Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-28T06:54:15.988Z Has data issue: false hasContentIssue false
  • English
  • Français

Biochemical and cellular mechanisms regulating Acanthamoeba castellanii adherence to host cells

Published online by Cambridge University Press:  26 November 2013

K. J. SOTO-ARREDONDO ,
L. L. FLORES-VILLAVICENCIO ,
J. J. SERRANO-LUNA ,
M. SHIBAYAMA  and
M. SABANERO-LÓPEZ
K. J. SOTO-ARREDONDO
Affiliation:
Departamento de Biología, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Noria Alta S/N Col. Noria Alta, C.P. 36050, Guanajuato, Guanajuato, México
L. L. FLORES-VILLAVICENCIO
Affiliation:
Departamento de Biología, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Noria Alta S/N Col. Noria Alta, C.P. 36050, Guanajuato, Guanajuato, México
J. J. SERRANO-LUNA
Affiliation:
Departamento de Biología Celular, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Av. Instituto Politecnico Nacional 2508, San Pedro Zacatenco, Gustavo A. Madero, 07360, Ciudad de México, México
M. SHIBAYAMA
Affiliation:
Departamento de Infectómica y Patogénesis Molecular, Centro de Investigación y Estudios Avanzados, Instituto Politécnico Nacional, Av. Instituto Politécnico Nacional 2508, San Pedro Zacatenco, Gustavo A. Madero, 07360, Ciudad de México, México
M. SABANERO-LÓPEZ*
Affiliation:
Departamento de Biología, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Noria Alta S/N Col. Noria Alta, C.P. 36050, Guanajuato, Guanajuato, México
*
* Corresponding author: Departamento de Biología, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Noria Alta S/N Col. Noria Alta, C.P. 36050, Guanajuato, Guanajuato, México. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Free-living amoebae belonging to the genus Acanthamoeba are the causative agents of infections such as amoebic keratitis (AK), granulomatous amoebic encephalitis (GAE) and cutaneous lesions. The mechanisms involved in the establishment of infection are unknown. However, it is accepted that the initial phase of pathogenesis involves adherence to the host tissue. In this work, we analysed surface molecules with an affinity for epithelial and neuronal cells from the trophozoites of Acanthamoeba castellanii. We also investigated the cellular mechanisms that govern the process of trophozoite adhesion to the host cells. We first used confocal and epifluorescence microscopy to examine the distribution of the A. castellanii actin cytoskeleton during interaction with the host cells. The use of drugs, as cytochalasin B (CB) and latrunculin B (LB), revealed the participation of cytoskeletal filaments in the adhesion process. In addition, to identify the proteins and glycoproteins on the surface of A. castellanii, the trophozoites were labelled with biotin and biotinylated lectins. The results revealed bands of surface proteins, some of which were glycoproteins with mannose and N-acetylglucosamine residues. Interaction assays of biotinylated amoebae proteins with epithelial and neuronal cells showed that some surface proteins had affinity for both cell types. The results of this study provide insight into the biochemical and cellular mechanisms of the Acanthamoeba infection process.

Keywords

Acanthamoeba castellaniiadhesioncytochalasinlatrunculinglycoproteinscytoskeleton
Type
Research Article
Information
Parasitology , Volume 141 , Issue 4 , April 2014 , pp. 531 - 541
Copyright
Copyright © Cambridge University Press 2013 

