Acta Parasitologica

, Volume 58, Issue 2, pp 139–148 | Cite as

Microsatellite loci-based distribution of Trypanosoma cruzi genotypes from Chilean chronic Chagas disease patients and Triatoma infestans is concordant with a specific host-parasite association hypothesis

  • Juan Venegas
  • Felipe Díaz
  • Tamara Rojas
  • Sandra Miranda
  • M. I. Jercic
  • Christian González
  • William Coñoepán
  • Alex Vargas
  • Sergio Pichuantes
  • Marta Gajardo
  • Jorge Rodríguez
  • Gittith Sánchez
Article

Abstract

The objective of this study was to investigate if there is specific host-parasite association in Chilean populations of Trypanosoma cruzi. For this purpose, two groups of parasites were analyzed, one from chronic chagasic patients, and the other from Triatoma infestans triatomines in three regions of the country. The first group consisted of four types of samples: parasites from peripheral blood of non-cardiopathic T. cruzi infected patients (NB); parasites from their corresponding xenodiagnosis (NX); parasites from peripheral blood of T. cruzi infected cardiopathic patients (CB) and parasites from their xenodiagnostics (CX). The T. infestans sample in turn was from three regions: III, V and M (Metropolitan). The genetic differentiation by the Fisher exact method, the lineage distribution of the samples, the molecular phylogeny and the frequency of multiclonality were analysed. The results show that not only are the groups of T. cruzi clones from Chagas disease patients and vectors genetically differentiated, but also all the sub-groups (NB, NX, CB and CX) from the III, V and M regions. The analysis of lineage distribution was concordant with the above results, because significant differences among the percentages of TcI, TcIII and hybrids (TcV or TcVI) were observed. The phylogenetic reconstruction with these Chilean T. cruzi samples was coherent with the above results because the four chagasic samples clustered together in a node with high bootstrap support, whereas the three triatomine samples (III, V and M) were located apart from that node. The topology of the tree including published T. cruzi clones and isolates was concordant with the known topology, which confirmed that the results presented here are correct and are not biased by experimental error. Taken together the results presented here are concordant with a specific host-parasite association between some Chilean T. cruzi populations.

Keywords

Chagas disease Trypanosoma cruzi Triatoma infestans population genetics phylogeny host-parasite interaction 

