Entamoeba histolytica uses ferritin as an iron source and internalises this protein by means of clathrin-coated vesicles

International Journal for Parasitology

Volumn 39, Issue 4, 2009, Pages 417-426

  López Soto, Fernando ^a   González Robles, Arturo ^a   Salazar Villatoro, Lizbeth ^a   León Sicairos, Nidia ^a,b,c   Piña Vázquez, Carolina ^a   Salazar, Eduardo Pérez ^a   de la Garza, Mireya ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b Hospital Pediátrico de Sinaloa Dr Rigoberto Aguilar Pico   (Mexico)

^c UNIVERSIDAD AUTÓNOMA DE SINALOA   (Mexico)

Author keywords

Amoebiasis; Clathrin coated pits; Endocytosis; Entamoeba histolytica; Iron; Parasite; Proteases

Indexed keywords

HEMOGLOBIN; IRON; PARASITE; PROTEIN; PROTIST; PROTOZOAN;

ANIMALS; CLATHRIN; CLATHRIN-COATED VESICLES; CYSTEINE ENDOPEPTIDASES; ENDOCYTOSIS; ENTAMOEBA HISTOLYTICA; FERRITINS; HEMOGLOBINS; TRANSFERRIN; TROPHOZOITES;

EID: 59149087490     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2008.08.010     Document Type: Article

References (45)

