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Molecular and Cellular Biology Volume 19, 1999 - Issue 11
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Cell and Organelle Structure and Assembly

Characterization of a Vacuolar Pyrophosphatase in Trypanosoma brucei and Its Localization to Acidocalcisomes

Claudia O. RodriguesLaboratory of Molecular Parasitology, Department of Pathobiology, University of Illinois at Urbana-Champaign, Urbana, Illinois61802
,
David A. ScottLaboratory of Molecular Parasitology, Department of Pathobiology, University of Illinois at Urbana-Champaign, Urbana, Illinois61802
&
Roberto DocampoLaboratory of Molecular Parasitology, Department of Pathobiology, University of Illinois at Urbana-Champaign, Urbana, Illinois61802Correspondence[email protected]
Pages 7712-7723 | Received 25 May 1999, Accepted 23 Aug 1999, Published online: 28 Mar 2023

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Guozhong Huang & Roberto Docampo. (2015) Proteomic analysis of acidocalcisomes of Trypanosoma brucei uncovers their role in phosphate metabolism, cation homeostasis, and calcium signaling . Communicative & Integrative Biology 8:2.
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Articles from other publishers (69)

Roberto Docampo & Guozhong Huang. (2022) New insights into the role of acidocalcisomes in trypanosomatids. Journal of Eukaryotic Microbiology 69:6.
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Roberto Docampo & Guozhong Huang. (2021) The IP3 receptor and Ca2+ signaling in trypanosomes. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1868:4, pages 118947.
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Emanuel Sanz-Luque, Devaki Bhaya & Arthur R. Grossman. (2020) Polyphosphate: A Multifunctional Metabolite in Cyanobacteria and Algae. Frontiers in Plant Science 11.
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Ursula Goodenough, Aaron A. Heiss, Robyn Roth, Jannette Rusch & Jae-Hyeok Lee. (2019) Acidocalcisomes: Ultrastructure, Biogenesis, and Distribution in Microbial Eukaryotes. Protist 170:3, pages 287-313.
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Keni Vidilaseris, Alexandros KiriazisAinoleena Turku, Ayman KhattabNiklas G. Johansson, Teppo O. Leino, Paula S. Kiuru, Gustav Boije af Gennäs, Seppo MeriJari Yli-Kauhaluoma, Henri Xhaard & Adrian Goldman. (2019) Asymmetry in catalysis by Thermotoga maritima membrane-bound pyrophosphatase demonstrated by a nonphosphorus allosteric inhibitor . Science Advances 5:5.
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Evgeniy Potapenko, Ciro D. Cordeiro, Guozhong Huang & Roberto Docampo. (2019) Pyrophosphate Stimulates the Phosphate-Sodium Symporter of Trypanosoma brucei Acidocalcisomes and Saccharomyces cerevisiae Vacuoles . mSphere 4:2.
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Evgeniy Potapenko, Ciro D. Cordeiro, Guozhong Huang, Melissa Storey, Christopher Wittwer, Amit K. Dutta, Henning J. Jessen, Vincent J. Starai & Roberto Docampo. (2018) 5-Diphosphoinositol pentakisphosphate (5-IP7) regulates phosphate release from acidocalcisomes and yeast vacuoles. Journal of Biological Chemistry 293:49, pages 19101-19112.
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Rafael Ratajczak & Thea A. Wilkins. 2018. Annual Plant Reviews online. Annual Plant Reviews online 142 184 .
Borka Jojic, Simona Amodeo, Irina Bregy & Torsten Ochsenreiter. (2018) Distinct 3’ UTRs regulate the life-cycle specific expression of two TCTP paralogs in Trypanosoma brucei . Journal of Cell Science.
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Arunima Biswas, Arijit Bhattacharya, Amit Vij & Pijush K. Das. (2017) Role of leishmanial acidocalcisomal pyrophosphatase in the cAMP homeostasis in phagolysosome conditions required for intra-macrophage survival. The International Journal of Biochemistry & Cell Biology 86, pages 1-13.
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Thais Russo-Abrahão, Carolina Macedo Koeller, Michael E. Steinmann, Stephanie Silva-Rito, Thaissa Marins-Lucena, Michele Alves-Bezerra, Naira Ligia Lima-Giarola, Iron Francisco de-Paula, Amaia Gonzalez-Salgado, Erwin Sigel, Peter Bütikofer, Katia Calp Gondim, Norton Heise & José Roberto Meyer-Fernandes. (2017) H+-dependent inorganic phosphate uptake in Trypanosoma brucei is influenced by myo-inositol transporter. Journal of Bioenergetics and Biomembranes 49:2, pages 183-194.
