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Licensed Unlicensed Requires Authentication Published by De Gruyter June 16, 2015

Trypanosoma cruzi DTU TcII presents higher blood parasitism than DTU TcI in an experimental model of mixed infection

Helioswilton Sales-Campos, Henrique Borges Kappel, Cristiane Pontes Andrade, Tiago Pereira Lima, Alessandra de Castilho, Luis Eduardo Ramirez Giraldo and Eliane Lages-Silva
From the journal Acta Parasitologica

Abstract

Trypanosoma cruzi (Tc), the causative agent of Chagas disease, affects millions of people worldwide. One of the major characteristics of T. cruzi is related to its heterogeneity due to the variability of its biological properties, parasite growth rates, infectivity, tissue tropism, morbidity and virulence among different isolates observed during experimental or human infection. Moreover, presence of mixed infections in the same host in endemic areas is a matter of study due to its impact on clinical manifestations and disease progression. In this study, we evaluated the biological behavior of two Tc I strains AQ1-7 (AQ) and MUTUM (MT) and one Tc II strain (JG) during the acute phase of infection, in unique and mixed infections. A patent blood parasitism was detected only in mice inoculated with JG strain . In addition blood parasitism parameters (peak and average blood parasitism) were positively associated when JG and AQ strains were combined. In contrast, a negative association was observed in the JG+MUTUM group. The predominance of TcII strain over TcI strains was highlighted using the LSSP-PCR technique, which was performed in samples from hemoculture. Thus, this study showed important biological differences between different T. cruzi strains and discrete typing units (DTUs) in acute phase. Finally, we observed that blood parasitism during early period of infection seems to be more related to DTU than to a specific strain.

References

Andrade L.O., Machado C.R., Chiari E., Pena S.D., Macedo A.M. 2002. Trypanosoma cruzi: role of host genetic background in the differential tissue distribution of parasite clonal populations. Experimental Parasitology, 100, 269-27510.1016/S0014-4894(02)00024-3Search in Google Scholar

Andrade S.G., Magalhaes J.B. 1996. Biodemes and zymodemes of Trypanosoma cruzi strains: correlations with clinical data and experimental pathology. Revista Sociedade Brasileira de Medicina Tropical, 30, 27-3510.1590/S0037-86821997000100006Search in Google Scholar

Anez N., Crisante G., da Silva F.M., Rojas A., Carrasco H., Umezawa E.S., Stolf A.M., Ramirez J.L., Teixeira M.M. 2004. Predominance of lineage I among Trypanosoma cruzi isolates from Venezuelan patients with different clinical profiles of acute Chagas’ disease. Tropical Medicine International Health, 9, 1319-1326. DOI:10.1111/j.1365-3156.2004.01333.x 10.1111/j.1365-3156.2004.01333.xSearch in Google Scholar

Bertoli M., Ando M.H., De Ornelas Toledo M.J., De Araujo S.M., Gomes M.L. 2006. Infectivity for mice of Trypanosoma cruzi I and II strains isolated from different hosts. Parasitology Research, 99, 7-13. doi:10.1007/s00436-005-0122-710.1007/s00436-005-0122-7Search in Google Scholar

Botero L.A., Mejia A.M., Triana O. 2007. [Biological and genetic characterization of two Colombian clones of Trypanosoma cruzi groups I and II]. Biomedica, 27 Suppl 1:64-7410.7705/biomedica.v27i1.249Search in 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, 4,389-396Search in Google Scholar

Brener Z., Gazzinelli R.T. 1997. Immunological control of Trypanosoma cruzi infection and pathogenesis of Chagas’ disease. International Archives of Allergy Immunology, 114, 103-11010.1159/000237653Search in Google Scholar

Breniere S.F., Bosseno M.F., Noireau F., Yacsik N., Liegeard P., Aznar C., Hontebeyrie M. 2002. Integrate study of a Bolivian population infected by Trypanosoma cruzi, the agent of Chagas disease. Memorias do Instituto Oswaldo Cruz, 97, 289-29510.1590/S0074-02762002000300002Search in Google Scholar

Brisse S., Dujardin J.C., Tibayrenc M. 2000. Identification of six Trypanosoma cruzi lineages by sequence-characterised amplified region markers. Molecular Biochemistry Parasitology, 111, 95-10510.1016/S0166-6851(00)00302-9Search in Google Scholar

