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Involvement of sulfated glycosaminoglycans on the development and attachment of Trypanosoma cruzi to the luminal midgut surface in the vector, Rhodnius prolixus

Published online by Cambridge University Press:  09 September 2011

MARCELO S. GONZALEZ ,
LUIZ-CLAUDIO F. SILVA ,
J. M. ALBUQUERQUE-CUNHA ,
NADIR F. S. NOGUEIRA ,
DÉBORA P. MATTOS ,
DANIELE P. CASTRO ,
PATRICIA AZAMBUJA  and
ELOI S. GARCIA
MARCELO S. GONZALEZ*
Affiliation:
Laboratório de Biologia de Insetos, Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense (UFF), Morro do Valonguinho s/n – Centro –Niterói, RJ, 24001-970, Brazil Instituto Nacional de Entomologia Molecular (INCT-EM, CNPq), Brazil
LUIZ-CLAUDIO F. SILVA
Affiliation:
Programa de Glicobiologia, Instituto de Bioquímica Médica, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, CEP 21941-590, Brazil Laboratório de Interações Celulares, Instituto de Ciências Biomédicas, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil
J. M. ALBUQUERQUE-CUNHA
Affiliation:
Laboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21045-900, Brazil
NADIR F. S. NOGUEIRA
Affiliation:
Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Avenida Alberto Lamego, 2000, Horto, Campos dos Goytacases, RJ, 28015-620, Brazil
DÉBORA P. MATTOS
Affiliation:
Laboratório de Biologia de Insetos, Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense (UFF), Morro do Valonguinho s/n – Centro –Niterói, RJ, 24001-970, Brazil
DANIELE P. CASTRO
Affiliation:
Laboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21045-900, Brazil Instituto Nacional de Entomologia Molecular (INCT-EM, CNPq), Brazil
PATRICIA AZAMBUJA
Affiliation:
Laboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21045-900, Brazil Instituto Nacional de Entomologia Molecular (INCT-EM, CNPq), Brazil
ELOI S. GARCIA
Affiliation:
Laboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21045-900, Brazil Instituto Nacional de Entomologia Molecular (INCT-EM, CNPq), Brazil
*
*Corresponding author: Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense, Morro do Valonguinho s/n° Centro –Niterói, RJ, 24001-970, Brazil. Tel: +55 2126292285. Fax: +55 2126292376. E-mail: msgonzalez@id.uff.br
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Summary

In the present study, we investigated the involvement of sulfated glycosaminoglycans in both the in vivo development and adhesion of T. cruzi epimastigotes to the luminal surface of the digestive tract of the insect vector, Rhodnius prolixus. Pre-incubation of T. cruzi, Dm 28c epimastigotes with heparin, chondroitin 4-sulfate, chondroitin 6-sulfate or protamine chloridrate inhibited in vitro attachment of parasites to the insect midgut. Enzymatic removal of heparan sulfate moieties by heparinase I or of chondroitin sulfate moieties by chondroitinase AC from the insect posterior midgut abolished epimastigote attachment in vitro. These treatments also reduced the labelling of anionic sites exposed at the luminal surface of the perimicrovillar membranes in the triatomine midgut epithelial cells. Inclusion of chondroitin 4-sulfate or chondroitin 6-sulfate and to a lesser extent, heparin, in the T. cruzi-infected bloodmeal inhibited the establishment of parasites in R. prolixus. These observations indicate that sulfated glycosaminoglycans are one of the determinants for both adhesion of the T. cruzi epimastigotes to the posterior midgut epithelial cells of the triatomine and the parasite infection in the insect vector, R. prolixus.

