1887

Abstract

Transferrin (Tf) is a host glycoprotein capable of binding two ferric-iron ions to become holotransferrin (holoTf), which transports iron in to all cells. is a parasitic protozoan able to use holoTf as a sole iron source . The mechanism by which this parasite scavenges iron from holoTf is unknown. An holoTf-binding protein (Tfbp) was purified by using an anti-human transferrin receptor (TfR) monoclonal antibody. Tfbp was identified by MS/MS analysis and database searches as acetaldehyde/alcohol dehydrogenase-2 (ADH2), an iron-dependent enzyme. Both Tfbp and ADH2 bound holoTf and were recognized by the anti-human TfR antibody, indicating that they correspond to the same protein. It was found that the amoebae internalized holoTf through clathrin-coated pits, suggesting that holoTf endocytosis could be important for the parasite during colonization and invasion of the intestinal mucosa and liver.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.040063-0
2011-01-01
2024-12-10
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/1/209.html?itemId=/content/journal/micro/10.1099/mic.0.040063-0&mimeType=html&fmt=ahah

References

  1. Andersson J. O., Hirt R. P., Foster P. G., Roger A. J. 2006; Evolution of four gene families with patchy phylogenetic distributions: influx of genes into protist genomes. BMC Evol Biol 6:27
    [Google Scholar]
  2. Avila E. E., Martínez-Alcaráz E., Barbosa-Sabanero G., Rivera-Baron E., Arias-Negrete S., Zazueta-Sandoval R. 2002; Subcellular localization of the NAD+-dependent alcohol dehydrogenase in Entamoeba histolytica trophozoites. J Parasitol 88:217–222
    [Google Scholar]
  3. Bailey G. B., Day D. B., Gasque J. W. 1985; Rapid polymerization of Entamoeba histolytica actin induced by interaction with target cells. J Exp Med 162:546–558
    [Google Scholar]
  4. Batista E. J., de Souza W. 2004; Involvement of protein kinases on the process of erythrophagocytosis by Entamoeba histolytica . Cell Biol Int 28:243–248
    [Google Scholar]
  5. Bierne H., Garandeau C., Pucciarelli M. G., Sabet C., Newton S., Garcia-del Portillo F., Cossart P., Charbit A. 2004; Sortase B, a new class of sortase in Listeria monocytogenes . J Bacteriol 186:1972–1982
    [Google Scholar]
  6. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
    [Google Scholar]
  7. Bruchhaus I., Tannich E. 1994; Purification and molecular characterization of the NAD+-dependent acetaldehyde/alcohol dehydrogenase from Entamoeba histolytica . Biochem J 303:743–748
    [Google Scholar]
  8. Bullen J. J., Rogers H. J., Griffiths E. 1978; Role of iron in bacterial infection. Curr Top Microbiol Immunol 80:1–35
    [Google Scholar]
  9. Chen M., Li E., Stanley S. Jr 2004; Structural analysis of the acetaldehyde dehydrogenase activity of Entamoeba histolytica alcohol dehydrogenase 2 ( Eh ADH2), a member of the ADHE enzyme family. Mol Biochem Parasitol 137:201–205
    [Google Scholar]
  10. Corrêa J. R., Atella G. C., Menna-Barreto R. S., Soares M. J. 2007; Clathrin in Trypanosoma cruzi : in silico gene identification, isolation, and localization of protein expression sites. J Eukaryot Microbiol 54:297–302
    [Google Scholar]
  11. Corrêa J. R., Atella G. C., Batista M. M., Soares M. J. 2008; Transferrin uptake in Trypanosoma cruzi is impaired by interference on cytostome-associated cytoskeleton elements and stability of membrane cholesterol but not by the obstruction of clathrin-dependent endocytosis. Exp Parasitol 119:58–66
    [Google Scholar]
  12. Daukas G., Zigmond S. 1985; Inhibition of receptor-mediated but not fluid-phase endocytosis in polymorphonuclear leukocytes. J Cell Biol 101:1673–1679
    [Google Scholar]
  13. Dautry-Varsat A., Ciechanover A., Lodish H. 1983; pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci U S A 80:2258–2262
    [Google Scholar]
  14. de la Garza M., Gallegos B., Meza I. 1989; Characterization of a cytochalasin D-resistant mutant of Entamoeba histolytica . J Protozool 36:556–560
    [Google Scholar]
