Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T06:21:10.987Z Has data issue: false hasContentIssue false
  • English
  • Français

Acidocalcisomes of Phytomonas françai Possess Distinct Morphological Characteristics and Contain Iron

Published online by Cambridge University Press:  01 October 2004

Kildare Miranda ,
Claudia O. Rodrigues ,
Joachim Hentchel ,
Anibal Vercesi ,
Helmut Plattner ,
Wanderley de Souza  and
Roberto Docampo
Kildare Miranda
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Av. Brigadeiro Trompovski, s/n., bloco G, Cidade Universitária, 21949-900, Rio de Janeiro, RJ, Brazil Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802
Claudia O. Rodrigues
Affiliation:
Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802
Joachim Hentchel
Affiliation:
Department of Biology, University of Konstanz, 78457 Konstanz, Germany
Anibal Vercesi
Affiliation:
Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802 Laboratório de Bioenergética, Núcleo de Medicina e Cirugia Experimental, Universidade Estadual Campinas, Campinas-SP, Brazil
Helmut Plattner
Affiliation:
Department of Biology, University of Konstanz, 78457 Konstanz, Germany
Wanderley de Souza
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Av. Brigadeiro Trompovski, s/n., bloco G, Cidade Universitária, 21949-900, Rio de Janeiro, RJ, Brazil
Roberto Docampo
Affiliation:
Laboratory of Molecular Parasitology, Department of Pathobiology and Center for Zoonoses Research, University of Illinois at Urbana–Champaign, Urbana, IL 61802
Get access

Abstract

Acidocalcisomes are acidic calcium storage compartments described initially in trypanosomatid and apicomplexan parasites, and recently found in other unicellular eukaryotes. The aim of this study was to identify the presence of acidocalcisomes in the plant trypanosomatid Phytomonas françai. Electron-dense organelles of P. françai were shown to contain large amounts of oxygen, sodium, magnesium, phosphorus, potassium, calcium, iron, and zinc as determined by X-ray microanalysis, either in situ or when purified using iodixanol gradient centrifugation or by elemental mapping. The presence of iron is not common in other acidocalcisomes. In situ, but not when purified, these organelles showed an elongated shape differing from previously described acidocalcisomes. However, these organelles also possessed a vacuolar H+-pyrophosphatase (V-H+-PPase) as determined by biochemical methods and by immunofluorescence microscopy using antibodies against the enzyme. Together, these results suggest that the electron-dense organelles of P. françai are homologous to the acidocalcisomes described in other trypanosomatids, although with distinct morphology and elemental content.

