Análisis de polimorfismos en los genes tripanotión reductasa y cruzipaína en cepas colombianas de Trypanosoma cruzi
Palabras clave:
Trypanosoma cruzi, genes protozoarios, polimorfismo, polimorfismo de longitud del fragmento de restricción, Colombia
Resumen
Introducción. Los estudios genéticos en Trypanosoma cruzi han buscado establecer asociaciones de variantes genéticas del parásito con manifestaciones clínicas de la enfermedad, origen biológico y geográfico de los aislamientos; sin embargo, los resultados de asociación con los marcadores comúnmente usados en estos estudios han generado mucha controversia, principalmente en la asociación de grupos con características clínicas y epidemiológicas de la enfermedad.Objetivo. Se planteó determinar la variabilidad de genes que codifican para las proteínas tripanotión reductasa y cruzipaína, involucradas en mecanismos de infección y supervivencia del parásito en el hospedador mamífero, y probar la asociación de variantes génicas con origen biológico y geográfico de cepas colombianas de T. cruzi.
Materiales y métodos. Se tipificaron por reacción en cadena de la polimerasa- polimorfismo de longitud del fragmento de restricción seis SNPs (Single Nucleotide Polymorphisms) en tripanotión reductasa y ocho SNPs en cruzipaína en 36 cepas colombianas de T. cruzi de diferentes regiones y origen biológico.
Resultados. Con las enzimas Acy I y Hae III se determinaron tres genotipos para tripanotión reductasa. Para cruzipaína se identificaron seis genotipos con las enzimas Rsa I, Ban I y Bsu 36I.
Conclusiones. Para tripanotión reductasa no fue posible establecer una asociación con el origen biológico o geográfico; sin embargo los alelos producidos en las posiciones 102 y 210, permitieron discriminar los grupos tradicionales I y II. Con los genotipos obtenidos para cruzipaína se establecieron relaciones a estos grupos, origen biológico y geográfico. Los resultados sugieren la utilidad de estos genes como marcadores moleculares para determinar y diferenciar variedades genéticas en T. cruzi.
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Referencias bibliográficas
1. Tibayrenc M, Kjellberg F, Ayala FJ. A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas and Trypanosoma and their medical and taxonomical consequences. Proc Natl Acad Sci USA 1990;87:2414-8.
2. Scharfstein J, Morrot A. A role for extracellular amastigotes in the immunopathology of Chagas disease. Mem Inst Oswaldo Cruz 1999;94(Suppl 1):51-63.
3. Brener Z. Biology of Trypanosoma cruzi. Annu Rev Microbiol 1973;27:347-82.
4. Melo RC, Brener Z. Tissue tropism of different Trypanosoma cruzi strains. J Parasitol 1978;64:475-82.
5. Andrade Z, Brener ZE. Trypanosoma cruzi e Doença de Chagas. Rio de Janeiro: Ed. Guanabar Koogan; 1979.
6. Andrade SG, Andrade V, Brodskyn C, Magalhaes JB, Netto MB. Immunological response of Swiss mice to infection with three different strains of Trypanosoma cruzi. Ann Trop Med Parasitol 1985;79:397-407.
7. de Castro SL, de Meirelles M de N. Effect of drugs on Trypanosoma cruzi and on its interaction with heart muscle cell in vitro. Mem Inst Oswaldo Cruz 1987;82:209-18.
8. Neal RA, van Bueren J. Comparative studies of drug susceptibility of five strains of Trypanosoma cruzi in vivo and in vitro. Trans R Soc Trop Med Hyg 1988;82:709-14.
9. Vago AR, Andrade LO, Leite AA, d'Avila Reis D, Macedo AM, Adad SJ, et al. Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic Chagas disease: differential distribution of genetic types into diverse organs. Am J Pathol 2000;156:1805-9.
