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Polyphosphate Content and Fine Structure of Acidocalcisomes of Plasmodium falciparum

Published online by Cambridge University Press:  01 October 2004

Felix A. Ruiz ,
Shuhong Luo ,
Silvia N.J. Moreno  and
Roberto Docampo
Felix A. Ruiz
Affiliation:
Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802
Shuhong Luo
Affiliation:
Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802
Silvia N.J. Moreno
Affiliation:
Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802
Roberto Docampo
Affiliation:
Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802
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Abstract

Although acidocalcisomes have been well characterized morphologically in other apicomplexan parasites, no such characterization has been done in Plasmodium spp. Here, we report that Plasmodium falciparum merozoites possess electron-dense organelles rich in phosphorus and calcium, as detected by X-ray microanalysis of intact cells, which are similar to the acidocalcisomes of other apicomplexans, but of more irregular form. In agreement with these results malaria parasites possess large amounts of short- and long-chain polyphosphate (polyP), which are associated with acidocalcisomes in other organisms. PolyP levels were highest in the trophozoite stage of the parasite. Treatment of isolated trophozoites with chloroquine resulted in a significant hydrolysis of polyP. Taken together, these results provide evidence that acidocalcisomes from Plasmodium falciparum do not differ significantly from acidocalcisomes of other apicomplexan parasites.

Keywords

PlasmodiumacidocalcisomesX-ray microanalysispolyphosphatecalcium
Type
Feature Articles
Information
Microscopy and Microanalysis , Volume 10 , Issue 5 , October 2004 , pp. 563 - 567
Copyright
© 2004 Microscopy Society of America

