Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T09:52:17.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Colonization of Rhodnius prolixus gut by Trypanosoma cruzi involves an extensive parasite killing

Published online by Cambridge University Press:  28 January 2016

ROBERTA CARVALHO FERREIRA ,
RAFAEL LUIS KESSLER ,
MARCELO GUSTAVO LORENZO ,
RAFAELA MAGALHÃES MACEDO PAIM ,
LUCIANA DE LIMA FERREIRA ,
CHRISTIAN MACAGNAN PROBST ,
JULIANA ALVES-SILVA  and
ALESSANDRA APARECIDA GUARNERI Open the ORCID record for ALESSANDRA APARECIDA GUARNERI [Opens in a new window]
ROBERTA CARVALHO FERREIRA
Affiliation:
Vector Behavior and Pathogen Interaction Group, Centro de Pesquisas René Rachou, Fiocruz, Av. Augusto de Lima, 1715, Belo Horizonte, Minas Gerais, Brazil
RAFAEL LUIS KESSLER
Affiliation:
Laboratory of Functional Genomic, Instituto Carlos Chagas, Fiocruz, Rua Prof. Algacyr Munhoz Mader, 3775, 81350-010 Curitiba, Paraná, Brazil
MARCELO GUSTAVO LORENZO
Affiliation:
Vector Behavior and Pathogen Interaction Group, Centro de Pesquisas René Rachou, Fiocruz, Av. Augusto de Lima, 1715, Belo Horizonte, Minas Gerais, Brazil
RAFAELA MAGALHÃES MACEDO PAIM
Affiliation:
Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Pres. Antônio Carlos 6627, Pampulha, 31270-901 Belo Horizonte, Minas Gerais, Brazil
LUCIANA DE LIMA FERREIRA
Affiliation:
Vector Behavior and Pathogen Interaction Group, Centro de Pesquisas René Rachou, Fiocruz, Av. Augusto de Lima, 1715, Belo Horizonte, Minas Gerais, Brazil
CHRISTIAN MACAGNAN PROBST
Affiliation:
Laboratory of Functional Genomic, Instituto Carlos Chagas, Fiocruz, Rua Prof. Algacyr Munhoz Mader, 3775, 81350-010 Curitiba, Paraná, Brazil
JULIANA ALVES-SILVA
Affiliation:
Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Pres. Antônio Carlos 6627, Pampulha, 31270-901 Belo Horizonte, Minas Gerais, Brazil
ALESSANDRA APARECIDA GUARNERI*
Affiliation:
Vector Behavior and Pathogen Interaction Group, Centro de Pesquisas René Rachou, Fiocruz, Av. Augusto de Lima, 1715, Belo Horizonte, Minas Gerais, Brazil
*
* Corresponding author: Vector Behavior and Pathogen Interaction Group, Centro de Pesquisas René Rachou, Avenida Augusto de Lima, 1715, CEP 30190-002, Belo Horizonte, Minas Gerais, Brazil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Trypanosoma cruzi, the etiological agent of Chagas disease, is ingested by triatomines during their bloodmeal on an infected mammal. Aiming to investigate the development and differentiation of T. cruzi inside the intestinal tract of Rhodnius prolixus at the beginning of infection we fed insects with cultured epimastigotes and blood trypomastigotes from infected mice to determine the amount of recovered parasites after ingestion. Approximately 20% of the ingested parasites was found in the insect anterior midgut (AM) 3 h after feeding. Interestingly, a significant reduction (80%) in the numbers of trypomastigotes was observed after 24 h of infection suggesting that parasites were killed in the AM. Moreover, few parasites were found in that intestinal portion after 96 h of infection. The evaluation of the numbers of parasites in the posterior midgut (PM) at the same periods showed a reduced parasite load, indicating that parasites were not moving from the AM. Additionally, incubation of blood trypomastigotes with extracts from R. prolixus AMs revealed that components of this tissue could induce significant death of T. cruzi. Finally, we observed that differentiation from trypomastigotes to epimastigotes is not completed in the AM; instead we suggest that trypomastigotes change to intermediary forms before their migration to the PM, where differentiation to epimastigotes takes place. The present work clarifies controversial points concerning T. cruzi development in insect vector, showing that parasite suffers a drastic decrease in population size before epimastigonesis accomplishment in PM.