10. Morel C, Chiari E, Camargo EP, Mattei DM, Romanha AJ, Simpson L. Strains and clones of Trypanosoma cruzi can be characterized by pattern of restriction endonuclease products of kinetoplast DNA minicircles. Proc Natl Acad Sci USA 1980;77:6810-4.
11. Souto RP, Zingales B. Sensitive detection and strain classification of Trypanosoma cruzi by amplification of a ribosomal RNA sequence. Mol Biochem Parasitol 1993;62:45-52.
12. Tibayrenc M, Neubauer K, Barnabe C, Guerrini F, Skarecky D, Ayala FJ. Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proc Natl Acad Sci USA 1993; 90:1335-9.
13. Souto RP, Fernandes O, Macedo AM, Campbell DA, Zingales B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol 1996;83:141-52.
14. Momen H. Taxonomy of Trypanosoma cruzi: a commentary on characterization and nomenclature. Mem Inst Oswaldo Cruz 1999;94(Suppl. 1):181-4.
15. Brisse S, Dujardin JC, Tibayrenc M. Identification of six Trypanosoma cruzi lineages by sequencecharacterized amplified region markers. Mol Biochem Parasitol 2000;111:95-105.
16. Brisse S, Barnabé C, Tibayrenc M. Trypanosoma cruzi: How many relevant phylogenetic subdivisions are there? Parasitol Today 1998;14:178-9.
17. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran A, et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005;309:409-15.
18. Machado CA, Ayala FJ. Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc Natl Acad Sci USA 2001;98:7396-401.
19. Krieger S, Schwarz W, Ariyanayagam MR, Fairlamb AH, Krauth-Siegel RL, Clayton C. Trypanosomes lacking trypanothione reductase are avirulent and show increased sensitivity to oxidative stress. Mol Microbiol 2000;35:542-52.
20.Schmidt A, Krauth-Siegel RL. Enzymes of the trypanothione metabolism as targets for antitrypanosomal drug development. Curr Top Med Chem 2002;11:1239-59.
21. Fairlamb AH, Cerami A. Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 1992;46:695-729.
22. Dumas C, Ouellette M, Tovar J, Cunningham ML, Fairlamb AH, Tamar S, et al. Disruption of the trypanothione reductase gene of Leishmania decreases its ability to survive oxidative stress in macrophages. EMBO J 1997;16:2590-8.
23. Eakin AE, Mills AA, Harth G, McKerrow JH, Crack CS. The sequence, organization, and expression of the major cysteine protease (cruzain) from Trypanosoma cruzi. J Biol Chem 1992;267:7411-20.
24. Campetella O, Henriksson J, Aslund A, Frasch AC, Petterson U, Cazzulo JJ. The major cysteine proteinase (cruzipain) from Trypanosoma cruzi is encoded by multiple polymorphic tandemly organized
genes located on different chromosomes. Mol Biochem Parasitol 1992;50:225-34.
25. Tomas AM, Kelly JM. Stage-regulated expression of cruzipain, the major cysteine protease of Trypanosoma cruzi is independent of the level of RNA1. Mol Biochem Parasitol 1996;76:91-103.
26. Lima AP, Tessier DC, Thomas DY, Scharfstein J, Storrer AC, Vernet T. Identification of new cysteine protease gene isoforms in Trypanosoma cruzi. Mol Biochem Parasitol 1994;67:333-8.
27. Lima AP, dos Reis FC, Serveau C, Lalmanach, Juliano L, Ménard R, et al. Cysteine protease isoforms from Trypanosoma cruzi, cruzipain 2 and cruzain, present different substrate preference and susceptibility to inhibitor. Mol Biochem Parasitol 2001;114:41-52.
28. Cazzulo JJ, Stoka V, Turk V. Cruzipain, the major cysteine proteinase from the protozoan parasite Trypanosoma cruzi. Biol Chem 1997;378:1-10.
29. Cazzulo JJ. Cruzipain, major cysteine proteinase of Trypanosoma cruzi: sequence and genomic organization of the codifying genes. Medicina (B Aires) 1999;59 (Suppl. 2):7-10.