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Natalia Mallo, Jesús Lamas, Ana-Paula de Felipe, Rosa-Ana Sueiro, Francisco Fontenla & José-Manuel Leiro. (2016) Role of H+-pyrophosphatase activity in the regulation of intracellular pH in a scuticociliate parasite of turbot: Physiological effects. Experimental Parasitology 169, pages 59-68.
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Roberto Docampo & Guozhong Huang. (2016) Acidocalcisomes of eukaryotes. Current Opinion in Cell Biology 41, pages 66-72.
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Roberto Docampo. 2016. Inorganic Polyphosphates in Eukaryotic Cells. Inorganic Polyphosphates in Eukaryotic Cells 35 48 .
NATALIA MALLO, JESÚS LAMAS, CARLA PIAZZON & JOSÉ M. LEIRO. (2014) Presence of a plant-like proton-translocating pyrophosphatase in a scuticociliate parasite and its role as a possible drug target. Parasitology 142:3, pages 449-462.
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Guozhong Huang, Paul N. Ulrich, Melissa Storey, Darryl Johnson, Julie Tischer, Javier A. Tovar, Silvia N. J. Moreno, Ron Orlando & Roberto Docampo. (2014) Proteomic Analysis of the Acidocalcisome, an Organelle Conserved from Bacteria to Human Cells. PLoS Pathogens 10:12, pages e1004555.
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André Luiz Fonseca-de-Souza, Anita Leocadio Freitas-Mesquita, Lisvane Paes Vieira, David Majerowicz, Nathalia Daflon-Yunes, Lia Carolina Almeida Soares-de-Medeiros, Kildare Miranda, Katia Calp Gondim & José Roberto Meyer-Fernandes. (2014) Identification and Characterization of an Ecto-Pyrophosphatase Activity in Intact Epimastigotes of Trypanosoma rangeli. PLoS ONE 9:9, pages e106852.
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Roberto Docampo, Silvia N.J. Moreno & Helmut Plattner. (2014) Intracellular calcium channels in protozoa. European Journal of Pharmacology 739, pages 4-18.
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I. Aderiye B.A. Oluwole O.. (2014) How to obtain the organelles of prokaryotic and microbial eukaryotic cells. Journal of Cell and Animal Biology 8:6, pages 95-109.
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Anita Leocadio Freitas-Mesquita, André Luiz Fonseca-de-Souza & José Roberto Meyer-Fernandes. (2014) Leishmania amazonensis: Characterization of an ecto-pyrophosphatase activity. Experimental Parasitology 137, pages 8-13.
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Noelia Lander, Paul N. Ulrich & Roberto Docampo. (2013) Trypanosoma brucei Vacuolar Transporter Chaperone 4 (TbVtc4) Is an Acidocalcisome Polyphosphate Kinase Required for in Vivo Infection. Journal of Biological Chemistry 288:47, pages 34205-34216.
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Roberto Docampo, Veronica Jimenez, Noelia Lander, Zhu-Hong Li & Sayantanee Niyogi. 2013. 69 113 .
Guozhong Huang, Jianmin Fang, Celso Sant'Anna, Zhu-Hong Li, Dianne L. Wellems, Peter Rohloff & Roberto Docampo. (2011) Adaptor Protein-3 (AP-3) Complex Mediates the Biogenesis of Acidocalcisomes and Is Essential for Growth and Virulence of Trypanosoma brucei. Journal of Biological Chemistry 286:42, pages 36619-36630.
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Roberto Docampo & Silvia N.J. Moreno. (2011) Acidocalcisomes. Cell Calcium 50:2, pages 113-119.
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Peter Rohloff, Kildare Miranda, Juliany C. F. Rodrigues, Jianmin Fang, Melina Galizzi, Helmut Plattner, Joachim Hentschel & Silvia N. J. Moreno. (2011) Calcium Uptake and Proton Transport by Acidocalcisomes of Toxoplasma gondii. PLoS ONE 6:4, pages e18390.
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Parvinder K. AleyAnna M. Mikolajczyk, Barbara Munz, Grant C. ChurchillAntony GalioneFelicitas Berger. (2010) Nicotinic acid adenine dinucleotide phosphate regulates skeletal muscle differentiation via action at two-pore channels. Proceedings of the National Academy of Sciences 107:46, pages 19927-19932.
