Abstract
Recent work has shown that acidocalcisomes, which are electron-dense acidic organelles rich in calcium and polyphosphate, are the only organelles that have been conserved during evolution from prokaryotes to eukaryotes. Acidocalcisomes were first described in trypanosomatids and have been characterized in most detail in these species. Acidocalcisomes have been linked with several functions, including storage of cations and phosphorus, polyphosphate metabolism, calcium homeostasis, maintenance of intracellular pH homeostasis and osmoregulation. Here, we review acidocalcisome ultrastructure, composition and function in different trypanosomatids and other organisms.
Key Points
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Acidocalcisomes are acidic and dense organelles ? both by weight and by electron microscopy ? with a high concentration of phosphorus present as pyrophosphate and polyphosphate (poly P) that is complexed with calcium, and other elements.
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Acidocalcisomes are related to organelles previously named volutin or metachromatic granules, and polyphosphate vacuoles, which were thought to function as storage granules.
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The acidocalcisome membrane can contain several pumps (Ca2+-ATPase, V-H+-ATPase, V-H+-PPase), exchangers (Na+/H+, Ca2+/H+), and channels (aquaporins), while its matrix contains enzymes related to pyrophosphate and polyphosphate metabolism (exopolyphosphatase, polyphosphate kinase, pyrophosphatase).
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After their identification in trypanosomatids, acidocalcisomes were found in other microorganisms such as Toxoplasma gondii, Plasmodium spp., the green alga Chlamydomonas reinhardtii, and the slime mould Dictyostelium discoideum. The recent identification of acidocalcisomes in bacteria (Agrobacterium tumefaciens, Rhodospirillum rubrum) and the finding that human platelet dense granules are homologous to acidocalcisomes, indicates that these organelles have been conserved during evolution from bacteria to humans.
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Acidocalcisomes have been linked with several functions, including storage of cations and phosphorus, polyphosphate metabolism, calcium homeostasis, maintenance of intracellular pH homeostasis, and osmoregulation. This review describes acidocalcisome ultrastructure, composition and function in different trypanosomatids with an overview of our knowledge of the organelle in other organisms.
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References
Urbina, J. A. & Docampo, R. Specific chemotherapy of Chagas disease: controversies and advances. Trends Parasitol. 19, 495–501 (2003).
Croft, S. L. & Coombs, G. H. Leishmaniasis ? current chemotherapy and recent advances in the search for new drugs. Trends Parasitol. 19, 502–508 (2003).
Fairlamb, A. Chemotherapy of human African trypanosomiasis: current and future prospects. Trends Parasitol. 19, 488–494 (2003).
Camargo, E. P. Phytomonas and other trypanosomatid parasites of plants and fruits. Adv. Parasitol. 42, 29–112 (1999).
Vercesi, A. E., Moreno, S. N. J. & Docampo, R. Ca2+/H+ exchange in acidic vacuoles of Trypanosoma brucei. Biochem. J. 304, 227–233 (1994).
Docampo, R., Scott, D. A., Vercesi, A. E. & Moreno, S. N. J. Intracellular Ca2+ storage in acidocalcisomes of Trypanosoma cruzi. Biochem. J. 310, 1005–1012 (1995).
Docampo, R. & Moreno, S. N. J. Acidocalcisome: a novel Ca2+ storage compartment in trypanosomatids and apicomplexan parasites. Parasitol. Today 15, 443–448 (1999).
Meyer, A. Orientierende untersuchungen über verbreitung. Morphologie, und chemie des volutins. Bot. Zeit. 62, 113–152 (1904).
Kornberg, A. Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J. Bacteriol. 177, 491–496 (1995).
Jensen, T. E. in Ultrastructure of Microalgae (ed. Berner, T.) 7–50 (CRC Press, Boca Raton, Florida, 1993).
Moreno, S. N. J. & Zhong, L. Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem. J. 313, 655–659 (1996).
Garcia, C. R. et al. Acidic calcium pools in intraerythrocytic malaria parasites. Eur. J. Cell Biol. 76, 133–138 (1998).