Keywords

Trypanosoma cruziRhodnius prolixustriatomid-parasite interactionposterior midgutperitrophic and perimicrovillar membraneglycosaminoglycans
Type
Research Article
Information
Parasitology , Volume 138 , Issue 14 , December 2011 , pp. 1870 - 1877
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Akhtar, J. and Shukla, D. (2009). Viral entry mechanisms: cellular and viral mediators of Herpex simplex virus entry. The FEBS Journal 276, 7228–7236.CrossRefGoogle Scholar
Albuquerque-Cunha, J. M., Gonzalez, M. S., Garcia, E. S., Melllo, C. B., Azambuja, P., Almeida, J. C. A., de Souza, W. and Nogueira, N. F. S. (2009). Cytochemical characterization of microvillar and perimicrovillar membranes in the posterior midgut epithelium of Rhodnius prolixus. Arthropod Structure and Development 38, 31–44.CrossRefGoogle ScholarPubMed
Alves, C. R., Albuquerque-Cunha, J. M., Melllo, C. B., Garcia, E. S., Nogueira, N. F. S., 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.CrossRefGoogle ScholarPubMed
Armitage, P., Berry, G. and Matthews, J. N. S. (2002). Comparison of several groups and experimental design. In Statistical Methods in Medical Research 4th Edn. (ed. Armitage, P.), pp. 208–256. Blackwell Science Publishing, Oxford, UK.CrossRefGoogle Scholar
Azambuja, P. and Garcia, E. S. (1997). Care and maintenance of triatomine colonies. In Molecular Biology of Insect Disease Vectors: a Methods Manual (ed. Crampton, J. M., Beard, C. B. and Louid, C.), pp. 56–64. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Azambuja, P., Ratcliffe, N. A. and Garcia, E. S. (2005). Towards an understanding of the interactions of Trypanosoma cruzi and Trypanosoma rangeli within the reduviid insect host, Rhodnius prolixus. Academia Brasileira de Ciências 77, 397–404.CrossRefGoogle ScholarPubMed
Bambino-Medeiros, R., Oliveira, F. O. R., Calvet, C. M., Vicente, D., Toma, L., Krieger, M. N., Meirelles, M. R. S. L. and Pereira, M. C. S. (2011). Involvement of host cell heparan sulfate proteoglycan in Trypanosoma cruzi amastigote attachment and invasion. Parasitology. doi:10.1017/S0031182010001678.CrossRefGoogle ScholarPubMed
Bonay, P., Molina, R. and Fresno, M. (2001). Binding of mannose-specific carbohydrate-binding protein from the cell surface of Trypanosoma cruzi. Glycobiology 11, 719–729.CrossRefGoogle ScholarPubMed
Bourguignon, S. C., Mello, C. B., Santos, D. O., Gonzalez, M. S. and Souto-Pádron, T. (2006). Biological aspects of the Trypanosoma cruzi (Dm 28c clone) intermediate form, between epimastigote and trypomastigote obtained in modified liver infusion tryptose (LIT) medium. Acta Tropica 98, 103–109.CrossRefGoogle Scholar
Burleigh, B. A. and Woolsey, A. M. (2002). Cell signaling and Trypanosoma cruzi invasion. Cellular Microbiology 4, 701–711.CrossRefGoogle ScholarPubMed
Calvet, C. M., Toma, L., Souza, F. R., Meirelles, M. R. S. L. 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
Carvalho-Moreira, C. J., Spata, M. C. D., Coura, J. R., Garcia, E. S., Azambuja, P., Gonzalez, M. S. and Mello, C. B. (2003). In vivo and in vitro metacyclogenesis tests of two strains of Trypanosoma cruzi in the triatomine vectors Triatoma pseudomaculata and Rhodnius neglectus: short, long-term and comparative study. Experimental Parasitology 103, 102–111.CrossRefGoogle ScholarPubMed
Chagas, C. (1909). Nova tripanosomíase humana. Estudos sobre a morfologia e o ciclo evolutivo do Schizotrypanum cruzi n. gen.,n. sp., agente etiológico de nova entidade mórbida do homem. Memórias do Instituto Oswaldo Cruz 1, 159–218.CrossRefGoogle Scholar
