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Subcellular distribution of the Entamoeba histolytica 140 kDa FN-binding molecule during host-parasite interaction

Published online by Cambridge University Press:  01 November 2006

V. I. HERNÁNDEZ-RAMÍREZ ,
A. RIOS ,
A. ANGEL ,
M. A. MAGOS ,
L. PÉREZ-CASTILLO ,
J. L. ROSALES-ENCINA ,
E. CASTILLO-HENKEL  and
P. TALAMÁS-ROHANA
V. I. HERNÁNDEZ-RAMÍREZ
Affiliation:
Superior School of Medicine, IPN, Plan de San Luis y Díaz Mirón, Col. Casco de Sto. Tomás México, D.F., 11340, México
A. RIOS
Affiliation:
Department of Experimental Pathology, CINVESTAV-IPN, Ave. IPN No. 2508, Col. San Pedro Zacatenco, México, D.F., 07360, México
A. ANGEL
Affiliation:
Department of Experimental Pathology, CINVESTAV-IPN, Ave. IPN No. 2508, Col. San Pedro Zacatenco, México, D.F., 07360, México
M. A. MAGOS
Affiliation:
Department of Genetics and Molecular Biology, CINVESTAV-IPN, Ave. IPN No. 2508, Col. San Pedro Zacatenco, México, D.F., 07360, México
L. PÉREZ-CASTILLO
Affiliation:
Department of Experimental Pathology, CINVESTAV-IPN, Ave. IPN No. 2508, Col. San Pedro Zacatenco, México, D.F., 07360, México
J. L. ROSALES-ENCINA
Affiliation:
Department of Experimental Pathology, CINVESTAV-IPN, Ave. IPN No. 2508, Col. San Pedro Zacatenco, México, D.F., 07360, México
E. CASTILLO-HENKEL
Affiliation:
Superior School of Medicine, IPN, Plan de San Luis y Díaz Mirón, Col. Casco de Sto. Tomás México, D.F., 11340, México
P. TALAMÁS-ROHANA
Affiliation:
Department of Experimental Pathology, CINVESTAV-IPN, Ave. IPN No. 2508, Col. San Pedro Zacatenco, México, D.F., 07360, México
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Abstract

Entamoeba histolytica trophozoites recovered from the host-parasite interface during abscess development obtain different stimuli compared with long-term cultured cells. In order to have a better understanding about the mechanisms in which the 140 kDa fibronectin (FN)-binding molecule (EhFNR) is involved during the invasive process, we decided to compare the regulation process of this molecule among long-term cultured trophozoites, FN-stimulated trophozoites, and trophozoites recently recovered from a liver abscess. A cDNA clone (5A) containing a fragment of the EhFNR that shows identity to the C-terminal region of the intermediate galactose lectin subunit Igl, was selected with a mAb (3C10). Identity of EhFNR with Igl was confirmed by immunoprecipitation with 3C10 and EH3015 (against the Gal/GalNAc intermediate subunit) mAbs. The 3C10 mAb was used as a tool to explore the modulation of the amoebic receptor (EhFNR). Our results showed specific regulation of the EhFNR in FN-interacted amoebas, as well as in trophozoites recovered at different stages of abscess development. This regulation involved mobilization of the receptor molecule from internal vesicles to the plasma membrane. Therefore, we suggest that in the host-parasite interface, the EhFNR (Igl) plays an important role in the adhesion process during abscess development.

Keywords

Entamoeba histolyticafibronectinfibronectin-binding moleculehost-parasite interfaceGal/GalNAc intermediate subunitvesicle mobilization
Type
Research Article
Information
Parasitology , Volume 134 , Issue 2 , February 2007 , pp. 169 - 177
Copyright
2006 Cambridge University Press