Luo, S., Marchesini, N., Moreno, S. N. J. & Docampo, R. A plant-like vacuolar H+-pyrophosphatase in Plasmodium falciparum. FEBS Lett. 460, 217–220 (1999).
Marchesini, N., Luo, S., Rodrigues, C. O., Moreno, S. N. J. & Docampo, R. Acidocalcisomes and a vacuolar H+-pyrophosphatase in malaria parasites. Biochem. J. 347, 243–253 (2000).
Ruiz, F. A., Marchesini, N., Seufferheld, M., Govindjee & Docampo, R. The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton pumping pyrophosphatase and are similar to acidocalcisomes. J. Biol. Chem. 276, 46196–46203 (2001).
Marchesini, N., Ruiz, F. A., Vieira, M. & Docampo, R. Acidocalcisomes are functionally linked to the contractile vacuole of Dictyostelium discoideum. J. Biol. Chem. 277, 8146–8153 (2002).
Seufferheld, M. et al. Identification in bacteria of organelles similar to acidocalcisomes of unicellular eukaryotes. J. Biol. Chem. 278, 29971–29978 (2003). First report of membrane-bound acidocalcisomes in bacteria, which were identified by X-ray microanalysis, subcellular fractionation and fluorescence and electron microscopy.
Seufferheld, M., Lea, C. R., Vieira, M., Oldfield, E. & Docampo, R. The H+-pyrophosphatase of Rhodospirillum rubrum is predominantly located in polyphosphate-rich acidocalcisomes. J. Biol. Chem. 279, 51193–51202 (2004).
Ruiz, F. A., Lea, C. R., Oldfield, E. & Docampo, R. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J. Biol. Chem. 279, 44250–44267 (2004). Shows that human platelet dense granules have morphological and structural similarities to acidocalcisomes, and contain polyphosphate that was released on thrombin stimulation.
Scott, D. A. & Docampo, R. Characterization of isolated acidocalcisomes of Trypanosoma cruzi. J. Biol. Chem. 275, 24215–22421 (2000). The purification method of acidocalcisomes using iodixanol gradient centrifugation was developed.
De Souza, W. Basic cell biology of Trypanosoma cruzi. Curr. Pharm. Design 8, 269–285 (2002).
Miranda, K. et al. Acidocalcisomes of Phytomonas françai possess distinct morphological characteristics and contain iron. Microsc. Microanal. 10, 647–655 (2004).
Lu, H. -G. et al. Ca2+ content and expression of an acidocalcisomal calcium pump are elevated in intracellular forms of Trypanosoma cruzi. Mol. Cell. Biol. 18, 2309–2323 (1998). First report of a PMCA-type Ca2+-ATPase in acidocalcisomes. The gene was cloned, sequenced, expressed and shown to complement yeast deficient in PMC1 , and the protein was shown to localize in acidocalcisomes.
Miranda, K., Benchimol, M., Docampo, R. & de Souza, W. The fine structure of acidocalcisomes of Trypanosoma cruzi. Parasitol. Res. 86, 373–384 (2000).
Scott, D. A., Docampo, R., Dvorak, J. A., Shi, S. & Leapman, R. D. In situ compositional analysis of acidocalcisomes of Trypanosoma cruzi. J. Biol Chem. 272, 28020–28029 (1997). Quantitative analysis of the elemental composition of acidocalcisomes. On the basis of the response to ionophores it was established that acidocalcisomes correspond to the electron-dense organelles previously identified in trypanosomes.
Miranda, K. et al. Dynamics of polymorphism of acidocalcisomes in Leishmania parasites. Histochem. Cell Biol. 121, 407–418 (2004).
Miranda, K., Docampo, R., Grillo, O. & de Souza, W. Acidocalcisomes of trypanosomatids have species-specific elemental composition. Protist 155, 395–405 (2004).
