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

Parasitology

Volumn 139, Issue 6, 2012, Pages 735-743

  Oliveira, F O R ^a   Alves, C R ^a   Souza Silva, F ^a   Calvet, C M ^a   Cortes L M C ^a   Gonzalez, M S ^b   Toma, L ^c   Boucas R I ^c   Nader, H B ^c   Pereira, M C S ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

epimastigotes; heparin binding proteins; Rhodnius prolixus parasite vector interaction; Trypanosoma cruzi

Indexed keywords

BIOTIN; CHONDROITIN SULFATE; HEPARAN SULFATE; HEPARIN BINDING PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; BIOSENSOR; CELL ADHESION; CHAGAS DISEASE; CONTROLLED STUDY; EPIMASTIGOTE; EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RHODNIUS; RHODNIUS PROLIXUS; SCANNING ELECTRON MICROSCOPY; SURFACE PLASMON RESONANCE BIOSENSOR; SURFACE PROPERTY; TRYPANOSOMA CRUZI;

ANIMALS; CELL ADHESION; EPITHELIAL CELLS; GASTROINTESTINAL TRACT; HEPARIN; HOST-PARASITE INTERACTIONS; PROTOZOAN PROTEINS; RHODNIUS; TRYPANOSOMA CRUZI;

HEXAPODA; MAMMALIA; RHODNIUS PROLIXUS; TRYPANOSOMA CRUZI;

EID: 84861084053     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011002344     Document Type: Article

References (49)

1. 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, 31-44.
2. 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, 44-52.
3. 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. 208-256. Blackwell, Oxford, UK.
4. 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, 234-239.
5. 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, 593-601.
6. 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, 218-226.
7. Bonay, P. and Fresno, M. (1995). Characterization of carbohydrate binding proteins in Trypanosoma cruzi. The Journal of Biological Chemistry 270, 11062-11070.
8. 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, 719-729.
9. Bordier, C. (1981). Phase separation of integral membrane proteins in Triton X-114 solution. The Journal of Biological Chemistry 256, 1604-1607.
10. 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, 4559-4568.
11. 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, 97-103.
12. 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, 93-100.
13. 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, 316-327.
14. 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, 251-260.
15. 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, 113-117.
16. 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, 38-42.
17. 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, 15882-15887.
18. 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, 409-429.
19. 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.
20. 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, 1925-1940.
21. 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. 44-47. Rio de Janeiro, Brazil: Fundação Oswaldo Cruz, World Health Organization.
22. 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, 605-610.
23. 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, 297-304.
24. 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, 553-560.
25. 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, 73-83.
26. 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, 504-519.
27. Linder, A., Soehnlein, O. and Akesson, P. (2010). Roles of heparinbinding protein in bacterial infections. Journal of Innate Immunity 2, 431-438.
28. Ly, M., Laremore, T. N. and Linhardt, R. J. (2010). Proteoglycomics: recent progress and future challenges. OMICS 14, 389-399.
29. Matthews, K. R. (2011). Controlling and coordinating development in vector-transmitted parasites. Science 331, 1149-1153.
30. 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, 120-128.
31. Nunes, M. C. and Scherf, A. (2007). Plasmodium falciparum during pregnancy: a puzzling parasite tissue adhesion tropism. Parasitology 134, 1863-1869.
32. 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, 503-511.
33. 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, 329-338.
34. Ortega-Barria, E. and Pereira, M. E. (1991). A novel T. cruzi heparinbinding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67, 411-421.
35. Pradel, G., Garapaty, S. and Frevert, U. (2002). Proteoglycans mediate malaria sporozoite targeting to the liver. Molecular Microbiology 45, 637-651.
36. 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, 11518-11524.
37. Romi, R. (2010). Arthropod-borne diseases in Italy: from a neglected matter to an emerging health problem. Ann Ist Super Sanita 46, 436-443.
38. 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, 18194-18201.
39. 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, 107-112.
40. Schmunis, G. A. (2007). Epidemiology of Chagas disease in non-endemic countries: the role of international migration. Memórias do Instituto Oswaldo Cruz 102, 75-85.
41. 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, 25376-25384.
42. 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, 631-635.
43. 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 SLAMnegative cell lines. Antiviral Research 80, 370-376.
44. Tyler, K. M. and Engman, D. M. (2001). The life cycle of Trypanosoma cruzi revisited. International Journal for Parasitology 31, 472-481.
45. 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, 1251-1260.
46. 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, 223-233.
47. World Health Organization (2005). Tropical disease research: progress 2003-2004. Special Programme for Research and Training in Tropical Disease. Programme Report 17, Geneva, Switzerland.
48. 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.
49. 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, 1473-1478.