Brisse S., Verhoef J., Tibayrenc M. 2001. Characterisation of large and small subunit rRNA and mini-exon genes further supports the distinction of six Trypanosoma cruzi lineages. International Journal of Parasitology, 31, 1218-1226. doi:S0020-7519(01) 00238-7 [pii] 10.1016/S0020-7519(01)00238-7Search in Google Scholar

Camara A.C., Varela-Freire A.A., Valadares H.M., Macedo A.M., D’Avila D.A., Machado C.R., Lages-Silva E., Chiari E., Galvao L.M. 2010. Genetic analyses of Trypanosoma cruzi isolates from naturally infected triatomines and humans in northeastern Brazil. Acta Tropica, 115, 205-211. DOI:10.1016/ j.actatropica.2010.03.003 10.1016/j.actatropica.2010.03.003Search in Google Scholar

Coronado X., Zulantay I., Albrecht H., Rozas 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 Hygiene, 74, 1008-101210.4269/ajtmh.2006.74.1008Search in Google Scholar

Coura J.R., Borges-Pereira J. 2012. Chagas disease. What is known and what should be improved: a systemic review. Revista da Sociedade Brasileira de Medicina Tropical, 45, 286-29610.1590/S0037-86822012000300002Search in Google Scholar

Coura J.R., Dias J.C. 2009. Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Memorias do Instituto Oswaldo Cruz, 104 Suppl 1:31-4010.1590/S0074-02762009000900006Search in Google Scholar

Cura C.I., Mejia-Jaramillo A.M., Duffy T., Burgos J.M., Rodriguero M., Cardinal M.V., Kjos S., Gurgel-Goncalves R., Blanchet D., De Pablos L.M., Tomasini N., da Silva A., Russomando G., Cuba C.A., Aznar C., Abate T., Levin M.J., Osuna A., Gurtler R.E., Diosque P., Solari A., Triana-Chavez O., Schijman A.G. 2010. Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of splicedleader genes. International Journal of Parasitol, 40, 1599-1607. DOI:10.1016/j.ijpara.2010.06.00610.1016/j.ijpara.2010.06.006Search in Google Scholar

D’Avila D.A., Macedo A.M., Valadares H.M., Gontijo E.D., de Castro A.M., Machado C.R., Chiari E., Galvao L.M. 2009. Probing population dynamics of Trypanosoma cruzi during progression of the chronic phase in chagasic patients. Journal of Clinical Microbiology, 47, 1718-1725. DOI:10.1128/JCM.01658-08 10.1128/JCM.01658-08Search in Google Scholar

de Lana M., Chiari C.A., Chiari E., Morel C.M., Goncalves A.M., Romanha A.J. 1996. Characterization of two isolates of Trypanosoma cruzi obtained from the patient Berenice, the first human case of Chagas’ disease described by Carlos Chagas in 1909. Parasitology Reseacrh, 82, 257-26010.1007/s004360050106Search in Google Scholar

Deane M.P., Mangia R.H., Pereira N.M., Momen H., Goncalves 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 10.1590/S0074-02761984000400016Search in Google Scholar

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. DOI:10.1371/journal.pntd.000068710.1371/journal.pntd.0000687Search in Google Scholar

Devera R., Fernandes O., Coura J.R. 2003. Should Trypanosoma cruzi be called “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, 1-1210.1590/S0074-02762003000100001Search in Google Scholar

Di Noia J.M., Buscaglia C.A., De Marchi C.R., Almeida I.C., Frasch A.C. 2002. A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas’ disease is due to a single parasite lineage. Journal of Experimental Medicine, 195, 401-41310.1084/jem.20011433Search in Google Scholar

Dias J.C., Silveira A.C., Schofield C.J. 2002. The impact of Chagas disease control in Latin America: a review. Memorias do Instituto Oswaldo Cruz, 97, 603-61210.1590/S0074-02762002000500002Search in Google Scholar

Diosque P., Barnabe C., Padilla A.M., Marco J.D., Cardozo R.M., Cimino R.O., Nasser J.R., Tibayrenc M., Basombrio M.A. 2003. Multilocus enzyme electrophoresis analysis of Trypanosoma cruzi isolates from a geographically restricted endemic area for Chagas’ disease in Argentina. International Journal of Parasitology, 33, 997-100310.1016/S0020-7519(03)00139-5Search in Google Scholar