  15. Diamond L. S., Harlow D. R., Cunnick C. C. 1978a; A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba . Trans R Soc Trop Med Hyg 72:431–432
    [Google Scholar]
  16. Diamond L. S., Harlow D. R., Phillips B. P., Keister D. B. 1978b; Entamoeba histolytica : iron and nutritional immunity. Arch Invest Med (Mex) 9:329–338
    [Google Scholar]
  17. Espinosa A., Yan L., Zhang Z., Foster L., Clark D., Li E., Stanley S. L. Jr 2001; The bifunctional Entamoeba histolytica alcohol dehydrogenase 2 ( Eh ADH2) protein is necessary for amoebic growth and survival and requires an intact C-terminal domain for both alcohol dehydrogenase and acetaldehyde dehydrogenase activity. J Biol Chem 276:20136–20143
    [Google Scholar]
  18. Espinosa A., Clark D., Stanley S. Jr 2004; Entamoeba histolytica alcohol dehydrogenase 2 ( Eh ADH2) as a target for anti-amoebic agents. J Antimicrob Chemother 54:56–59
    [Google Scholar]
  19. Espinosa A., Pedrizet G., Paz-Y-Miño C. G., Lanfranchi R., Phay M. 2009; Effects of iron depletion on Entamoeba histolytica alcohol dehydrogenase 2 ( Eh ADH2) and trophozoite growth: implications for antiamoebic therapy. J Antimicrob Chemother 63:675–678
    [Google Scholar]
  20. Falkowska-Hansen B., Falkowski M., Metharom P., Krunic D., Goerdt S. 2007; Clathrin-coated vesicles form a unique net-like structure in liver sinusoidal endothelial cells by assembling along undisrupted microtubules. Exp Cell Res 313:1745–1757
    [Google Scholar]
  21. Flores B. M., Stanley S. Jr, Yong T., Ali M., Yang W., Diedrich D., Torian B. 1996; Surface localization, regulation and biologic properties of the 96 kDa alcohol/aldehyde deydrogenase (EhADH2) of pathogenic Entamoeba histolytica . J Infect Dis 173:226–231
    [Google Scholar]
  22. Gat O., Zaide G., Inbar I., Grosfeld H., Chitlaru T., Levy H., Shafferman A. 2008; Characterization of Bacillus anthracis iron-regulated surface determinant (Isd) proteins containing NEAT domains. Mol Microbiol 70:983–999
    [Google Scholar]
  23. Genco C. A., Desai P. J. 1996; Iron acquisition in the pathogenic Neisseria . Trends Microbiol 4:179–184
    [Google Scholar]
  24. Ghosh S. K., Samuelson J. 1997; Involvement of p21racA, phosphoinositide 3-kinase, and vacuolar ATPase in phagocytosis of bacteria and erythrocytes by Entamoeba histolytica : suggestive evidence for coincidental evolution of amebic invasiveness. Infect Immun 65:4243–4249
    [Google Scholar]
  25. Gitler C., Mirelman D. 1986; Factors contributing to the pathogenic behaviour of Entamoeba histolytica . Annu Rev Microbiol 40:237–261
    [Google Scholar]
  26. Grab D. J., Wells C. W., Shaw M. K., Webster P., Russo D. C. 1992; Endocytosed transferrin in African trypanosomes is delivered to lysosomes and may not be recycled. Eur J Cell Biol 59:398–404
    [Google Scholar]
  27. Hernandez Y., Castillo C., Roychowdhury S., Hehld A., Aley S. B., Dasc S. 2007; Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia . Int J Parasitol 37:21–32
    [Google Scholar]
  28. Heuser J. E., Anderson R. G. 1989; Hypertonic media inhibit receptor mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389–400
    [Google Scholar]
  29. Juárez P., Sánchez-López R., Stock R. P., Olvera A., Ramos M. A., Alagón A. 2001; Characterization of the Ehrab 8 gene, a marker of the late stages of the secretory pathway of Entamoeba histolytica . Mol Biochem Parasitol 116:223–228
    [Google Scholar]
  30. Lama A., Kucknoor A., Mundodi V., Alderete J. 2009; Glyceraldehyde-3-phosphate dehydrogenase is a surface-associated, fibronectin-binding protein of Trichomonas vaginalis . Infect Immun 77:2703–2711
    [Google Scholar]
  31. León-Sicairos N., Reyes-Lopez M., Canizalez-Roman A., Bermúdez-Cruz R. M., Serrano-Luna J., Arroyo R., de la Garza M. 2005; Human holo-lactoferrin: endocytosis and use as an iron source by the parasite Entamoeba histolytica . Microbiology 151:3859–3871
    [Google Scholar]