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

Bailey, G. B., Day, D. B. and Gasque, J. W. (1985). Rapid polymerization of Entamoeba histolytica actin induced by interaction with target cells. Journal of Experimental Medicine 162, 546–558. doi: 10.1084/jem.162.2.546.Google Scholar
Beckerle, M. C. (1998). Spatial control of actin filament review assembly: lessons from Listeria . Cell 95, 741–748. doi: 10.1016/S0092-8674(00)81697-9.CrossRefGoogle ScholarPubMed
Bellin, R. M., Kubicek, J. D., Frigault, M. J., Kamien, A. J., Steward, R. L., Barnes, H. M., DiGiacomo, M. B., Duncan, L. J., Edgerly, C. K., Morse, E. M., Park, C. Y., Fredberg, J. J., Cheng, C. M. and LeDuc, P. R. (2009). Defining the role of syndecan-4 in mechanotransduction using surface modification approaches. Proceedings of the National Academy of Sciences USA 106, 22102–22107. doi: 10.1073/pnas.0902639106.CrossRefGoogle ScholarPubMed
Bracha, R. and Mirelman, D. (1983). Adherence and ingestion of Escherichia coli serotype 055 by trophozoites of Entamoeba histolytica . Infection and Immunity 40, 882–887.CrossRefGoogle ScholarPubMed
Burchard, G. D. and Bilke, R. (1992). Adherence of pathogenic and non-pathogenic Entamoeba histolytica strains to neutrophils. Parasitology Research 78, 146–153. doi: 10.1007/BF00931657.Google Scholar
Casanova, M., Lopez-Ribot, J. L., Martinez, J. P. and Sentandreu, R. (1992). Characterization of cell wall proteins from yeast and mycelial cells of Candida albicans by labeling with biotin: comparison with other techniques. Infection and Immunity 60, 4898–4906.Google Scholar
Castillo-Romero, A., León-Avila, G., Pérez-Rangel, A., Cortes-Zarate, R., García-Tovar, C. and Hernández, J. M. (2009). Participation of actin on Giardia lamblia growth and encystation. PLoS One 4, e7156. doi: 10.1371/journal.pone.0007156.CrossRefGoogle ScholarPubMed
Cervantes-Sandoval, I., Serrano-Luna, J. J., Pacheco-Yépez, J., Silva-Olivares, A., Tsutsumi, V. and Shibayama, M. (2010). Differences between Naegleria fowleri and Naegleria gruberi in expression of mannose and fucose glycoconjugates. Parasitology Research 106, 695–701. doi: 10.1007/s00436-010-1727-z.Google Scholar
Chen, S. H., Stins, M. F., Huang, S. H., Chen, Y. H., Kwon-Chung, K. J., Chang, Y., Kim, K. S., Suzuki, K. and Jong, A. Y. (2003). Cryptococcus neoformans induces alterations in the cytoskeleton of human brain microvascular endothelial cells. Journal of Medical Microbiology 52, 961–970. doi: 10.1099/jmm.0.05230-0.Google ScholarPubMed
Freshney, R. I. (2000). Culture of Animal Cells: A Manual of Basic Technique, 4th Edn. John Wiley & Sons, New York, USA.Google Scholar
Fürstner, A., Kirk, D., Fenster, M. D., Aïssa, C., De Souza, D. and Müller, O. (2005). Diverted total synthesis: preparation of a focused library of latrunculin analogues and evaluation of their actin-binding properties. Proceedings of the National Academy of Sciences USA 102, 8103–8108. doi: 10.1073/pnas.0501441102.Google Scholar
Garate, M., Cubillos, I., Marchant, J. and Panjwani, N. (2005). Biochemical characterization and functional studies of Acanthamoeba mannose-binding protein. Infection and Immunity 73, 5775–5781. doi: 10.1128/IAI.73.9.5775-5781.Google Scholar
Garate, M., Marchant, J., Cubillos, I., Cao, Z., Khan, N. A. and Panjwani, N. (2006). In vitro pathogenicity of Acanthamoeba is associated with the expression of the mannose-binding protein. Investigative Ophthalmology and Visual Science 47, 1056–1062. doi: 10.1167/iovs.05-0477.CrossRefGoogle ScholarPubMed
González-Robles, A., Castañón, G., Hernández-Ramírez, V. I., Salazar-Villatoro, L., González-Lázaro, M., Omaña-Molina, M., Talamás-Rohana, P. and Martínez-Palomo, A. (2008). Acanthamoeba castellanii: identification and distribution of actin cytoskeleton. Experimental Parasitology 119, 411–417. doi: 10.1016/j.exppara.2008.04.004.Google Scholar
Grollo, L., Chua, B. and Jackson, D. C. (2005). Methods in molecular biology. Production of polyclonal antibodies in rabbits. Immunochemical protocols. In Immunology and Cell Biology (ed. Burns, R.), pp. 584–585. Humana Press, Totowa, NJ, USA.Google Scholar
Karkowska-Kuleta, J., Rapala-Kozik, M. and Kozik, A. (2009). Fungi pathogenic to humans: molecular bases of virulence of Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus . Acta Biochimica Polonica 56, 211–224.Google Scholar
Karlsson, K. A. (1989). Animal glycosphingolipids as membrane attachment sites for bacteria. Annual Review of Biochemistry 58, 309–350. doi: 10.1146/annurev.bi.58.070189.001521.CrossRefGoogle ScholarPubMed
Kennett, M. J., Hook, R. R. Jr., Franklin, C. L. and Riley, L. K. (1999). Acanthamoeba castellanii: characterization of an adhesin molecule. Experimental Parasitology 92, 161–169. doi: 10.1006/expr.1999.4417.Google Scholar
