Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-26T08:41:17.064Z Has data issue: false hasContentIssue false

Evolutionary history of Trypanosoma cruzi according to antigen genes

Published online by Cambridge University Press:  14 August 2008

M. ROZAS
Affiliation:
Programa de Biología Celular y Molecular, ICBM, Facultad de Medicina, Universidad de Chile, Santiago, Chile Institute of Tropical Medicine, Molecular Parasitology, Antwerp, Belgium
S. DE DONCKER
Affiliation:
Institute of Tropical Medicine, Molecular Parasitology, Antwerp, Belgium
X. CORONADO
Affiliation:
Programa de Biología Celular y Molecular, ICBM, Facultad de Medicina, Universidad de Chile, Santiago, Chile
C. BARNABÉ
Affiliation:
Génétique et Evolution des Maladies Infectieuses, UMR CNRS/IRD 2724, Montpellier, France
M. TIBYARENC
Affiliation:
Génétique et Evolution des Maladies Infectieuses, UMR CNRS/IRD 2724, Montpellier, France
A. SOLARI
Affiliation:
Programa de Biología Celular y Molecular, ICBM, Facultad de Medicina, Universidad de Chile, Santiago, Chile
J.-C. DUJARDIN*
Affiliation:
Institute of Tropical Medicine, Molecular Parasitology, Antwerp, Belgium
*
*Corresponding author: Institute of Tropical Medicine, Molecular Parasitology, Nationalestraat 155, Antwerp, Belgium. Tel: +32 3 2476355. Fax: +32 3 2476359. E-mail: jcdujard@itg.be

Summary

Trypanosoma cruzi, the agent of Chagas disease is associated with a very high clinical and epidemiological pleomorphism. This might be better understood through studies on the evolutionary history of the parasite. We explored here the value of antigen genes for the understanding of the evolution within T. cruzi. We selected 11 genes and 12 loci associated with different functions and considered to be involved in host-parasite interaction (cell adhesion, infection, molecular mimicry). The polymorphism of the respective genes in a sample representative of the diversity of T. cruzi was screened by PCR-RFLP and evolutionary relationships were inferred by phenetic analysis. Our results support the classification of T. cruzi in 2 major lineages and 6 discrete typing units (DTUs). The topology of the PCR-RFLP tree was the one that better fitted with the epidemiological features of the different DTUs: (i) lineage I, being encountered in sylvatic as well as domestic transmission cycles, (ii) IIa/c being associated with a sylvatic transmission cycle and (iii) IIb/d/e being associated with a domestic transmission cycle. Our study also supported the hypothesis that the evolutionary history of T. cruzi has been shaped by a series of hybridization events in the framework of a predominant clonal evolution pattern.

Type
Original Articles
Copyright
Copyright © 2008 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.)