Chagas, C. (1911). Nova entidade mórbida do homem; resumo geral de estudos etiológicos e clínicos. Memórias do Instituto Oswaldo Cruz 3, 219–275.CrossRefGoogle Scholar
Costa-Filho, A., Souza, M. L. S., Martins, R. C. L., dos Santos, A. V. F., Silva, G. V., Comaru, M. W., Moreira, M. F., Atella, G. C., Allodi, S., Nasciutti, L. E., Masuda, H. and Silva, L. C. F. (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.CrossRefGoogle ScholarPubMed
Costa-Filho, A., Werneck, C. C., Nasciutti, L. E., Masuda, H., Atella, G. C. and Silva, L. C. F. (2001). Sulfated glycosaminoglycans from ovary of Rhodnius prolixus. Insect Biochemistry and Molecular Biology 31, 31–40.CrossRefGoogle ScholarPubMed
Dietrich, C. P., Nader, H. B., Toma, L., Azambuja, P. and Garcia, E. S. (1987). A relationship between the inhibition of heparan sulfate and chondroitin sulfate synthesis and the inhibition of molting by selenate in the hemipteran Rhodnius prolixus. Biochemical and Biophysical Research Communications 146, 652–658.CrossRefGoogle ScholarPubMed
Didraga, M., Barroso, B. and Bischoff, R. (2006). Recent developments in proteoglycan purification and analysis. Current Pharmaceutical Analysis 2, 323–27.CrossRefGoogle Scholar
Dinglasan, R. R., Alaganan, A., Ghosh, A. K., Saito, A., van Kuppevelt, T. H. and Jacobs-Lorena, N. (2007). Plasmodium falciparum ookinetes require mosquito midgut chondroitin proteoglycans for cell invasion. Proceedings of the National Academy of Sciences, USA 104, 15882–15887.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, 409–429.CrossRefGoogle ScholarPubMed
Ennes-Vidal, V., Menna-Barreto, R. F. S., Santos, A. L. S., 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. doi:10.1371/journal.pone.0018371.CrossRefGoogle ScholarPubMed
Gandhi, N. S. and Mancera, R. L. (2008). The structure of glycosaminoglycans and their interactions with proteins. Chemical Biological and Drug Design 72, 455–482.CrossRefGoogle ScholarPubMed
Garcia, E. S. and Azambuja, P. (1997). Infection of triatomines with Trypanosoma cruzi. In Molecular Biology of Insect Disease Vectors: A Methods Manual. (ed. Crampton, J.M., Beard, C.B. and Louid, C.), pp. 146–155. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Garcia, E. S., Azambuja, P., Forster, H. and Rembold, H. (1984). Feeding and molt inhibition by azadirachtins A, B and 7-acetylazadirachtin A in Rhodnius prolixus nymphs. Zeitschrift für Naturforschung 29, 1155–1158.CrossRefGoogle Scholar
Garcia, E. S., Azambuja, P., Nader, H. B. and Dietrich, C. P. (1986). Biosynthesis of sulfated glycosaminoglycans in the hemipteran Rhodnius prolixus. Enhancement of chondroitin sulfate synthesis by phenylxyloside. Insect Biochemistry 16, 347–352.CrossRefGoogle Scholar
Garcia, E. S., Genta, F. A., Azambuja, P. and Schaub, G. A. (2010). Interactions between intestinal compounds of triatomines and Trypanosoma cruzi. Trends in Parasitology 26, 499–505.CrossRefGoogle ScholarPubMed
Garcia, E. S., Gonzalez, M. S., Azambuja, P., Baralle, F. E., Frainderaich, D., Torres, H. N. and Flawia, M. M. (1995). Induction of Trypanosoma cruz metacyclogenesis in the gut of hematophagous insect vector, Rhodnius prolixus, by hemoglobin and peptides carrying α D-globin sequences. Experimental Parasitology 81, 255–261.CrossRefGoogle Scholar