30. Engel JC, Doyle PS, Hsieh I, McKerrow JH. Cysteine protease inhibitors cure an experimental Trypanosoma cruzi infection. J Exp Med 1998;188:725-34.
31. Klemba M, Goldberg DE. Biological roles of proteases in parasitic protozoa. Annu Rev Biochem 2002;71:275-305.
32. Del Nery E, Juliano MA, Lima AP, Schafstein J, Juliano L. Kininogenase activity by the major cysteinyl proteinase (cruzipain) from Trypanosoma cruzi. J Biol Chem 1997;272:25713-8.
33. Scharfstein J, Schmitz V, Morandi V, Capella MM, Lima AP, Morrot A, et al. Host cell invasion by Trypanosoma cruzi is potentiated by activation of bradykinin B(2) receptors. J Exp Med 2000;192:1289-300.
34. Aparicio IM, Scharfstein J, Lima AP. A new cruzipain-mediated pathway of human cell invasion by Trypanosoma cruzi requires trypomastigote membranes. Infect Immun 2004;72:5892-902.
35. Berasain P, Carmona C, Frangione B, Cazzulo JJ, Goni F. Specific cleavage sites on human IgG subclasses by cruzipain, the major cysteine proteinase from Trypanosoma cruzi. Mol Biochem Parasitol
2003;130:23-9.
36. Camargo EP. Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop Sao Paulo 1964;12:93-100.
37. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988;16:1215.
38. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning. A laboratory manual. Second edition. Cold Spring: Harbor Laboratory Press; 1989.
39. Xia X , Xie Z. DAMBE: software package for data analysis in molecular biology and evolution. J Hered 2001;92:371-3.
40. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003;19:2496-7.
41. Carreño H, Rojas C, Aguilera X, Apt W, Miles MA, Solari A. Schizodeme analyses of Trypanosoma cruzi zymodemes from Chile. Exp Parasitol 1987;64:252-60.
42. Macedo AM, Pena SD. Genetic variability of Trypanosoma cruzi: implications for the pathogenesis of Chagas disease. Parasitol Today 1998;14:119-23.
43. Solari A, Wallace A, Ortiz S, Venegas J, Sánchez G. Biological characterization of Trypanosoma cruzi stocks from Chile. Exp Parasitol 1998;89:312-22.
44. Bogliolo AR, Lauria-Pires L, Gibson W. Polymorphisms in Trypanosoma cruzi: evidence of genetic recombination. Acta Trop 1996;61:31-40.
45. Gaunt MW, Yeo M, Frame IA, Stothard JR, Carrascos HJ, Taylor MC, et al. Mechanism of genetic exchange in American trypanosomes. Nature 2003;421:936-9.
46. Brisse S, Henriksson J, Bernabé C, Douzery EJ, Berkvens D, Serrano M, et al. Evidence for genetic exchange and hybridization in Trypanosoma cruzi base on nucleotide sequences and molecular karyotype. Infect Genet Evol 2003;2:173-83.
47. Sturm NR, Vargas NS, Westenberger SJ, Zingales B, Campbell DA. Evidence for multiple hybrid groups in Trypanosoma cruzi. Int J Parasitol 2003;33:269-79.
48. Paulino M, Iribarne F, Dubin M, Aguilera-Morales S, Tapia O, Stoppani AO. The chemotherapy of Chagas' disease: an overview. Mini Rev Med Chem 2005;5:499-519.
49. Meiering S, Inhoff O, Mies J, Vincek A, Garcia G, Kramer B, et al. Inhibitors of Trypanosoma cruzi trypanothione reductase revealed by virtual screening and parallel synthesis. J Med Chem 2005;48:4793-802.
50. Zimmer EA, Martin SL, Beverly SM, Kan YM, Wilson AC. Rapid duplication and loss of genes coding for the a chain of haemoglobin. Proc Natl Acad Sci USA 1980;77:2158-62.