Keywords

Phytomonasacidocalcisomeselemental mappingpyrophosphatasecalciumtransmission electron microscopy
Type
Feature Articles
Information
Microscopy and Microanalysis , Volume 10 , Issue 5 , October 2004 , pp. 647 - 655
Copyright
© 2004 Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anonymous. (1997). Tropical Disease Research, Thirteenth Programme Report, UNDP/World Bank/World Health Organization Special Programme for Research and Training in Tropical Diseases. Geneva: World Health Organization.
Benaim, G. (1996). Intracellular calcium regulation and signaling in Leishmania. In Molecular and Immune Mechanisms in the Pathogenesis of Cutaneous Leishmaniasis, Tapia, F.J., Cáceres-Dittmar, G. & Sánchez, M.A. (Eds.), pp. 89–106. Georgetown, Texas: Landes Company.
Berridge, M.J. (1997). Elementary and global aspects of calcium signaling. J Physiol 499, 291–306.Google Scholar
Camargo, E. (1999). Phytomonas and other Trypanosomatid parasites of plants and fruit. Adv Parasitol 42, 29–112.Google Scholar
Carvalho, T.U. & de Souza, W. (1977). Fine structure and X-ray microanalysis of electron-dense granules in Herpetomonas samuelpessoai. J Parasitol 63, 1116–1117.Google Scholar
Catarino, L.M., Serrano, M.G., Covazzana Jr., M., Almeida, M.L., Kaneshina, E.K., Campaner, M., Jankevicius, J.V., Teixeira, M.M.G., & Itow-Jankevicius, S. (2001). Classification of trypanosomatids from fruits and seed using morphological, biochemical and molecular markers revealed several genera amoung fruit isolates. FEMS Microbiol Lett 201, 65–72.Google Scholar
Chou, A.C. & Fitch, C.D. (1980). Hemolysis of mouse erythrocytes by ferriprotoporphyrin IX and chloroquine. Chemotherapeutic implications. J Clin Invest 66, 856–858.Google Scholar
Coppens, I., Baudhin, P., Opperdoes, F.R., & Courtoy, P.J. (1993). Role of acidic compartments in Trypanosoma brucei, with special reference to low density lipoprotein processing. Mol Biochem Parasitol 58, 223–232.Google Scholar
Correa, A.F.S., Andrade, L.R., & Soares, M.J. (2002). Elemental composition of acidocalcisomes of Trypanosoma cruzi bloodstream trypomastigote forms. Parasitol Res 88, 875–880.Google Scholar
Docampo, R. & Moreno, S.N.J. (1996). The role of Ca2+ in the process of cell invasion by intracellular parasites. Parasitol Today 12, 61–65.Google Scholar
Docampo, R. & Moreno, S.N.J. (1999). Acidocalcisome: A novel Ca2+ storage compartment in trypanosomatids and apicomplexan parasites. Parasitol Today 15, 443–448.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
Docampo, R. & Vercesi, A.E. (1989a). Ca2+ transport by coupled Trypanosoma cruzi mitochondria in situ. J Biol Chem 264, 108–111.Google Scholar
Docampo, R. & Vercesi, A.E. (1989b). Characteristics of Ca2+ transport by Trypanosoma cruzi mitochondria in situ. Arch Biochem Biophys 272, 122–129.Google Scholar
Dollet, M., Giannotti, J., & Ollagnier, M. (1977). Observation de protozoaires flagellés dans tubes cribles de palmiers à huile malades. C R Acad Sci 284, 643–645.Google Scholar
Dvorak, J.A., Engel, J.C., Leapman, R.D., Swyt, C.R., & Pella, P.A. (1988). Trypanosoma cruzi: Elemental composition of cloned stocks. Mol Biochem Parasitol 31, 19–26.Google Scholar
Kitajima, E.W., Vainstein, M.H., & Silveira, J.S.M. (1986). Flagellate protozoan associated with poor development of the root system of cassava in the Espirito Santo State, Brazil. Phytopathology 76, 638–642.Google Scholar
Lafont, A. (1909). Sur la presence d'un Leptomonas, parasite de la classe des Flagellés, dans le latex de 'Euphorbia pilulifera. C R Soc Seances Soc Biol Fil 66, 1011–1013.Google Scholar
Lu, H.-G., Zhong, L., Chang, K.P., & Docampo, R. (1997). Intracellular Ca2+ pool content and signaling and expression of a calcium pump are linked to virulence in Leishmania mexicana amazonensis amastigotes. J Biol Chem 272, 9464–9673.Google Scholar
Miranda, K., Benchimol, M., Docampo, R., & De Souza, W. (2000). The fine structure of acidocalcisomes in Trypanosoma cruzi. Parasitol Res 86, 373–384.Google Scholar