Garcia, E. S., Ratcliffe, N. A., Whitten, M. M., Gonzalez, M. S. and Azambuja, P. (2007). Exploring the role of insect host factors in the dynamics of Trypanosoma cruzi-Rhodnius prolixus interactions. Journal of Insect Physiology 53, 11–21.CrossRefGoogle ScholarPubMed
Garcia-Abreu, J., Mendes, F. A., Onofre, G. R., Freitas, M. S., Silva, L. C. F., Moura Neto, V. and Cavalcante, L. A. (2000). Contribution of heparan sulfate to the non-permissive role of the midline glia to the growth of midbrain neuritis. Glia 29, 260–272.3.0.CO;2-I>CrossRefGoogle Scholar
Gasic, G. J., Berwick, L. and Sorrentino, M. (1968). Positive and negative colloidal iron as cell surface electron stains. Laboratory Investigations 18, 63–71.Google ScholarPubMed
Gillet, J. D. (1935). The genital sterna of the immature stages of Rhodnius prolixus (Hemiptera). Transactions of the Royal Entomological Society of London 83, 1–5.CrossRefGoogle Scholar
Gonzalez, M. S., Hamedi, A., Albuquerque-Cunha, J. M., Nogueira, N. F. S., 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.CrossRefGoogle ScholarPubMed
Gonzalez, M. S. and Garcia, E. S. (1992). Effect of azadirachtin on the development of Trypanosoma cruzi in different species of triatomine insect vectors: Long-term and comparative studies. Journal of Invertebrate Pathology 60, 201–205.CrossRefGoogle ScholarPubMed
Gonzalez, M. S., Nogueira, N. F. S., Feder, D., de Souza, W., Azambuja, P. and Garcia, E. S. (1998). Role of the head in the ultrastructural midgut organization in Rhodnius prolixus: evidence from head transplantation experiments and ecdysone therapy. Journal of Insect Physiology 44, 553–560.CrossRefGoogle Scholar
Gonzalez, M. S., Nogueira, N. F. S., Mello, C. B., de Souza, W., Schaub, G. A., Azambuja, P. and Garcia, E. S. (1999). Influence of brain on the midgut arrangement and Trypanosoma cruzi development in the vector, Rhodnius prolixus. Experimental Parasitology 92, 100–108.CrossRefGoogle Scholar
Houk, E. J., Hardy, J. L. and Chiles, R. E. (1986). Mesenteronal epithelial cell surface charge of the mosquito, Culex tarsalis Coquillett, binding of colloidal iron hydroxide, native ferritin and cationized ferritin. Journal of Submicroscope Cytology and Pathology 18, 385–396.Google ScholarPubMed
Lent, H. and Juberg, J. (1969). O Genero Rhodnius Stal, 1859, com um estudo sobre a genitalia das especies (Hemiptera, Reduviidae, Triatominae). Revista Brasileira de Biologia 29, 487–560.Google Scholar
Moncayo, A. and Silveira, A. C. (2009). Current epidemiological trends for Chagas disease in Latin America and future challenges in epidemiology, surveillance and health policy. Memórias do Instituto Oswaldo Cruz 104, 17–30.CrossRefGoogle ScholarPubMed
Nadanaka, S. and Kitagawa, H. (2008). Heparan sulphate biosynthesis and disease. Journal of Biochemistry 144, 7–14.CrossRefGoogle ScholarPubMed
Nader, H. B., Lopes, C. C., Rocha, H. A. O., Santos, E. A. and Dietrich, C. (2004). Heparins and heparinoids: occurrence, structure and mechanism of antithrombotic and hemorrhagic activities. Current Pharmacological Design 10, 951–966.CrossRefGoogle ScholarPubMed
Ni Ainle, F., Preston, R. J. S., Jenkis, P. V., Nel, H. J., Johnson, J. A., Smith, O. P., White, B., Fallon, P. G. and O'Donnell, J. S. (2009). Protamine sulfate down-regulates thrombin generation by inhibiting factor V activation. Blood 114, 1658–1665.CrossRefGoogle ScholarPubMed
