Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-23T07:28:53.613Z Has data issue: false hasContentIssue false

Trypanosoma cruzi heparin-binding proteins mediate the adherence of epimastigotes to the midgut epithelial cells of Rhodnius prolixus

Published online by Cambridge University Press:  07 February 2012

F. O. R. OLIVEIRA -Jr
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, RJ, Brazil
C. R. ALVES
Affiliation:
Laboratório de Biologia Molecular e Doenças Endêmicas, Instituto Oswaldo Cruz/FIOCRUZ, RJ, Brazil
F. SOUZA-SILVA
Affiliation:
Laboratório de Biologia Molecular e Doenças Endêmicas, Instituto Oswaldo Cruz/FIOCRUZ, RJ, Brazil
C. M. CALVET
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, RJ, Brazil
L. M. C. CÔRTES
Affiliation:
Laboratório de Biologia Molecular e Doenças Endêmicas, Instituto Oswaldo Cruz/FIOCRUZ, RJ, Brazil
M. S. GONZALEZ
Affiliation:
Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense, RJ, Brazil
L. TOMA
Affiliation:
Departamento de Bioquímica, Universidade Federal de São Paulo, UNIFESP, SP, Brazil
R. I. BOUÇAS
Affiliation:
Departamento de Bioquímica, Universidade Federal de São Paulo, UNIFESP, SP, Brazil
H. B. NADER
Affiliation:
Departamento de Bioquímica, Universidade Federal de São Paulo, UNIFESP, SP, Brazil
M. C. S. PEREIRA*
Affiliation:
Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz/FIOCRUZ, RJ, Brazil
*
*Corresponding author: Laboratório de Ultra-estrutura Celular, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil 4365, Manguinhos, 21040-900 Rio de Janeiro, RJ, Brazil. Tel: +55 21 2598 4330. Fax: +55 21 2598 4330. E-mail: [email protected]

Summary

Heparin-binding proteins (HBPs) have been demonstrated in both infective forms of Trypanosoma cruzi and are involved in the recognition and invasion of mammalian cells. In this study, we evaluated the potential biological function of these proteins during the parasite-vector interaction. HBPs, with molecular masses of 65·8 kDa and 59 kDa, were isolated from epimastigotes by heparin affinity chromatography and identified by biotin-conjugated sulfated glycosaminoglycans (GAGs). Surface plasmon resonance biosensor analysis demonstrated stable receptor-ligand binding based on the association and dissociation values. Pre-incubation of epimastigotes with GAGs led to an inhibition of parasite binding to immobilized heparin. Competition assays were performed to evaluate the role of the HBP-GAG interaction in the recognition and adhesion of epimastigotes to midgut epithelial cells of Rhodnius prolixus. Epithelial cells pre-incubated with HBPs yielded a 3·8-fold inhibition in the adhesion of epimastigotes. The pre-treatment of epimastigotes with heparin, heparan sulfate and chondroitin sulfate significantly inhibited parasite adhesion to midgut epithelial cells, which was confirmed by scanning electron microscopy. We provide evidence that heparin-binding proteins are found on the surface of T. cruzi epimastigotes and demonstrate their key role in the recognition of sulfated GAGs on the surface of midgut epithelial cells of the insect vector.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Albuquerque-Cunha, J. M., Gonzalez, M. S., Garcia, E. S., Mello, C. B., Azambuja, P., Almeida, J. C., de Souza, W. and Nogueira, N. F. (2009). Cytochemical characterization of microvillar and perimicrovillar membranes in the posterior midgut epithelium of Rhodnius prolixus. Arthropod Structure & Development 38, 3144.CrossRefGoogle ScholarPubMed
Alves, C. R., Albuquerque-Cunha, J. M., Mello, C. B., Garcia, E. S., Nogueira, N. F., Bourguingnon, S. C., de Souza, W., Azambuja, P. and Gonzalez, M. S. (2007). Trypanosoma cruzi: attachment to perimicrovillar membrane glycoproteins of Rhodnius prolixus. Experimental Parasitology 116, 4452.CrossRefGoogle ScholarPubMed