Keywords

Trypanosoma cruziRhodnius prolixusepimastigogenesistrypanosomeChagas disease
Type
Research Article
Information
Parasitology , Volume 143 , Issue 4 , April 2016 , pp. 434 - 443
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Albesa, I. and Eraso, A. J. (1981). Primary isolation of Trypanosoma cruzi using hemoculture: effect of media composition on epimastigote differentiation. Revista Argentina de Microbiología 13, 53–58.Google Scholar
Amino, R., Martins, R. M., Procopio, J., Hirata, I. Y., Juliano, M. A. and Schenkman, S. (2002). Trialysin, a novel pore-forming protein from saliva of hematophagous insects activated by limited proteolysis. Journal of Biological Chemistry 277, 6207–6213.Google Scholar
Araújo, C. A., Cabello, P. H. and Jansen, A. M. (2007). Growth behaviour of two Trypanosoma cruzi strains in single and mixed infections: in vitro and in the intestinal tract of the blood-sucking bug, Triatoma brasiliensis . Acta Tropica 101, 225–231.Google Scholar
Azambuja, P., Guimarães, J. and Garcia, E. (1983). Haemolytic factor from the crop of Rhodnius prolixus: evidence and partial characterization. Journal of Insect Physiology 29, 833–837.Google Scholar
Azambuja, P., Feder, D. and Garcia, E. (2004). Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Experimental Parasitology 107, 89–96.Google 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 . Anais da Academia Brasileira de Ciencias 77, 397–404.CrossRefGoogle ScholarPubMed
Bonney, K. M. (2014). Chagas disease in the 21st Century: a public health success or an emerging threat? Parasite 21, 11.CrossRefGoogle ScholarPubMed
Botto-Mahan, C. (2009). Trypanosoma cruzi induces life-history trait changes in the wild kissing bug Mepraia spinolai: implications for parasite transmission. Vector-Borne and Zoonotic Diseases 9, 505–510.Google Scholar
Brener, Z. (1962). Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi . Revista do Instituto de Medicina Tropical de Sao Paulo 4, 389–396.Google ScholarPubMed
Brener, Z. and Chiari, E. (1963). Variações morfológicas observadas em diferentes amostras de Trypanosoma cruzi . Revista do Instituto de Medicina Tropical de Sao Paulo 5, 220–224.Google Scholar
Caldas, S., Caldas, I. S., de Figueiredo Diniz, L., de Lima, W. G., de Paula Oliveira, R., Cecílio, A. B., Ribeiro, I., Talvani, A. and Bahia, M. T. (2012). Real-time PCR strategy for parasite quantification in blood and tissue samples of experimental Trypanosoma cruzi infection. Acta Tropica 123, 170–177.Google Scholar
Carvalho-Moreira, C., Spata, M., Coura, J., Garcia, E., Azambuja, P., Gonzalez, M. and Mello, C. (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
Castro, D. P., Moraes, C. S., Gonzalez, M. S., Ratcliffe, N. A., Azambuja, P. and Garcia, E. S. (2012). Trypanosoma cruzi immune response modulation decreases microbiota in Rhodnius prolixus gut and is crucial for parasite survival and development. PLoS ONE 7, e36591.CrossRefGoogle ScholarPubMed
Chagas, C. J. (1909). Nova tripanozomíase humana. Estudos sobre a morfologia e ciclo evolutivo do Schizotrypanum cruzi n.gen., n.sp. agente etiológico de nova entidade mórbida do homem. Memorias do Instituto Oswaldo Cruz 1, 159–218.Google Scholar
Chuenkova, M. V. and Pereira, M. A. (2000). A trypanosomal protein synergizes with the cytokines ciliary neurotrophic factor and leukemia inhibitory factor to prevent apoptosis of neuronal cells. Molecular Biology of the Cell 11, 1487–1498.CrossRefGoogle ScholarPubMed
Contreras, V. T., Lima, A. R. and Navarro, M. C. (2006). Trypanosoma cruzi morphogenesis: relevant factors for in vitro differentiation. Acta Biológica Venezuelica 26, 49–60.Google Scholar
Cordero, E. M., Gentil, L. G., Crisante, G., Ramírez, J. L., Yoshida, N., Anez, N. and da Silveira, J. F. (2008). Expression of GP82 and GP90 surface glycoprotein genes of Trypanosoma cruzi during in vivo metacyclogenesis in the insect vector Rhodnius prolixus . Acta Tropica 105, 87–91.Google Scholar