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Isabela B. Ramos, Kildare Miranda, Douglas A. PaceKatherine C. VerbistFu-Yang LinYonghui ZhangEric OldfieldEdnildo A. Machado, Wanderley De Souza & Roberto Docampo. (2010) Calcium- and polyphosphate-containing acidic granules of sea urchin eggs are similar to acidocalcisomes, but are not the targets for NAADP. Biochemical Journal 429:3, pages 485-495.
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Roberto Docampo, Paul Ulrich & Silvia N. J. Moreno. (2010) Evolution of acidocalcisomes and their role in polyphosphate storage and osmoregulation in eukaryotic microbes. Philosophical Transactions of the Royal Society B: Biological Sciences 365:1541, pages 775-784.
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SILVIA N. J. MORENO & ROBERTO DOCAMPO. (2009) The Role of Acidocalcisomes in Parasitic Protists. Journal of Eukaryotic Microbiology 56:3, pages 208-213.
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Lucimar S. Motta, Isabela B. Ramos, Fabio M. Gomes, Wanderley de Souza, Donald E. Champagne, Marcelo F. Santiago, Roberto Docampo, Kildare Miranda & Ednildo A. Machado. (2009) Proton-pyrophosphatase and polyphosphate in acidocalcisome-like vesicles from oocytes and eggs of Periplaneta americana. Insect Biochemistry and Molecular Biology 39:3, pages 198-206.
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María Laura Salto, Theresa Kuhlenschmidt, Mark Kuhlenschmidt, Rosa M. de Lederkremer & Roberto Docampo. (2008) Phospholipid and glycolipid composition of acidocalcisomes of Trypanosoma cruzi. Molecular and Biochemical Parasitology 158:2, pages 120-130.
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Sébastien Besteiro, Daniela Tonn, Laurence Tetley, Graham H. Coombs & Jeremy C. Mottram. (2008) The AP3 adaptor is involved in the transport of membrane proteins to acidocalcisomes of Leishmania . Journal of Cell Science 121:5, pages 561-570.
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Wanderley de Souza, José Andrés Morgado-Diaz & Narcisa L. Cunha-e-Silva. 2008. 2D PAGE: Sample Preparation and Fractionation. 2D PAGE: Sample Preparation and Fractionation 313 331 .
Jianmin FangPeter RohloffKildare MirandaRoberto Docampo. (2007) Ablation of a small transmembrane protein of Trypanosoma brucei (TbVTC1) involved in the synthesis of polyphosphate alters acidocalcisome biogenesis and function, and leads to a cytokinesis defect . Biochemical Journal 407:2, pages 161-170.
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Melissa J. Rodgers, Joseph P. Albanesi & Margaret A. Phillips. (2007) Phosphatidylinositol 4-Kinase III-β Is Required for Golgi Maintenance and Cytokinesis in Trypanosoma brucei . Eukaryotic Cell 6:7, pages 1108-1118.
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Anthony J. MorganAntony Galione. (2007) NAADP induces pH changes in the lumen of acidic Ca2+ stores. Biochemical Journal 402:2, pages 301-310.
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Shuhong Luo, Jianmin Fang & Roberto Docampo. (2006) Molecular Characterization of Trypanosoma brucei P-type H+-ATPases. Journal of Biological Chemistry 281:31, pages 21963-21973.
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Norma Marchesini, Mauricio Vieira, Shuhong Luo, Silvia N.J. Moreno & Roberto Docampo. (2005) A Malaria Parasite-encoded Vacuolar H+-ATPase Is Targeted to the Host Erythrocyte. Journal of Biological Chemistry 280:44, pages 36841-36847.
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Bernardo Luiz Moraes Moreira, Lia Carolina A. Soares Medeiros, Kildare Miranda, Wanderley de Souza, Joachim Hentschel, Helmut Plattner & Hector Barrabin. (2005) Kinetics of pyrophosphate-driven proton uptake by acidocalcisomes of Leptomonas wallacei. Biochemical and Biophysical Research Communications 334:4, pages 1206-1213.
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Megumi Hirono, Hisatoshi Mimura, Yoichi Nakanishi & Masayoshi Maeshima. (2005) Expression of Functional Streptomyces coelicolor H+-Pyrophosphatase and Characterization of Its Molecular Properties. The Journal of Biochemistry 138:2, pages 183-191.
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Lia Carolina A. Soares Medeiros, Bernardo Luis Moraes Moreira, Kildare Miranda, Wanderley de Souza, Helmut Plattner, Joachim Hentschel & Hector Barrabin. (2005) A proton pumping pyrophosphatase in acidocalcisomes of Herpetomonas sp.. Molecular and Biochemical Parasitology 140:2, pages 175-182.