Rodrigues, C. O., Scott, D. A. & Docampo, R. Characterization of a vacuolar pyrophosphatase in Trypanosoma brucei and its localization to acidocalcisomes. Mol. Cell. Biol. 19, 7712–7723 (1999).
Ruiz, F. A., Luo, S., Moreno, S. N. J. & Docampo, R. Polyphosphate content and fine structure of acidocalcisomes of Plasmodium falciparum. Microsc. Microanal. 10, 563–567 (2004).
Montalvetti, A., Rohloff, P. & Docampo, R. A functional aquaporin co-localizes with the vacuolar proton pyrophosphatase to acidocalcisomes and the contractile vacuole complex of Trypanosoma cruzi. J. Biol. Chem. 279, 38673–38682 (2004).
Luo, S., Rohloff, P., Cox, J., Uyemura, S. A. & Docampo, R. Trypanosoma brucei plasma membrane-type Ca2+-ATPase 1 (TbPMC1) and 2 (TbPMC2) genes encode functional Ca2+-ATPases localized to the acidocalcisomes and plasma membrane, and essential for Ca2+ homeostasis and growth. J. Biol. Chem. 279, 14427–14439 (2004).
Luo, S., Vieira, M., Graves, J., Zhong, L. & Moreno, S. N. J. A plasma membrane-type Ca2+-ATPase co-localizes with a vacuolar H+-pyrophosphatase to acidocalcisomes of Toxoplasma gondii. EMBO J. 20, 55–64 (2001). Identification of a Ca2+-ATPase and its co-localization with the V-H+-PPase in acidocalcisomes of T. gondii.
Moniakis, J., Coukell, M. B. & Forer, A. Molecular cloning of an intracellular P-type ATPase from Dictyostelium that is up-regulated in calcium-adapted cells. J. Biol. Chem. 270, 28276–29281 (1995).
Cunningham, K. W. & Fink, G. R. Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases. J. Cell Biol. 124, 351–363 (1994).
Ghosh, S. K., Rosenthal, B., Rogers, R. & Samuelson, J. Vacuolar localization of an Entamoeba histolytica homologue of the plasma membrane ATPase (PMCA). Mol. Biochem. Parasitol. 108, 125–130 (2000).
Bowman, E. J., Siebers, A. & Altendorf, K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl Acad. Sci. USA 85, 7972–7976 (1988).
Scott, D. A., Moreno, S. N. J. & Docampo, R. Ca2+ storage in Trypanosoma brucei: the influence of cytoplasmic pH and importance of vacuolar acidity. Biochem. J. 310, 789–794 (1995).
Lu, H. -G. et al. 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 (1997).
Mendoza, M. et al. Physiological and morphological evidences for the presence of acidocalcisomes in Trypanosoma evansi: single cell fluorescence and 31P NMR studies. Mol. Biochem. Parasitol. 125, 23–33 (2002).
Benchimol, M. et al. Functional expression of a vacuolar-type H+-ATPase in the plasma membrane and intracellular vacuoles of Trypanosoma cruzi. Biochem. J. 332, 695–702 (1998).
Scott, D. A. et al. Presence of a plant-like proton-pumping pyrophosphatase in acidocalcisomes of Trypanosoma cruzi. J. Biol. Chem. 273, 22151–22158 (1998). First report and biochemical characterization of a V-H+-PPase in a unicellular eukaryotic parasite.
Lemercier, G. et al. A vacuolar-type H+ pyrophosphatase governs maintenance of functional acidocalcisomes and growth of the insect and bloodstream forms of Trypanosoma brucei. J. Biol. Chem. 277, 37369–37376 (2002).
Rodrigues, C. O., Scott, D. A. & Docampo, R. 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 (1999).
Rodrigues, C. O. et al. Vacuolar proton pyrophosphatase activity and pyrophosphate (PPi) in Toxoplasma gondii as possible chemotherapeutic targets. Biochem. J. 349, 737–745 (2000).
