dendritic cells. Blood 109, 3856–3864.Google Scholar
Robson, S. C., Sevigny, J. and Zimmermann, H. (2006). The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance. Purinergic Signal 2, 409–430.CrossRefGoogle ScholarPubMed
Ruckert, C., Stuepp Cdos, S., Gottardi, B., Rosa, J., Cisilotto, J., Borges, F. P., Rosemberg, D. B., Bogo, M. R., Tasca, T., De Carli, G. A. and Bonan, C. D. (2010). Trichomonas vaginalis: dehydroepiandrosterone sulfate and 17beta-estradiol alter NTPDase activity and gene expression. Experimental Parasitology 125, 187–195. doi: 10.1016/j.exppara.2010.01.029.CrossRefGoogle ScholarPubMed
Sanchez, R., Franco, A., Gacto, M., Notario, V. and Cansado, J. (2003). Characterization of gdp1+ as encoding a GDPase in the fission yeast Schizosaccharomyces pombe. FEMS Microbiology letters 228, 33–38.CrossRefGoogle ScholarPubMed
Sansom, F. M., Newton, H. J., Crikis, S., Cianciotto, N. P., Cowan, P. J., d'Apice, A. J. and Hartland, E. L. (2007). A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cellular Microbiology 9, 1922–1935.CrossRefGoogle ScholarPubMed
Sansom, F. M., Riedmaier, P., Newton, H. J., Dunstone, M. A., Muller, C. E., Stephan, H., Byres, E., Beddoe, T., Rossjohn, J., Cowan, P. J., d'Apice, A. J., Robson, S. C. and Hartland, E. L. (2008 a). Enzymatic properties of an ecto-nucleoside triphosphate diphosphohydrolase from Legionella pneumophila: substrate specificity and requirement for virulence. The Journal of Biological Chemistry 283, 12909–12918. doi: M801006200 [pii]10.1074/jbc.M801006200.Google Scholar
Sansom, F. M., Robson, S. C. and Hartland, E. L. (2008 b). Possible effects of microbial ecto-nucleoside triphosphate diphosphohydrolases on host-pathogen interactions. Microbiology and Molecular Biology Reviews 72, 765–781, Table of Contents. doi: 72/4/765 [pii]10.1128/MMBR.00013-08.CrossRefGoogle ScholarPubMed
Santos, R. F., Possa, M. A., Bastos, M. S., Guedes, P. M., Almeida, M. R., Demarco, R., Verjovski-Almeida, S., Bahia, M. T. and Fietto, J. L. (2009). Influence of Ecto-nucleoside triphosphate diphosphohydrolase activity on Trypanosoma cruzi infectivity and virulence. PLoS Neglected Tropical Diseases 3, e387. doi: 10.1371/journal.pntd.0000387.CrossRefGoogle ScholarPubMed
Sibley, L. D., Niesman, I. R., Asai, T. and Takeuchi, T. (1994). Toxoplasma gondii: secretion of a potent nucleoside triphosphate hydrolase into the parasitophorous vacuole. Experimental Parasitology 79, 301–311.Google Scholar
Silverman, J. A., Qi, H., Riehl, A., Beckers, C., Nakaar, V. and Joiner, K. A. (1998). Induced activation of the Toxoplasma gondii nucleoside triphosphate hydrolase leads to depletion of host cell ATP levels and rapid exit of intracellular parasites from infected cells. The Journal of Biological Chemistry 273, 12352–12359.CrossRefGoogle ScholarPubMed
Sissons, J., Alsam, S., Jayasekera, S. and Khan, N. A. (2004). Ecto-ATPases of clinical and non-clinical isolates of Acanthamoeba. Microbial pathogenesis, 37(5), 231–239.CrossRefGoogle ScholarPubMed
Souza, V. L., Veras, P. S., Welby-Borges, M., Silva, T. M., Leite, B. R., Ferraro, R. B., Meyer-Fernandes, J. R., Barral, A., Costa, J. M. and de Freitas, L. A. (2011). Immune and inflammatory responses to Leishmania amazonensis isolated from different clinical forms of human leishmaniasis in CBA mice. Memorias do Instituto Oswaldo Cruz 106, 23–31.CrossRefGoogle ScholarPubMed
Spath, G. F., Epstein, L., Leader, B., Singer, S. M., Avila, H. A., Turco, S. J. and Beverley, S. M. (2000). Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proceedings of the National Academy of Sciences, USA 97, 9258–9263. doi: 10.1073/pnas.160257897.CrossRefGoogle ScholarPubMed