  32. Liu J., Qiao X., Du D., Lee M. G. 2000; Receptor-mediated endocytosis in the procyclic form of Trypanosoma brucei . J Biol Chem 275:12032–12040
    [Google Scholar]
  33. Loftus B., Anderson I., Davies R., Alsmark U. C., Samuelson J., Amedeo P., Roncaglia P., Berriman M., Hirt R. P. other authors 2005; The genome of the protist parasite Entamoeba histolytica . Nature 433:865–868
    [Google Scholar]
  34. López-Soto F., González-Robles A., Salazar-Villatoro L., León-Sicairos N., Piña-Vázquez C., Pérez E., de la Garza M. 2009a; Entamoeba histolytica uses ferritin as an iron source and internalises this protein by means of clathrin-coated vesicles. Int J Parasitol 39:417–426
    [Google Scholar]
  35. López-Soto F., León-Sicairos N., Reyes-López M., Serrano-Luna J., Ordaz-Pichardo C., Piña-Vázquez C., Ortiz-Estrada G., de la Garza M. 2009b; Use and endocytosis of iron-containing proteins by Entamoeba histolytica trophozoites. Infect Genet Evol 9:1038–1050
    [Google Scholar]
  36. Maier A., Steverding D. 1996; Low affinity of Trypanosoma brucei transferrin receptor to apo-transferrin at pH 5 explains the fate of the ligand during endocytosis. FEBS Lett 396:87–89
    [Google Scholar]
  37. Maresso A. W., Schneewind O. 2006; Iron acquisition and transport in Staphylococcus aureus . Biometals 19:193–203
    [Google Scholar]
  38. Marion S., Laurent C., Guillen N. 2005; Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell Microbiol 7:1504–1518
    [Google Scholar]
  39. Mazmanian S. K., Skaar E. P., Gaspar A. H., Humayun M., Gorrincki P., Jalenska J., Joachmiak A., Missiakas D. M., Scheewind O. 2003; Passage of heme-iron across the envelope of Staphylococcus aureus . Science 299:906–909
    [Google Scholar]
  40. Merschjohann K., Steverding D. 2006; In vitro growth inhibition of bloodstream forms of Trypanosoma brucei and Trypanosoma congolense by iron chelators. Kinetoplastid Biol Dis 5:3
    [Google Scholar]
  41. Meza I., Clarke M. 2004; Dynamics of endocytic traffic of Entamoeba histolytica revealed by confocal microscopy and flow cytometry. Cell Motil Cytoskeleton 59:215–226
    [Google Scholar]
  42. Modun B., Williams P. 1999; The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect Immun 67:1086–1092
    [Google Scholar]
  43. Morgan G. W., Allen C. L., Jefries T. R., Hollinshead M., Field M. C. 2001; Developmental and morphological regulation of clathrin-mediated endocytosis in Trypanosoma brucei . J Cell Sci 114:2605–2615
    [Google Scholar]
  44. Nakada-Tsukui K., Okada H., Mitra B. N., Nozaki T. 2009; Phosphatidylinositol-phosphates mediate cytoskeleton reorganization during phagocytosis via a unique modular protein consisting of RhoGEF/DH and FYVE domains in the parasitic protozoan Entamoeba histolytica . Cell Microbiol 11:1471–1491
    [Google Scholar]
  45. Natesan S. K., Peacock L., Matthews K., Gibson W., Field M. C. 2007; Activation of endocytosis as an adaptation to the mammalian host by trypanosomes. Eukaryot Cell 6:2029–2037
    [Google Scholar]
  46. Neuhaus E. M., Almers W., Soldati T. 2002; Morphology and dynamics of the endocytic pathway in Dictyostelium discoideum . Mol Biol Cell 13:1390–1407
    [Google Scholar]
  47. Paz-y-Miño C. G., Espinosa A. 2010; Integrating horizontal gene transfer and common descent to depict evolution and contrast it with “Common Design”. J Eukaryot Microbiol 57:11–18
    [Google Scholar]
  48. Pintor M., Ferreiros C. M., Criado M. T. 1993; Characterization of the transferrin-iron uptake system in Neisseria meningitidis . FEMS Microbiol Lett 112:159–165
    [Google Scholar]
  49. Qian Z. M., Tang P. L. 1995; Mechanisms of iron uptake by mammalian cells. Biochim Biophys Acta 1269:205–214
    [Google Scholar]
  50. Qualmann B., Kessels M. M., Kelly R. B. 2000; Molecular links between endocytosis and the actin cytoskeleton. J Cell Biol 150:F111–F116
    [Google Scholar]
  51. Ravdin J. I., Murphy C. F., Schlesinger P. H. 1988; The cellular regulation of vesicle exocytosis by Entamoeba histolytica . J Protozool 35:159–163
    [Google Scholar]