Hill, J., Scott, D. A., Luo, S. & Docampo, R. Cloning and functional expression of a gene encoding a vacuolar-type proton-translocating pyrophosphatase from Trypanosoma cruzi. Biochem. J. 351, 281–288 (2000). First cloning and functional expression of a V-H+-PPase from an organism that is neither a bacteria or plant.
Rodrigues, C. O., Ruiz, F. A., Rohloff, P., Scott, D. A. & Moreno, S. N. J. Characterization of isolated acidocalcisomes from Toxoplasma gondii tachyzoites reveals a novel pool of hydrolysable polyphosphate. J. Biol. Chem. 277, 48650–48656 (2002).
Martinez, R. et al. A proton pumping pyrophosphatase in the Golgi apparatus and plasma membrane vesicles of Trypanosoma cruzi. Mol. Biochem. Parasitol. 120, 205–213 (2002).
Vercesi, A. E. & Docampo, R. Sodium-proton exchange stimulates Ca2+ release from acidocalcisomes of Trypanosoma brucei. Biochem. J. 315, 265–270 (1996).
Vercesi, A. E., Grijalba, M. T. & Docampo, R. Inhibition of Ca2+ release from Trypanosoma brucei acidocalcisomes by 3,5-dibutyl-4-hydroxytoluene (BHT): role of the Na+/H+ exchange. Biochem. J. 328, 479–482 (1997).
Vercesi, A. E., Rodrigues, C. O., Catisti, R. & Docampo, R. Presence of a Na+/H+ exchanger in acidocalcisomes of Leishmania donovani and their alkalization by anti-leishmanial agents. FEBS Lett. 473, 203–206 (2000).
Moreno, S. N. J., Docampo, R. & Vercesi, A. E. Calcium homeostasis in procyclic and bloodstream forms of Trypanosoma brucei. Lack of inositol 1,4,5-trisphosphate-sensitive Ca2+ release. J. Biol. Chem. 267, 6020–6026 (1992).
Moreno, S. N. J., Vercesi, A. E., Pignataro, O. P. & Docampo, R. Calcium homeostasis in Trypanosoma cruzi amastigotes. Presence of inositol phosphates and lack of an inositol 1,4,5-trisphosphate-sensitive calcium pool. Mol. Biochem. Parasitol. 52, 251–262 (1992).
Docampo, R., Moreno, S. N. J. & Vercesi, A. E. Effect of thapsigargin on calcium homeostasis in Trypanosoma cruzi trypomastigotes and epimastigotes. Mol. Biochem. Parasitol. 59, 305–314 (1993).
Urbina, J. A. et al. Trypanosoma cruzi contains major pyrophosphate stores and its growth in vitro and in vivo is blocked by pyrophosphate analogs. J. Biol. Chem. 274, 33609–33615 (1999). Pyrophosphate is found in trypanosomes at greater concentrations than ATP and localized in acidocalcisomes, which establishes pyrophosphate metabolism as a therapeutic target.
Dvorak, J. A., Engel, J. C., Leapman, R. D., Swyt, C. R. & Pella, P. A. Trypanosoma cruzi: elemental composition hetereogeneity of cloned stocks. Mol. Biochem. Parasitol. 31, 19–26 (1988).
LeFurgey, A., Ingram, P. & Blum, J. J. Elemental composition of polyphosphate-containing vacuoles and cytoplasm of Leishmania major. Mol. Biochem. Parasitol. 40, 77–86 (1990).
LeFurgey, A., Ingram, P. & Blum, J. J. Compartmental responses to acute osmotic stress in Leishmania major result in rapid loss of Na+ and Cl−. Comp. Biochem. Physiol. Mol. Integr. Physiol. 128, 385–394 (2001).
Correa, A. F., Andrade, L. R. & Soares., M. J. Elemental composition of acidocalcisomes of Trypanosoma cruzi bloodstream trypomastigote forms. Parasitol Res. 88, 875–880 (2002).
Moreno, B. et al. 31P NMR spectroscopy of Trypanosoma brucei, Trypanosoma cruzi and Leishmania major: Evidence for high levels of condensed inorganic phosphates. J. Biol. Chem. 275, 28356–28362 (2000).
