25
Views
70
CrossRef citations to date
0
Altmetric
Cell and Organelle Structure and Assembly

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

, &
Pages 7712-7723 | Received 25 May 1999, Accepted 23 Aug 1999, Published online: 28 Mar 2023

REFERENCES

  • Balscheffsky, M., S. Nadanaciva, and J. Schultz 1998. A pyrophosphatase synthase gene: molecular cloning and sequencing of the cDNA encoding the inorganic pyrophosphate synthase from Rhodospirillum rubrum. Biochim. Biophys. Acta 1364:301–306.
  • Böhler, P., S. Stein, W. Dairman, and J. Udenfriend 1973. Fluorometric assay of proteins in the nanogram range. Arch. Biochem. Biophys. 155:213–220.
  • Bowman, B. J., and J. Bowman 1986. H+-ATPases from mitochondria, plasma membranes, and vacuoles of fungal cells. J. Membr. Biol. 94:83–97.
  • Brightman, A. O., P. Navas, N. M. Minnifield, and J. Morré 1992. Pyrophosphate-induced acidification of trans cisternal elements of rat liver Golgi apparatus. Biochim. Biophys. Acta Bio-Membr. 1104:188–194.
  • Brun, R., and J. Schönenberg 1979. Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop. 36:289–292.
  • Cazzulo, J. J., E. Valle, R. Docampo, and J. Cannata 1980. Intracellular distribution of CO2 fixing enzymes in Trypanosoma cruzi and Crithidia fasciculata. J. Gen. Microbiol. 117:271–274.
  • Coppens, I., P. Baudhin, F. R. Opperdoes, and J. Courtoy 1993. Role of acidic compartments in Trypanosoma brucei, with special reference to low-density lipoprotein processing. Mol. Biochem. Parasitol. 58:223–232.
  • Coppens, I., and J. Courtoy 1995. Exogenous and endogenous sources of sterols in the culture-adapted procyclic trypomastigotes of Trypanosoma brucei. Mol. Biochem. Parasitol. 73:179–188.
  • Coppens, I., T. Levade, and J. Courtoy 1995. Host plasma low density lipoprotein particles as an essential source of lipids for the bloodstream forms of Trypanosoma brucei. J. Biol. Chem. 270:5736–5741.
  • Cross, G. A. M. 1975. Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitology 71:393–417.
  • Diaz, R., and J. Stahl 1989. Digitonin permeabilization procedures for the study of endosome acidification and function. Methods Cell Biol. 31:25–43.
  • Docampo, R., D. A. Scott, A. E. Vercesi, and J. Moreno 1995. Intracellular Ca2+ storage in acidocalcisomes of Trypanosoma cruzi. Biochem. J. 310:1005–1012.
  • Dröse, S., and J. Altendorf 1997. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol. 200:1–8.
  • Dvorak, J. A., J. C. Engel, R. D. Leapman, C. R. Swyt, and J. Pella 1988. Trypanosoma cruzi: elemental composition heterogeneity of cloned stocks. Mol. Biochem. Parasitol. 31:19–26.
  • Finbow, M., and J. Harrison 1997. The vacuolar H+-ATPase: a universal proton pump of eukaryotes. Biochem. J. 324:697–712.
  • Forgac, M. 1998. Structure, function and regulation of the vacuolar (H+)-ATPases. FEBS Lett. 440:258–263.
  • Harvey, W. R., and J. Wieczorek 1997. Animal plasma membrane energization by chemiosmotic H+ V-ATPases. J. Exp. Biol. 200:203–216.
  • Ikeda, M., M. D. Rahman, C. Moritani, K. Umami, Y. Tanimura, R. Akagi, Y. Tanaka, M. Maeshima, and J. Watanabe 1999. A vacuolar H+-pyrophosphatase in Acetabularia acetabulum: molecular cloning and comparison with higher plants and a bacterium. J. Exp. Bot. 50:139–140.
  • Jenkins, W. T. 1991. The pyruvate kinase-coupled assay for ATPases, a critical analysis. Anal. Biochem. 194:136–139.
  • LeFurgey, A., P. Ingram, and J. Blum 1990. Elemental composition of polyphosphate-containing vacuoles and cytoplasm of Leishmania major. Mol. Biochem. Parasitol. 40:77–86.
  • Leriche, M. A., and J. Dubremetz 1991. Characterization of the protein content of rhoptries and dense granules of Toxoplasma gondii tachyzoites by subcellular fractionation and monoclonal antibodies. Mol. Biochem. Parasitol. 45:249–260.
  • Lichko, L., and J. Okorokov 1991. Purification and some properties of membrane bound and soluble pyrophosphatase of yeast vacuoles. Yeast 7:805–812.
  • Lu, H.-G., L. Zhong, K. P. Chang, and J. Docampo 1997. Intracellular Ca2+ pool content and signaling, and expression of a calcium pump are linked to virulence in Leishmania mexicana amazonensis. J. Biol. Chem. 272:9464–9473.
  • Lu, H.-G., L. Zhong, W. de Souza, M. Benchimol, S. N. J. Moreno, and J. Docampo 1998. Ca2+ content and expression of an acidocalcisomal calcium pump are elevated in intracellular forms of Trypanosoma cruzi. Mol. Cell. Biol. 18:2309–2323.
