Surface Coat Differences between Invasive Entamoeba histolytica and Non-Invasive Entamoeba dispar

Arturo González-Robles; Bibiana Chávez-Munguía; Lizbeth  Salazar‑Villatoro; Anel Lagunes-Guillén; Verónica Ivonne Hernández-Ramírez; Patricia Talamás-Rohana; Adolfo Martínez-Palomo

Surface Coat Differences between Invasive Entamoeba histolytica and Non-Invasive Entamoeba dispar

Publication date: 13.07.2015

Acta Protozoologica, 2015, Volume 54, Issue 3, pp. 209 - 218

https://doi.org/10.4467/16890027AP.15.017.3214

Authors

Pobierz pełny tekst

PDF

Titles

Surface Coat Differences between Invasive Entamoeba histolytica and Non-Invasive Entamoeba dispar

Abstract

Using ultrastructural cytochemical techniques we have found differences in the distribution of surface coat components between the invasive protozoan parasite Entamoeba histolytica and the non-invasive Entamoeba dispar. Carbohydrate-containing components and anionic sites in the cell surface of both species were detected by staining with ruthenium red and cationized ferritin, respectively. Ruthenium red staining revealed a thicker surface coat in E. histolytica trophozoites, whereas trophozoites of E. dispar showed a higher concentration of cationized ferritin particles on its surface. Mannose or glucose residues were found at the plasma membrane of both parasites treated with Concanavalin A (Con A)-peroxidase; the surface reaction product was more evident in E. dispar, compared with E. histolytica. Con A rapidly produced surface caps in E. histolytica trophozoites, whereas E. dispar showed a much less efficient mobilization of surface Con A receptors. Agglutination with Con A produced much larger clumps in E. histolytica in comparison with E. dispar. In turn, biotinylation assays revealed striking differences in the composition of surface membrane proteins in both amebic species. Overall, these results further emphasize the phenotypic differences between these two common parasites of the human intestinal tract, once considered to be the same protozoan.

Keywords

Amebiasis, Entamoeba histolytica, Entamoeba dispar, Cell surface, Concanavalin A.

References

Download references

Ackers J., Clark C. G., Diamond L. S., Duchene M., Espinosa-Cantellano M., Jackson T. F. H. G., Martínez-Palomo A., Mirelman D., Muñoz-Hernández O. (1997) WHO/PAHO/UNESCO report. A consultation with experts on amoebiasis. Mexico City. Mexico 28–29 January. 1997. Epidemiol. Bull. PAHO. 18: 13–14

Arroyo R., Orozco E. (1987) Localization and identification of an Entamoeba histolytica adhesin. Mol. Biochem. Parasitol. 23: 151–158

Bernhard W., Avrameas S. (1971) Ultrastructural visualization of cellular carbohydrate components by means of concanavalin A. Exp. Cell. Res. 64: 232–236

Biller L., Matthiesen V. K., Kühne V., Lotter H., Handal G., Nozaki T., Saito-Nakano Y., Schümann M., Roeder T., Tannich E., Krause E., Bruchhaus I. (2014) The cell surface proteome of Entamoeba histolytica. Mol. Cell Proteomics. Jan. 13(1): 132–144. doi: 10.1074/mcp.M113.031393. Epub 2013 Oct 17

Boettner D. R., Huston Ch. D., Sullivan J. A., Petri W. A. Jr. (2005) Entamoeba histolytica and Entamoeba dispar utilize externalized phosphatidylserine for recognition and phagocytosis. Infect. Immun. 73: 3422–3430

Brumpt E. (1925) Etude sommaire de l’ “Entamoeba dispar” n. sp. Amibe a kystes quadrinuclées, parasite de l’ homme. Bull. Acadé. Méd. (Paris) 94: 943–952

Campos-Rodríguez R., Jarillo-Luna A. (2005) The pathogenicity of Entamoeba histolytica is related to the capacity of evading innate immunity. Parasite Immunol. 27: 1–8

Chávez-Munguía B., Talamás-Rohana P., Castañón G., Salazar-Villatoro L., Hernández-Ramírez V., Martínez-Palomo A. (2012) Differences in cap formation between invasive Entamoeba histolytica and non-invasive Entamoeba dispar. Parasitol. Res. 111: 215–221