Ruiz, F. A., Rodrigues, C. O. & Docampo, R. Rapid changes in polyphosphate content within acidocalcisomes in response to cell growth, differentiation, and environmental stress in Trypanosoma cruzi. J. Biol. Chem. 276, 26114–26121 (2001).
Moreno, B. et al. Magic-angle spinning 31P NMR spectroscopy of condensed phosphates in parasitic protozoa: visualizing the invisible. FEBS Lett. 523, 207–212 (2002).
Rohloff, P., Rodrigues, C. O. & Docampo, R. Regulatory volume decrease in Trypanosoma cruzi involves amino acid efflux and changes in intracellular calcium. Mol. Biochem. Parasitol. 126, 219–230 (2003).
Rodrigues, C. O., Ruiz, F. A., Vieira, M., Hill, J. E. & Docampo, R. An acidocalcisomal exopolyphosphatase from Leishmania major with higher affinity for short-term polyphosphate. J. Biol. Chem. 277, 50899–50906 (2002).
Lemercier, G. et al. A pyrophosphatase regulating polyphosphate metabolism in acidocalcisomes is essential for Trypanosoma brucei virulence in mice. J. Biol. Chem. 279, 3420–3425 (2004).
Xiong, Z. -H., Ridgley, E. L., Enis, D., Olness, F. & Ruben, L. Selective transfer of calcium from an acidic compartment to the mitochondrion of Trypanosoma brucei: measurements with targeted aequorin. J. Biol. Chem. 272, 31022–31028 (1997).
Rohloff, P., Montalvetti, A. & Docampo, R. Acidocalcisomes and the contractile vacuole complex are involved in osmoregulation in Trypanosoma cruzi. J. Biol. Chem. 279, 52270–52281 (2004). The role of acidocalcisomes and the contractile vacuole of trypanosomes in osmoregulation is shown.
Bringaud, F., Baltz, D. & Baltz, T. Functional and molecular characterization of a glycosomal PPi-dependent enzyme in trypanosomatids: pyruvate, phosphate dikinase. Proc. Natl Acad. Sci. USA 95, 7963–7968 (1998).
Ho, A. M., Johnson, M. D. & Kingsley, D. M. Role of the mouse ank gene in control of tissue calcification and arthritis. Science 289, 265–270 (2000).
Wadsworth, S. J. & Van Rossum, G. D. V. Role of vacuolar adenosine triphosphate in the regulation of cytosolic pH in hepatocytes. J. Membrane Biol. 142, 21–34 (1994).
Bronk, S. F. & Gores, G. J. Efflux of protons from acidic vesicles contributes to cytosolic acidification of hepatocytes during ATP depletion. Hepatology 14, 626–633 (1991).
Madshus, I. H., Tonnessen, T. I., Olsnes, S. & Sandvig, K. Effect of potassium depletion of Hep 2 cells on intracellular pH and on chloride uptake by anion antiport. J. Cell Physiol. 131, 6–13 (1987).
Castro, C. D., Koretsky, A. P. & Domach, M. M. NMR-observed phosphate trafficking and polyphosphate dynamics in wild-type and vph1-1 mutant Saccharomyces cerevisiae in response to stresses. Biotechnol. Prog. 15, 65–73 (1999).
Allen, R. D. & Naitoh, Y. Osmoregulation and contractile vacuoles of protozoa. Int. Rev. Cytol. 215, 351–394 (2002).
Clark, T. B. Comparative morphology of four genera of trypanosomatidae. J. Protozool. 6, 227–232 (1959).
Linder, J. C. & Staehelin, L. A. A novel model for fluid secretion by the trypanosomatid contractile vacuole apparatus. J. Cell Biol. 83, 371–382 (1979).
Attias, M., Vommaro, R. C. & de Souza, W. Computer aided three-dimensional reconstruction of the free-living protozoan Bodo sp. (Kinetoplastida:Bodonidae). Cell Struct. Funct. 21, 297–306 (1996).
