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The interaction between the amoeba Balamuthia mandrillaris and extracellular matrix glycoproteins in vitro

Published online by Cambridge University Press:  11 October 2006

B. ROCHA-AZEVEDO ,
M. JAMERSON ,
G. A. CABRAL ,
F. C. SILVA-FILHO  and
F. MARCIANO-CABRAL
B. ROCHA-AZEVEDO
Affiliation:
Programa de Bioengenharia e Biotecnologia Animal, Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil Department of Microbiology and Immunology, School of Medicine, Virginia Commonwealth University, Richmond, Virginia, USA
M. JAMERSON
Affiliation:
Department of Microbiology and Immunology, School of Medicine, Virginia Commonwealth University, Richmond, Virginia, USA
G. A. CABRAL
Affiliation:
Department of Microbiology and Immunology, School of Medicine, Virginia Commonwealth University, Richmond, Virginia, USA
F. C. SILVA-FILHO
Affiliation:
Programa de Bioengenharia e Biotecnologia Animal, Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
F. MARCIANO-CABRAL
Affiliation:
Department of Microbiology and Immunology, School of Medicine, Virginia Commonwealth University, Richmond, Virginia, USA
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Abstract

Balamuthia mandrillaris, a soil amoeba, is the causative agent of Balamuthia granulomatous amoebic encephalitis, a life-threatening brain infection. This amoeba is acquired from contaminated soil and may enter the host through cutaneous lesions or through nasal passages, migrating to the lungs or brain. During invasion, B. mandrillaris has access to components of the extracellular matrix (ECM) of the host. Therefore, we investigated the interaction of B. mandrillaris with 3 ECM glycoproteins (collagen-I, fibronectin and laminin-1) that are encountered in host connective tissues and at the basal lamina. Using optical microscopy, amoeba association on ECM-coated surfaces was examined. Binding of amoebae on laminin was greater than that on collagen or fibronectin. Laminin-adhered B. mandrillaris exhibited elongated and spread forms, distinctive from those observed for amoebae on a plastic surface. Collagen and fibronectin-adhered B. mandrillaris presented elongated shapes with cellular expansions. Binding to collagen, fibronectin, or laminin was inhibited when amoebae were pre-treated with sialic acid. Treatment with galactose resulted in diminished binding of amoebae on laminin, while mannose increased binding in all coating conditions tested. Dependence of divalent cations on amoeba binding was demonstrated for laminin-amoeba interaction. Collectively, the results indicate that B. mandrillaris recognizes specific glycoproteins of the mammalian extracellular matrix.

Keywords

Balamuthia mandrillarisfree-living amoebaeprotozoaextracellular matrixcollagen Ifibronectinlamininpathogen-ECM interaction
Type
Research Article
Information
Parasitology , Volume 134 , Issue 1 , January 2007 , pp. 51 - 58
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P. ( 2002). Molecular Biology of the Cell, 4th Edn. Garland Science, New York.