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References

REFERENCES

Adams, S. A., Robson, S. C., Gathiram, V., Jackson, T. F., Pillai, T. S., Kirsh, R. F. and Makgoba, M. W. ( 1993). Immunological similarity between the 170 kD amoebic adherence glycoprotein and human beta 2 integrins. Lancet 341, 17–19.CrossRefGoogle Scholar
Aley, S. B., Scott, W. A. and Cohn, Z. ( 1980). Plasma membrane of Entamoeba histolytica. Journal of Experimental Medicine 152, 391–404.CrossRefGoogle Scholar
Bainton, D. F., Miller, L. J., Kishimoto, T. K. and Springer, T. A. ( 1987). Leukocyte adhesion receptors are stored in peroxidase-negative granules of human neutrophils. Journal of Experimental Medicine 166, 1641–1653.CrossRefGoogle Scholar
Beck, D. L., Roettner, D. R., Dragulev, B., Ready, K., Nozaky, T. and Petri, W. A. Jr. ( 2005). Identification and gene expression analysis of a large family of transmembrane kinases related to the Gal/GalNAc lectin in Entamoeba histolytica. Eukaryotic Cell 4, 722–732. DOI: 10.1128/EC.4.4.722-732.2005.CrossRefGoogle Scholar
Bruchhaus, I., Roeder, T., Lotter, H., Schwerdtfeger, M. and Tannich, E. ( 2002). Differential gene expression in Entamoeba histolytica isolated from amoebic liver abscess. Molecular Microbiology 44, 1063–1072. DOI: 10.1046/j.1365-2958.2002.02941.x.CrossRefGoogle Scholar
Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J. and Deurs, B. ( 2000). Rab7: A key to lysosome biogenesis. Molecular Biology of the Cell 11, 467–480.CrossRefGoogle Scholar
Chávez-Munguía, B., Hernández-Ramírez, V. I., Angel, A., Rios, A., Talamás-Rohana, P., González-Robles, A., González-Lázaro, M. and Martínez-Palomo, A. ( 2004). Entamoeba histolytica: Ultrastructure of trophozoites recovered from experimental liver lesions. Experimental Parasitology 107, 39–46.CrossRefGoogle Scholar
Cheng, X.-J., Hughes, M. A., Huston, C. D., Loftus, B., Gilchrist, C. A., Lockhart, L. A., Ghosh, S., Miller-Sims, V., Mann, B. J., Petri, W. A. Jr. and Tachibana, H. ( 2001). Intermediate subunit of the Gal/GalNac lectin of Entamoeba histolytica is a member of a gene family containing multiple CXXC sequence motifs. Infection and Immunity 69, 5892–5898. DOI: 10.1128/IAI.69.9.5892-5898.2001.CrossRefGoogle Scholar
Cheng, X.-J. and Tachibana, H. ( 2001). Protection of hamsters from amebic liver abscess formation by immunization with the 150- and 170-kDa surface antigens of Entamoeba histolytica. Parasitology Research 87, 126–130. DOI: 10.1007/S004360000323.CrossRefGoogle Scholar
Cheng, X.-J., Tachibana, H. and Kaneda, Y. ( 1999). Protection of hamsters from amebic liver abscess formation by a monoclonal antibody to a 150-kDa surface lectin of Entamoeba histolytica. Parasitology Research 85, 78–80. DOI: 10.1007/S004360050510.CrossRefGoogle Scholar
Diamond, L. S., Harlow, D. R. and Cunnick, C. C. ( 1978). A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 431–432.CrossRefGoogle Scholar
Flores-Robles, D., Rosales, C., Rosales-Encina, J. L. and Talamás-Rohana, P. ( 2003). Entamoeba histolytica: a β1 integrin-like fibronectin receptor assembles a signaling complex similar to those of mammalian cells. Experimental Parasitology 103, 8–15. DOI: 10.1016/S0014-4894(03)00062-6.CrossRefGoogle Scholar
Guillén, N. ( 1993). Cell signaling and motility in Entamoeba histolytica. Parasitology Today 9, 364–369. DOI: 10.1016/0169-4758(93)90084-S.CrossRefGoogle Scholar
