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Involvement of host cell heparan sulfate proteoglycan in Trypanosoma cruzi amastigote attachment and invasion

Published online by Cambridge University Press:  27 January 2011

R. BAMBINO-MEDEIROS ,
F. O. R. OLIVEIRA Jr ,
C. M. CALVET ,
D. VICENTE ,
L. TOMA ,
M. A. KRIEGER ,
M. N. MEIRELLES  and
M. C. S. PEREIRA
R. BAMBINO-MEDEIROS
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
F. O. R. OLIVEIRA Jr
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
C. M. CALVET
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
D. VICENTE
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
L. TOMA
Affiliation:
Departamento de Bioquímica Universidade Federal de São Paulo, UNIFESP, SP, Rua Tres de Maio, 100 Vila Clementino - São Paulo, SP, 04044-020, Brazil
M. A. KRIEGER
Affiliation:
Instituto Carlos Chagas, Instituto de Biologia Molecular do Paraná/FIOCRUZ, Rua Professor Algacyr Munhoz Mader 3775, Curitiba, PR, 81350-010, Brazil
M. N. MEIRELLES
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
M. C. S. PEREIRA*
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ, 21045-900, Brazil
*
*Corresponding author: Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, Manguinhos, 21045-900 Rio de Janeiro, RJ, Brazil. Tel: +5521 25984330; Fax: +5521 22604434. E-mail: [email protected]
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Summary

Cell surface glycosaminoglycans (GAGs) play an important role in the attachment and invasion process of a variety of intracellular pathogens. We have previously demonstrated that heparan sulfate proteoglycans (HSPG) mediate the invasion of trypomastigote forms of Trypanosoma cruzi in cardiomyocytes. Herein, we analysed whether GAGs are also implicated in amastigote invasion. Competition assays with soluble GAGs revealed that treatment of T. cruzi amastigotes with heparin and heparan sulfate leads to a reduction in the infection ratio, achieving 82% and 65% inhibition of invasion, respectively. Other sulfated GAGs, such as chondroitin sulfate, dermatan sulfate and keratan sulfate, had no effect on the invasion process. In addition, a significant decrease in infection occurred after interaction of amastigotes with GAG-deficient Chinese Hamster Ovary (CHO) cells, decreasing from 20% and 28% in wild-type CHO cells to 5% and 9% in the mutant cells after 2 h and 4 h of infection, respectively. These findings suggest that amastigote invasion also involves host cell surface heparan sulfate proteoglycans. The knowledge of the mechanism triggered by heparan sulfate-binding T. cruzi proteins may provide new potential candidates for Chagas disease therapy.

Keywords

cardiomyocytesTrypanosoma cruziamastigotesheparan sulfaterecognition process
Type
Research Article
Information
Parasitology , Volume 138 , Issue 5 , April 2011 , pp. 593 - 601
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Alves, M. J. and Mortara, R. (2009). A century of research: what have we learned about the interaction of trypanosome cruzi with host cells? Memórias do Instituto Oswaldo Cruz 104, 76–88.CrossRefGoogle ScholarPubMed
Araújo-Jorge, T. C. and De Souza, W. (1998). Interaction of Trypanosoma cruzi with macrophages. Involvement of surface galactose and N-acetyl-D-galactosamine residues on the recognition process. Acta Tropica 45, 127–136.Google Scholar