Bresalier, R. S., Yan, P. S., Byrd, J. C., Lotan, R. and Raz, A. ( 1997). Expression of the endogenous galactose-binding protein galectin-3 correlates with the malignant potential of tumors in the central nervous system. Cancer 80, 776–787.3.0.CO;2-Q>CrossRefGoogle Scholar
Burridge, K. and Chrzanowska-Wodnicka, M. ( 1996). Focal adhesions, contractility, and signaling. Annual Reviews of Cell and Developmental Biology 12, 463–519.CrossRefGoogle Scholar
Carbajal, M. E., Manning-Cela, R., Pina, A., Franco, E. and Meza, I. ( 1996). Fibronectin-induced intracellular calcium rise in Entamoeba histolytica trophozoites: effect on adhesion and the actin cytoskeleton. Experimental Parasitology 82, 11–20.CrossRefGoogle Scholar
Chammas, R., Jasiulionis, M. G., Jin, F., Villa-Verde, D. M. and Reinhold, V. N. ( 1994). Carbohydrate-binding proteins in cell-matrix interactions. Brazilian Journal of Medical Biological Research 9, 2169–2179.Google Scholar
Crouch, M. L. and Alderete, J. F. ( 1999). Trichomonas vaginalis interaction with fibronectin and laminin. Microbiology 145, 2835–2843.CrossRefGoogle Scholar
Crouch, M. L., Benchimol, M. and Alderete, J. F. ( 2001). Binding of fibronectin by Trichomonas vaginalis is influenced by iron and calcium. Microbial Pathogenesis 31, 131–144.CrossRefGoogle Scholar
Dunnebacke, T. H., Schuster, F. L., Yagi, S. and Booton, G. C. ( 2004). Balamuthia mandrillaris from soil samples. Microbiology 150, 2837–2842.CrossRefGoogle Scholar
Eda, S. and Sherman, I. W. ( 2004). Plasmodium falciparum-infected erythrocytes bind to the RGD motif of fibronectin via the band 3-related adhesin. Experimental Parasitology 107, 157–162.CrossRefGoogle Scholar
Fuller, G. M. and Shields, D. ( 1998). Molecular Basis of Medical Cell Biology, 1st Edn. Appleton and Lange, Stanford.
Giancotti, F. G. and Ruoslathi, E. ( 1999). Integrin signaling. Science 285, 1028–1032.CrossRefGoogle Scholar
Ghosh, A., Kole, L., Bandyopadhay, K., Sarkar, K. and Das, P. K. ( 1996). Evidence of a laminin binding protein on the surface of Leishmania donovani. Biochemical and Biophysical Research Communications 226, 101–106.CrossRefGoogle Scholar
Gonzalez, A., Gomez, B. L., Restrepo, A., Hamilton, A. J. and Cano, L. E. ( 2005). Recognition of extracellular matrix proteins by Paracoccidioides brasiliensis yeast cells. Medical Mycology 43, 637–645.CrossRefGoogle Scholar
Gordon, V. R., Asem, E. K., Vodkin, M. H. and McLaughlin, G. L. ( 1993). Acanthamoeba binds to extracellular matrix proteins in vitro. Investigative Ophthalmology and Visual Science 34, 658–662.Google Scholar
Guillen, N. ( 1996). Role of signalling and cytoskeletal rearrangements in the pathogenesis of Entamoeba histolytica. Trends in Parasitology 4, 191–197.CrossRefGoogle Scholar
Hamilton, A. J., Jeavons, L., Youngchim, S. and Vanittanakom, N. ( 1999). Recognition of fibronectin by Penicillium marneffei conidia via a sialic acid-dependent process and its relationship to the interaction between conidia and laminin. Infection and Immunity 67, 5200–5205.Google Scholar
Han, K. L., Lee, H. J., Shin, M. H., Shin, H. J., Im, K. I. and Park, S. J. ( 2004). The involvement of an integrin-like protein and protein kinase C in amoebic adhesion to fibronectin and amoebic cytotoxicity. Parasitology Research 94, 53–60.CrossRefGoogle Scholar
Hughes R. C. ( 1992). Role of glycosylation in cell interactions with extracellular matrix. Biochemical Society Transactions 20, 279–284.CrossRefGoogle Scholar