Cortez, M., Gonzalez, M., Cabral, M., Garcia, E. and Azambuja, P. (2002). Dynamic development of Trypanosoma cruzi in Rhodnius prolixus: role of decapitation and ecdysone therapy. Parasitology Research 88, 697–703.Google Scholar
Cummings, K. L. and Tarleton, R. L. (2003). Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Molecular and Biochemical Parasitology 129, 53–59.Google Scholar
De Lima, A. R., Aparicio, A., Berrocal, A., Navarro, M. C., Graterol, D. and Contreras, V. (2007). Epimastigogénesis de Trypanosoma cruzi en medio axénico: cambios peptídicos, glicopeptídicos y enzimáticos. Revista de la Facultad de Ciencias de la Salud, Universidad de Carabobo 11, 39–47.Google Scholar
Dias, E. (1934). Estudos sobre o Schizotrypanum cruzi . Memorias do Instituto Oswaldo Cruz 28, 1–110.Google Scholar
Eichler, S. and Schaub, G. (2002). Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Experimental Parasitology 100, 17–27.Google Scholar
Elliot, S. L., Rodrigues, J. O., Lorenzo, M. G., Martins-Filho, O. A. and Guarneri, A. A. (2015). Trypanosoma cruzi, etiological agent of Chagas disease, is virulent to its triatomine vector Rhodnius prolixus in a temperature-dependent manner. PLOS Neglected Tropical Diseases 9, e0003646.Google Scholar
Fellet, M. R., Lorenzo, M. G., Elliot, S. L., Carrasco, D. and Guarneri, A. A. (2014). Effects of infection by Trypanosoma cruzi and Trypanosoma rangeli on the reproductive performance of the vector Rhodnius prolixus . PLoS ONE 9, e105255.CrossRefGoogle ScholarPubMed
Garcia, E. and Azambuja, P. (1991). Development and interactions of Trypanosoma cruzi within the insect vector. Parasitology Today 7, 240–244.CrossRefGoogle ScholarPubMed
Garcia, E. S. and Gilliam, F. C. (1980). Trypanosoma cruzi development is independent of protein digestion in the gut of Rhodnius prolixus . Journal of Parasitology 66, 1052–1053.Google Scholar
Garcia, E. S., Gonzalez, M. S., Deazambuja, P., Baralle, F. E., Fraidenraich, D., Torres, H. N. and Flawia, M. M. (1995). Induction of Trypanosoma cruzi metacyclogenesis in the gut of the hematophagous insect vector, Rhodnius prolixus, by hemoglobin and peptides carrying α d-globin sequences. Experimental Parasitology 81, 255–261.Google Scholar
Garcia, E. S., Genta, F. A., de Azambuja, P. and Schaub, G. A. (2010). Interactions between intestinal compounds of triatomines and Trypanosoma cruzi . Trends in Parasitology 26, 499–505.CrossRefGoogle ScholarPubMed
Graterol, D., Arteaga, R. Y., Navarro, M. C., Domínguez, M. I., De Lima, A. R. and Contreras, V. T. (2013). The amastigote stadium precedes epimastigote evolution during in vitro Trypanosoma cruzi epimastigogenesis. Revista de la Sociedad Venezolana de Microbiología 33, 72–79.Google Scholar
Hashimoto, K. and Schofield, C. J. (2012). Elimination of Rhodnius prolixus in Central America. Parasites and Vectors 5, 45.CrossRefGoogle ScholarPubMed
Hoare, C. A. and Wallace, F. G. (1966). Developmental stages of trypanosomatid flagellates: a new terminology. Nature 212, 1385–1386.CrossRefGoogle Scholar
Hotez, P. J., Bottazzi, M. E., Franco-Paredes, C., Ault, S. K. and Periago, M. R. (2008). The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLOS Neglected Tropical Diseases 2, e300.Google Scholar
Kollien, A. and Schaub, G. (2000). The development of Trypanosoma cruzi in triatominae. Parasitology Today 16, 381–387.Google Scholar
Kollien, A., Schmidt, J. and Schaub, G. (1998). Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans . Acta Tropica 70, 127–141.CrossRefGoogle ScholarPubMed
Lent, H. and Wygodzinsky, P. (1979). Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’ disease. Revisión de los Triatominae (Hemiptera, Reduviidae) y su significado como vectores del mal de Chagas. Bulletin of the American Museum of Natural History 163, 123–520.Google Scholar