Barbosa, H. S. and de Meirelles, M. N. (1992). Ultrastructural detection in vitro of WGA-, RCA I-, and Con A-binding sites involved in the invasion of heart muscle cells by Trypanosoma cruzi. Parasitology Research 78, 404–409.CrossRefGoogle ScholarPubMed
Barrias, E. S., Dutra, J. M., De Souza, W. and Carvalho, T. M. (2007). Participation of macrophage membrane rafts in Trypanosoma cruzi invasion process. Biochemical and Biophysical Research Communications 363, 828–834.CrossRefGoogle ScholarPubMed
Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. and Zako, M. (1999). Functions of cell surface heparan sulfate proteoglycans. Annual Review of Biochemistry 68, 729–777.CrossRefGoogle ScholarPubMed
Calvet, C. M., Meuser, M., Almeida, D., Meirelles, M. N. and Pereira, M. C. (2004). Trypanosoma cruzi-cardiomyocyte interaction: role of fibronectin in the recognition process and extracellular matrix expression in vitro and in vivo. Experimental Parasitolology 107, 20–30.CrossRefGoogle ScholarPubMed
Calvet, C. M., Toma, L., De Souza, F. R., Meirelles, M. N. and Pereira, M. C. (2003). Heparan sulfate proteoglycans mediate the invasion of cardiomyocytes by Trypanosoma cruzi. Journal of Eukaryotic Microbiology 50, 97–103.CrossRefGoogle ScholarPubMed
Chen, Q., Sivakumar, P., Barley, C., Peters, D. M., Gomes, R. R., Farach-Carson, M. C. and Dallas, S. L. (2007). Potential role for heparan sulfate proteoglycans in regulation of transforming growth factor-beta (TGF-beta) by modulating assembly of latent TGF-beta-binding protein-1. The Journal of Biological Chemistry 282, 26418–26430.CrossRefGoogle ScholarPubMed
Chen, Y., Goette, M., Liu, J. and Park, P. W. (2008). Microbial subversion of heparan sulfate proteoglycans. Molecular and Cells 26, 415–426.CrossRefGoogle ScholarPubMed
Chu, C. L., Buczek-Thomas, J. A. and Nugent, M. A. (2004). Heparan sulphate proteoglycans modulate fibroblast growth factor-2 binding through a lipid raft-mediated mechanism. The Biochemical Journal 379, 331–341.CrossRefGoogle ScholarPubMed
Dietrich, C. P., Tersariol, I. L., Toma, L., Moraes, C. T., Porcionatto, M. A., Oliveira, F. W. and Nader, H. B. (1998). Structure of heparan sulfate: identification of variable and constant oligosaccharide domains in eight heparan sulfates of different origins. Cell and Molecular Biology 44, 417–429.Google ScholarPubMed
Dreyfuss, J. L., Regatieri, C. V., Jarrouge, T. R., Cavalheiro, R. P., Sampaio, L. O. and Nader, H. B. (2009). Heparan sulfate proteoglycans: structure, protein interactions and cell signaling. Academia Brasileira de Ciências 81, 409–429.CrossRefGoogle ScholarPubMed
Fernandes, A. B. and Mortara, R. A. (2004). Invasion of MDCK epithelial cells with altered expression of Rho GTPases by Trypanosoma cruzi amastigotes and metacyclic trypomastigotes of strains from the two major phylogenetic lineages. Microbes and Infection 6, 460–467.CrossRefGoogle ScholarPubMed
Fernandes, A. B., Neira, I., Ferreira, A. T. and Mortara, R. A. (2006). Cell invasion by Trypanosoma cruzi amastigotes of distinct infectivities: studies on signaling pathways. Parasitology Research 100, 59–68.CrossRefGoogle ScholarPubMed
Fernandes, M. C., Cortez, M., Geraldo Yoneyama, K. A., Straus, A. H., Yoshida, N. and Mortara, R. A. (2007). Novel strategy in Trypanosoma cruzi cell invasion: implication of cholesterol and host cell microdomains. International Journal for Parasitology 37, 1431–1441.CrossRefGoogle ScholarPubMed