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References

  1. Apt W., Aguilera X., Arribada A., Gomez L., et al. 1987. Characterization of Trypanosoma cruzi sylvatic transmission cycles and their association with cardiopathy populations by zymodemes: correlation with clinical picture. American Journal of Tropical Medicine and Hygiene, 37, 302–307.PubMedGoogle Scholar
  2. Bowcock A.M., Ruíz-Linares A., Tomfohrde J., Minch E., Kidd J.R., Cavalli-Sforza L.L. 1994. High resolution human evolutionary trees with polymorphic microsatellites. Nature, 368, 455–457. DOI: 10.1038/368455a0.PubMedCrossRefGoogle Scholar
  3. Brenière, S.T., Carlier Y., Tibayrenc M. 1992. Direct identification of Trypanosoma cruzi natural clones in vectors and mammalian hosts by polymerase chain reaction amplification. American Journal of Tropical Medicine and Hygiene, 46, 335–341.PubMedGoogle Scholar
  4. Breniere S.F., Bosseno M.F., Telleria J. et al. 1998. Diferent behaviour of two Trypanosoma cruzi major clones: transmission and circulation in young Bolivian children. Experimental Parasitology, 98, 285–295. DOI: 10.1006/expr.1998.4295.CrossRefGoogle Scholar
  5. Brisse S., Barnabé C., Tibayrenc M. 2000. Identification of six Trypanosoma cruzi phylogenetic lineages by random amplified polymorphic DNA and multilocus enzyme electrophoresis. International Journal for Parasitology, 30, 35–44. DOI:10.1016/S0020-7519(99)00168-X.PubMedCrossRefGoogle Scholar
  6. Burgos J.M., Altcheh J., Bisio M., Duffy T., Valadares H.M.S., Seidenstein M.E., Piccinali R., Freitas J.M., Levin M.J., Macchi L., Macedo A.M., Freilij H., Schijman A.G. 2007. Direct molecular profiling of minicircle signatures and lineages of Trypanosoma cruzi bloodstream populations causing congenital Chagas disease. International Journal for Parasitology, 37, 1319–1327. DOI: 10.1016/j.ijpara.2007.04.015PubMedCrossRefGoogle Scholar
  7. Coronado X., Zulantay, I., Albrecht H., Rosas M., Apt W., Ortiz S., Rodriguez J., Sanchez G., Solari A. 2006. Variation in Trypanosoma cruzi clonal composition detected in blood patients and xenodiagnosis triatomines: implications in the molecular epidemiology of Chile. American Journal of Tropical Medicine and Hygiene, 74, 1008–1012.PubMedGoogle Scholar
  8. Deane M.P., Mangia R.H.R., Pereira N.M., Momen H., Gonçalves A.M., Morel C.M. 1984. Trypanosoma cruzi: strain selection by different schedules of mouse passage of an initially mixed infection. Memorias do Instituto Oswaldo Cruz, 79, 495–497. DOI: 10.1590/S0074-02761984000400016.PubMedCrossRefGoogle Scholar
  9. Devera R., Fernandes O., Coura J.R. 2003. Should Trypanosoma cruzi be Called. T. cruzi. Complex? A review of the Parasite Diversity and the Potential of Selecting Population after in Vitro Culturing and Mice Infection. Memorias do Instituto Oswaldo Cruz, 98, 1–12.PubMedCrossRefGoogle Scholar
  10. De Freitas J.M., Augusto-Pinto L., Pimenta J.R., Bastos-Rodrigues L., Gonçalves, V.F., Teixeira S.M.R., Chiari E., Junqueira A.C.V., Fernandes O., Macedo A.M., Machado C.R., Pena S.D.J. 2006. Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLOS Pathogens, 2, 226–235. DOI: 10.1371/journal.ppat.0020024.CrossRefGoogle Scholar
  11. Del Puerto R., Nishizawa J.E., Kikuchi M., Iihoshi N., Roca Y., Avilas C., Gianella A., Lora J., Velarde F.U., Renjel L.A., Miura S., Higo H., Komiya N., Maemura K., Hirayama K. 2010. Lineage analysis of circulating Trypanosoma cruzi parasites and their association with clinical forms of Chagas disease in Bolivia. PLoS Neglected Tropical Disease, 4, e687.CrossRefGoogle Scholar
  12. Dorn P.L., Engelke D., Rods A., Rosales R., Melgar S., Braney B., Flores J., Monroy C. 1999. Utility of the polymerase chain reaction in detection of Trypanosoma cruzi in Guatemalan Chagas’ disease vectors. American Journal of Tropical Medicine and Hygiene, 60, 740–745.PubMedGoogle Scholar
  13. Felsenstein J. 1989. PHYLIP — Phylogeny Inference Package (Version 3.2). Cladistics, 5, 164–166.Google Scholar
  14. Gaunt M.W., Yeo M., Frame I.A., Stothard J.R., Carrasco H.J., Taylor M.C., Mena S.S., Veazey P., Miles G.A.J., Acosta N., De Arias A.R., Miles M.A. 2003. Mechanism of genetic exchange in american trypanosomes. Nature, 421, 936–939. DOI: 10.1038/nature01438.PubMedCrossRefGoogle Scholar