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References

REFERENCES

Adovelande, J., Bastide, B., Deleze, J., & Schrevel, J. (1993). Cytosolic free calcium in Plasmodium falciparum-infected erythrocytes and the effect of verapamil: A cytofluorometric study. Exp Parasitol 76, 247–258.Google Scholar
Alleva, L.M. & Kirk, K. (2001). Calcium regulation in the intraerythrocytic malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 117, 121–128.Google Scholar
Ault-Riché, D., Fraley, C.D., Tzeng, C.M., & Kornberg, A. (1998). Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J Bacteriol 180, 1841–1847.Google Scholar
Blackman, M.J. (1994). Purification of Plasmodium falciparum merozoites for analysis of the processing of merozoite surface protein-1. Methods Cell Biol 45, 213–220.Google Scholar
Dluzewski, A.R., Ling, I.T., Rangachari, K., Bates, P.A., & Wilson, R.J.M. (1984). A simple method for isolating viable mature parasites of Plasmodium falciparum from cultures. Trans Roy Soc Trop Med Hyg 78, 622–624.Google Scholar
Docampo, R. & Moreno, S.N.J. (2001). The acidocalcisome. Mol Biochem Parasitol 33, 151–159.Google Scholar
Docampo, R., Scott, D.A., Vercesi, A.E., & Moreno, S.N.J. (1995). Intracellular Ca2+ storage in acidocalcisomes of Trypanosoma cruzi. Biochem J 310, 1005–1012.Google Scholar
Drozdowicz, Y.M., Shaw, M., Nishi, M., Striepen, B., Liwinski, H.A., Roos, D.S., & Rea, P.A. (2003). 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.Google Scholar
Garcia, C.R., Ann, S.E., Tavares, E.S., Dluzewski, A.R., Mason, W.T., & Paiva, F.B. (1998). Acidic calcium pools in intraerythrocytic malaria parasites. Eur J Cell Biol 76, 133–138.Google Scholar
Gazarini, M.L., Thomas, A.P., Pozzan, T., & Garcia, C.R.S. (2003). Calcium signaling in a low calcium environment: How the intracellular malaria parasite solves the problem. J Cell Biol 161, 103–110.Google Scholar
Haldar, K., Elmendorf, H.G., Das, A., & Li, W.L. (1994). In vitro secretory assays with erythrocytes-free malaria parasites. Methods Cell Biol 45, 221–230.Google Scholar
Harold, F.M. (1966). Inorganic polyphosphate in biology: Structure, metabolism and function. Bacteriol Rev 30, 772–794.Google Scholar
Hase, E., Miyachi, S., & Mihara, S. (1963). A preliminary note on the phosphorous compounds in chloroplasts and volutin granules isolated from Chlorella cells. Plant Cell Physiol (Tokyo) 4, 619–626.Google Scholar
Jacobson, L., Halmann, M., & Yariv, J. (1982). The molecular composition of the volutin granule of yeast. Biochem J 201, 473–479.Google Scholar
Kornberg, A. (1995). Inorganic polyphosphate: Toward making a forgotten polymer unforgettable. J Bacteriol 177, 491–496.Google Scholar
Luo, S., Vieira, M., Graves, J., Zhong, L., & Moreno, S.N.J. (2001). A plasma membrane-type Ca2+-ATPase co-localizes with a vacuolar H+-pyrophosphatase to acidocalcisomes of Toxoplasma gondii. EMBO J 20, 55–56.Google Scholar
Magowan, C., Brown, J.T., Liang, J., Heck, J., Coppel, R.L., Mohandas, N., & Meyer-Ilse, W. (1997). Intracellular structures of normal and aberrant Plasmodium falciparum malaria parasites imaged by soft x-ray microscopy. Proc Natl Acad Sci USA 94, 6222–6227.Google Scholar
Marchesini, N., Luo, S., Rodrigues, C.O., Moreno, S.N.J., & Docampo, R. (2000). Acidocalcisomes and a vacuolar H+-pyrophosphatase in malaria parasites. Biochem J 347, 243–253.Google Scholar
Marchesini, N., Ruiz, F.A., Vieira, M., & Docampo, R. (2002). Acidocalcisomes are linked to the contractile vacuole of Dictyostelium discoideum. J Biol Chem 277, 8146–8153.Google Scholar
McIntosh, M.T. & Vaidya, A.B. (2002). Vacuolar type H+ pumping pyrophosphatases of parasitic protozoa. Int J Parasitol 32, 1–14.Google Scholar
Meyer, A. (1904). Orientierende Untersuchungen ueber Verbreitung. Morphologie, und Chemie des Volutins. Bot Zeit 62, 113–152.Google Scholar
Miranda, K., Rodrigues, C.O., Hentchel, J., Vercesi, A.E., Plattner, H., de Souza, W., & Docampo, R. (2004). Acidocalcisomes of Phytomonas françai possess distinct morphological characteristics and contain iron. Microsc Microanal 10, xxx (this issue).Google Scholar
Moreno, S.N.J. & Zhong, L. (1996). Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem J 313, 655–659.Google Scholar
Ormerod, W.E. (1958). A comparative study of cytoplasmic inclusions (volutin granules) in different species of trypanosomes. J Gen Microbiol 19, 271–288.Google Scholar
Rodrigues, C.O., Ruiz, F.A., Rohloff, P., Scott, D.A., & Moreno, S.N.J. (2002). Characterization of isolated acidocalcisomes from Toxoplasma gondii tachyzoites reveals a novel pool of hydrolyzable polyphosphate. J Biol Chem 277, 48650–48656.Google Scholar
Rodrigues, C.O., Scott, D.A, Bailey, B.N., de Souza, W., Benchimol, M., Moreno, B., Urbina, J.A., Oldfield, E., & Moreno, S.N.J. (2000). Vacuolar proton pyrophosphatase activity and pyrophosphate (PPi) in Toxoplasma gondii as possible chemotherapeutic targets. Biochem J 349, 737–745.Google Scholar
Rosenberg, H. (1966). The isolation and identification of “volutin” granules from Tetrahymena. Exp Cell Res 41, 397–410.Google Scholar
Ruiz, F.A., Marchesini, N., Seufferheld, M., Govindjee, & Docampo, R. (2001a). The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 276, 46196–46203.Google Scholar
Ruiz, F.A., Rodrigues, C.O., & Docampo, R. (2001b). 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.Google Scholar
Schwab, J.C., Beckers, C.J., & Joiner, K.A. (1994). The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci USA 91, 509–513.Google Scholar
Scott, D.A., de Souza, W., Benchimol, M., Zhong, L., Lu, H.-G., Moreno, S.N.J., & Docampo, R. (1998). Presence of a plant-like proton-pumping pyrophosphatase in acidocalcisomes of Trypanosoma cruzi. J Biol Chem 273, 22151–22158.Google Scholar
Scott, D.A. & Docampo, R. (2000). Characterization of isolated acidocalcisomes of Trypanosoma cruzi. J Biol Chem 275, 24215–24221.Google Scholar
Trager, W. & Jensen, J.B. (1976). Human malaria parasites in continuous culture. Science 193, 673–675.Google Scholar
Vercesi, A.E., Moreno, S.N.J., & Docampo, R. (1994). Ca2+/H+ exchange in acidic vacuoles of Trypanosoma brucei. Biochem J 304, 227–233.Google Scholar
Wiame, J.J. (1947). Etude d'une substance polyphosphoré, basophile et métachromatique chez les levures. Biochim Biophys Acta 1, 234–255.Google Scholar