Moreno, S.N.J., Silva, J., Vercesi, A.E., & Docampo, R. (1994). Cytosolic-free calcium elevation in Trypanosoma cruzi is required for cell invasion. J Exp Med 180, 1535–1540.Google Scholar
Parthasarathy, M.V., Van Slobbe, W.G., & Soudant, C. (1976). Trypanosomatid flagellate in the phloem of diseased coconut palms. Science 192, 1346–1348.Google Scholar
Rodrigues, C.O., Scott, D.A., & Docampo, R. (1999a). Characterization of a vacuolar pyrophosphatase in Trypanosoma brucei and its localization to acidocalcisomes. Mol Cell Biol 19, 7712–7723.Google Scholar
Rodrigues, C.O., Scott, D.A., & Docampo, R. (1999b). 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.Google Scholar
Schmitt, T.H., Frezzati, W.A., & Schreider, S. (1993). Hemin-induced lipid membrane disorder and increased permeability: A molecular model for the mechanism of cell lysis. Arch Biochem Biophys 307, 96–103.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
Scott, D.A., Docampo, R., Dvorak, J.A., Shi, S., & Leapman, R.D. (1997). In situ compositional analysis of acidocalcisomes in Trypanosoma cruzi. J Biol Chem 272, 28020–28029.Google Scholar
Stahel, G. (1931). Zur kenntnis der siebroehrenkrankheit (Phloemnekrose) des kaffeebaumes in Surinam. I. Mikroskopische untersuchungen und infektionsversuche. Phytopathol Zeitsch 4, 65–82.Google Scholar
Vainstein, M.H. & Roitman, I. (1985). Cultivation of Phytomonas françai associated with poor development of root of cassava. J Protozool 33, 511–513.Google Scholar
Vannier-Santos, M.A., Martiny, A., Lins, U., Urbina, J.A., Borges, V.M., & De Souza, W. (1999). Impairment of sterol biosynthesis leads to phosphorous and calcium accumulation in Leishmania acidocalcisomes. Microbiology 145, 3213–3220.Google Scholar
Vercesi, A.E., Bernardes, C.F., Hoffmann, M.E., Gadelha, F.R., & Docampo, R. (1991a). Digitonin permeabilization does not affect mitochondrial function and allows the determination of the mitochondrial membrane potential of Trypanosoma cruzi in situ. J Biol Chem 266, 14431–14434.Google Scholar
Vercesi, A.E. & Docampo, R. (1996). Sodium-proton exchange stimulates Ca2+ release from acidocalcisomes of Trypanosoma brucei. Biochem J 315, 265–270.Google Scholar
Vercesi, A.E., Grijalba, M., & Docampo, R. (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.Google Scholar
Vercesi, A.E., Hoffmann, M.E., Bernardes, C.F., & Docampo, R. (1991b). Regulation of intracellular calcium homeostasis in Trypanosoma cruzi. Effects of calmidazolium and trifluoperazine. Cell Calcium 12, 361–369.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
Vercesi, A.E., Rodrigues, C.O., Catisti, R., & Docampo, R. (2000). Presence of a Na+/H+ exchanger in acidocalcisomes of Leishmania donovani and their alkalinization by ant-leishmanial drugs. FEBS Lett 473, 203–206.Google Scholar
Vermeulen, H.A. (1963). A wilt Coffea liberica in Surinam and association with a flagellate, Phytomonas leptovasorum. J Protozool 10, 216–222.Google Scholar
Vickerman, K. & Tetley, L. (1977). Recent ultrastructural studies on Trypanosomes. Ann Soc Belge Med Trop 57, 441–455.Google Scholar
Vieira, M.C.F. & Moreno, S.N.J. (2000). Mobilization of intracellular calcium upon attachment of Toxoplasma gondii tachyzoites to human fibroblasts is required for invasion. Mol Biochem Parasitol 106, 157–162.Google Scholar
Warren, L.G. (1960). Metabolism of Schizotrypanum cruzi. Chagas. I. Effect of culture age and substrate concentration on respiratory rate. J Parasitol 46, 529–539.Google Scholar
Zhen, R.G., Baykov, A.A., Bakuleva, N.P., & Rea, P.A. (1994). Amynomethylenediphosphonate: A potent type-specific inhibitor of both plant and phototrophic bacterial H+-pyrophosphatase. Plant Physiol 104, 153–159.Google Scholar
Zhen, R.-G., Kim, E.J., & Rea, P.A. (1997). Acidic residues necessary for pyrophosphate-energized pumping and inhibition of the vacuolar H+-pyrophosphatase by N,N′-diclyclohexylcarbodiimide. J Biol Chem 272, 22340–22348.Google Scholar