Dujardin J.P., Tibayrenc M., Venegas E., Maldonado L., Desjeux P., Ayala F.J. 1987. Isozyme evidence of lack of speciation between wild and domestic Triatoma infestans (Heteroptera: Reduviidae) in Bolivia. Journal of Medical Entomology, 24, 40-4510.1093/jmedent/24.1.40Search in Google Scholar

Freitas J.M., Lages-Silva E., Crema E., Pena S.D., Macedo A.M. 2005. Real time PCR strategy for the identification of major lineages of Trypanosoma cruzi directly in chronically infected human tissues. International Journal of Parasitology, 35, 411-417. DOI:S0020-7519(04)00260-7 [pii] 10.1016/j.ijpara. 2004.10.02310.1016/j.ijpara.2004.10.023Search in Google Scholar

Gazzinelli R.T., Oswald I.P., Hieny S., James S.L., Sher A. 1992. The microbicidal activity of interferon-gamma-treated macrophages against Trypanosoma cruzi involves an L-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-beta. European Journal of Immunology, 22, 2501-2506. DOI:10.1002/eji.183022100610.1002/eji.1830221006Search in Google Scholar

Gomes M.L., Macedo A.M., Vago A.R., Pena S.D., Galvao L.M., Chiari E. 1998. Trypanosoma cruzi: optimization of polymerase chain reaction for detection in human blood. Experimental Parasitology, 88, 28-33. DOI:10.1006/expr.1998.419110.1006/expr.1998.4191Search in Google Scholar

Krettli A.U., Weisz-Carrington P., Nussenzweig R.S. 1979. Membranebound antibodies to bloodstream Trypanosoma cruzi in mice: strain differences in susceptibility to complement-mediated lysis. Clinical Experimental Immunology, 37, 416-423Search in Google Scholar

Llewellyn M.S., Miles M.A., Carrasco H.J., Lewis M.D., Yeo M., Vargas J., Torrico F., Diosque P., Valente V., Valente S.A., Gaunt M.W. 2009. Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog, 5, e1000410. DOI:10.1371/journal.ppat.100041010.1371/journal.ppat.1000410Search in Google Scholar

Macedo A.M., Pena S.D. 1998. Genetic Variability of Trypanosoma cruzi:Implications for the Pathogenesis of Chagas Disease. Parasitology Today, 14, 119-12410.1016/S0169-4758(97)01179-4Search in Google Scholar

Miles M.A., Souza A., Povoa M., Shaw J.J., Lainson R., Toye P.J. 1978. Isozymic heterogeneity of Trypanosoma cruzi in the first autochthonous patients with Chagas’ disease in Amazonian Brazil. Nature, 272, 819-82110.1038/272819a0Search in Google Scholar

Miles M.A., Toye P.J., Oswald S.C., Godfrey D.G. 1977. The identification by isoenzyme patterns of two distinct straingroups of Trypanosoma cruzi, circulating independently in a rural area of Brazil. Transactions of the Royal Society of Tropical Medicine Hygiene, 71, 217-22510.1016/0035-9203(77)90012-8Search in Google Scholar

Morel C.M., Deane M.P., Goncalves A.M. 1986. The complexity of Trypanosoma cruzi populations revealed by schizodeme analysis. Parasitology Today, 2, 97-10110.1016/0169-4758(86)90038-4Search in Google Scholar

Oliveira R.P., Broude N.E., Macedo A.M., Cantor C.R., Smith C.L., Pena S.D. 1998. Probing the genetic population structure of Trypanosoma cruzi with polymorphic microsatellites. Procedures of the National Academy of Science U S A, 95, 3776-378010.1073/pnas.95.7.3776Search in Google Scholar

Pena D.A., Eger I., Nogueira L., Heck N., Menin A., Bafica A., Steindel M. 2011. Selection of TcII Trypanosoma cruzi population following macrophage infection. Journal of Infectious Disease, 204, 478-486. doi:10.1093/infdis/jir29210.1093/infdis/jir292Search in Google Scholar