  52. Reeves R. E., Warren L. G., Susskind B., Lo H. 1977; An energy conserving pyruvate to acetate pathway in Entamoeba histolytica . J Biol Chem 252:726–731
    [Google Scholar]
  53. Reyes-López M., Serrano-Luna J. J., Negrete-Abascal E., , León-Sicairos N., Guerrero-Barrera A. L., de la Garza M. 2001; Entamoeba histolytica : transferrin binding proteins. Exp Parasitol 99:132–140
    [Google Scholar]
  54. Richardson D. R., Ponka P. 1997; The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta 13311–40
    [Google Scholar]
  55. Robibaro B., Hope H. C., Yang M., Coppens I., Ngô H. M., Stedman T. T., Pprotka K., Joiner K. A. 2001; Endocytosis in different lifestyles of protozoan parasitism: role in nutrient uptake with special reference to Toxoplasma gondii . Int J Parasitol 31:1343–1353
    [Google Scholar]
  56. Romero-Díaz M., Gómez C., López-Reyes I., Martínez M., Orozco E., Rodríguez M. 2007; Structural and functional analysis of the Entamoeba histolytica EhrabB gene promoter. BMC Mol Biol 8:82
    [Google Scholar]
  57. Sahoo N., , Labruyère E., Bhattacharya S., Sen P., Guillén N., Bhattacharya A. 2004; Calcium binding protein 1 of the protozoan parasite Entamoeba histolytica interacts with actin and is involved in cytoskeleton dynamics. J Cell Sci 117:3625–3634
    [Google Scholar]
  58. Serrano-Luna J. J., Negrete E., Reyes-López M., de la Garza M. 1998; Entamoeba histolytica HM1 : IMSS: haemoglobin-degrading neutral cysteine proteases. Exp Parasitol 89:71–77
    [Google Scholar]
  59. Slepnev V. I., De Camilli P. 2000; Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat Rev Neurosci 1:161–172
    [Google Scholar]
  60. Tanaka T., Abe Y., Inoue N., Kim W., Kumura H., Nagasawa H., Igarashi I., Shimazaki K. 2004; The detection of bovine lactoferrin binding protein on Trypanosoma brucei . J Vet Med Sci 66:619–625
    [Google Scholar]
  61. Taylor J. M., Heinrichs D. E. 2002; Transferrin binding in Staphylococcus aureus : involvement of a cell wall-anchored protein. Mol Microbiol 43:1603–1614
    [Google Scholar]
  62. Temesvari L. A., Harris D. N., Stanley S. L., Cardelli J. 1999; Early and late endosomal compartments of Entamoeba histolytica are enriched in cysteine proteases, acid phosphatase and several Ras-related Rab-GTPases. Mol Biochem Parasitol 103:225–241
    [Google Scholar]
  63. Testa U. 2002; Transferrin. In Proteins of Iron Metabolism pp 143–247 Edited by Testa U. Boca Raton, FL: CRC Press;
    [Google Scholar]
  64. Thorstensen K., Romslo I. 1990; The role of transferrin in the mechanism of cellular iron uptake. Biochem J 271:1–9
    [Google Scholar]
  65. Tovy A., Tov R. S., Gaentzsch R., Helm M., Ankri S. 2010; A new nuclear function of the Entamoeba histolytica glycolytic enzyme enolase: the metabolic regulation of cytosine-5 methyltransferase 2 (Dnmt2) activity. PLoS Pathog 6:e1000775
    [Google Scholar]
  66. Towbin H., Staehelin T., Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350–4354
    [Google Scholar]
  67. Weinberg E. D. 2009; Iron availability and infection. Biochim Biophys Acta 1790600–605
    [Google Scholar]
  68. Welter B. H., Laughlin R. C., Temesvari L. A. 2002; Characterization of a Rab7-like GTPase, EhRab7: a marker for the early stages of endocytosis in Entamoeba histolytica . Mol Biochem Parasitol 121:254–264
    [Google Scholar]
  69. Welter B. H., Powell R. R., Laughlin R. C., McGugan G. C., Bonner M., King A., Temesvari L. A. 2006; Entamoeba histolytica : comparison of the role of receptors and filamentous actin among various endocytic processes. Exp Parasitol 113:91–99
    [Google Scholar]
  70. Yang W., Li E., Kairong T., Stanley S. L. Jr 1994; Entamoeba histolytica has an alcohol dehydrogenase homologous to the multifunctional adhE gene product of Escherichia coli . Mol Biochem Parasitol 64:253–260
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.040063-0
Loading
/content/journal/micro/10.1099/mic.0.040063-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error