51. Lynch M, Conery LM. The evolutionary fate and consequences of duplicate genes. Science 2000;290:1151-5.
52. Hurles M. Gene duplication: the genomic trade in spare parts. PloS Biol 2004;2:E206.
53. Saravia NG, Holguín AF, Cibulskis RE, D´Alessandro A. Divergent isoenzyme profiles of sylvatic and domiciliary Trypanosoma cruzi in the Eastern plains, piedmont, and highlands of Colombia. Am J Trop Med Hyg 1987;36:59-69.
54. Cuervo P, Cupolillo E, Segura I, Saravia N, Fernandes O. Genetic diversity of Colombian sylvatic Trypanosoma cruzi isolates revealed by the ribosomal DNA. Mem Inst Oswaldo Cruz 2002;97:877-80.
55. Jaramillo N, Moreno J, Triana O, Arcos-Burgos M, Muñoz S, Solari A. Genetic structure and phylogenetic relationships of Colombian Trypanosoma cruzi populations as determined by schizodeme and
isoenzyme markers. Am J Trop Med Hyg 1999;61:986-93.
56. Moncayo A. Chagas disease: current epidemiological trends after the interruption of vectorial and transfusional transmission in the Southern Cone countries. Mem Inst Oswaldo Cruz 2003;98:577-91.
57. Guhl F, Restrepo M, Angulo VM, Antunes CMF, Campbell-Lendrum D, Davies CR. Lessons from a national survey of Chagas disease transmission risk in Colombia. Trends Parasitol 2005;21:259-62.
58. Hartl CL, Clark AG. Principles of population genetics. Sunderland, Massachusetts; Sinauer Associate: 1997.
59. Garcia ES, Gonzalez MS, Azambuja P. Biological factors involving Trypanosoma cruzi life cycle in the invertebrate vector, Rhodnius prolixus. Mem Inst Oswaldo Cruz 1999;94(Suppl. 1):213-6.
60. Azambuja P, Garcia ES, Ratcliffe NA. Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 2005;21:568-72.
61. Rodríguez P, Escalante M, Díez H, Cuervo C, Montilla M, Nicholls RS, et al. Estudio de la variabilidad de seis cepas colombianas de Trypanosoma cruzi mediante polimorfismos de longitud de los fragmentos de restricción (RFLP) y amplificación aleatoria de ADN polimórfico (RAPD). Biomédica 2002;22:263-71.
2. Scharfstein J, Morrot A. A role for extracellular amastigotes in the immunopathology of Chagas disease. Mem Inst Oswaldo Cruz 1999;94(Suppl 1):51-63.
3. Brener Z. Biology of Trypanosoma cruzi. Annu Rev Microbiol 1973;27:347-82.
4. Melo RC, Brener Z. Tissue tropism of different Trypanosoma cruzi strains. J Parasitol 1978;64:475-82.
5. Andrade Z, Brener ZE. Trypanosoma cruzi e Doença de Chagas. Rio de Janeiro: Ed. Guanabar Koogan; 1979.
6. Andrade SG, Andrade V, Brodskyn C, Magalhaes JB, Netto MB. Immunological response of Swiss mice to infection with three different strains of Trypanosoma cruzi. Ann Trop Med Parasitol 1985;79:397-407.
7. de Castro SL, de Meirelles M de N. Effect of drugs on Trypanosoma cruzi and on its interaction with heart muscle cell in vitro. Mem Inst Oswaldo Cruz 1987;82:209-18.
8. Neal RA, van Bueren J. Comparative studies of drug susceptibility of five strains of Trypanosoma cruzi in vivo and in vitro. Trans R Soc Trop Med Hyg 1988;82:709-14.
9. Vago AR, Andrade LO, Leite AA, d'Avila Reis D, Macedo AM, Adad SJ, et al. Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic Chagas disease: differential distribution of genetic types into diverse organs. Am J Pathol 2000;156:1805-9.
