Innate trypanolytic factors in triatomine hemolymph against Trypanosoma rangeli and T. cruzi: a comparative study in eight Chagas disease vectors
Portada 44 (170) 2020
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Suárez-Quevedo, Y., Barbosa-Vinasco, H. J. ., Gutiérrez-Garnizo, S. A., Olaya-Morales, J. L., Zabala-González, D., Carranza-Martínez, J. C. ., … Vallejo, G. A. (2020). Innate trypanolytic factors in triatomine hemolymph against Trypanosoma rangeli and T. cruzi: a comparative study in eight Chagas disease vectors. Revista De La Academia Colombiana De Ciencias Exactas, Físicas Y Naturales, 44(170), 88–104. https://doi.org/10.18257/raccefyn.1097

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Abstract

There is limited information about the innate immunity of triatomines against Trypanosoma rangeli, an infectious, non-pathogenic human parasite, and T. cruzi, the causative agent of Chagas’ disease. This study aimed at addressing this gap by studying the in vitro trypanolytic hemolymph activity from insects not infected by T. rangeli or T. cruzi. Eight triatomine species were examined including Rhodnius prolixus, R. robustus, R. colombiensis, R. pallescens, R. pictipes, Triatoma dimidiata, T. maculata, and Panstrongylus geniculatus. The hemolymph of R. prolixus and R. robustus laboratory colonies demonstrated strong trypanolytic activity during the first 14 hours of parasite incubation with 81% lysis for the T. rangeli C genotype, 90% for the E genotype, 95% for T. cruzi discrete taxonomic unit (DTU) TcII, 94% for TcV, 96% for TcVI, 94% for Tcbat, and 90% for Tcmarinkellei. No lysis activity was detected 14 or 24 hours after parasite incubation with the hemolymph of insects from R. pictipes R. pallescens, P. geniculatus, and T. maculata colonies. Identical results (absence of lysis) were observed using hemolymph from R. colombiensis and T. dimidiata laboratory colonies and specimens captured in sylvatic environments. The hemolymph lytic activity against recently obtained cultures (95% decrease in live parasite count) and long-term T. cruzi TcII ones (96% decrease) was similar. Lytic activity was similar in hemolymph from R. prolixus nymphs, males and females and insects fed on chicken or mouse blood. This is the first comparative study of the trypanolytic activity of hemolymph from different triatomine species against T. rangeli and T. cruzi genotypes. Although the chemical structures of such lysis factors and the mechanisms determining their expression have not been fully determined, their identification furthers our understanding of triatomines’ innate immunity and their role in Trypanosoma transmission.

https://doi.org/10.18257/raccefyn.1097

Keywords

Trypanosoma cruzi; Trypanosoma rangeli; Rhodnius prolixus; Rhodnius robustus; trypanolytic factors; vectorial ability; insect immunity
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References

Alvarenga, N.J. & Bronfen, E. (1982). Incapacity of the evolution of Trypanosoma cruzi in the hemocele of triatomids. Mem Inst Oswaldo Cruz. 77(4): 431-6. Portuguese.

Azambuja, P., García, E.S., Waniek, P.J., Vieira, C.S., Figueiredo, M.B., Gonzalez, M.S., Mello, C.B., Castro, D.P., Ratcliffe, N.A. (2017). Rhodnius prolixus: From physiology by Wigglesworth to recent studies of immune system modulation by Trypanosoma cruzi and Trypanosoma rangeli. J Insect Physiol. 97: 45-65. Doi: 10.1016/j.jinsphys.2016.11.006

Baker, J.R., Miles, M.A., Godfrey, D.G., Barrett, T.V. (1978). Biochemical characterization of some species of Trypanosoma (Schizotrypanum) from bats (Microchiroptera). Am J Trop Med Hyg. 27(3): 483-91.