Stanley, R. G., Ngaiza, J. R., Wambayi, E., Lewis, J. and Doenhoff, M. J. (2003). Platelets as an innate defence mechanism against Schistosoma mansoni infections in mice. Parasite Immunology 25, 467–473.Google Scholar
Stommel, E. W., Cho, E., Steide, J. A., Seguin, R., Barchowsky, A., Schwartzman, J. D. and Kasper, L. H. (2001). Identification and role of thiols in Toxoplasma gondii egress. Experimental Biology and Medicine 226, 229–236.Google Scholar
Stommel, E. W., Ely, K. H., Schwartzman, J. D. and Kasper, L. H. (1997). Toxoplasma gondii: dithiol-induced Ca2+ flux causes egress of parasites from the parasitophorous vacuole. Experimental Parasitology 87, 88–97.CrossRefGoogle ScholarPubMed
Tanowitz, H. B., Burns, E. R., Sinha, A. K., Kahn, N. N., Morris, S. A., Factor, S. M., Hatcher, V. B., Bilezikian, J. P., Baum, S. G. and Wittner, M. (1990). Enhanced platelet adherence and aggregation in Chagas’ disease: a potential pathogenic mechanism for cardiomyopathy. The American Journal of Tropical Medicine and Hygiene 43, 274–281.CrossRefGoogle ScholarPubMed
Tasca, T., Bonan, C. D., De Carli, G. A., Sarkis, J. J. and Alderete, J. F. (2005). Heterogeneity in extracellular nucleotide hydrolysis among clinical isolates of Trichomonas vaginalis. Parasitology 131, 71–78.CrossRefGoogle ScholarPubMed
Taylor, M. C., Huang, H. and Kelly, J. M. (2011). Genetic techniques in Trypanosoma cruzi. Advances in Parasitology 75, 231–250. doi: 10.1016/B978-0-12-385863-4.00011-3.Google Scholar
Umekita, L. F., Piazza, R. M. and Mota, I. (1994). Role of platelets and complement in the clearance of epimastigote forms of Trypanosoma cruzi. Brazilian Journal of Medical and Biological Research 27, 2391–2399.Google ScholarPubMed
Van der Pol, B. (2007). Trichomonas vaginalis infection: the most prevalent nonviral sexually transmitted infection receives the least public health attention. Clinical Infectious Diseases 44, 23–25.CrossRefGoogle ScholarPubMed
Vasconcelos, E. G., Ferreira, S. T., Carvalho, T. M., Souza, W., Kettlun, A. M., Mancilla, M., Valenzuela, M. A. and Verjovski-Almeida, S. (1996). Partial purification and immunohistochemical localization of ATP diphosphohydrolase from Schistosoma mansoni. Immunological cross-reactivities with potato apyrase and Toxoplasma gondii nucleoside triphosphate hydrolase. The Journal of Biological Chemistry 271, 22139–22145.Google Scholar
Vasconcelos, E. G., Nascimento, P. S., Meirelles, M. N., Verjovski-Almeida, S. and Ferreira, S. T. (1993). Characterization and localization of an ATP-diphosphohydrolase on the external surface of the tegument of Schistosoma mansoni. Molecular and Biochemical Parasitology 58, 205–214.CrossRefGoogle ScholarPubMed
Vivian, J. P., Riedmaier, P., Ge, H., Le Nours, J., Sansom, F. M., Wilce, M. C., Byres, E., Dias, M., Schmidberger, J. W., Cowan, P. J., d'Apice, A. J., Hartland, E. L., Rossjohn, J. and Beddoe, T. (2010). Crystal structure of a Legionella pneumophila ecto-triphosphate diphosphohydrolase, a structural and functional homolog of the eukaryotic NTPDases. Structure 18, 228–238. doi: S0969-2126(09)00480-8 [pii]10.1016/j.str.2009.11.014.CrossRefGoogle Scholar
Zhang, D., Gaji, R. Y. and Howe, D. K. (2006). Identification of a dithiol-dependent nucleoside triphosphate hydrolase in Sarcocystis neurona. International Journal for Parasitology 36, 1197–1204.Google Scholar
Zimmermann, H., Beaudoin, A. R., Bollen, M., Goding, J. W., Guidotti, G., Kirley, T. L., Robson, S. C. and Sano, K (2000). Nomenclature for two families of novel ecto-nucleotidases. In Second International Workshop on Ecto-ATPases and Related Ecto-nucleotidases (ed. Vanduffel, L. and Lemmens, R.), pp. 1–8. Shaker Publishing BV, Maastricht, The Netherlands.Google Scholar