  • Lundin, M., S. W. Deopujari, L. Lichko, L. Pereira da Silva, and J. Baltscheffsky 1992. Characterization of a mitochondrial inorganic pyrophosphatase in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1098:217–223.
  • Macri, F., and J. Vianello 1987. ADP- or pyrophosphate-dependent proton pumping of pea tonoplast-enriched vesicles. FEBS Lett. 215:47–52.
  • Macri, F., M. Zancani, E. Petrussa, P. Dell’Antone, and J. Vianello 1995. Pyrophosphate and H+-pyrophosphatase maintain the vacuolar proton gradient in metabolic inhibitor-treated Acer pseudoplatanus cells. Biochim. Biophys. Acta 1229:323–328.
  • Mellman, I., R. Fuchs, and J. Helenius 1986. Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55:663–700.
  • Michels, P. A. M., N. Chevalier, F. R. Opperdoes, M. H. Rider, and J. Rigden 1997. The glycosomal ATP-dependent phosphofructokinase of Trypanosoma brucei must have evolved from an ancestral pyrophosphate-dependent enzyme. Eur. J. Biochem. 250:698–704.
  • Moreno, S. N. J., and J. Zhong 1996. Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem. J. 313:655–659.
  • Ochoa, S. 1955. Isocitric deshydrogenase system (TPN) from pig heart. Methods Enzymol. 1:699–704.
  • Padh, H., M. Lavasa, and J. Steck 1991. Endosomes are acidified by association with discrete proton-pumping vacuoles in Dictyostelium. J. Biol. Chem. 266:5514–5520.
  • Rea, P. A., and J. Poole 1993. Vacuolar H+-translocating pyrophosphatase. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:157–180.
  • Rodrigues, C. O., D. A. Scott, and J. Docampo 1999. Presence of a vacuolar H+-pyrophosphatase in promastigotes of Leishmania donovani and its localization to a different compartment from the vacuolar H+-ATPase. Biochem. J. 340:759–766.
  • Scott, D. A., S. N. J. Moreno, and J. Docampo 1995. Ca2+ storage in Trypanosoma brucei: the influence of cytoplasmic pH and importance of vacuolar acidity. Biochem. J. 310:780–794.
  • Scott, D. A., and J. Docampo 1998. Two types of H+-ATPase are involved in the acidification of internal compartments in Trypanosoma cruzi. Biochem. J. 331:583–589.
  • Scott, D. A., R. Docampo, J. A. Dvorak, S. Shi, and J. Leapman 1997. In situ compositional analysis of acidocalcisomes in Trypanosoma cruzi. J. Biol. Chem. 272:28020–28029.
  • Scott, D. A., W. de Souza, M. Benchimol, L. Zhong, H.-G. Lu, S. N. J. Moreno, and J. Docampo 1998. Presence of a plant-like proton-pumping pyrophosphatase in acidocalcisomes of Trypanosoma cruzi. J. Biol. Chem. 273:22151–22158.
  • Solioz, M. 1984. Dicyclohexylcarbodiimide as a probe for proton translocating enzymes. Trends Biochem. Sci. 9:309–312.
  • Steiger, R. F., F. R. Opperdoes, and J. Bontemps 1980. Subcellular fractionation of Trypanosoma brucei bloodstream forms with special reference to hydrolases. Eur. J. Biochem. 105:163–175.
  • UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases. 1997. Tropical disease research: progress 1995–1996: thirteenth programme report of the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases. World Health Organization, Geneva, Switzerland.
  • Vercesi, A. E., S. N. J. Moreno, and J. Docampo 1994. Ca2+/H+ exchange in acidic vacuoles of Trypanosoma brucei. Biochem. J. 304:227–233.
  • Vercesi, A. E., and J. Docampo 1996. Sodium-proton exchange stimulates Ca2+ release from acidocalcisomes of Trypanosoma brucei. Biochem. J. 315:265–270.
  • Vercesi, A. E., M. Grijalba, and J. Docampo 1997. Inhibition of Ca2+ release from Trypanosoma brucei acidocalcisomes by 3,5-dibutyl-4-hydroxytoluene: role of the Na+/H+ exchanger. Biochem. J. 328:479–482.
  • Vickerman, K., and J. Tetley 1977. Recent ultrastructural studies on trypanosomes. Ann. Soc. Belge Med. Trop. 57:441–455.
  • Waggoner, A. S. 1988. Mechanisms of membrane potential probes, p. 211–215. In R. Gunn, J. L. Parker (ed.), Cell physiology of blood The Rockefeller University Press, New York, N.Y.
  • Wang, Y., R. A. Leigh, K. H. Kaestner, and J. Sze 1986. Electrogenic H+-pumping pyrophosphatase in tonoplast vesicles of oat root. Plant Physiol. 81:497–502.
  • Webb, M. R. 1992. A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc. Natl. Acad. Sci. USA 89:4884–4887.
  • Williamson, J., and J. McLaren 1981. Localization of phosphatases in Trypanosoma rhodesiense. J. Protozool. 28:460–467.
  • Zhen, R.-G., A. A. Baykov, N. P. Bakuleva, and J. Rea 1994. Aminomethylenediphosphonate: a potent type-specific inhibitor of both plant and phototrophic bacterial H+-pyrophosphatases. Plant Physiol. 104:153–159.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.