Janitschke, K., Martinez, A. J., Visvesvara, G. S. and Schuster, F. L. ( 1996). Animal model Balamuthia mandrillaris CNS infection: contrast and comparison in immunodeficient and immunocompetent mice: a murine model of “granulomatous” amebic encephalitis. Journal of Neuropathology and Experimental Neurology 55, 815–821.CrossRefGoogle Scholar
Jayasekera, S., Matin, A., Sissons, J., Maghsood, A. H. and Khan, N. A. ( 2005). Balamuthia mandrillaris stimulates interleukin-6 release in primary human brain microvascular endothelial cells via a phosphatidylinositol 3-kinase-dependent pathway. Microbes and Infection 13, 1345–1351.CrossRefGoogle Scholar
Kiderlen, A. F. and Laube, U. ( 2004). Balamuthia mandrillaris, an opportunistic agent of granulomatous amebic encephalitis, infects the brain via the olfactory nerve pathway. Parasitology Research 94, 49–52.CrossRefGoogle Scholar
Klotz, S. A. ( 1994). Plasma and extracellular matrix proteins mediate in the fate of Candida albicans in the human host. Medical Hypotheses 42, 328–334.CrossRefGoogle Scholar
Lauwaet, T., Oliveira, M. J., Mareel, M. and Leroy, A. ( 2000). Molecular mechanisms by cancer cells, leukocytes and microorganisms. Microbes and Infection 2, 923–931.CrossRefGoogle Scholar
Leffler, H., Carlsson, S., Hedlund, M., Qian, Y. and Poirier, F. ( 2004). Introduction to galectins. Glycoconjugate Journal 19, 433–440.Google Scholar
Marciano-Cabral, F. and Fulford, D. E. ( 1986). Cytopathology of pathogenic and nonpathogenic Naegleria species for cultured rat neuroblastoma cells. Applied and Environmental Microbiology 51, 1133–1137.Google Scholar
Mareel, M. and Leroy, A. ( 2003). Clinical, cellular, and molecular aspects of cancer invasion. Physiology Reviews 83, 337–376.CrossRefGoogle Scholar
Martinez, A. J. and Visvesvara, G. S. ( 2001). Balamuthia mandrillaris infection. Journal of Medical Microbiology 50, 205–507.Google Scholar
Meza, I. ( 2000). Extracellular matrix-induced signaling in Entamoeba histolytica: its role in invasiveness. Parasitology Today 16, 23–28.CrossRefGoogle Scholar
Munoz, M. L., Das, P. and Tovar, R. ( 2001). Entamoeba histolytica trophozoites activated by collagen type I and Ca(2+) have a structured cytoskeleton during collagenase secretion. Cell Motility and the Cytoskeleton 50, 45–54.CrossRefGoogle Scholar
Ouassi, M. A., Capron, A. and Grimaud, J. A. ( 1984). Fibronectin receptors on Trypanosoma cruzi trypomastigotes and their biological function. Nature, London 308, 380–382.CrossRefGoogle Scholar
Pettit, D. A., Williamson, J., Cabral, G. A. and Marciano-Cabral, F. ( 1996). In vitro destruction of nerve cell cultures by Acanthamoeba spp.: a transmission and scanning electron microscopy study. Journal of Parasitology 82, 769–777.Google Scholar
Plow, E. F., Haas, T. A., Zhang, L., Loftus, J. and Smith, J. W. ( 2000). Ligand binding to integrins. Journal of Biological Chemistry 275, 21782–21788.CrossRefGoogle Scholar
Ramkumar, R. and Podder, S. K. ( 2000). Elucidation of the mechanism of interaction of sheep spleen galectin-1 with splenocytes and its role in cell-matrix adhesion. Journal of Molecular Recognition 13, 299–309.3.0.CO;2-O>CrossRefGoogle Scholar
Rideout, B. A., Gardiner, C. H., Stalis, I. H., Zuba, J. R., Hadfield, T. and Visvesvara, G. S. ( 1997). Fatal infections with Balamuthia mandrillaris (a free-living amoeba) in Gorillas and other old world primates. Veterinary Pathology 34, 15–22.CrossRefGoogle Scholar