Armitage, P., Berry, G. and Matthews, J. N. S. (2002). Comparision of several groups and experimental design. In Statistical Methods in Medical Research 4th Edn (ed. Armitage, P.), pp. 208256. Blackwell, Oxford, UK.CrossRefGoogle Scholar
Azevedo-Pereira, R. L., Pereira, M. C., Oliveira-Junior, F. O., Brazil, R. P., Côrtes, L. M., Madeira, M. F., Santos, A. L., Toma, L. and Alves, C. R. (2007). Heparin binding proteins from Leishmania (Viannia) braziliensis promastigotes. Veterinary Parasitology 145, 234239.CrossRefGoogle ScholarPubMed
Bambino-Medeiros, R., Oliveira, F. O., Calvet, C. M., Vicente, D., Toma, L., Krieger, M. A., Meirelles, M. N. and Pereira, M. C. (2011). Involvement of host cell heparan sulfate proteoglycan in Trypanosoma cruzi amastigote attachment and invasion. Parasitology 138, 593601.CrossRefGoogle ScholarPubMed
Bouças, R. I., Trindade, E. S., Tersariol, I. L. S., Dietrich, C. P. and Nader, H. B. (2008). Development of an enzyme-linked immunosorbent assay (ELISA)-like fluorescence assay to investigate the interactions of glycosaminoglycans to cells. Analytica Chimica Acta 618, 218226.CrossRefGoogle ScholarPubMed
Bonay, P. and Fresno, M. (1995). Characterization of carbohydrate binding proteins in Trypanosoma cruzi. The Journal of Biological Chemistry 270, 1106211070.CrossRefGoogle ScholarPubMed
Bonay, P., Molina, R. and Fresno, M. (2001). Binding specificity of mannose-specific carbohydrate-binding protein from the cell surface of Trypanosoma cruzi. Glycobiology 11, 719729.CrossRefGoogle ScholarPubMed
Bordier, C. (1981). Phase separation of integral membrane proteins in Triton X-114 solution. The Journal of Biological Chemistry 256, 16041607.CrossRefGoogle ScholarPubMed
Boyle, M. J., Richards, J. S., Gilson, P. R., Chai, W. and Beeson, J. G. (2010). Interactions with heparin-like molecules during erythrocyte invasion by Plasmodium falciparum merozoites. Blood 115, 45594568.CrossRefGoogle ScholarPubMed
Calvet, C. M., Toma, L., De Souza, F. R., Meirelles, M. N. and Pereira, M. C. S. (2003). Heparan sulfate proteoglycans mediate the invasion of cardiomyocytes by Trypanosoma cruzi. The Journal of Eukaryotic Microbiology 50, 97103.CrossRefGoogle ScholarPubMed
Camargo, E. P. (1964). Growth and differentiation in Trypanosoma cruzi. I – Origin of metacyclic trypanosomes in liquid media. Revista do Instituto de Medicina Tropical de São Paulo 6, 93100.Google ScholarPubMed
Coppi, A., Tewari, R., Bishop, J. R., Bennett, B. L., Lawrence, R., Esko, J. D., Billker, O. and Sinnis, P. (2007). Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host & Microbe 2, 316327.CrossRefGoogle ScholarPubMed
Costa-Filho, A., Souza, M. L., Martins, R. C., dos Santos, A. V., Silva, G. V., Comaru, M. W., Moreira, M. F., Atella, G. C., Allodi, S., Nasciutti, L. E., Masuda, H. and Silva, L. C. (2004). Identification and tissue-specific distribution of sulfated glycosaminoglycans in the blood-sucking bug Rhodnius prolixus (Linnaeus). Insect Biochemistry and Molecular Biology 34, 251260.CrossRefGoogle ScholarPubMed
Coura, J. R. (2006). Transmission of chagasic infection by oral route in the natural history of Chagas disease. Revista da Sociedade Brasileira de Medicina Tropical 3, 113117.Google Scholar
Develoux, M., Lescure, F. X., Jaureguiberry, S., Jeannel, D., Elghouzzi, M. H., Gay, F., Paris, L., Le Loup, G., Danis, M. and Pialoux, G. (2010). Emergence of Chagas’ disease in Europe: description of the first cases observed in Latin American immigrants in mainland France. Médicine Tropicale 70, 3842.Google ScholarPubMed
Dinglasan, R. R., Alaganan, A., Ghosh, A. K., Saito, A., van Kuppevelt, T. H. and Jacobs-Lorena, M. (2007). Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion. Proceedings of the National Academy of Sciences, USA 104, 1588215887.CrossRefGoogle 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. Anais da Academia Brasileira de Ciências 81, 409429.CrossRefGoogle ScholarPubMed