Ferreira, D., Cortez, M., Atayde, V. D. and Yoshida, N. (2006). Actin cytoskeleton-dependent and -independent host cell invasion by Trypanosoma cruzi is mediated by distinct parasite surface molecules. Infection and Immunity 74, 5522–5528.CrossRefGoogle ScholarPubMed
Fuki, I. V., Meyer, M. E. and Williams, K. J. (2000). Transmembrane and cytoplasmic domains of syndecan mediate a multi-step endocytic pathway involving detergent-insoluble membrane rafts. The Biochemical Journal 351, 607–612.CrossRefGoogle ScholarPubMed
Granés, F., Urena, J. M., Rocamora, N. and Vilaró, S. (2000). Ezrin links syndecan-2 to the cytoskeleton. Journal of Cell Science 113, 1267–1276.CrossRefGoogle ScholarPubMed
Jacquet, A., Coulon, L., De Nève, J., Daminet, V., Haumont, M., Garcia, L., Bollen, A., Jurado, M. and Biemans, R. (2001). The surface antigen SAG3 mediates the attachment of Toxoplasma gondii to cell-surface proteoglycans. Molecular and Biochemical Parasitology 116, 35–44.CrossRefGoogle ScholarPubMed
Kahn, S., Wleklinski, M., Aruffo, A., Farr, A., Coder, D. and Kahn, M. (1995). Trypanosoma cruzi amastigote adhesion to macrophages is facilitated by the mannose receptor. Journal of Experimental Medicine 182, 1243–1258.CrossRefGoogle ScholarPubMed
Kahn, S. J., Wleklinski, M., Ezekowitz, R. A., Coder, D., Aruffo, A. and Farr, A. (1996). The major surface glycoprotein of Trypanosoma cruzi amastigotes are ligands of the human serum mannose-binding protein. Infection and Immunity 64, 2649–2656.CrossRefGoogle ScholarPubMed
Kawamura, S., Miyamoto, S. and Brown, J. H. (2003). Initiation and transduction of stretch-induced RhoA and Rac1 activation through caveolae: cytoskeletal regulation of ERK translocation. The Journal of Biological Chemistry 278, 31111–31117.CrossRefGoogle ScholarPubMed
Ley, V., Andrews, N. W., Robbins, E. S. and Nussenzweig, V. (1988). Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. The Journal of Experimental Medicine 168, 649–659.CrossRefGoogle ScholarPubMed
Meirelles, M. N., de Araujo-Jorge, T. C., Miranda, C. F., de Souza, W. and Barbosa, H. S. (1986). Interaction of Trypanosoma cruzi with heart muscle cells: ultrastructural and cytochemical analysis of endocytic vacuole formation and effect upon myogenesis in vitro. European Journal of Cell Biology 41, 198–206.Google ScholarPubMed
Menna-Barreto, R. F. S., Corrêa, J. R., Pinto, A. V., Soares, M. J. and de Castro, S. L. (2007). Mitochondrial disruption and DNA fragmentation in Trypanosoma cruzi induced by naphthoimidazoles synthesized from β-lapachone. Parasitology Research 101, 895–905.CrossRefGoogle ScholarPubMed
Moelleken, K. and Hegemann, J. H. (2008). The Chlamydia outer membrane protein OmcB is required for adhesion and exhibits biovar-specific differences in glycosaminoglycan binding. Molecular Microbiology 67, 403–419.CrossRefGoogle ScholarPubMed
Mortara, R. A. (1991). Trypanosoma cruzi: amastigotes and trypomastigotes interact with different structures on the surface of HeLa cells. Experimental Parasitololy 73, 1–14.CrossRefGoogle ScholarPubMed
Mortara, R. A., Andreoli, W. K., Fernandes, M. C., da Silva, C. V., Fernandes, A. B., L'Abbate, C. and da Silva, S. (2008). Host cell actin remodeling in response to Trypanosoma cruzi: trypomastigote versus amastigote entry. Subcellular Biochemistry 47, 101–109.Google ScholarPubMed