1. Affonso A.L., de Almeida J.C., and Benchimol M. Partial characterization of cytoplasmic compartments involved in the endocytic process of Tritrichomonas foetus. Eur. J. Cell Biol. 72 (1997) 247-256
2. Arosio P., and Levi S. Ferritin, iron homeostasis, and oxidative damage. Free Radic. Biol. Med. 33 (2002) 457-463
3. Blum J.S., Fiani M.L., and Stahl P.D. Proteolytic cleavage of ricin A chain in endosomal vesicles. J. Biol. Chem. 266 (1991) 22091-22095
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
5. Bruchhaus I., Loftus B.J., Hall N., and Tannich E. The intestinal protozoan parasite Entamoeba histolytica contains 20 cysteine protease genes, of which only a small subset is expressed during in vitro cultivation. Eukaryot. Cell 2 (2003) 501-509
6. Clague M.J., Thorpe C., and Jones A.T. Phosphatidylinositol 3-kinase regulation of fluid phase endocytosis. FEBS Lett. 367 (1995) 272-274
7. Chiancone E., Ceci P., Ilari A., Ribacchi F., and Stefanini S. Iron and proteins for iron storage and detoxification. Biometals 17 (2004) 197-202
8. Diamond L.S., Harlow D.R., and Cunnick C.C. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. R. Soc. Trop. Med. Hyg. 72 (1978) 431-432
9. Eichenbaum Z., Muller E., Morse S.A., and Scott J.R. Acquisition of iron from host proteins by the group A Streptococcus. Infect. Immun. 64 (1996) 5428-5429
10. Eskelinen E.L., Cuervo A.M., Taylor M.R.G., Nishino I., Blum S., Dice F., Sandoval I.V., Lippincott-Schwartz J., Thomas J.A., and Saftig P. Unifying nomenclature for the isoforms of the lysosomal membrane protein LAMP-2. Traffic 6 (2005) 1058-1061
11. Espinosa-Cantellano M., and Martinez-Palomo A. Pathogenesis of intestinal amebiasis: from molecules to disease. Clin. Microbiol. Rev. 13 (2000) 318-331
12. Fan J.Y., Carpentier J.L., Gorden P., Van Obberghen E., Blackett N.M., Grunfeld C., and Orci L. Receptor-mediated endocytosis of insulin: role of microvilli, coated pits, and coated vesicles. Proc. Natl. Acad. Sci. USA 79 (1982) 7788-7791
13. Gonzalez-Robles A., Castanon G., Cristobal-Ramos A.R., Lazaro-Haller A., Omana-Molina M., Bonilla P., and Martinez-Palomo A. Acanthamoeba castellanii: structural basis of the cytopathic mechanisms. Exp. Parasitol. 114 (2006) 133-140
14. Grunfelder C.G., Engstler M., Weise F., Schwarz H., Stierhof Y.D., Morgan G.W., Field M.C., and Overath P. Endocytosis of a glycosylphosphatidylinositol-anchored protein via clathrin-coated vesicles, sorting by default in endosomes, and exocytosis via RAB11-positive carriers. Mol. Biol. Cell 14 (2003) 2029-2040
15. Harrison P.M., and Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275 (1996) 161-203
16. Hernandez Y., Castillo C., Roychowdhury S., Hehl A., Aley S.B., and Das S. Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia. Int. J. Parasitol. 37 (2007) 21-32
17. Heussen C., and Dowdle E.B. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal. Biochem. 102 (1980) 196-202
18. Hulet S.W., Heyliger S.O., Powers S., and Connor J.R. Oligodendrocyte progenitor cells internalize ferritin via clathrin-dependent receptor mediated endocytosis. J. Neurosci. Res. 61 (2000) 52-60
19. Ivanov A.I. Pharmacological inhibition of endocytic pathways: Is it specific enough to be useful?. Methods Mol. Biol. 440 (2008) 15-33
20. Larson J.A., Howie H.L., and So M. Neisseria meningitidis accelerates ferritin degradation in host epithelial cells to yield an essential iron source. Mol. Microbiol. 53 (2004) 807-820
21. Latour N.G., and Reeves R.E. An iron-requirement for growth of Entamoeba histolytica in culture, and the antiamoebal activity of 7-iodo-8-hydroxy-quinoline-5-sulfonic acid. Exp. Parasitol. 17 (1965) 203-209
22. Lehker M.W., and Alderete J.F. Iron regulates growth of Trichomonas vaginalis and the expression of immunogenic trichomonad proteins. Mol. Microbiol. 6 (1992) 123-132
23. Leon-Sicairos N., Reyes-Lopez M., Canizalez-Roman A., Bermudez-Cruz R.M., Serrano-Luna J., Arroyo R., and de la Garza M. Human hololactoferrin: endocytosis and use as an iron source by the parasite Entamoeba histolytica. Microbiology 151 (2005) 3859-3871
24. Liu X., and Theil E.C. Ferritin as an iron concentrator and chelator target. Ann. NY Acad. Sci. 1054 (2005) 136-140
25. Moody M.D. Microorganisms and iron limitation. Bioscience 36 (1986) 618-623
26. Moss D., Hibbs A.R., Stenzel D., Powell L.W., and Halliday J.W. The endocytic pathway for H-ferritin established in live MOLT-4 cells by laser scanning confocal microscopy. Br. J. Haematol. 88 (1994) 746-753
27. Orlandi P.A., and Fishman P.H. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domain. J. Cell Biol. 141 (1998) 905-915
28. Passaniti A., and Roth T.F. Coated vesicles from chicken liver bind ferritin. J. Cell Sci. 92 Pt. 2 (1989) 187-196
29. Que X., and Reed S.L. Cysteine proteinases and the pathogenesis of amebiasis. Clin. Microbiol. Rev. 13 (2000) 196-206
30. Reed S.L., Keene W.E., and McKerrow J.H. Thiol proteinase expression and pathogenicity of Entamoeba histolytica. J. Clin. Microbiol. 27 (1989) 2772-2777
31. Reyes-Lopez M., Serrano-Luna J.J., Negrete-Abascal E., Leon-Sicairos N., Guerrero-Barrera A.L., and de la Garza M. Entamoeba histolytica: transferrin binding proteins. Exp. Parasitol. 99 (2001) 132-140
32. San Martin C.D., Garri C., Pizarro F., Walter T., Theil E.C., and Nunez M.T. Caco-2 intestinal epithelial cells absorb soybean ferritin by mu2 (AP2)-dependent endocytosis. J. Nutr. 138 (2008) 659-666
33. Serrano-Luna J.J., Negrete E., Reyes M., and de la Garza M. Entamoeba histolytica HM1:IMSS: hemoglobin-degrading neutral cysteine proteases. Exp. Parasitol. 89 (1998) 71-77
34. Smith J.M., and Meerovitch E. Specificity of iron requirements of Entamoeba histolytica in vitro. Arch. Invest. Med. (Mex.) 13 Suppl. 3 (1982) 63-69
35. Stanley Jr. S.L., Zhang T., Rubin D., and Li E. Role of the Entamoeba histolytica cysteine proteinase in amebic liver abscess formation in severe combined immunodeficient mice. Infect. Immun. 63 (1995) 1587-1590
36. Tougard C., Louvard D., Picart R., and Tixier-Vidal A. Antibodies against a lysosomal membrane antigen recognize a prelysosomal compartment involved in the endocytic pathway in cultured prolactin cells. J. Cell Biol. 100 (1985) 786-793
37. Tovar R., Murguia-Lopez M.L., and s Munoz M. Immunolocalization of clathrin during electron-dense granule secretion in Entamoeba histolytica. Arch. Med. Res. 31 (2000) S143-144
38. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76 (1979) 4350-4354
39. Trissl D., Martinez-Palomo A., Arguello C., de la Torre M., and de la Hoz R. Surface properties related to concanavalin A-induced agglutination. A comparative study of several Entamoeba strains. J. Exp. Med. 145 (1977) 652-665
40. Vohra H., Mahajan R.C., and Ganguly N.K. Role of serum in regulating the Entamoeba histolytica cell cycle: a flow cytometric analysis. Parasitol. Res. 84 (1998) 835-838
41. Weinberg E.D. The role of iron in protozoan and fungal infectious diseases. J. Eukaryot. Microbiol. 46 (1999) 231-238
42. Whitby P.W., Vanwagoner T.M., Springer J.M., Morton D.J., Seale T.W., and Stull T.L. Burkholderia cenocepacia utilizes ferritin as an iron source. J. Med. Microbiol. 55 (2006) 661-668
43. Wu X., Zhao X., Puertollano R., Bonifacino J.S., Eisenberg E., and Greene L.E. Adaptor and clathrin exchange at the plasma membrane and trans-Golgi network. Mol. Biol. Cell 14 (2003) 516-528
44. Young A. Structural insights into the clathrin coat. Semin. Cell Dev. Biol. 18 (2007) 448-458
45. Zhang X., Zhang Z., Alexander D., Bracha R., Mirelman D., and Stanley Jr. S.L. Expression of amoebapores is required for full expression of Entamoeba histolytica virulence in amebic liver abscess but is not necessary for the induction of inflammation or tissue damage in amebic colitis. Infect. Immun. 72 (2004) 678-683