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Roberto Docampo, Wanderley de Souza, Kildare Miranda, Peter Rohloff & Silvia N. J. Moreno. (2005) Acidocalcisomes ? conserved from bacteria to man. Nature Reviews Microbiology 3:3, pages 251-261.
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Felix A. Ruiz, Christopher R. Lea, Eric Oldfield & Roberto Docampo. (2004) Human Platelet Dense Granules Contain Polyphosphate and Are Similar to Acidocalcisomes of Bacteria and Unicellular Eukaryotes. Journal of Biological Chemistry 279:43, pages 44250-44257.
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Kildare Miranda, Claudia O. Rodrigues, Joachim Hentchel, Anibal Vercesi, Helmut Plattner, Wanderley de Souza & Roberto Docampo. (2004) Acidocalcisomes of Phytomonas françai Possess Distinct Morphological Characteristics and Contain Iron . Microscopy and Microanalysis 10:5, pages 647-655.
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Guillaume Lemercier, Benoit Espiau, Felix A. Ruiz, Mauricio Vieira, Shuhong Luo, Theo Baltz, Roberto Docampo & Norbert Bakalara. (2004) A Pyrophosphatase Regulating Polyphosphate Metabolism in Acidocalcisomes Is Essential for Trypanosoma brucei Virulence in Mice. Journal of Biological Chemistry 279:5, pages 3420-3425.
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Manfredo Seufferheld, Mauricio C.F. Vieira, Felix A. Ruiz, Claudia O. Rodrigues, Silvia N.J. Moreno & Roberto Docampo. (2003) Identification of Organelles in Bacteria Similar to Acidocalcisomes of Unicellular Eukaryotes. Journal of Biological Chemistry 278:32, pages 29971-29978.
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Wanderley de Souza & Narcisa Leal da Cunha-e-Silva. (2003) Cell fractionation of parasitic protozoa: a review. Memórias do Instituto Oswaldo Cruz 98:2, pages 151-170.
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Kevin J. Saliba, Richard J.W. Allen, Stephanie Zissis, Patrick G. Bray, Stephen A. Ward & Kiaran Kirk. (2003) Acidification of the Malaria Parasite's Digestive Vacuole by a H+-ATPase and a H+-pyrophosphatase. Journal of Biological Chemistry 278:8, pages 5605-5612.
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Yolanda M. Drozdowicz, Michael Shaw, Manami Nishi, Boris Striepen, Helene A. Liwinski, David S. Roos & Philip A. Rea. (2003) Isolation and Characterization of TgVP1, a Type I Vacuolar H+-translocating Pyrophosphatase fromToxoplasma gondii. Journal of Biological Chemistry 278:2, pages 1075-1085.
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Claudia O. Rodrigues, Felix A. Ruiz, Peter Rohloff, David A. Scott & Silvia N.J. Moreno. (2002) Characterization of Isolated Acidocalcisomes from Toxoplasma gondii Tachyzoites Reveals a Novel Pool of Hydrolyzable Polyphosphate. Journal of Biological Chemistry 277:50, pages 48650-48656.
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Claudia O. Rodrigues, Felix A. Ruiz, Mauricio Vieira, Janet E. Hill & Roberto Docampo. (2002) An Acidocalcisomal Exopolyphosphatase from Leishmania major with High Affinity for Short Chain Polyphosphate. Journal of Biological Chemistry 277:52, pages 50899-50906.
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M Mendoza, A Mijares, H Rojas, J.P Rodrı́guez, J.A Urbina & R DiPolo. (2002) Physiological and morphological evidences for the presence acidocalcisomes in Trypanosoma evansi. Molecular and Biochemical Parasitology 125:1-2, pages 23-33.
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Guillaume Lemercier, Sandrine Dutoya, Shuhong Luo, Felix A. Ruiz, Claudia O. Rodrigues, Théo Baltz, Roberto Docampo & Norbert Bakalara. (2002) A Vacuolar-type H+-Pyrophosphatase Governs Maintenance of Functional Acidocalcisomes and Growth of the Insect and Mammalian Forms of Trypanosoma brucei. Journal of Biological Chemistry 277:40, pages 37369-37376.
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Narcisa L Cunha-e-Silva, Geórgia C Atella, Isabel A Porto-Carreiro, Jose A Morgado-Diaz, Miria G Pereira & Wanderley Souza. (2002) Isolation and characterization of a reservosome fraction from Trypanosoma cruzi . FEMS Microbiology Letters 214:1, pages 7-12.