McConville, M. J., Mullin, K. A., Ilgoutz, S. C. & Teasdale, R. D. Secretory pathway of trypanosomatid parasites. Microbiol. Mol. Biol. Rev. 66, 122–154 (2002).
Morgan, G. W., Hall, B. S., Denny, P. W., Field, M. C. & Carrington, M. The endocytic apparatus of the kinetoplastida. Part II: machinery and components of the system. Trends Parasitol. 118, 540–546 (2002).
Docampo, R. & Moreno, S. N. J. (2001) The acidocalcisome. Mol. Biochem. Parasitol. 114, 151–159.
Drozdowicz, Y. M. et al. Isolation and characterization of TgVP1, a type I vacuolar H+-translocating pyrophosphatase from Toxoplasma gondii. The dynamics of its subcellular localization and the cellular effects of a diphosphonate inhibitor. J. Biol. Chem. 278, 1075–1085 (2003).
Dutoya, S. et al. A novel C-terminal kinesin is essential for maintaining functional acidocalcisomes in Trypanosoma brucei. J. Biol. Chem. 276, 49117–49124 (2001).
Zhang, K. et al. Leishmania salvage of host sphingolipids accompanied by remodeling to form parasite-specific inositol phosphoceramide is required for acidocalcisome biogenesis and parasite survival. Mol. Microbiol. (in the press). A role for sphingolipid biosynthesis in acidocalcisome biogenesis is established.
Saliba, K. J. et al. Acidification of the malaria parasite's digestive vacuole by a H+-ATPase and a H+-pyrophosphatase. J. Biol. Chem. 278, 5605–5612 (2003).
Biagini, G., Bray, P. G., Spiller, D. G., White, M. R. H. & Ward, S. A. The digestive food vacuole of the malaria parasite is a dynamic intracellular Ca2+ store. J. Biol. Chem. 278, 27910–27915 (2003).
Maeshima, M. Tonoplast transporters: organization and function. Annu. Rev. Plant Physiol. 52, 469–497 (2001).
Lindmark, D. G. & Müller, M. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem. 248, 7724–7728 (1973).
Bui, E. T., Bradley, P. J. & Johnson, P. J. A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl Acad. Sci. USA 93, 9651–9656 (1996).
Dyall, S. D. & Johnson, P. J. Origins of hydrogenosomes and mitochondria. Evolution and organelle biogenesis. Curr. Opin. Microbiol. 3, 404–411 (2000).
Ribeiro, K. C., Benchimol, M. & Farina, M. Contribution of cryofixation and freeze-substitution to analytical microscopy: a study of Tritrichomonas foetus hydrogenosomes. Microsci. Res. Tech. 53, 87–92 (2001).
Benchimol, M., Aquino Almeida, J. C., Lins, U., Rodrigues Gonçalves, N. & de Souza, W. Electron microscopy study of the effect of Zn on Tritrichomonas foetus. Antimicrob. Agents Chemother. 37, 2722–2726 (1993).
Biagini, G. A., van der Giezen, M., Hill, B., Winters, C. & Lloyd, D. Ca2+ accumulation in the hydrogenosomes of Neocallimastix frontalis L2: a mitochondrial-like physiological role. FEMS Microbiol Lett. 149, 227–232 (1997).
Jiang, L. et al. The protein storage vacuole: a unique compound organelle. J. Cell Biol. 155, 991–1002 (2001).
Ferguson, M. A. J., Haldar, K. & Cross, G. A. M. Trypanosoma brucei variant surface glycoprotein has a sn-1,2-dimyristoylglycerol membrane anchor at its COOH terminus. J. Biol Chem. 260, 4963–4968 (1985).
Ferguson, M. A. J. The structure, biosynthesis and functions of glycosylphosphatidylinositol, and the contributions of trypanosome research. J. Cell Sci. 112, 2799–2809 (1999).