Beltrame-Botelho, I.T., Talavera-López, C., Andersson, B., Grisard, E.C., Stoco, P.H. (2016). A Comparative In Silico Study of the Antioxidant Defense Gene Repertoire of Distinct Lifestyle Trypanosomatid Species. Evol Bioinform Online. 12: 263-275.

Brehélin, M., Drift, L., Baud, L., Boemare, N. (1989). Insect haemolymph: Cooperation between humoral and cellular factors in Locusta migratoria. Insect Biochem. 19: 301-309.

Brisse, S., Verhoef, J., Tibayrenc, M. (2001). Characterisation of large and small subunit rRNA and mini-exon genes further support the distinction of six Trypanosoma cruzi lineages. Int J Parasitol. 31 (11): 1218-26. Doi: 10.1016/S0020-7519(01)00238-7

Buarque, D.S., Braz, G.R., Martins, R.M., Tanaka-Azevedo, A.M., Gomes, C.M., Oliveira, F.A., Schenkman, S., Tanaka, A.S. (2013). Differential expression profiles in the midgut of Triatoma infestans infected with Trypanosoma cruzi. PLoS Negl. Trop. Dis. 5: e61203.

Castro, D.P., Moraes, C.S., Gonzalez, M.S., Ratcliffe, N.A., Azambuja, P., 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.

Cerenius, L., Lee, B.L., Söderhäll, K. (2008). The proPO-system: Pros and cons for its role in invertebrate immunity. Trends Immunol. 29: 263-271. Doi: 10.1016/j.it.2008.02.009.

De Fuentes-Vicente, J.A., Cabrera-Bravo, M., Enríquez-Vara, J.N., Bucio-Torres, M.I., Gutiérrez-Cabrera, A.E., Vidal-López, D.G., Martínez-Ibarra, J.A., Salazar-Schettino, P.M., Córdoba-Aguilar, A. (2016). Relationships between altitude, triatomine (Triatoma dimidiata) immune response and virulence of Trypanosoma cruzi, the causal agent of Chagas’ disease. Med. Vet. Entomol. 31: 63-71.

De Stefani-Márquez, M.D., Rodrigues-Ottaiano, C., Mônica Oliveira, R., Pedrosa, A.L., Cabrine-Santos, M., Lages-Silva, E., Ramírez, L.E. (2006). Susceptibility of different triatomine species to Trypanosoma rangeli experimental infection. Vector Borne Zoonotic Dis. 6 (1): 50-56.

Figueiredo, M.B., Genta, F.A, Garcia, E.S., Azambuja, P. (2008). Lipid mediators and vector infection: Trypanosoma rangeli inhibits Rhodnius prolixus hemocyte phagocytosis by modulation of phospholipase A2 and PAF-cetylhydrolase activities. J Insect Physiol. 54: 1528-37.

Galvão, C. & Justi, S.A. (2015). An overview on the ecology of Triatominae (Hemiptera: Reduviidae). Acta Trop. 151: 116-25. Doi: 10.1016/j.actatropica.2015.06.006.

García, E.S., Machado, E.M., Azambuja, P. (2004a). Inhibition of hemocyte microaggregation reactions in Rhodnius prolixus larvae orally infected with Trypanosoma rangeli. Exp Parasitol. 107: 31-8.

García, E.S., Machado, E.M., Azambuja, P. (2004b). Effects of eicosanoid biosynthesis inhibitors on the prophenoloxidase-activating system and microaggregation reactions in the hemolymph of Rhodnius prolixus infected with Trypanosoma rangeli. J Insect Physiol. 50: 157-65.

Guhl, F. & Vallejo, G.A. (2003). Trypanosoma (Herpetosoma) rangeli Tejera, 1920: An updated review. Mem Inst Oswaldo Cruz. 98(4): 435-42.

Gurgel-Gonçalves, R., Ramalho, E.D., Duarte, M.A., Palma, A.R., Abad-Franch, F., Carranza, J.C., Cuba-Cuba, C.A. (2004). Enzootic transmission of Trypanosoma cruzi and T. rangeli in the Federal District of Brazil. Rev Inst Med Trop Sao Paulo. 46 (6):323-30.

Hoare, C.A. (1972). The trypanosomes of mammals: A zoological monograph. Oxford: Blackwell Scientific Publications. 749 p.p.

Kanost, M.R., Gorman, M.J. (2008). Phenoloxidases in insect immunity. In: Beckage,N. (Ed.), Insect Immunology. Academic Press/Elsevier, San Diego, p. 69-96.

López, L., Morales, G., Ursic, R., Wolff, M., Lowenberger, C. (2003). Isolation and characterization of a novel insect defensin from Rhodnius prolixus: A vector of Chagas disease. Insect Biochem. Mol. Biol. 33: 349-447.

Maia Da Silva, F., Junqueira, A.C., Campaner, M., Rodrigues, A.C., Crisante, G., Ramírez, L.E., Caballero, Z.C., Monteiro, F.A., Coura, J.R., Añez, N., Teixeira, M.M. (2007). Comparative phylogeography of Trypanosoma rangeli and Rhodnius (Hemiptera: Reduviidae) supports a long coexistence of parasite lineages and their sympatric vectors. Mol Ecol. 16 (16): 3361-73.

Marcili, A., Lima, L., Cavazzana, M., Junqueira, A.C., Veludo, H.H., Maia Da Silva, F., Campaner, M., Paiva, F., Nunes, V.L., Teixeira, M.M. (2009). A new genotype of Trypanosoma cruzi associated with bats evidenced by phylogenetic analyses using SSU rDNA, cytochrome b and Histone H2B genes and genotyping based on ITS1 rDNA. Parasitology. 136 (6): 641-55.

Mello, C.B., García, E.S., Ratcliffe, N.A., Azambuja, P. (1995). Trypanosoma cruzi and Trypanosoma rangeli: Interplay with hemolymph components of Rhodnius prolixus. J Invertebr Pathol. 65 (3): 261-8.

Mello, C.B., Azambuja, P., Garcia, E.S., Ratcliffe, N.A. (1996). Differential in vitro and in vivo behavior of three strains of Trypanosoma cruzi in the gut and hemolymph of Rhodnius prolixus. Exp. Parasitol. 82: 112-121.

Pereira ME, Andrade AF, Ribeiro JM. (1981). Lectins of distinct specificity in Rhodnius prolixus interact selectively with Trypanosoma cruzi. Science. 211: 597-600.

Pulido, X.C., Pérez, G., Vallejo, G.A. (2008). Preliminary characterization of a Rhodnius prolixus hemolymph trypanolytic protein, this being a determinant of Trypanosoma rangeli KP1(+) and KP1(-) subpopulations’ vectorial ability. Memorias do Instituto Oawaldo Cruz. 103 (2):172-179.

Salazar-Antón, F., Urrea, D.A., Guhl, F., Arévalo, C., Azofeifa G., Urbina A., Blandón-Naranjo, M., Sousa, O.E., Zeledón, R., Vallejo, G.A. (2009). Trypanosoma rangeli genotypes association with Rhodnius prolixus and R. pallescens allopatric distribution in Central America. Infection, Genetics and Evolution. 9: 1306-1310.

Salcedo-Porras, N. & Lowenberger, C. (2019). The innate immune system of kissing bugs, vectors of chagas disease. Dev Comp Immunol. 98: 119-128. Doi: 10.1016/j.dci.2019.04.007.

Sánchez, I.P., Pulido, X.C., Carranza, J.C., Triana, O., Vallejo, G.A. (2005). Inmunidad Natural de Rhodnius prolixus (Hemiptera: Reduviidae: Triatominae) frente a la infección con Trypanosoma (Herpetosoma) rangeli KP1(-) aislados de Rhodnius pallescens, R. colombiensis y R. ecuadoriensis. Revista de la Asociación Colombiana de Ciencias Biológicas. 17: 108-118.

Söderhäll, K. & Cerenius, L. (1998). Role of the prophenoloxidase-activating system ininvertebrates. Curr Opi. Immunol. 10: 23-28

Souto, R.P. & Zingales, B. (1993). Sensitive detection and strain classification of Trypanosoma cruzi by amplification of a ribosomal RNA sequence. Mol Biochem Parasitol. 62 (1): 45-52. Doi: /10.10160166-6851(93)90176-X

Souto, R.P., Fernandes, O., Macedo, A.M., Campbell, D.A., Zingales, B. (1996). DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol. 83(2): 141-52. Doi: 10.1016/S0166-6851(96) 02755-7

Stoco, P.H., Wagner, G., Talavera-Lopez, C., Gerber, A., Zaha, A., Thompson, C.E., Bartholomeu, D.C., Lückemeyer, D.D., Bahia, D., Loreto, E., Prestes, E.B., Lima, F.M., Rodrigues-Luiz, G., Vallejo, G.A., Filho, J.F., Schenkman, S., Monteiro, K.M., Tyler, K.M., Almeida, L.G., Ortiz, M.F., Chiurillo, M.A., Moraes, M.H., Cunha Ode. L., Mendonça-Neto, R., Silva, R., Teixeira, S.M., Murta, S.M., Sincero, T.C., Mendes, T.A., Urmenyi, T.P., Silva, V.G., Da Rocha, W.D., Andersson, B., Romanha, A.J., Steindel, M., Vasconcelos, A.T., Grisard, E.C. (2014). Genome of the Avirulent Human-Infective Trypanosome-Trypanosoma rangeli. PLoS Negl. Trop. Dis. 8 (9): e3176. Doi: 10.1371/journal.pntd.0003176

Urrea, D.A., Carranza, J.C., Cuba-Cuba, C.A., Gurgel-Gonçalves, R., Guhl, F., Schofield, C.J., Triana O., Vallejo, G.A. (2005). Molecular characterisation of Trypanosoma rangeli strains isolated from Rhodnius ecuadoriensis in Perú, R. colombiensis in Colombia and R. pallescens in Panamá supports a co-evolutionary association between parasites and vectors. Infection, Genetics and Evolution. 5 (2): 123-129.

Urrea, D.A., Herrera, C.P., Falla, A., Carranza, J.C., Cuba-Cuba, C., Triana-Chávez, O., Grisard, E.C., Guhl, F., Vallejo, G.A. (2011). Sequence analysis of the splicedleader intergenic region (SL-IR) and random amplified polymorphic DNA (RAPD) of Trypanosoma rangeli strains isolated from Rhodnius ecuadoriensis, R. colombiensis, R. pallescens and R. prolixus suggests a degree of co-evolution between parasites and vectors. Acta Tropica. 120: 59-66.

Ursic-Bedoya, R.J., Nazzari, H., Cooper, D., Triana, O., Wolff, M., Lowenberger, C. (2008). Identification and characterization of two novel lysozymes from Rhodnius prolixus, a vector of Chagas disease. J. Insect. Physiol. 54: 593-603.

Ursic-Bedoya, R., Buchhop, J., Joy, J.B., Durvasula, R., Lowenberger, C. (2011). Prolixicin: A novel antimicrobial peptide isolated from Rhodnius prolixus with differential activity against bacteria and Trypanosoma cruzi. Insect. Mol. Biol. 20: 775-786.

Vallejo, G. A., Marinkelle, C. J., Guhl, F., de Sánchez, N. (1986). Mantenimiento en el laboratorio de Trypanosoma (Herpetosoma) rangeli Tejera, 1920. Revista de biología tropical. 34(1): 75-81.

Vallejo, G.A., Marinkelle, C.J., Guhl, F., de Sánchez, N. (1988). Behavior of the infection and morphologic differentiation of Trypanosoma cruzi and T. rangeli in the intestine of the vector Rhodnius prolixus. Rev Bras Biol. 48 (3): 577-87. Spanish.

Vallejo, G.A., Guhl, F., Carranza, J.C., Lozano, L.E., Sánchez, J.L., Jaramillo, J.C., Gualtero, D., Castañeda, N., Silva, J.C., Steindel, M. 2002. kDNA markers define two major Trypanosoma rangeli lineages in Latin-America. Acta Trop. 81(1): 77-82.

Vallejo, G.A., Suárez, Y., Olaya, J.L., Gutiérrez, S.A., Carranza, J.C. (2015). Trypanosoma rangeli: un protozoo infectivo y no patógeno para el humano que contribuye al entendimiento de la transmisión vectorial and la infección por Trypanosoma cruzi, agente causal de la Chagas’ disease. Rev. Acad. Col. Cienc. Exac. Fís. Nat. 39(150): 111-122.

Vieira, C.S., Waniek, P.J., Mattos, D.P., Castro, D.P., Mello, C.B., Ratcliffe, N.A., García, E.S., Azambuja, P. (2014). Humoral responses in Rhodnius prolixus: Bacterial feeding induces differential patterns of antibacterial activity and enhances mRNA levels of antimicrobial peptides in the midgut. Parasit Vectors. 7: 232. Doi:10.1186/1756-3305-7-232

Vieira, C.S., Mattos, D.P., Waniek, P.J., Santangelo, J.M., Figueiredo, M.B., Gumiel, M., da Mota, F.F., Castro, D.P., Garcia, E.S., Azambuja, P. (2015). Rhodnius prolixus interaction with Trypanosoma rangeli: Modulation of the immune system and microbiota population. Parasit Vectors. 8: 135. Doi: 10.1186/s13071-015-0736-2

Vieira, C.S., Waniek, P.J., Castro, D.P., Mattos, D.P., Moreira, O.C., Azambuja, P. (2016). Impact of Trypanosoma cruzi on antimicrobial peptide gene expression and activity in the fat body and midgut of Rhodnius prolixus. Parasit.Vectors. 9: 119. Doi: 10.1186/s13071-016-1398-4

Villa, L.M., Guhl, F., Zabala, D., Ramírez, J.D., Urrea, D.A., Hernández, D.C., Cucunubá, Z., Montilla, M., Carranza, J.C., Rueda, K., Trujillo, J.E., Vallejo, G.A. (2013). The identification of two Trypanosoma cruzi I genotypes from domestic and sylvatic transmission cycles in Colombia based on a single polymerase chain reaction amplification of the splicedleader intergenic region. Mem Inst Oswaldo Cruz. 108 (7): 932-5. Doi: 10.1590/0074-0276130201

Walters, J. & Ratcliffe, N.A. (1983). Studies on the in vivo cellular reactions of insects: Fate of pathogenic and non-pathogenic bacteria in Galleria mellonellanodules. J Insect Physio. 29:417-424. Doi: 10.1016/0022-1910(83)90069-0

Whitten, M., Sun, F., Tew, I., Schaub, G., Soukou, C., Nappi, A., Ratcliffe, N. (2007). Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli, Trypanosoma cruzi and bacterial cell wall components. Insect Biochem. Molec. Biol. 37: 440-452.

Zingales, B., Andrade, S.G., Briones, M.R., Campbell, D.A., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, A.M., Machado, C.R., Miles, M.A., Romanha, A.J., Sturm, N.R., Tibayrenc, M., Schijman, A.G. (2009). Second Satellite Meeting. A new consensus for Trypanosoma cruzi intraspecific nomenclature: Second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz. 104 (7): 1051-4.

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., Sturm, N.R. (2012). The revised Trypanosoma cruzi subspecific nomenclature: Rationale, epidemiological relevance and research applications. Infect Genet Evol. 12 (2): 240-53. Doi:10.1016/j.meegid.2011.12.009

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