Ennes-Vidal, V., Menna-Barreto, R. F., Santos, A. L., Branquinha, M. H. and d'Avila-Levy, C. M. (2011). MDL28170, a Calpain Inhibitor, Affects Trypanosoma cruzi Metacyclogenesis, Ultrastructure and Attachment to Rhodnius prolixus Midgut. PLoS One 6, e18371.CrossRefGoogle ScholarPubMed
Fang, Y., Ferrie, A. M., Fontaine, N. H., Mauro, J. and Balakrishnan, J. (2006). Resonant waveguide grating biosensor for living cell sensing. Biophysical Journal 91, 19251940.CrossRefGoogle ScholarPubMed
Garcia, E. S., Azambuja, P. and Contreras, V. T. (1984). Large-scale rearing of Rhodnius prolixus and production of metacyclic trypomastigotes of Trypanosoma cruzi. In Genes and Antigens of Parasites a Laboratory Manual (ed. Morel, C. M.), pp. 4447. Rio de Janeiro, Brazil: Fundação Oswaldo Cruz, World Health Organization.Google Scholar
Garcia, E. S., Castro, D. P., Figueiredo, M. B. and Azambuja, P. (2010). Immune homeostasis to microorganisms in the guts of triatomines (Reduviidae) – a review. Memórias do Instituto Oswaldo Cruz 105, 605610.CrossRefGoogle ScholarPubMed
Gonzalez, M. S., Hamedi, A., Albuquerque-Cunha, J. M., Nogueira, N. F., De Souza, W., Ratcliffe, N. A., Azambuja, P., Garcia, E. S. and Mello, C. B. (2006). Antiserum against perimicrovillar membranes and midgut tissue reduces the development of Trypanosoma cruzi in the insect vector, Rhodnius prolixus. Experimental Parasitology 114, 297304.CrossRefGoogle ScholarPubMed
Gonzalez, M. S., Nogueira, N. F. S., Feder, D., de Souza, W., Feder, D., Nogueira, N. F. and Gonzalez, M. S. (1998). Role of the head in the ultrastructural midgut organization in Rhodnius prolixus larvae: evidence from head transplantation experiments and ecdysone therapy. Journal of Insect Physiology 44, 553560.CrossRefGoogle Scholar
Herrera, E. M., Ming, M., Ortega-Barria, E. and Pereira, M. E. (1994). Mediation of Trypanosoma cruzi invasion by heparan sulfate receptors on host cells and penetrin counter-receptors on the trypanosomes. Molecular and Biochemical Parasitology 65, 7383.CrossRefGoogle ScholarPubMed
Lefèvre, T. and Thomas, F. (2008). Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infection, Genetics and Evolution 8, 504519.CrossRefGoogle ScholarPubMed
Linder, A., Soehnlein, O. and Akesson, P. (2010). Roles of heparin-binding protein in bacterial infections. Journal of Innate Immunity 2, 431438.CrossRefGoogle ScholarPubMed
Ly, M., Laremore, T. N. and Linhardt, R. J. (2010). Proteoglycomics: recent progress and future challenges. OMICS 14, 389399.CrossRefGoogle ScholarPubMed
Matthews, K. R. (2011). Controlling and coordinating development in vector-transmitted parasites. Science 331, 11491153.CrossRefGoogle ScholarPubMed
Nogueira, N. F., Gonzalez, M. S., Gomes, J. E., de Souza, W., Garcia, E. S., Azambuja, P., Nohara, L. L., Almeida, I. C. and Zingales, B. (2007). Trypanosoma cruzi: involvement of glycoinositolphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus. Experimental Parasitology 116, 120128.CrossRefGoogle Scholar
Nunes, M. C. and Scherf, A. (2007). Plasmodium falciparum during pregnancy: a puzzling parasite tissue adhesion tropism. Parasitology 134, 18631869.CrossRefGoogle ScholarPubMed
Oli, M. W., McArthur, W. P. and Brady, L. J. (2006). A whole cell BIAcore assay to evaluate P1-mediated adherence of Streptococcus mutans to human salivary agglutinin and inhibition by specific antibodies. Journal of Microbiological Methods 65, 503511.CrossRefGoogle ScholarPubMed
Oliveira, F. O. Jr., Alves, C. R., Calvet, C. M., Toma, L., Bouças, R. I., Nader, H. B., Côrtes, L. M., Krieger, M. A., Meirelles Mde, N. and Pereira, M. C. (2008). Trypanosoma cruzi heparin-binding proteins and the nature of the host cell heparan sulfate-binding domain. Microbial Pathogenesis 44, 329338.CrossRefGoogle ScholarPubMed