Gull, K. The cytoskeleton of trypanosomatid parasites. Annu. Rev. Microbiol. 53, 629–655 (1999).
Moreira-Leite, F. F., Sherwin, T., Kohl, L. & Gull, K. A trypanosome structure involved in transmitting cytoplasmic information during cell division. Science 294, 610–612 (2001).
Ziemann, H. Eine methode der doppelfärbung bei flagellaten, pilzen, spirillen und bakterien, sowie bei einigen amöben. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. 24, 945–955 (1898).
Shapiro, T. A. & Englund, P. The structure and replication of kinetoplast DNA. Annu. Rev. Microbiol. 49, 117–143 (1995).
Benne, R. et al. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46, 819–826 (1986).
Blum, B., Bakalara, N. & Simpson, L. A model for RNA editing in kinetoplastid mitochondria: 'guide' RNA molecules transcribed from maxicircle DNA provide the edited information. Cell 60, 189–198 (1990).
Boothroyd, J. C. & Cross, G. A. M. Transcripts encoding for variant surface glycoproteins of Trypanosoma brucei have a short, identical exon at their 5′ end. Gene 20, 281–289 (1982).
Liang, X. -H., Haritan, A., Uliel, S. & Michaeli, S. Trans and cis splicing in trypanosomatids: mechanism, factors, and regulation. Eukaryot. Cell 2, 830–840 (2003).
Opperdoes, F. R. & Borst, P. Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett. 80, 360–364 (1977).
Parsons, M. Glycosomes: parasites and the divergence of peroxisomal function. Mol. Microbiol. 53, 717–724 (2004).
Fairlamb, A. H., Blackburn, P., Ulrich, P., Chait, B. T. & Cerami, A. Trypanothione: a novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science 227, 1485–1487 (1985).
Muller, S., Liebau, E., Walter, R. D. & Krauth-Siegel, R. L. Thiol-based redox metabolism of protozoan parasites. Trends Parasitol. 19, 320–328 (2003).
Kornberg, A., Rao, N. N., & Ault-Riché, D. Inorganic polyphosphate: a molecule of many functions. Annu. Rev. Biochem. 68, 89–125 (1999).
Kulaev, I. & Kulakovskaya, T. Polyphosphate and phosphate pump. Annu. Rev. Microbiol. 54, 709–734 (2000).
Chapman, A. G. & Atkinson, D. E. Adenine nucleotide concentrations and turnover rates. Their correlation with biological activity in bacteria and yeast. Adv. Microbiol. Physiol. 15, 253–306 (1977).
Rao, N. N. & Kornberg, A. Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J. Bacteriol. 178, 1394–1400 (1996).
Castro, C. D., Meehan, A. J., Koretsky, A. P. & Domach, M. M. In situ31P nuclear magnetic resonance for observation of polyphosphate and catabolite responses of chemostat-cultivated Saccharomyces cerevisiae after alkalinization. Appl. Environ. Microbiol. 61, 4448–4453 (1995).
Yang, Y. C., Bastos, M. & Chen, K. Y. Effects of osmotic stress and growth stage on cellular pH and polyphosphate metabolism in Neurospora crassa as studied by 31P nuclear magnetic resonance spectroscopy. Biochim. Biophys. Acta 1179, 141–147 (1993).
Pick, U. & Weiss, M. Polyphosphate hydrolysis within acidic vacuoles in response to amine-induced alkaline stress in the halotolerant alga Dunaliella salina. Plant Physiol. 97, 1234–1240 (1991).
Weiss, M., Bental, M. & Pick, U. Hydrolysis of polyphosphates and permeability changes in response to osmotic shocks in cells of the halotelerant alga Dunaliella. Plant Physiol. 97, 1241–1248 (1991).
Pick, U., Zeelon, O. & Weiss, M. Amine accumulation in acidic vacuoles protects the halotolerant alga Dunaliella salina against alkaline stress. Plant Physiol. 97, 1226–1233 (1991).