References

REFERENCES

Aguillon, J. C., Ferreira, L., Perez, C., Colombo, A., Molina, M. C., Wallace, A., Solari, A., Carvallo, P., Galindo, M., Galanti, N., Orn, A., Billetta, R. and Ferreira, A. (2000). Tc45, a dimorphic Trypanosoma cruzi immunogen with variable chromosomal localization, is calreticulin. American Journal of Tropical Medicine and Hygiene 63, 306312.Google Scholar
Brisse, S., Dujardin, J. C. and Tibayrenc, M. (2000 a). Identification of six Trypanosoma cruzi lineages by sequence-characterised amplified region markers. Molecular and Biochemical Parasitology 111, 95105.CrossRefGoogle ScholarPubMed
Brisse, S., Barnabe, C. and Tibayrenc, M. (2000 b). Identification of six Trypanosoma cruzi phylogenetic lineages by random amplified polymorphic DNA and multilocus enzyme electrophoresis. International Journal for Parasitology 30, 3544.Google Scholar
Brisse, S., Henriksson, J., Barnabe, C., Douzery, E. J., Berkvens, D., Serrano, M., De Carvalho, M. R., Buck, G. A., Dujardin, J. C. and Tibayrenc, M. (2003). Evidence for genetic exchange and hybridization in Trypanosoma cruzi based on nucleotide sequences and molecular karyotype. Infection Genetics and Evolution 2, 173183.CrossRefGoogle ScholarPubMed
Campbell, D. A., Westenberger, S. J. and Sturm, N. R. (2004). The determinants of Chagas disease: connecting parasite and host genetics. Current Molecular Medicine 4, 549562.CrossRefGoogle ScholarPubMed
Campetella, O., Henriksson, J., Aslund, L., Frasch, A. C., Pettersson, U. and Cazzulo, J. J. (1992). The major cysteine proteinase (cruzipain) from Trypanosoma cruzi is encoded by multiple polymorphic tandemly organized genes located on different chromosomes. Molecular and Biochemical Parasitology 50, 225234.Google Scholar
Cooper, R., Inverso, J. A., Espinosa, M., Nogueira, N. and Cross, G. A. (1991). Characterization of a candidate gene for GP72, an insect stage-specific antigen of Trypanosoma cruzi. Molecular and Biochemical Parasitology 49, 4559.Google Scholar
Coronado, X., Zulantay, I., Albrecht, H., Rozas, M., Apt, W., Ortiz, S., Rodriguez, J., Sanchez, G. and 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, 10081012.Google Scholar
Costa, F., Pereira-Chioccola, V. L., Ribeirão, M., Schenkman, S. and Rodrigues, M. M. (1999). Trans-sialidase delivered as a naked DNA vaccine elicits an immunological response similar to a Trypanosoma cruzi infection. Brazilian Journal of Medical and Biological Research 32, 235239.Google Scholar
Cuevas, I. C., Cazzulo, J. J. and Sanchez, D. O. (2003). Gp63 homologues in Trypanosoma cruzi: surface antigens with metalloprotease activity and a possible role in host cell infection. Infection and Immunity 71, 57395749.CrossRefGoogle Scholar
Dias, J. C. P. (1992). Epidemiology of Chagas disease. In Chagas Disease (American Trypanosomiasis): its Impact on Transfusion and Clinical Medicine (ed.Wendel, S., Brener, Z., Camargo, M. E. and Rassi, A.), pp. 4983. ISBT Brazil, São Paulo, Brazil.Google Scholar
Elias, M. C., Vargas, N., Tomazi, L., Pedroso, A., Zingales, B., Schenkman, S. and Briones, M. R. (2005). Comparative analysis of genomic sequences suggests that Trypanosoma cruzi CL Brener contains two sets of non-intercalated repeats of satellite DNA that correspond to T. cruzi I and T. cruzi II types. Molecular and Biochemical Parasitology 140, 221227.Google Scholar
Fonseca, S. G., Moins-Teisserenc, H., Clave, E., Ianni, B., Nunes, V. L., Mady, C., Iwai, L. K., Sette, A., Sidney, J., Marin, M. L., Goldberg, A. C., Guilherme, L., Charron, D., Toubert, A., Kalil, J. and Cunha-Neto, E. (2005). Identification of multiple HLA-A*0201-restricted cruzipain and FL-160 CD8+ epitopes recognized by T cells from chronically Trypanosoma cruzi-infected patients. Microbes and Infection 7, 688697.CrossRefGoogle Scholar