Khan, N. A. (2003). Pathogenesis of Acanthamoeba infections. Microbial Pathogenesis 34, 277–285. doi: 10.1016/S0882-4010(03)00061-5.Google Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685. doi: 10.1038/227680a0.Google Scholar
Lee, J. C. and King, R. D. (1983). Characterization of Candida albicans adherence to human vaginal epithelial cells in vitro . Infection and Immunity 41, 1024–1030.CrossRefGoogle ScholarPubMed
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265–275.Google Scholar
Martínez-Palomo, A., González-Robles, A., Chávez, B., Orozco, E., Fernández-Castelo, S. and Cervantes, A. (1985). Structural bases of the cytolytic mechanisms of Entamoeba histolytica . Journal of Protozoology 32, 166–175. doi: 10.1111/j.1550-7408.1985.tb03033.x.Google Scholar
Meza, I., Talamás-Rohana, P. and Vargas, M. A. (2006). The cytoskeleton of Entamoeba histolytica: structure, function, and regulation by signaling pathways. Archives of Medical Research 37, 234–243. doi: 10.1016/j.arcmed.2005.09.008.CrossRefGoogle ScholarPubMed
Moore, M. B., Ubelaker, J. E., Martin, J. H., Silvany, R., Dougherty, J. M., Meyer, D. R. and McCulley, J. P. (1991). In vitro penetration of human corneal epithelium by Acanthamoeba castellanii: a scanning and transmission electron microscopy study. Cornea 10, 291–298.CrossRefGoogle ScholarPubMed
Morton, L. D., McLaughlin, G. L. and Whiteley, H. E. (1991). Effects of temperature, amebic strain, and carbohydrates on Acanthamoeba adherence to corneal epithelium in vitro . Infection and Immunity 59, 3819–3822.Google Scholar
Omaña-Molina, M., Navarro-García, F., González-Robles, A., Serrano-Luna, J. J., Campos-Rodríguez, R., Martínez-Palomo, A., Tsutsumi, V. and Shibayama, M. (2004). Induction of morphological and electrophysiological changes in hamster cornea after in vitro interaction with trophozoites of Acanthamoeba spp. Infection and Immunity 72, 3245–3251. doi: 10.1128/IAI.72.6.3245-3251.2004.Google Scholar
Pacheco-Yépez, J., Campos-Rodríguez, R., Rojas-Hernández, S., Serrano-Luna, J. J., Rivera-Aguilar, V., Villa-Treviño, S., Martínez-Palomo, A., Tsutsumi, V. and Shibayama, M. (2009). Differential expression of surface glycoconjugates on Entamoeba histolytica and Entamoeba dispar . Parasitology International 58, 171–177. doi: 10.1016/j.parint.2009.02.003.Google Scholar
Panjwani, N., Ahmad, S. and Raizman, M. B. (1995). Cell surface glycoproteins of corneal epithelium. Investigative Ophthalmology and Visual Science 36, 355–363.Google Scholar
Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453–465. doi: 10.1016/S0092-8674(03)00120-X.Google Scholar
Ravdin, J. I., Croft, B. Y. and Guerrant, R. L. (1980). Cytopathogenic mechanisms of Entamoeba histolytica . Journal of Experimental Medicine 152, 377–390. doi: 10.1084/jem.152.2.377.Google Scholar
Rivera, F., Medina, F., Ramírez, P., Alcocer, J., Vilaclara, G. and Robles, E. (1984). Pathogenic and free-living protozoa cultured from the nasopharyngeal and oral region of dental patients. Environmental Research 33, 428–440. doi: 10.1016/0013-9351(84)90040-9.CrossRefGoogle ScholarPubMed
Sandoval-Bernal, G., Barbosa-Sabanero, G., Shibayama, M., Perez-Torres, A., Tsutsumi, V. and Sabanero, M. (2011). Cell wall glycoproteins participate in the adhesion of Sporothrix schenckii to epithelial cells. Mycopathologia 171, 251–259. doi: 10.1007/s11046-010-9372-8.Google Scholar
Schuster, F. L. and Visvesvara, G. S. (2004). Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. International Journal for Parasitology 34, 1001–1027. doi: 10.1016/j.ijpara.2004.06.004.Google Scholar
Serrano-Luna, J. J., Cervantes-Sandoval, I., Calderón, J., Navarro-García, F., Tsutsumi, V. and Shibayama, M. (2006). Protease activities of Acanthamoeba polyphaga and Acanthamoeba castellanii . Canadian Journal of Microbiology 52, 16–23. doi: 10.1139/w05-114.Google Scholar
Shibayama, M., Martínez-Castillo, M., Silva-Olivares, A., Galindo-Gómez, S., Navarro-García, F., Escobar-Herrera, J., Sabanero, M., Tsutsumi, V. and Serrano-Luna, J. J. (2013). Disruption of MDCK cell tight junctions by the free-living amoeba Naegleria fowleri . Microbiology 159, 392–401. doi: 10.1099/mic.0.063255-0.Google Scholar
Taylor, W. M., Pidherney, M. S., Alizadeh, H. and Niederkorn, J. Y. (1995). In vitro characterization of Acanthamoeba castellanii cytopathic effect. Journal of Parasitology 81, 603–609.CrossRefGoogle ScholarPubMed
Torno, M. S. Jr., Babapour, R., Gurevitch, A. and Witt, M. D. (2000). Cutaneous acanthamoebiasis in AIDS. Journal of the American Academy of Dermatology 42, 351–354. doi: 10.1016/S0190-9622(00)90110-5.Google Scholar
Towbin, H., Staehelin, T. and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrilamid gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences USA 76, 4350–4354.Google Scholar
Yang, Z., Cao, Z. and Panjwani, N. (1997). Pathogenesis of Acanthamoeba keratitis: carbohydrate-mediated host-parasite interactions. Infection and Immunity 65, 439–445.Google Scholar