Clark C. G., Cantellano M. E., Bhattacharya A. (2000) Entamoeba histolytica: an overview of the biology of the organism. In: Ravdin J. I., editor. Amebiasis, vol. 2. London (UK): Imperial College Press, 1–46

Danon D., Goldstein L., Marikovsky Y., Skutelsky E. (1972) Use of cationized ferritin as a label of negative charges on cell surfaces. J. Ultrastruct. Res. 38: 500–510

De Souza W., Martínez-Palomo A., González-Robles A. (1978) The cell surface of Trypanosoma cruzi: cytochemistry and freeze-fracture. J. Cell Sci. 33: 285–299

Diamond L. S., Harlow D. R., Cunnick C. C. (1978) A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. Roy. Soc. Trop. Med. Hyg. 72: 431–432

Diamond L. S., Clark G. (1993) A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. J. Euk. Microbiol. 40: 340–344

Diamond L. S., Clark C. G., Cunick C. C. (1995) YI-S, a casein free medium for axenic cultivation of Entamoeba histolytica, related Entamoeba, Giardia intestinalis and Trichomonas vaginalis. J. Eukaryot. Microbiol.

Espinosa-Cantellano M., Martínez-Palomo A. (1994) Entamoeba histolytica: mechanism of surface capping. Exp. Parasitol. 79: 424–435

Espinosa-Cantellano M., Chávez B., González-Robles A., Castañón G., Argüello C., Lázaro-Haller A., Martínez-Palomo A. (1998) Entamoeba dispar: Ultrastructure, surface properties and cytopathic effect. J. Euk. Microbiol. 45: 265–272

Girard-Misguich F., Sachse M., Santi-Rocca J., Guillén N. (2008) The endoplasmic reticulum chaperone calreticulin is recruited to the uropod during capping of surface receptors in Entamoeba histolytica. Mol. Biochem. Parasitol. 157: 236–240

González-Robles A., Cristóbal-Ramos A. R. (2002) Ultrastructural cytochemical observations of the cell coat of two Trichomonas vaginalis isolates with different degree of virulence. J. Submicrosc. Cytol. Pathol. 34: 207–210

González-Robles A., Espinosa-Cantellano M., Argüello C., Anaya-Velázquez F., Lázaro-Haller A., Martínez-Palomo A. (2004) Surface properties and in vitro cytopathic effect of various strains of Trichomonas vaginalis. J. Submicrosc. Cytol. Pathol. 36: 77–83

González-Robles A., Castañón G., Cristóbal-Ramos A. R., Hernández-Ramírez V. I., Omaña-Molina M., Martínez-Palomo A.

(2007) Cell surface differences of Naegleria fowleri and Naegleria lovaniensis exposed with surface markers. Exp. Parasitol. 117: 399–404

Hernández-Ramírez V. I., Rios A., Angel A., Magos M. A., Pérez-Castillo L., Rosales-Encina J. L., Castillo-Henkel E., Talamás-Rohana P. (2007) Subcellular distribution of the Entamoeba histolytica 140 kDa FN-binding molecule during host-parasite interaction. Parasitology 134: 169–177

Jamerson M., da Rocha-Azevedo B., Cabral G. A., Marciano-Cabral F. (2012) Pathogenic Naegleria fowleri and non-pathogenic Naegleria lovaniensis exhibit differential adhesión to, and invasion of, extracellular matrix proteins. Microbiology 158: 791–803

Leippe M., Tannich E., Nickel R., Gisou van der Goot R. N., Pattus F., Horstmann R. D., Müller-Eberhard H. J. (1992) Primary and secondary structure of the pore-forming peptide of pathogenic Entamoeba histolytica. EMBO J. 11: 3501–3506

Luft J. H. (1964) Electron microscopy of cells extraneous coats as revealed by ruthenium red staining. J. Cell Biol. 23: 54A–55A

McCoy J. J., Mann B. J., Petri W. A. Jr. (1994) Adherence and cytotoxicity of Entamoeba histolytica or how lectins let parasites stick around. Infect. Immun. 62: 3045–3050