Mortara, R. A., Andreoli, W. K., Taniwaki, N. N., Fernandes, A. B., Silva, C. V., Fernandes, M. C., L'Abbate, C. and Silva, S. (2005). Mammalian cell invasion and intracellular trafficking by Trypanosoma cruzi infective forms. Academia Brasileira de Ciências 77, 77–94.CrossRefGoogle ScholarPubMed
Oliveira, F. O. Jr, Alves, C. R., Calvet, C. M., Toma, L., Bouças, R. I., Nader, H. B., Castro, Côrtes, L. M., Krieger, M. A., Meirelles, M. N. and Pereira, M. C. S. (2008). Trypanosoma cruzi heparin-binding proteins and the nature of the host cell heparan sulfate-binding domain. Microbial Pathogenesis 44, 329–338.CrossRefGoogle ScholarPubMed
Ori, A., Wilkinson, M. C. and Fernig, D. G. (2008). The heparanome and regulation of cell function: structures, functions and challenges. Frontiers in Bioscience 13, 4309–4338.CrossRefGoogle ScholarPubMed
Ortega-Barria, E. and Pereira, M. E. (1991). A novel Trypanosoma cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67, 411–421.CrossRefGoogle ScholarPubMed
Plotkowski, M. C., Costa, A. O., Morandi, V., Barbosa, H. S., Nader, H. B., de Bentzmann, S. and Puchelle, E. (2001). Role of heparan sulphate proteoglycans as potential receptors for non-piliated Pseudomonas aeruginosa adherence to non-polarised airway epithelial cells. Journal of Medical Microbiology 50, 183–190.CrossRefGoogle ScholarPubMed
Reddi, H. V. and Lipton, H. L. (2002). Heparan sulfate mediates infection of high-neurovirulence Theiler's viruses. The Journal of Virology 76, 8400–8407.CrossRefGoogle ScholarPubMed
Scharfstein, J. and Morrot, A. (1999). A role for extracellular amastigotes in the immunopathology of Chagas disease. Memórias do Instituto Oswaldo Cruz 94, 51–63.CrossRefGoogle ScholarPubMed
Schuksz, M., Fuster, M. M., Brown, J. R., Crawford, B. E., Ditto, D. P., Lawrence, R., Glass, C. A., Wang, L., Tor, Y. and Esko, J. D. (2008). Surfen, a small molecule antagonist of heparan sulfate. Proceedings of the National Academy of Sciences, USA 105, 13075–13080.CrossRefGoogle ScholarPubMed
Stan, R. V. (2002). Structure and function of endothelial caveolae. Microscopy Research and Technique 57, 350–364.CrossRefGoogle ScholarPubMed
Tehrani, S., Tomasevic, N., Weed, S., Sakowicz, R. and Cooper, J. A. (2007). Src phosphorylation of cortactin enhances actin assembly. Proceedings of the National Academy of Sciences, USA 104, 11933–11938.CrossRefGoogle ScholarPubMed
Tomlinson, S., Vandekerckhove, F., Frevert, U. and Nussenzweig, V. (1995). The induction of Trypanosoma cruzi trypomastigote to amastigote transformation by low pH. Parasitology 110, 547–554.CrossRefGoogle ScholarPubMed
Tossavainen, H., Pihlajamaa, T., Huttunen, T. K., Raulo, E., Rauvala, H., Permi, P. and Kilpeläinen, I. (2006). The layered fold of the TSR domain of P. falciparum TRAP contains a heparin binding site. Protein Science 15, 1760–1768.CrossRefGoogle ScholarPubMed
Yokoyama, N., Okamura, M. and Igarashi, I. (2006). Erythrocyte invasion by Babesia parasites: current advances in the elucidation of the molecular interactions between the protozoan ligands and host receptors in the invasion stage. Veterinary Parasitology 138, 22–32.CrossRefGoogle ScholarPubMed
Yoshida, N. and Cortez, M. (2008). Trypanosoma cruzi: parasite and host cell signaling during the invasion process. Subcellular Biochemistry 47, 82–91.CrossRefGoogle ScholarPubMed
Yung, S. and Chan, T. M. (2007). Glycosaminoglycans and proteoglycans: overlooked entities? Peritoneal Dialysis International 27, 104–109.CrossRefGoogle ScholarPubMed