10. Morel C, Chiari E, Camargo EP, Mattei DM, Romanha AJ, Simpson L. Strains and clones of Trypanosoma cruzi can be characterized by pattern of restriction endonuclease products of kinetoplast DNA minicircles. Proc Natl Acad Sci USA 1980;77:6810-4.
11. Souto RP, Zingales B. Sensitive detection and strain classification of Trypanosoma cruzi by amplification of a ribosomal RNA sequence. Mol Biochem Parasitol 1993;62:45-52.
12. Tibayrenc M, Neubauer K, Barnabe C, Guerrini F, Skarecky D, Ayala FJ. Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proc Natl Acad Sci USA 1993; 90:1335-9.
13. Souto RP, Fernandes O, Macedo AM, Campbell DA, Zingales B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol 1996;83:141-52.
14. Momen H. Taxonomy of Trypanosoma cruzi: a commentary on characterization and nomenclature. Mem Inst Oswaldo Cruz 1999;94(Suppl. 1):181-4.
15. Brisse S, Dujardin JC, Tibayrenc M. Identification of six Trypanosoma cruzi lineages by sequencecharacterized amplified region markers. Mol Biochem Parasitol 2000;111:95-105.
16. Brisse S, Barnabé C, Tibayrenc M. Trypanosoma cruzi: How many relevant phylogenetic subdivisions are there? Parasitol Today 1998;14:178-9.
17. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran A, et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005;309:409-15.
18. Machado CA, Ayala FJ. Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc Natl Acad Sci USA 2001;98:7396-401.
19. Krieger S, Schwarz W, Ariyanayagam MR, Fairlamb AH, Krauth-Siegel RL, Clayton C. Trypanosomes lacking trypanothione reductase are avirulent and show increased sensitivity to oxidative stress. Mol Microbiol 2000;35:542-52.
20.Schmidt A, Krauth-Siegel RL. Enzymes of the trypanothione metabolism as targets for antitrypanosomal drug development. Curr Top Med Chem 2002;11:1239-59.
21. Fairlamb AH, Cerami A. Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 1992;46:695-729.
22. Dumas C, Ouellette M, Tovar J, Cunningham ML, Fairlamb AH, Tamar S, et al. Disruption of the trypanothione reductase gene of Leishmania decreases its ability to survive oxidative stress in macrophages. EMBO J 1997;16:2590-8.
23. Eakin AE, Mills AA, Harth G, McKerrow JH, Crack CS. The sequence, organization, and expression of the major cysteine protease (cruzain) from Trypanosoma cruzi. J Biol Chem 1992;267:7411-20.
24. Campetella O, Henriksson J, Aslund A, Frasch AC, Petterson U, Cazzulo JJ. The major cysteine proteinase (cruzipain) from Trypanosoma cruzi is encoded by multiple polymorphic tandemly organized
genes located on different chromosomes. Mol Biochem Parasitol 1992;50:225-34.
25. Tomas AM, Kelly JM. Stage-regulated expression of cruzipain, the major cysteine protease of Trypanosoma cruzi is independent of the level of RNA1. Mol Biochem Parasitol 1996;76:91-103.
26. Lima AP, Tessier DC, Thomas DY, Scharfstein J, Storrer AC, Vernet T. Identification of new cysteine protease gene isoforms in Trypanosoma cruzi. Mol Biochem Parasitol 1994;67:333-8.
27. Lima AP, dos Reis FC, Serveau C, Lalmanach, Juliano L, Ménard R, et al. Cysteine protease isoforms from Trypanosoma cruzi, cruzipain 2 and cruzain, present different substrate preference and susceptibility to inhibitor. Mol Biochem Parasitol 2001;114:41-52.
28. Cazzulo JJ, Stoka V, Turk V. Cruzipain, the major cysteine proteinase from the protozoan parasite Trypanosoma cruzi. Biol Chem 1997;378:1-10.