Jiménez-Delgadillo, B., Chaudhuri, P. P., Baylón-Pacheco, L., López-Monteon, A., Talamás-Rohana, P. and Rosales-Encina, J. L. ( 2004). Entamoeba histolytica: cDNAs cloned as 30 kDa collagen-binding proteins (CBP) belong to an antioxidant molecule family. Protection of hamsters from amoebic liver abscess by immunization with recombinant CBP. Experimental Parasitology 108, 7–17. DOI: 10.1016/j.exppara.2004.06.007.CrossRefGoogle Scholar
Kawakami, K., Tatsumi, H. and Sokabe, M. ( 2001). Dynamics of integrin clustering at focal contacts of endothelial cells studied by multimode imaging microscopy. Journal of Cell Science 114, 3125–3135.Google Scholar
Laukaitis, C. M., Weeb, D. J., Donais, K. and Horwitz, A. F. ( 2001). Differential dynamics of β5 integrin, paxillin, and α-actinin during formation and disassembly of adhesions in migrating cells. Journal of Cell Biology 153, 1427–1440. DOI: 10.1083/jcb.153.7.1427.CrossRefGoogle Scholar
Loftus, B., Anderson, I., Davies, R., Alsmark, U. C. M., Samuelson, J., Amedeo, P., Roncaglia, P., Berriman, M., Hirt, R. P., Mann, B. J., Nozaki, T., Suh, B., Pop, M., Duchene, M., Ackers, J., Tannich, E., Leippe, M., Hofer, M., Bruchhaus, I., Willhoeft, U., Bhattacharya, A., Chillingworth, T., Churcher, C., Hance, Z., Harris, B., Harris, D., Jagels, K., Moule, S., Mungall, K., Ormond, D., Squares, R., Whitehead, S., Quail, M. A., Rabbinowitsch, E., Norbertczak, H., Price, C., Wang, Z., Guillén, N., Gilchrist, C., Stroup, S. E., Bhattacharya, S., Lohia, A., Foster, P. G., Sicheritz-Ponten, T., Weber, C., Singh, U., Mukherjee, C., El-Sayed, N. M., Petri, W. A. Jr., Clark, C. G., Embley, T. M., Barrell, B., Fraser, C. M. and Hall, N. ( 2005). The genome of the protist parasite Entamoeba histolytica. Nature 433, 865–868. DOI: 10.1038/nature03291.CrossRefGoogle Scholar
López-Monteón, A., Ramos-Ligonio, A., Pérez-Castillo, L., Talamás-Rohana, P. and Rosales-Encina, J. L. ( 2003). Specific antibody immune response against the parasitic portion of a glutathione-S-transferase fusion protein. The FASEB Journal 17, 621–627.CrossRefGoogle Scholar
Mann, B. J. ( 2002). Structure and function of the Entamoeba histolytica Gal/GalNac lectin. International Review of Cytology 216, 59–80.CrossRefGoogle Scholar
Meza, I. ( 2000). Extracellular matrix-induced signaling in Entamoeba histolytica: its role in invasiveness. Parasitology Today 16, 23–28. DOI: 10.1016/S0169-4758(99)01586-0.CrossRefGoogle Scholar
Nash, T. E. ( 2002). Surface antigenic variation in Giardia lamblia. Molecular Microbiolgy. 45, 585–590. DOI: 10.1046/j.1365-2958.2002.03029.x.CrossRefGoogle Scholar
Novick, P. and Zerial, M. ( 1997). The diversity of Rab proteins in vesicle transport. Current Opinion in Cell Biology 9, 496–504.CrossRefGoogle Scholar
Patra, A. K., Mukhopadhyay, R., Mukhija, R., Krishnan, A., Garg, L. C. and Panda, A. K. ( 2000). Optimization of inclusion body solubilization and renaturation of recombinant human growth hormone from Escherchiia coli. Protein Expression and Purification 18, 182–192. DOI: 10.1006/prep.1999.1179.CrossRefGoogle Scholar
Petri, W. A. Jr., Haque, R. and Mann, B. J. ( 2002). The bittersweet interface of parasite and host: lectin-carbohydrate interactions during human invasion by the parasite Entamoeba histolytica. Annual Review of Microbiology 56, 3–64. DOI: 10.1146/annurev.micro.56.012302.160959.CrossRefGoogle Scholar
Pfeffer, S. R. ( 2001). Rab GTPases: specifying and deciphering organelle identity and function. Trends in Cell Biology 11, 487–491. DOI: 10.1016/S0962-8924(01)02147-X.CrossRefGoogle Scholar