Garcia, A. L., Kindt, A., Quispe-Tintaya, K. W., Bermudez, H., Llanos, A., Arevalo, J., Banuls, A. L., De Doncker, S., Le Ray, D. and Dujardin, J. C. (2005). American tegumentary leishmaniasis: antigen-gene polymorphism, taxonomy and clinical pleomorphism. Infection Genetics and Evolution 5, 109116.Google Scholar
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., Acosta, N., de Arias, A. R. and Miles, M. A. (2003). Mechanism of genetic exchange in American trypanosomes. Nature, London 421, 936939.CrossRefGoogle ScholarPubMed
Giambiagi-deMarval, M., Souto-Padron, T. and Rondinelli, E. (1996). Characterization and cellular distribution of heat-shock proteins HSP70 and HSP60 in Trypanosoma cruzi. Experimental Parasitology 83, 335345.CrossRefGoogle ScholarPubMed
Gonzalez, A., Lerner, T. J., Huecas, M., Sosa-Pineda, B., Nogueira, N. and Lizardi, P. M. (1985). Apparent generation of a segmented mRNA from two separate tandem gene families in Trypanosoma cruzi. Nucleic Acids Research 13, 57895804.Google Scholar
Gupta, S. and Anderson, R. (1999). Population structure of pathogens: the role of immune selection. Parasitology Today 15, 497501.CrossRefGoogle ScholarPubMed
Henriksson, J., Aslund, L., Macina, R. A., Franke de Cazzulo, B. M., Cazzulo, J. J., Frasch, A. C. and Pettersson, U. (1990). Chromosomal localization of seven cloned antigen genes provides evidence of diploidy and further demonstration of karyotype variability in Trypanosoma cruzi. Molecular and Biochemical Parasitology 42, 213223.Google Scholar
Kahn, S., Colbert, T. G., Wallace, J. C., Hoagland, N. A. and Eisen, H. (1991). The major 85-kDa surface antigen of the mammalian-stage forms of Trypanosoma cruzi is a family of sialidases. Proceedings of the National Academy of Sciences, USA 15, 44814485.CrossRefGoogle Scholar
Kahn, S. J., Nguyen, D., Norsen, J., Wleklinski, M., Granston, T. and Kahn, M. (1999). Trypanosoma cruzi: monoclonal antibodies to the surface glycoprotein superfamily differentiate subsets of the 85-kDa surface glycoproteins and confirm simultaneous expression of variant 85-kDa surface glycoproteins. Experimental Parasitology 92, 4856.Google Scholar
Klein, K. G., Olson, C. L., Donelson, J. E. and Engman, D. M. (1995). Molecular comparison of the mitochondrial and cytoplasmic hsp70 of Trypanosoma cruzi, Trypanosoma brucei and Leishmania major. Journal of Eukaryotic Microbiology 42, 473476.CrossRefGoogle ScholarPubMed
Machado, C. A. and Ayala, F. J. (2001). Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proceedings of the National Academy of Sciences, USA 98, 73967401.Google Scholar
McKerrow, J. H., Sun, E., Rosenthal, P. J. and Bouvier, J. (1993). The proteases and pathogenicity of parasitic protozoa. Annual Reviews of Microbiology 47, 821853.CrossRefGoogle ScholarPubMed
Mendonca, M. B., Nehme, N. S., Santos, S. S., Cupolillo, E., Vargas, N., Junqueira, A., Naiff, R. D., Barrett, T. V., Coura, J. R., Zingales, B. and Fernandes, O. (2002). Two main clusters within Trypanosoma cruzi zymodeme 3 are defined by distinct regions of the ribosomal RNA cistron. Parasitology 124, 177184.Google Scholar
Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K. and Opas, M. (1999). Calreticulin: one protein, one gene, many functions. Biochemistry Journal 344, 281292.Google Scholar
Nei, M. and Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences, USA 76, 52695273.CrossRefGoogle ScholarPubMed
Nordborg, M. (2000). Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154, 923929.CrossRefGoogle ScholarPubMed