  15. Goldstein D.B., Ruiz-Linares A., Cavalli-Sforza L.L., Feldman M.W. 1995. Genetic absolute dating based on microsatellites and the origin of modern humans. Proceeding of National Academic of Science USA, 92, 6723–6727.CrossRefGoogle Scholar
  16. Machado C.A., Ayala F.J. 2001. Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proceeding of National Academic of Science USA, 98, 7396–7401. DOI: 10.1073/pnas.12118719.CrossRefGoogle Scholar
  17. Marcili A., Lima L., Valente V.C., Valente S.A., Batista J.S., Junqueira A.C.V., Souza A.I., Rosa J.A., Campaner M., Lewis M.D., Llewellyn M.S., Miles M.A., Teixeira M.M.G. 2009. Comparative phylogeography of Trypanosoma cruzi TCIIc: new host, association with terrestrial ecotopes, and spacial clustering. Infection Genetics and Evolution, 9, 1265–1274. DOI: 10.1016/j.meegid.2009.07.003.CrossRefGoogle Scholar
  18. Miles M.A., Llewellyn M.S., Lewis M.D., Yeo M., Baleela R., Fitzpatrick S., Gaunt M.W., Mauricio I.L. 2009. The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future. Parasitology, 136, 1509–1528.PubMedCrossRefGoogle Scholar
  19. Momen H. 1999, Taxonomy of Trypanosoma cruzi: a Commentary on Characterization and Nomenclature. Memorias do Instituto Oswaldo Cruz, 94 (Suppl. I): 181–184.PubMedCrossRefGoogle Scholar
  20. Oliveira R.P., Broude N.E., Macedo A.M., Cantor C.R., Smith C.L., Pena S.D.J. 1998. Probing the genetic population structure of Trypanosoma cruzi with polymorphic microsatellites. Proceeding of National Academic of Science USA, 95, 3776–3780.CrossRefGoogle Scholar
  21. Paetkau D., Calver W., Stirling I., Strobeck C. 1995. Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology, 4, 347–354.PubMedCrossRefGoogle Scholar
  22. Ramos-Ligonio A., Torres-Montero J., López-Monteon A., Dumonteil E. 2012. Extensive diversity of Trypanosoma cruzi discrete typing units circulating in Triatoma dimidiata from central Veracruz, México. Infection, Genetics and Evolution, 12, 1341–1343.PubMedCrossRefGoogle Scholar
  23. Rannala B., Mountain J.L. 1997. Detecting immigration by using multilocus genotypes. Proceeding of National Academic of Science USA, 94, 9197–9201.CrossRefGoogle Scholar
  24. Raymond M., Rousset F. 1995a. An exact test for population differentiation. Evolution, 49, 1283–1286.CrossRefGoogle Scholar
  25. Raymond M., Rousset F. 1995b. GENEPOP Version 1.2: population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248–249.Google Scholar
  26. Rodrigues J., Borges-Pereira J. 2010. Chagas disease: 100 years after its discovery. A systemic review. Acta Tropica, 115, 5–13. DOI: 10.1016/j.actatropica.2010.03.008.CrossRefGoogle Scholar
  27. Saitou N., Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.PubMedGoogle Scholar
  28. Sanchez G., Wallace A., Muñoz S., Venegas J., Ortiz S., Solari A. 1993. Characterization of Trypanosoma cruzi populations by several molecular markers support a clonal mode of reproduction. Biological Research, 26, 167–176.PubMedGoogle Scholar
  29. Schmidt J., Kleffmann T., Schaub G.A. 1998. Hydrophobic attachment of Trypanosoma cruzi to a superficial layer of the rectal cuticle in the bug Triatoma infestans. Parasitology Research, 84, 527–536. DOI: 10.1007/s004360050443.PubMedCrossRefGoogle Scholar
  30. Solari A., Campillay R., Ortiz S., Wallace A. 2001. Identification of Trypanosoma cruzi genotypes circulating in Chilean chagasic patients. Experimental Parasitology 97, 226–233.PubMedCrossRefGoogle Scholar
  31. Souto R-P., Fernandes O., Macedo A.M., Campbell D.A., Zingales B. 1996. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Molecular Biochemistry Parasitology 83, 141–152.CrossRefGoogle Scholar
  32. Telleria J., Lafay B., Virreira M., Barnabé C., Tibayrenc M., Svoboda M. 2006. Trypanosoma cruzi: Sequence analysis of the variable region of kinetoplast minicircles. Experimental Parasitology, 114, 279–288. DOI: 10.1016/j.exppara.2006.04.005.PubMedCrossRefGoogle Scholar
  33. Tibayrenc M. 2003. Genetic subdivisions within Trypanosoma cruzi (Discrete Typing Units) and their relevance for molecular epidemiology and experimental evolution. Kinetoplastid Biology and Disease, 3, 2–12. DOI: 10.1186/1475-9292-2-12.Google Scholar
  34. Tibayrenc M., Ayala F.J. 1988. Isozyme variability in Trypanosoma cruzi, the agent of Chagas’ disease: genetical, taxonomical, and epidemiological significance. Evolution, 42, 277–292.CrossRefGoogle Scholar