Saito-Nakano, Y., Yasuda, T., Nakada-Tsukuit, K., Leippe, M. and Nosaki, T. ( 2004). Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. The Journal of Biological Chemistry 279, 49497–49507. DOI: 10.1074/jbc.M403987200.CrossRefGoogle Scholar
Sengupta, K., Hernández-Ramírez, V. I. and Talamás-Rohana, P. ( 2000). Monoclonal antibody specific to the β1 integrin-like molecule (140 kDa) immunoprecipitates a protein complex of Entamoeba histolytica. Archives of Medical Research 31, S147–S148.CrossRefGoogle Scholar
Sengupta, K., Hernández-Ramírez, V. I., Rios, A., Mondragón, R. and Talamás-Rohana, P. ( 2001). Entamoeba histolytica: monoclonal antibody against the β1 integrin-like molecule (140 kDa) inhibits cell adhesion to extracellular matrix components. Experimental Parasitology 98, 83–89. DOI: 10.1006/expr.2001.4621.CrossRefGoogle Scholar
Talamás-Rohana, P., Hernández-Ramírez, V. I., Pérez-García, J. N. and Ventura-Juárez, J. ( 1998). Entamoeba histolytica contains a β1 integrin-like molecule similar to fibronectin receptors from eukaryotic cells. Journal of Eukaryotic Microbiology 45, 356–360.CrossRefGoogle Scholar
Talamás-Rohana, P., Hernández, V. I. and Rosales-Encina, J. L. ( 1994). A β1 integrin-like molecule in Entamoeba histolytica. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 596–599.CrossRefGoogle Scholar
Talamás-Rohana, P. and Meza, I. ( 1988). Interaction between pathogenic amebas and fibronectin: substrate degradation and changes in cytoskeleton organization. The Journal of Cell Biology 106, 1787–1794.CrossRefGoogle Scholar
Talamás-Rohana, P., Rosales-Encina, J. L., Gutierrez, M. C. and Hernández, V. I. ( 1992). Identification and partial purification of an Entamoeba histolytica membrane protein that binds fibronectin. Archives of Medical Research 23, 119–123.Google Scholar
Temesvari, L. A., Harris, E. N., Stanley, S. L. Jr. and Cardelli, J. A. ( 1999). Early and late endosomal compartments of Entamoeba histolytica are enriched in cysteine proteases, acid phosphatase, and several Ras-related Rab GTPases. Molecular and Biochemical Parasitology 103, 225–241. DOI: 10.1016/S0166-6851(99)00133-4.CrossRefGoogle Scholar
Tunggal, P., Smyth, N., Paulsson, M. and Ott, M. C. ( 2000). Laminins: structure and genetic regulation. Microscopy Research and Technique 51, 214–227.3.0.CO;2-J>CrossRefGoogle Scholar
Vázquez-Prado, J. and Meza, I. ( 1992). Fibronectin “receptor” in Entamoeba histolytica: purification and association with the cytoskeleton. Archives of Medical Research 23, 125–128.Google Scholar
Vines, R. R., Ramakrisnan, G., Rogers, B. J., Lockhart, A. L., Mann, J. B. and Petri, A. W. Jr. ( 1998). Regulation of adherence and virulence by the Entamoeba histolytica lectin cytoplasmic domain, which contains a β2 integrin motif. Molecular Biology of the Cell 9, 2069–2079.CrossRefGoogle Scholar
Weeb, D. J., Parsons, J. T. and Horwitz, A. F. ( 2002). Adhesion assembly, disassembly and turnover in migrating cells-over and over and over again. Nature Cell Biology 4, E97–E100. DOI: 10.1038/ncb0402-e97.CrossRefGoogle Scholar
Welter, B. H., Laughlin, R. C. and Temesvari, L. A. ( 2002). Characterization of a Rab7-like GTPase, EhRab7: a marker for the early stages of endocytosis in Entamoeba histolytica. Molecular and Biochemical Parasitology 121, 254–264. DOI: 10.1016/S0166-6851(02)00047-6.CrossRefGoogle Scholar
Whyte, J. R. C. and Munro, S. ( 2002). Vesicle tetherin complexes in membrane traffic. Journal of Cell Science 115, 2627–2637.Google Scholar