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Benjamin Moreno, Claudia O Rodrigues, Brian N Bailey, Julio A Urbina, Silvia N.J Moreno, Roberto Docampo & Eric Oldfield. (2002) Magic-angle spinning 31 P NMR spectroscopy of condensed phosphates in parasitic protozoa: visualizing the invisible . FEBS Letters 523:1-3, pages 207-212.
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José R Pérez-Castiñeira, Jorge Alvar, Luis M Ruiz-Pérez & Aurelio Serrano. (2002) Evidence for a wide occurrence of proton-translocating pyrophosphatase genes in parasitic and free-living protozoa. Biochemical and Biophysical Research Communications 294:3, pages 567-573.
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Norma Marchesini, Felix A. Ruiz, Mauricio Vieira & Roberto Docampo. (2002) Acidocalcisomes Are Functionally Linked to the Contractile Vacuole of Dictyostelium discoideum. Journal of Biological Chemistry 277:10, pages 8146-8153.
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Michael T. McIntosh & Akhil B. Vaidya. (2002) Vacuolar type H+ pumping pyrophosphatases of parasitic protozoa. International Journal for Parasitology 32:1, pages 1-14.
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Sandrine Dutoya, Stephanie Gibert, Guillaume Lemercier, Xavier Santarelli, Dominique Baltz, Theo Baltz & Norbert Bakalara. (2001) A Novel C-terminal Kinesin Is Essential for Maintaining Functional Acidocalcisomes in Trypanosoma brucei. Journal of Biological Chemistry 276:52, pages 49117-49124.
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CLAUDIA O. RODRIGUES, ROSANA CATISTI, SERGIO A. UYEMURA, ANIBAL E. VERCESI, RENEE LIRA, CARLOS RODRIGUEZ, JULIO A. URBINA & ROBERTO DOCAMPO. (2001) The Sterol Composition of Trypanosoma cruzi Changes After Growth in Different Culture Media and Results in Different Sensitivity to Digitonin-Permeabilization. The Journal of Eukaryotic Microbiology 48:5, pages 588-594.
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Christina M. Szabo & Eric Oldfield. (2001) An Investigation of Bisphosphonate Inhibition of a Vacuolar Proton-Pumping Pyrophosphatase. Biochemical and Biophysical Research Communications 287:2, pages 468-473.
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Felix A. Ruiz, Claudia O. Rodrigues & Roberto Docampo. (2001) Rapid Changes in Polyphosphate Content within Acidocalcisomes in Response to Cell Growth, Differentiation, and Environmental Stress inTrypanosoma cruzi. Journal of Biological Chemistry 276:28, pages 26114-26121.
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WANDERLEY DE SOUZA, ISABEL PORTO CARREIRO, KILDARE MIRANDA & NARCISA L. CUNHA E SILVA. (2000) Two special organelles found in Trypanosoma cruzi. Anais da Academia Brasileira de Ciências 72:3, pages 421-432.
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Benjamin Moreno, Julio A. Urbina, Eric Oldfield, Brian N. Bailey, Claudia O. Rodrigues & Roberto Docampo. (2000) 31P NMR Spectroscopy of Trypanosoma brucei, Trypanosoma cruzi, and Leishmania major. Journal of Biological Chemistry 275:37, pages 28356-28362.
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David A. Scott & Roberto Docampo. (2000) Characterization of Isolated Acidocalcisomes of Trypanosoma cruzi. Journal of Biological Chemistry 275:31, pages 24215-24221.
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Anibal E. Vercesi, Claudia O. Rodrigues, Rosana Catisti & Roberto Docampo. (2000) Presence of a Na + /H + exchanger in acidocalcisomes of Leishmania donovani and their alkalization by anti-leishmanial drugs . FEBS Letters 473:2, pages 203-206.
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Jaap J. Van Hellemond, Philippe Neuville, Ralph T. Schwarz, Keith R. Matthews & Jeremy C. Mottram. (2000) Isolation of Trypanosoma brucei CYC2 andCYC3 Cyclin Genes by Rescue of a Yeast G1Cyclin Mutant. Journal of Biological Chemistry 275:12, pages 8315-8323.
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Rosana Catisti, Sergio A Uyemura, Roberto Docampo & Anibal E Vercesi. (2000) Calcium mobilization by arachidonic acid in trypanosomatids. Molecular and Biochemical Parasitology 105:2, pages 261-271.
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R Docampo & S.N.J Moreno. (1999) Acidocalcisome: A Novel Ca2+ Storage Compartment in Trypanosomatids and Apicomplexan Parasites. Parasitology Today 15:11, pages 443-448.
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