  35. Torres J.P., Ortiz S., Munoz S., Solari A. 2004. Trypanosoma cruzi isolates from Chile are heterogeneous and composed of mixed populations when characterized by schizodeme and Southern analyses. Parasitology, 128, 161–168. DOI: 10.1017/S0031182003004475.PubMedCrossRefGoogle Scholar
  36. Veas F., Cuny G., Brenière S.F., Tibayrenc M. 1990. SubspeciWc kDNA probes for major clones of Trypanosoma cruzi. Acta Tropica, 48, 79–82.PubMedCrossRefGoogle Scholar
  37. Venegas J., Coñepan W., Pichuantes S., Miranda S., Jercic M.I., Gajardo M., Sánchez G. 2009a. Phylogenetic analysis of microsatellite markers further supports the two hybridization events hypothesis as the origin of the Trypanosoma cruzi lineages. Parasitology Research, 105, 191–199. DOI: 10.1007/s00436-009-1386-0.PubMedCrossRefGoogle Scholar
  38. Venegas J., Coñepan W., Pichuantes S., Miranda S., Apt W., Arribada A., Zulantay I., Coronado X., Rodriguez J., Reyes E., Solari A., Sánchez G. 2009b. Differential distribution of Trypanosama cruzi clones in human chronic cardiopathic and noncardiopathic individuals. Acta Tropica, 109, 187–193. DOI: 10.1016/j.actatropica.2008.11.007.PubMedCrossRefGoogle Scholar
  39. Venegas J., Miranda S., Coñepan W., Pichuantes S., Jercic M.I., González C., Gajardo M., Apt W., Arribada A., Sánchez G. 2010. Microsatellite marker analysis shows differentiation among Trypanosoma cruzi populations of peripheral blood and dejections of Triatoma infestans fed on the same chronic chagasic patients. Parasitology Research, 107, 855–863. DOI: 10.1007/s00436-010-1939-2.PubMedCrossRefGoogle Scholar
  40. Venegas J., Rojas T., Díaz F., Miranda S., Jercic M.I., González C., Coñoepán W., Pichuantes S., Rodríguez J., Gajardo M., Sánchez G. 2011. Geographical structuring of Trypanosoma cruz populations from Chilean Triatoma infestans triatomines and their genetic relationship with other Latino American counterparts. Annals of Tropical Medicine and Parasitology, 105, 625–646. DOI: 10.1179/2047773211Y.0000000002.PubMedCrossRefGoogle Scholar
  41. World Health Organization. 2000. Chagas Disease interrupted in Chile. TDR News 61: 10.Google Scholar
  42. World Health Organization. 2002. Control of chagas disease: second report of the WHO expert committee Strategic Direction for Research, pp. 1–159. WHO Geneva Switzerland.Google Scholar
  43. Yeo M., Acosta N., Llewellyn M., Sanchez H., Adamson S., Miles G.A.J., Lopez E., Gonzalez N., Patterson J.S., Gaunt M.W. 2005. Origins of Chagas disease: Didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. International Journal for Parasitology, 35, 225–233. DOI: 10.1016/j.ijpara.2004.10.024.PubMedCrossRefGoogle Scholar
  44. Zingales B., Souto R.P., Mangia R.H., Lisboa C.V., Campbell D.A., Coura J.R., Jansen A., Fernandes O. 1998. Molecular epidemiology of American trypanosomiasis in Brazil based on dimorphisms of rRNA and mini-exon gene sequences. International Journal for Parasitology, 28, 105–112. DOI: 10.1016/ S0020-7519(97)00178-1.PubMedCrossRefGoogle Scholar
  45. Zingales B., Andrade S.G., Briones M.R.S., 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. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memorias do Instituto Oswaldo Cruz, 104, 1051–1054. DOI: 10.1590/S0074-02762009000700021.PubMedCrossRefGoogle Scholar
  46. Zingales B., Miles M., Campbell D.A., c, Tibayrenc M., Macedo A.M.,e, Teixeira M.M.G., 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. Infection, Genetics and Evolution, 12, 240–253. DOI: 10.1016/j.meegid.2012.04.024.CrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2013

Authors and Affiliations

  • Juan Venegas
    • 1
  • Felipe Díaz
    • 1
  • Tamara Rojas
    • 1
  • Sandra Miranda
    • 1
  • M. I. Jercic
    • 2
  • Christian González
    • 2
  • William Coñoepán
    • 1
  • Alex Vargas
    • 1
  • Sergio Pichuantes
    • 1
  • Marta Gajardo
    • 3
  • Jorge Rodríguez
    • 4
  • Gittith Sánchez
    • 5
  1. 1.Programa de Biología Celular y MolecularInstituto de Ciencias Biomédicas, Facultad de Medicina, correoSantiago 7Chile
  2. 2.Laboratorio de Referencia en ParasitologíaInstituto de Salud PúblicaSantiagoChile
  3. 3.Departamento de Patología, Facultad de OdontologíaUniversidad de ChileComuna de Independencia, SantiagoChile
  4. 4.Departamento de Salud Publica Dr. Salvador Allende, Facultad de MedicinaU. de ChileSantiagoChile
  5. 5.Programa de Genética HumanaInstituto de Ciencias Biomédicas, Facultad de MedicinaSantiagoChile

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