29. Cazzulo JJ. Cruzipain, major cysteine proteinase of Trypanosoma cruzi: sequence and genomic organization of the codifying genes. Medicina (B Aires) 1999;59 (Suppl. 2):7-10.
30. Engel JC, Doyle PS, Hsieh I, McKerrow JH. Cysteine protease inhibitors cure an experimental Trypanosoma cruzi infection. J Exp Med 1998;188:725-34.
31. Klemba M, Goldberg DE. Biological roles of proteases in parasitic protozoa. Annu Rev Biochem 2002;71:275-305.
32. Del Nery E, Juliano MA, Lima AP, Schafstein J, Juliano L. Kininogenase activity by the major cysteinyl proteinase (cruzipain) from Trypanosoma cruzi. J Biol Chem 1997;272:25713-8.
33. Scharfstein J, Schmitz V, Morandi V, Capella MM, Lima AP, Morrot A, et al. Host cell invasion by Trypanosoma cruzi is potentiated by activation of bradykinin B(2) receptors. J Exp Med 2000;192:1289-300.
34. Aparicio IM, Scharfstein J, Lima AP. A new cruzipain-mediated pathway of human cell invasion by Trypanosoma cruzi requires trypomastigote membranes. Infect Immun 2004;72:5892-902.
35. Berasain P, Carmona C, Frangione B, Cazzulo JJ, Goni F. Specific cleavage sites on human IgG subclasses by cruzipain, the major cysteine proteinase from Trypanosoma cruzi. Mol Biochem Parasitol
2003;130:23-9.
36. Camargo EP. Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop Sao Paulo 1964;12:93-100.
37. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988;16:1215.
38. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning. A laboratory manual. Second edition. Cold Spring: Harbor Laboratory Press; 1989.
39. Xia X , Xie Z. DAMBE: software package for data analysis in molecular biology and evolution. J Hered 2001;92:371-3.
40. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003;19:2496-7.
41. Carreño H, Rojas C, Aguilera X, Apt W, Miles MA, Solari A. Schizodeme analyses of Trypanosoma cruzi zymodemes from Chile. Exp Parasitol 1987;64:252-60.
42. Macedo AM, Pena SD. Genetic variability of Trypanosoma cruzi: implications for the pathogenesis of Chagas disease. Parasitol Today 1998;14:119-23.
43. Solari A, Wallace A, Ortiz S, Venegas J, Sánchez G. Biological characterization of Trypanosoma cruzi stocks from Chile. Exp Parasitol 1998;89:312-22.
44. Bogliolo AR, Lauria-Pires L, Gibson W. Polymorphisms in Trypanosoma cruzi: evidence of genetic recombination. Acta Trop 1996;61:31-40.
45. Gaunt MW, Yeo M, Frame IA, Stothard JR, Carrascos HJ, Taylor MC, et al. Mechanism of genetic exchange in American trypanosomes. Nature 2003;421:936-9.
46. Brisse S, Henriksson J, Bernabé C, Douzery EJ, Berkvens D, Serrano M, et al. Evidence for genetic exchange and hybridization in Trypanosoma cruzi base on nucleotide sequences and molecular karyotype. Infect Genet Evol 2003;2:173-83.
47. Sturm NR, Vargas NS, Westenberger SJ, Zingales B, Campbell DA. Evidence for multiple hybrid groups in Trypanosoma cruzi. Int J Parasitol 2003;33:269-79.
48. Paulino M, Iribarne F, Dubin M, Aguilera-Morales S, Tapia O, Stoppani AO. The chemotherapy of Chagas' disease: an overview. Mini Rev Med Chem 2005;5:499-519.
49. Meiering S, Inhoff O, Mies J, Vincek A, Garcia G, Kramer B, et al. Inhibitors of Trypanosoma cruzi trypanothione reductase revealed by virtual screening and parallel synthesis. J Med Chem 2005;48:4793-802.
50. