Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T04:06:38.957Z Has data issue: false hasContentIssue false
  • English
  • Français

Triatoma infestans susceptibility to different Trypanosoma cruzi strains: parasite development and early escape from anterior midgut

Published online by Cambridge University Press:  17 September 2020

Larissa F. Paranaiba ,
Rodrigo P. Soares  and
Alessandra A. Guarneri Open the ORCID record for Alessandra A. Guarneri [Opens in a new window]
Larissa F. Paranaiba
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz. Av. Augusto de Lima, 1715, 30.190-009, Belo Horizonte, Minas Gerais, Brazil Departamento de Parasitologia, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Rodrigo P. Soares*
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz. Av. Augusto de Lima, 1715, 30.190-009, Belo Horizonte, Minas Gerais, Brazil
Alessandra A. Guarneri*
Affiliation:
Instituto René Rachou, Fundação Oswaldo Cruz. Av. Augusto de Lima, 1715, 30.190-009, Belo Horizonte, Minas Gerais, Brazil
*
Authors for correspondence: Alessandra A. Guarneri, E-mail: [email protected]; Rodrigo P. Soares, E-mail: [email protected]
Authors for correspondence: Alessandra A. Guarneri, E-mail: [email protected]; Rodrigo P. Soares, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The escape kinetics from the anterior midgut (AM) of Trypanosoma cruzi during the initial steps of infection was assessed in Triatoma infestans, as well as its ability to survive migration in the digestive tract of the vector. All the four strains evaluated survived and reached variable parasite densities. After 49–50 days, YuYu [discrete typing units (DTU) I] strain reached the highest parasite numbers in the rectum followed by Bug (DTU V), CL-Brener (DTU VI) and Dm28c (DTU I). All strains accomplished metacyclogenesis. Bug strain reached the highest numbers of metacyclic trypomastigotes followed by YuYu and CL-Brener/Dm28c. A remarkable parasite reduction in the AM for Bug strain, but not Dm28c was noticed at 72 h of infection. In the posterior midgut + rectum high densities of parasites from both strains were detected at this period indicating the parasites crossed the AM. For Dm28c strain, in infections initiated with trypomastigotes, parasites left AM faster than those starting with epimastigotes. In conclusion, T. cruzi strains from different DTUs were able to infect T. infestans reaching variable parasite densities. The kinetics of migration in the digestive tract may be affected by strain and/or the evolutive form used for infection.

Keywords

Parasite developmentparasite–vector interactionstrainsTriatoma infestansTrypanosoma cruzi
Type
Research Article
Information
Parasitology , Volume 148 , Issue 3 , March 2021 , pp. 295 - 301
Check for updates
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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.)

Footnotes

*

Those authors contributed equally to this manuscript.

References

Alvarenga, NJ and Brener, Z (1978) Development of Trypanosoma Cruzi in the vector in the absence of blood. Acta Tropica 35, 315–317.Google ScholarPubMed
Alvarenga, NJ and Bronfen, E (1997) Metaciclogênese do Trypanosoma Cruzi como parâmetro de interação do parasita com o triatomíneo vetor. Revista da Sociedade Brasileira de Medicina Tropical 30, 247–250.CrossRefGoogle Scholar
Amino, R, Martins, RM, Procopio, J, Hirata, IY, Juliano, MA and Schenkman, S (2002) Trialysin, a novel pore-forming protein from saliva of hematophagous insects activated by limited proteolysis. The Journal of Biological Chemistry 277, 6207–6213.CrossRefGoogle ScholarPubMed
Asin, S and Catala, S (1995) Development of Trypanosoma Cruzi in Triatoma infestans: influence of temperature and blood consumption. The Journal of Parasitology 1, 1–7.CrossRefGoogle Scholar
Brener, Z (1962) Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi. Revista do Instituto de Medicina Tropical de São Paulo 4, 389–396.Google ScholarPubMed
Brener, Z (1972) A new aspect of Trypanosoma Cruzi life-cycle in the invertebrate host. The Journal of Protozoology 19, 23–27.CrossRefGoogle ScholarPubMed
Brener, Z (1973) Biology of Trypanosoma Cruzi. Annual Review of Microbiololgy 27, 347–382.CrossRefGoogle ScholarPubMed
Brenière, SF, Waleckx, E and Barnabé, C (2016) Over six thousand Trypanosoma Cruzi Strains classified into discrete typing units (DTUs): attempt at an inventory. PLoS Neglected Tropical Diseases 10, e0004792.CrossRefGoogle ScholarPubMed
de Lana, M, da Pinto, AS, Barnabé, C, Quesney, V, Noël, S and Tibayrenc, M (1998) Trypanosoma Cruzi: compared vectorial transmissibility of three major clonal genotypes by Triatoma infestans. Experimental Parasitology 90, 20–25.CrossRefGoogle ScholarPubMed
Dias, E (1934) Estudos sobre o Schizotrypanum cruzi. Memorias do Instituto Oswaldo Cruz 28, 1–110.CrossRefGoogle Scholar
Dias, E (1939) Chaga's disease: a comparative study of the susceptibility of four natural vectors to the experimental development of Schizotrypanum cruzi. Third International Congress of Microbiology, 421–422, New York.Google Scholar
Dias, FA, Guerra, B, Vieira, LR, Perdomo, HD, Gandara, AC, Amaral, RJ, Vollu, RE, Gomes, SA, Lara, FA, Sorgine, MH, Medei, E, de Oliveira, PL and Salmon, D (2015) Monitoring of the parasite load in the digestive tract of Rhodnius prolixus by combined qPCR analysis and imaging techniques provides new insights into the trypanosome life cycle. PLoS Neglected Tropical Diseases 9, e0004186.CrossRefGoogle Scholar
Ferreira, RC, Kessler, RL, Lorenzo, MG, Paim, RMM, Ferreira, LDL, Probst, CM, Alves-Silva, J and Guarneri, AA (2016) Colonization of Rhodnius prolixus gut by Trypanosoma Cruzi involves an extensive parasite killing. Parasitology 143, 434–443.CrossRefGoogle ScholarPubMed
Guarneri, AA (2020) Infecting triatomines with trypanosomes. In Michels, PAM, Ginger, ML and Zilberstein, D (eds), Trypanosomatids. New York, NY: Humana, pp. 69–79.CrossRefGoogle Scholar
Guarneri, AA and Lorenzo, MG (2017) Triatomine physiology in the context of trypanosome infection. Journal of Insect Physiology 97, 66–76.CrossRefGoogle ScholarPubMed
Hoare, CA and Wallace, FG (1966) Developmental stages of trypanosomatid flagellates: a new terminology. Nature 212, 1385–1386.CrossRefGoogle Scholar
Jansen, AM, Xavier, SCC and Roque, ALR (2015) The multiple and complex and changeable scenarios of the Trypanosoma Cruzi transmission cycle in the sylvatic environment. Acta Tropica 151, 1–15.CrossRefGoogle ScholarPubMed
Jansen, AM, das Xavier, SCC and Roque, ALR (2018) Trypanosoma Cruzi transmission in the wild and its most important reservoir hosts in Brazil. Parasitology & Vectors 11, 502.CrossRefGoogle ScholarPubMed
Kessler, RL, Contreras, VT, Marliére, NP, Guarneri, AA, Silva, LHV, Mazzarotto, GA, Batista, M, Soccol, VT, Krieger, MA and Probst, CM (2017) Recently differentiated epimastigotes from Trypanosoma Cruzi are infective to the mammalian host. Molecular Microbiology 104, 712–736.CrossRefGoogle ScholarPubMed