Magnelli P., Cipollo J. F., Ratner D. M., Cui J., Kelleher D., Gilmore R., Costello C. E., Robbins W. P., Samuelson J. (2008) Unique Asn-linked Oligosaccharides of the Human Pathogen Entamoeba histolytica. J. Biol. Chem. 283: 18355–18364

Makioka A., Kumagai M., Kobayashi S., Takeuchi T. (2007) Differences in protein profiles of the isolates of E. histolytica and E. dispar by surface-enhanced laser desorption ionization time-

of-flight mass spectrometry (SELDI_TOF MS) Protein Chip assays. Parasit. Res. 102: 103–110

Mann B. J. (2002) Structure and function of the Entamoeba histolytica Gal/GalNAc lectin. Int. Rev. Cytol. 216: 59–80

Martínez-Palomo A. (1970) The surface coats of animal cells.Int. Rev. Cytol. 29: 29–75

Martínez-Palomo A., González-Robles A., de la Torre M. (1973) Selective agglutination of pathogenic strains of Entamoeba histolytica induced Con A. Nature New Biol. 245: 186–187

Martinez-Palomo A. (1982) The Biology of Entamoeba histolytica. Research Studies Press, New York

Moody S., Becker S., Nuchamowits Y., Mirelman D. (1998) Identification of significant variation in the composition of lipophosphoglycans-like molecules of E.histolytica and E. dispar. J. Euk. Microbiol. 45: 9S–12S

Nickel R., Ott C., Dandekar T., Leippe M. (1999) Pore-forming peptides of Entamoeba dispar Similarity and divergence to amoebapores in structure, expression and activity. Eur J. Biochem. 265: 1002–1007

Petri W. A. Jr., Haque R., Mann B. J. (2002) The bittersweet interface of parasite and host: lectin-carbohydrate interactions during human invasion by the parasite Entamoeba histolytica. Ann. Rev. Microbiol. 56: 39–64

Pinto da Silva P., Martínez-Palomo A., González-Robles A. (1975) Membrane structure and surface coat of Entamoeba histolytica. J. Cell Biol. 64: 538–550

Pimenta P. F. P., Diamond L.S., Mirelman D. (2002) Entamoeba histolytica (Schaudinn, 1903) and Entamoeba dispar Brumpt, 1925: Differences in their cell surfaces and in the bacteria-containing vacuoles. J. Eukariot. Microbiol. 49: 209–219

Sargeaunt P. G. (1992) Entamoeba histolytica is a complex of two species. Trans. Roy. Soc. Trop. Med. Hyg. 86: 348

Schaudinn F. (1903) Untersuchugen über die Fortpflanzung eininger Rhizopoden. Arbeiten aus dem Kaiserlichen Gesundheitsamte 19: 547–576

Sengupta K., Hernández-Ramírez V. I., Rios A., Mondragón R., Talamás-Rohana P. (2001) Entamoeba histolytica monoclonal antibody against the β1 integrin-like molecule (140 kDa) inhibits cell adhesión to extracelular matrix components. Exp. Parasitol. 98: 83–89

Sumiyoshi M., Ricciuto J., Tisdale A., Gipson I. K., Mantell F., Argüeso P. (2008) Antiadhesive character of mucin O-glycans at the apical surface of corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 49: 197–203

Talamás-Rohana P., Hernández V. I., Rosales-Encina J. L. (1994) A β1 integrin-like molecule in Entamoeba histolytica. Trans. Roy. Soc. Trop. Med. Hyg. 88: 596–599

Talamás-Lara D., Chávez-Munguía B., González-Robles A., Talamás-Rohana P., Salazar-Villatoro L., Durán-Días A., Martínez-Palomo A. (2014) Etytrophagocytosis in Entamoeba histolytica and Entamoeba dispar: A comparative study. BioMed Research International. Volume 2014, Article ID 626259, http://dx.doi.org/10.1155/2014/626259

Information

Information: Acta Protozoologica, 2015, Volume 54, Issue 3, pp. 209 - 218

DOI: https://doi.org/10.4467/16890027AP.15.017.3214

Article type: Original article