Wurts, H., Shiba, T. & Kornberg, A. The gene for a major exopolyphosphatase of Saccharomyces cerevisiae. J. Bacteriol. 177, 898–906 (1995).
Sethuraman, A., Rao, N. N. & Kornberg, A. The endopolyphosphatase gene: essential in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 98, 8542–8547 (2001).
Kornberg, A. Biochemistry matters. Nature Struct. Mol. Biol. 6, 493 (2004).
Gomez-Garcia, M. R. & Kornberg, A. Formation of an actin-like filament concurrent with the enzymatic synthesis of inorganic polyphosphate. Proc. Natl Acad. Sci. USA 101, 15876–15880 (2004). A polyphosphate kinase of possible acidocalcisome localization is identified as a complex of actin-related proteins.
Leon, G. et al. Electron probe analysis and biochemical characterization of electron-dense granules secreted by Entamoeba histolytica. Mol. Biochem. Parasitol. 85, 233–242 (1997).
Mortara, R. Studies on trypanosomatid actin. I. Immunochemical and biochemical identification. J. Protozool. 36, 8–13 (1989).
Babes, V. Beobachtungen über die metachromatischen körperchen, sporenbildung, verzwiegung, kolben- und kapsel-bildung pathogener bakterien. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. 20, 412–420 (1895).
Grimme, A. Die wichtigsten methoden der bakterenfärbung in ihrer wirkung auf die membran, den protoplasten und die einschlüsse der bakterienzelle. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. 32, 161–165 (1902).
Kunze, W. Uber Orcheobius herpobdellae schuberg et kunze. Arch. Protistenk. 9, 382–390 (1907).
Swellengrebel, N. H. La volutine chez les trypanosomes. C. R. Soc. Biol. Paris 64, 38–43 (1908).
Erdnmann, R. Kern und metachromatische körper bei sarkosporidien. Arch. Protistenk. 20, 239–243 (1910).
Wiame, J. H. Etude d'une substance polyphosphorée, basophile et métachromatique chez les levures. Biochim. Biophys. Acta 1, 234–255 (1947)
Ebel, J. P. Recherches sur les polyphosphates contenus dans diverses cellules vivantes. II. Etude chromatographique et potentiométrique des polyphosphates de levure. Bull. Soc. Chim. Biol. 34, 330 (1952).
Vickerman, K. & Tetley, L. Recent ultrastructural studies on trypanosomes. Ann. Soc. Belge Méd. Trop. 57, 441–455 (1977).
Benchimol, M. & de Souza, W. Fine structure and cytochemistry of the hydrogenosome of Tritrichomonas foetus. J. Protozool. 30, 422–425 (1983).
de Souza, W. et al. Two special organelles found in Trypanosoma cruzi. An. Acad. Bras. Ciênc. 72, 421–432 (2000).
Acknowledgements
Work in our laboratories was funded by the US National Institutes of Health (to R.D. and S.N.J.M.), the Burroughs Wellcome Fund (to R.D. and S.N.J.M.) and Programa de Núcleos de Excelência (to W.S.).
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DATABASES
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Glossary
- AXONEME
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A cytoskeletal structure of microtubules that forms flagella and cilia.
- CYTOSTOME
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An invagination of the plasma membrane that is used to incorporate external material.
- MORPHOMETRIC STUDY
-
The diameter of acidocalcisomes in electron microscopy sections is measured and their volume is calculated assuming that they are perfect spheres.
- DIGENETIC TRYPANOSOMATIDS
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Trypanosomes that have two hosts, in contrast to monogenetic trypanosomatids which only have one host.
- SPONGIOME
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Tubules and vacuoles that are connected to the contractile vacuole.
- PULSATION PERIOD
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The period of time between contractions of the contractile vacuole.
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Docampo, R., de Souza, W., Miranda, K. et al. Acidocalcisomes ? conserved from bacteria to man. Nat Rev Microbiol 3, 251–261 (2005). https://doi.org/10.1038/nrmicro1097
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DOI: https://doi.org/10.1038/nrmicro1097