Nogueira, N. F. S., Gonzalez, M. S., Garcia, E. S., Mello, C. B. and de Souza, W. (1997). Effects of azadirachtin on the fine structure of the midgut of Rhodnius prolixus. Journal of Invertebrate Pathology 69, 58–63.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., Zingales, B. and Colli, W. (2007). Trypanosoma cruzi: Involvement of glycoinositolphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus. Experimental Parasitology 116, 120–128.CrossRefGoogle Scholar
Oliveira, F. O. R., Alves, C. R., Calvet, C. M., Toma, L., Bouças, R. I., Nader, H. B., Côrtes, L. M. C., Krieger, M. A., Meirelles, M. N. S. L. 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
Pereira, M. E. A., Andrade, A. F. B. and Ribeiro, J. M. C. (1981). Lectins of distinct specificity in Rhodnius prolixus interact selectively with Trypanosoma cruzi. Science 211, 597–600.CrossRefGoogle ScholarPubMed
Sapp, M. and Bienkowska-Haba, M. (2009). Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus. The FEBS Journal 276, 7206–7216.CrossRefGoogle Scholar
Schaub, G. A. (2009). Interactions of trypanosomatids and triatomines. In Advances in Insect Physiology 37, 177–242.CrossRefGoogle Scholar
Sinnis, P., Coppi, A., Toida, T., Toyoda, H., Hinoshita-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.CrossRefGoogle ScholarPubMed
Souza, M. L. S., Sarquis, O., Gomes, T. F., Moreira, M. F., Lima, M. M. and Silva, L. C. F. (2004). Sulfated glycosaminoglycans in two hematophagous arthropod vectors of Chagas disease, Triatoma brasiliensis and Rhodnius prolixus (Hemiptera: Reduviidae). Comparative Biochemistry and Physiology B 139, 631–634.CrossRefGoogle ScholarPubMed
Tan, H. and Andrews, N. W. (2002). Don't bother to knock – the cell invasion strategy of Trypanosoma cruzi. Trends in Parasitology 18, 427–428.CrossRefGoogle ScholarPubMed
Taylor, K. R. and Gallo, R. L. (2006). Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB Journal 20, 9–22.CrossRefGoogle ScholarPubMed
Terra, W. R. (1990). Evolution of digestive system of insects – review. Annual Review of Entomology 35, 181–200.CrossRefGoogle Scholar
Tonnaer, E. L. G. M., Hafmans, T. G., van Kuppevelt, T. H., Sanders, E. A. M., Verwejj, P. E. and Curfs, J. H. A. J. (2006). Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells. Microbes and Infection 8, 316–322.CrossRefGoogle ScholarPubMed
Tyler, K. M. and Engman, D. M. (2000). Flagellar elongation induced by glucose limitation is preadaptive for Trypanosoma cruzi differentiation. Cell Motility and the Cytoskeleton 46, 269–278.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Tyler, K. M. and Engman, D. M. (2001). The life cycle of Trypanosoma cruzi revisited. International Journal for Parasitology 31, 472–481.CrossRefGoogle ScholarPubMed
Volpi, N. (2006). Advances in chondroitin sulfate analysis: application in physiological and pathological states of connective tissue and during pharmacological treatment of osteoarthritis. Current Pharmaceutical Design 12, 639–58.CrossRefGoogle ScholarPubMed
Yamada, S. and Sugahara, K. (2008). Potential therapeutic application of chondroitin sulfate/dermatan sulfate. Current Drug Discovery Technologies 5, 289–301.CrossRefGoogle ScholarPubMed
World Health Organization (2002). Chagas' disease. UNPD World Bank WHO, Special Program for Research and Training in Tropical Disease (TDR), Strategic Direction for Research. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2007). Reporte sobre la enfermedad de Chagas. UNICEF UNPD World Bank WHO, Special Program for Research and Training in Tropical Disease (TDR), Strategic Direction for Research. World Health Organization, Geneva, Switzerland.Google Scholar