Mello, C., Azambuja, P., Garcia, E. and Ratcliffe, N. (1996). Differential in vitro and in vivo behavior of three strains of Trypanosoma cruzi in the gut and hemolymph of Rhodnius prolixus . Experimental Parasitology 82, 112–121.Google Scholar
Pereira, M., Andrade, A. and Ribeiro, J. (1981). Lectins of distinct specificity in Rhodnius prolixus interact selectively with Trypanosoma cruzi . Science 211, 597–600.Google Scholar
Ribeiro, J. M. C. and Francischetti, I. M. B. (2003). Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annual Review of Entomology 48, 73–88.Google Scholar
Roffê, E., Rothfuchs, A. G., Santiago, H. C., Marino, A. P. M., Ribeiro-Gomes, F. L., Eckhaus, M., Antonelli, R. L. V. and Murphy, P. M. (2012). IL-10 limits parasite burden and protects against fatal myocarditis in a mouse model of Trypanosoma cruzi infection. Journal of Immunology 188, 649–660.Google Scholar
Rondinelli, E., Silva, R., Carvalho, J. F., de Almeida Soares, C. M., de Carvalho, E. F. and de Castro, F. T. (1988). Trypanosoma cruzi: an in vitro cycle of cell differentiation in axenic culture. Experimental Parasitology 66, 197–204.CrossRefGoogle Scholar
Schaub, G. and Böker, C. (1986). Colonization of the rectum of Triatoma infestans by Trypanosoma cruzi: influence of starvation studied by scanning electron microscopy. Acta Tropica 43, 349–354.Google Scholar
Schofield, C. J. and Galvão, C. (2009). Classification, evolution, and species groups within the Triatominae. Acta Tropica 110, 88–100.Google Scholar
Soares, A. C., Carvalho-Tavares, J., Gontijo, N. D., Dos Santos, V. C., Teixeira, M. M. and Pereira, M. H. (2006). Salivation pattern of Rhodnius prolixus (Reduviidae; Triatominae) in mouse skin. Journal of Insect Physiology 52, 468–472.Google Scholar
Soares, T. S., Buarque, D. S., Queiroz, B. R., Gomes, C. M., Braz, G. R., Araújo, R. N., Pereira, M. H., Guarneri, A. A. and Tanaka, A. S. (2015). A Kazal-type inhibitor is modulated by Trypanosoma cruzi to control microbiota inside the anterior midgut of Rhodnius prolixus . Biochimie 112, 41–48.Google Scholar
Turner, C., Barry, J. and Vickerman, K. (1988). Loss of variable antigen during transformation of Trypanosoma brucei rhodesiense from bloodstream to procyclic forms in the tsetse fly. Parasitology Research 74, 507–511.Google Scholar
Tyler, K. and Engman, D. (2001). The life cycle of Trypanosoma cruzi revisited. International Journal for Parasitology 31, 472–481.Google Scholar
Uehara, L. A., Moreira, O. C., Oliveira, A. C., Azambuja, P., Lima, A. P. C. A., Britto, C., dos Santos, A. L. S., Branquinha, M. H. and d'Avila-Levy, C. M. (2012). Cruzipain promotes Trypanosoma cruzi adhesion to Rhodnius prolixus midgut. PLOS Neglected Tropical Diseases 6, e1958.Google Scholar
Ursic-Bedoya, R. J., Nazzari, H., Cooper, D., Triana, O., Wolff, M. and Lowenberger, C. (2008). Identification and characterization of two novel lysozymes from Rhodnius prolixus, a vector of Chagas disease. Journal of Insect Physiology 54, 593–603.Google Scholar
Van Den Abbeele, J., Claes, Y., Van Bockstaele, D., Le Ray, D. and Coosemans, M. (1999). Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118, 469–478.Google Scholar
Whitten, M., Sun, F., Tew, I., Schaub, G., Soukou, C., Nappi, A. and Ratcliffe, N. (2007). Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli, T. cruzi and bacterial cell wall components. Insect Biochemistry and Molecular Biology 37, 440–452.Google Scholar
Zingales, B., Miles, M. A., Campbell, D. A., Tibayrenc, M., Macedo, A. M., Teixeira, M. M., Schijman, A. G., Llewellyn, M. S., Lages-Silva, E., Machado, C. R., Andrade, S. G. and Sturm, N. R. (2012). The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infection, Genetics and Evolution 12, 240–253.Google Scholar