Rigothier, M. C., Coconnier, M. H., Servin, A. L. and Gayral, P. ( 1991). A new in vitro model of Entamoeba histolytica adhesion, using the human colon carcinoma cell line Caco-2: scanning electron microscopic study. Infection and Immunity 59, 4142–4146.Google Scholar
Roberts, D. D., Olson, L. D., Barile, M. F., Ginsburg, V. and Krivan, H. C. ( 1989). Sialic acid-dependent adhesion of Mycoplasma pneumoniae to purified glycoproteins. Journal of Biological Chemistry 264, 9289–9293.Google Scholar
Schuster, F. L. ( 2002). Cultivation of pathogenic and opportunistic free-living amoebas. Clinical Microbiology Reviews 15, 342–354.CrossRefGoogle Scholar
Schuster, F. L. and Visvesvara, G. S. ( 1996). Axenic growth and drug sensitivity studies of Balamuthia mandrillaris, an agent of amebic meningoencephalitis in humans and other animals. Journal of Clinical Microbiology 34, 385–388.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.CrossRefGoogle Scholar
Schuster, F. L., Dunnebacke, T. H., Booton, G. C., Yagi, S., Kohlmeier, C. K., Glaser, C., Vugia, D., Bakardjiev, A., Azimi, P., Maddux-Gonzalez, M., Martinez, A. J. and Visvesvara, G. S. ( 2003). Environmental isolation of Balamuthia mandrillaris associated with a case of amebic encephalitis. Journal of Clinical Microbiology 41, 3175–3180.CrossRefGoogle Scholar
Schwarz-Linek, U., Hook, M. and Potts, J. R. ( 2004). The molecular basis of fibronectin-mediated bacterial adherence to host cells. Molecular Microbiology 52, 631–641.CrossRefGoogle Scholar
Silva-Filho, F. C. ( 1998). Focal adhesion in Trichomonas vaginalis. Memorias do Instituto Oswaldo Cruz 95, 40.Google Scholar
Silva-Filho, F. C. and Arroyo, R. ( 1998). YIGSR is the preferential laminin-1 residing adhesion sequence for Trichomonas vaginalis. Experimental Parasitology 88, 240–242.CrossRefGoogle Scholar
Silva-Filho, F. C., de Souza, W. and Lopes, J. D. ( 1988). Presence of laminin-binding proteins in trichomonads and their role in adhesion. Proceedings of the National Academy of Sciences, USA 85, 8042–8046.CrossRefGoogle Scholar
Smirnov, A., Nassonova, E., Berney, C., Fahrni J., Bolivar, I. and Pawlowski, J. ( 2005). Molecular phylogeny and classification of the Lobose amoebae. Protist 156, 129–142.CrossRefGoogle Scholar
Somner, E. A., Black, J. and Pasvol, G. ( 2000). Multiple human serum components act as bridging molecules in rosette formation by Plasmodium falciparum-infected erythrocytes. Blood 95, 674–682.Google Scholar
Talamas-Rohana, P. and Meza, I. ( 1988). Interaction between pathogenic amebas and fibronectin: substrate degradation and changes in cytoskeleton organization. Journal of Cell Biology 106, 1787–1794.CrossRefGoogle Scholar
Tronchin, G., Esnault, K., Sanchez, M., Larcher, G., Marot-Leblond, A. and Bouchara, J. P. ( 2002). Purification and partial characterization of a 32-kilodalton sialic acid-specific lectin from Aspergillus fumigatus. Infection and Immunity 70, 6891–6895.CrossRefGoogle Scholar
Vazquez-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
Wadstrom, T. and Ljungh, A. ( 1999). Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. Journal of Medical Microbiology 48, 223–233.CrossRefGoogle Scholar
Wang, L., Asem, E. K. and McLaughlin, G. L. ( 1994). Calcium enhances Acanthamoeba polyphaga binding to extracellular matrix proteins. Investigative Ophthalmology and Visual Science 35, 2421–2426.Google Scholar
Westerlund, B. and Korhonen, T. K. ( 1993). Bacterial proteins binding to the mammalian extracellular matrix. Molecular Microbiology 9, 687–694.CrossRefGoogle Scholar