Prata A. 2001. Clinical and epidemiological aspects of Chagas disease. The Lancet Infectious Disease, 1, 92-100. DOI:10.1016/S1473-3099(01)00065-210.1016/S1473-3099(01)00065-2Search in Google Scholar

Rodriguez I.B., Botero A., Mejia-Jaramillo A.M., Marquez E.J., Ortiz S., Solari A., Triana-Chavez O. 2009. Transmission dynamics of Trypanosoma cruzi determined by low-stringency single primer polymerase chain reaction and southern blot analyses in four indigenous communities of the Sierra Nevada de Santa Marta, Colombia. American Journal of Tropical Medicine and Hygiene, 81, 396-40310.4269/ajtmh.2009.81.396Search in Google Scholar

Sales-Campos H., Kappel H.B., Andrade C.P., Lima T.P., Mattos M.E., Jr., de Castilho A., Correia D., Giraldo L.E., Lages- Silva E. 2014. A DTU-dependent blood parasitism and a DTU-independent tissue parasitism during mixed infection of Trypanosoma cruzi in immunosuppressed mice. Parasitology Research, 113, 375-385. DOI:10.1007/s00436-013-3665-z 10.1007/s00436-013-3665-zSearch in Google Scholar

Tarleton R.L. 2007. Immune system recognition of Trypanosoma cruzi. Current Opinion in Immunology, 19, 430-434. DOI: 10.1016/j.coi.2007.06.00310.1016/j.coi.2007.06.003Search in Google Scholar

Tibayrenc M. 1998. Beyond strain typing and molecular epidemiology: integrated genetic epidemiology of infectious diseases. Parasitology Today, 14, 323-32910.1016/S0169-4758(98)01286-1Search in Google Scholar

Tibayrenc M., Ward P., Moya A., Ayala F.J. 1986. Natural populations of Trypanosoma cruzi, the agent of Chagas disease, have a complex multiclonal structure. Procedures of the National Academy of Science U S A, 83, 115-11910.1073/pnas.83.1.115Search in Google Scholar

Torrico M.C., Solano M., Guzman J.M., Parrado R., Suarez E., Alonzo-Vega C., Truyens C., Carlier Y., Torrico F. 2005. [Estimation of the parasitemia in Trypanosoma cruzi human infection: high parasitemias are associated with severe and fatal congenital Chagas disease]. Revista da Sociedade Brasileira de Medicina Tropical, 38 Suppl 2, 58-61Search in Google Scholar

Tzelepis F., de Alencar B.C., Penido M.L., Claser C., Machado A.V., Bruna-Romero O., Gazzinelli R.T., Rodrigues M.M. 2008. Infection with Trypanosoma cruzi restricts the repertoire of parasite-specific CD8+ T cells leading to immunodominance. Journal of Immunology, 180, 1737-174810.4049/jimmunol.180.3.1737Search in Google Scholar

Wallace A., Sanchez G., Venegas J., Solari A. 1995. Lack of crossreactivity of lytic antibodies with bloodstream forms of Trypanosoma cruzi zymodemes generated in a mouse experimental model. Experimental Parasitology, 80, 176-185. DOI:10.1006/expr.1995.102210.1006/expr.1995.1022Search in Google Scholar

WHO (2010) First WHO report on neglected tropical diseases: working to overcome the global impact of neglected tropical diseases. World Health Organization, WHO Press Search in Google Scholar

Yeo M., Acosta N., Llewellyn M., Sanchez H., Adamson S., Miles G.A., Lopez E., Gonzalez N., Patterson J.S., Gaunt M.W., de Arias A.R., Miles M.A. 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 of Parasitology, 35, 225-233. DOI:10.1016/j.ijpara.2004.10.02410.1016/j.ijpara.2004.10.024Search in Google Scholar

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. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memorias do Instituto Oswaldo Cruz, 104, 1051-105410.1590/S0074-02762009000700021Search in 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., Sturm N.R. 2012. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infection Genetic Evolution, 12, 240-253. DOI:10.1016/j.meegid.2011.12.00910.1016/j.meegid.2011.12.009Search in Google Scholar

Received: 2014-11-6
Revised: 2015-2-4
Accepted: 2015-3-12
Published Online: 2015-6-16
Published in Print: 2015-9-1

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