Ortega-Barria, E. and Pereira, M. E. (1991). A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67, 411421.CrossRefGoogle ScholarPubMed
Pradel, G., Garapaty, S. and Frevert, U. (2002). Proteoglycans mediate malaria sporozoite targeting to the liver. Molecular Microbiology 45, 637651.CrossRefGoogle ScholarPubMed
Rathore, D., McCutchan, T. F., Garboczi, D. N., Toida, T., Hernáiz, M. J., LeBrun, L. A., Lang, S. C. and Linhardt, R. J. (2001). Direct Measurement of the Interactions of Glycosaminoglycans and a Heparin Decasaccharide with the Malaria Circumsporozoite Protein. Biochemistry 40, 1151811524.CrossRefGoogle Scholar
Romi, R. (2010). Arthropod-borne diseases in Italy: from a neglected matter to an emerging health problem. Ann Ist Super Sanita 46, 436443.Google Scholar
Sava, I. G., Zhang, F., Toma, I., Theilacker, C., Li, B., Baumert, T. F., Holst, O., Linhardt, R. J. and Huebner, J. (2009). Novel interactions of glycosaminoglycans and bacterial glycolipids mediate binding of enterococci to human cells. The Journal of Biological Chemistry 284, 1819418201.CrossRefGoogle ScholarPubMed
Scagliarini, A., Gallina, L., Dal Pozzo, F., Battilani, M., Ciulli, S. and Prosperi, S. (2004). Heparin binding activity of orf virus F1L protein. Virus Research 105, 107112.CrossRefGoogle ScholarPubMed
Schmunis, G. A. (2007). Epidemiology of Chagas disease in non-endemic countries: the role of international migration. Memórias do Instituto Oswaldo Cruz 102, 7585.CrossRefGoogle ScholarPubMed
Sinnis, P., Coppi, A., Toida, T., Kinoshita-Toyoda, A., Xie, J., Kemp, M. M. and Linhardt, R. J. (2007). Mosquito heparan sulfate and its potential role in malaria infection and transmission. The Journal of Biological Chemistry 282, 2537625384.CrossRefGoogle ScholarPubMed
Souza, M. L., Sarquis, O., Gomes, T. F., Moreira, M. F., Lima, M. M. and Silva, L. C. (2004). Sulfated glycosaminoglycans in two hematophagous arthropod vectors of Chagas disease, Triatoma brasiliensis and Rhodnius prolixus (Hemiptera: Reduviidae). Comparative Biochemistry and Physiology 139, 631635.CrossRefGoogle ScholarPubMed
Terao-Muto, Y., Yoneda, M., Seki, T., Watanabe, A., Tsukiyama-Kohara, K., Fujita, K. and Kai, C. (2008). Heparin-like glycosaminoglycans prevent the infection of measles virus in SLAM-negative cell lines. Antiviral Research 80, 370376.CrossRefGoogle ScholarPubMed
Tyler, K. M. and Engman, D. M. (2001). The life cycle of Trypanosoma cruzi revisited. International Journal for Parasitology 31, 472481.CrossRefGoogle ScholarPubMed
Villalta, F., Scharfstein, J., Ashton, A. W., Tyler, K. M., Guan, F., Mukherjee, S., Lima, M. F., Alvarez, S., Weiss, L. M., Huang, H., Machado, F. S. and Tanowitz, H. B. (2009). Perspectives on the Trypanosoma cruzi-host cell receptor interactions. Parasitology Research 104, 12511260.CrossRefGoogle ScholarPubMed
Wadström, T. and Ljungh, A. (1999). Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. Journal of Medical Microbiology 48, 223233.CrossRefGoogle ScholarPubMed
World Health Organization (2005). Tropical disease research: progress 2003–2004. Special Programme for Research and Training in Tropical Disease. Programme Report 17, Geneva, Switzerland.Google Scholar
Williams, C. R., Bader, C. A., Kearney, M. R., Ritchie, S. A. and Russel, R. C. (2010). The extinction of dengue through natural vulnerability of its vectors. PLoS Neglected Tropical Diseases 4, e922.CrossRefGoogle ScholarPubMed
Zimmermann, L. T., Folly, E., Gomes, M. T. and Alviano, D. S., Alviano, C. S., Silva-Filho, F. C., Atella, G. C. and Lopes, A. H. (2010). Effects of platelet-activating factor on the interaction of Trypanosoma cruzi with Rhodnius prolixus. Parasitology Research 108, 14731478.CrossRefGoogle ScholarPubMed