Nunes, L. R., de Carvalho, M. R. and Buck, G. A. (1997). Trypanosoma cruzi strains partition into two groups based on the structure and function of the spliced leader RNA and rRNA gene promoters. Molecular and Biochemical Parasitology 86, 211224.Google Scholar
Ramos, R., Juri, M., Ramos, A., Hoecker, G., Lavandero, S., Pena, P., Morello, A., Repetto, Y., Aguillon, J. C. and Ferreira, A. (1991). An immunogenetically defined and immunodominant Trypanosoma cruzi antigen. American Journal of Tropical Medicine and Hygiene 44, 314322.CrossRefGoogle ScholarPubMed
Rozas, M., De Doncker, S., Adaui, V., Coronado, X., Barnabé, C., Tibyarenc, M., Solari, A. and Dujardin, J. C. (2007). Multilocus polymerase chain reaction restriction fragment–length polymorphism genotyping of Trypanosoma cruzi (Chagas Disease): taxonomic and clinical applications. Journal of Infectious Diseases 195, 13811388.CrossRefGoogle ScholarPubMed
Sher, A. and Snary, D. (1982). Specific inhibition of the morphogenesis of Trypanosoma cruzi by a monoclonal antibody. Nature, London 300, 639640.CrossRefGoogle ScholarPubMed
Souto, R. P., Fernandes, O., Macedo, A. M., Campbell, D. A. and Zingales, B. (1996). DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Molecular and Biochemical Parasitology 83, 141152.Google Scholar
Sturm, N. R., Vargas, N. S., Westenberger, S. J., Zingales, B. and Campbell, D. A. (2003). Evidence for multiple hybrid groups in Trypanosoma cruzi. International Journal for Parasitology 33, 269279.CrossRefGoogle ScholarPubMed
Tibayrenc, M., Ward, P., Moya, A. and Ayala, F. J. (1986). Natural populations of Trypanosoma cruzi, the agent of Chagas disease, have a complex multiclonal structure. Proceedings of the National Academy of Sciences, USA 83, 115119.Google Scholar
Tibayrenc, M., Neubauer, K., Barnabe, C., Guerrini, F., Skarecky, D. and Ayala, F. J. (1993). Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proceedings of the National Academy of Sciences, USA 90, 13351339.CrossRefGoogle ScholarPubMed
Tibayrenc, M. (1995). Population genetics and strain typing of microorganisms: how to detect departures from panmixia without individualizing alleles and loci. Comptes Rendus de l'Académie des Sciences III 318, 135139.Google Scholar
Thomas, M. C., Garcia-Perez, J. L., Alonso, C. and Lopez, M. C. (2000). Molecular characterization of KMP11 from Trypanosoma cruzi: a cytoskeleton-associated protein regulated at the translational level. DNA Cell Biology 19, 4757.CrossRefGoogle ScholarPubMed
Van Voorhis, W. C., Barrett, L., Koelling, R. and Farr, A. G. (1993). FL-160 proteins of Trypanosoma cruzi are expressed from a multigene family and contain two distinct epitopes that mimic nervous tissues. Journal of Experimental Medicine 178, 681694.Google Scholar
Victoir, K. and Dujardin, J. C. (2002). How to succeed in parasitic life without sex? Asking Leishmania. Trends in Parasitology 18, 8185.CrossRefGoogle ScholarPubMed
Westenberger, S. J., Barnabe, C., Campbell, D. A. and Sturm, N. R. (2005). Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 171, 527543.CrossRefGoogle ScholarPubMed
Westenberger, S. J., Sturm, N. R. and Campbell, D. A. (2006). Trypanosoma cruzi 5S rRNA arrays define five groups and indicate the geographic origins of an ancestor of the heterozygous hybrids. International Journal for Parasitology 36, 337346.Google Scholar
World Health Organization (1991). Control of Chagas disease. Technical Reports No. 811. WHO, Geneva, Switzerland.Google Scholar
Zingales, B., Stolf, B. S., Souto, R. P., Fernandes, O. and Briones, M. R. (1999). Epidemiology, biochemistry and evolution of Trypanosoma cruzi lineages based on ribosomal RNA sequences. Memorias Instituto Oswaldo Cruz 1, 159164.Google Scholar