Kollien, AH, Schmidt, J and Schaub, GA (1998) Modes of association of Trypanosoma Cruzi with the intestinal tract of the vector Triatoma infestans. Acta Tropica 70, 127–141.CrossRefGoogle ScholarPubMed
Kulkarni, MM, Karafova, A, Kamysz, W, Schenkman, S, Pelle, R and McGwire, BS (2013) Secreted trypanosome cyclophilin inactivates lytic insect defense peptides and induces parasite calcineurin activation and infectivity. Journal of Biological Chemistry 288, 8772–8784.CrossRefGoogle ScholarPubMed
Little, JW, Tay, J and Francisco, BF (1966) A study on the susceptibility of triatomid bugs to some Mexican strains of Trypanosoma cruzi. Journal of Medical Entomology 3, 252–255.CrossRefGoogle Scholar
Marcili, A, Lima, L, Cavazzana, M, Junqueira, ACV, Veludo, HH, Maia Da Silva, F, Campaner, M, Paiva, F and Teixeira, MMG (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, 641–655.CrossRefGoogle ScholarPubMed
Pereira, MH, Gontijo, NF, Guarneri, AA, Sant'Anna, MR and Diotaiuti, L (2006) Competitive displacement in Triatominae: the Triatoma infestans success. Trends in Parasitology 22, 516–520.CrossRefGoogle ScholarPubMed
Perlowagora-Szumlewicz, A and Müller, CA (1982) Studies in search of a suitable experimental insect model for xenodiagnosis of hosts with Chagas’ disease. 1-Comparative xenodiagnosis with nine Triatomine species of animals with acute infections by Trypanosoma cruzi. Memorias do Instituto Oswaldo Cruz 77, 37–53.CrossRefGoogle ScholarPubMed
Perlowagora-Szumlewicz, A, Muller, CA and Moreira, CJ (1990) Studies in search of a suitable experimental insect model for xenodiagnosis of hosts with Chagas’ disease. 4 -The reflection of parasite stock in the responsiveness of different vector species to chronic infection with different Trypanosoma Cruzi stocks. Revista de Saude Publica 24, 165–177.CrossRefGoogle ScholarPubMed
Schaub, GA (1989) Trypanosoma Cruzi: quantitative studies of development of two strains in small intestine and rectum of the vector Triatoma infestans. Experimental Parasitology 68, 260–273.CrossRefGoogle ScholarPubMed
Schmidt, J, Kleffmann, T and Schaub, GA (1998) Hydrophobic attachment of Trypanosoma Cruzi to a superficial layer of the rectal cuticle in the bug Triatoma infestans. Parasitology Research 84, 527–536.CrossRefGoogle ScholarPubMed
Silveira, AC, Feitosa, VR and Borges, R (1984) Distribution of triatominae captured in a domestic environment, 1975/83, Brazil. Revista Brasileira de Malariologia e Doencas Tropicais 36, 15–312.Google Scholar
Soares, AC, Carvalho-Tavares, J, Gontijo, NF, dos Santos, VC, Teixeira, MM and Pereira, MH (2006) Salivation pattern of Rhodnius prolixus (Reduviidae; Triatominae) in mouse skin. Journal of Insect Physiology 52, 468–472.CrossRefGoogle Scholar
Waleckx, E, Gourbière, S and Dumonteil, E (2015) Intrusive versus domiciliated triatomines and the challenge of adapting vector control practices against Chagas disease. Memorias do Instituto Oswaldo Cruz 110, 324–338.CrossRefGoogle ScholarPubMed
World Health Organization (2015) Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Weekly Epidemiological Record 90, 33–34. Available at http://www.who.int/wer/2015/wer9006/en/ (Accessed 22 July 2020).Google Scholar
Zingales, B (2018) Trypanosoma Cruzi genetic diversity: something new for something known about Chagas disease manifestations, serodiagnosis and drug sensitivity. Acta Tropica 184, 38–52.CrossRefGoogle ScholarPubMed
Zingales, B, Andrade, S, Briones, M, Campbell, D, Chiari, E, Fernandes, O, Guhl, F, Lages-Silva, E, Macedo, A, Machado, C, Miles, M, Romanha, A, Sturm, N, Tibayrenc, M and Schijman, A (2009) A new consensus for Trypanosoma Cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memorias do Instituto Oswaldo Cruz 104, 1051–1054.CrossRefGoogle ScholarPubMed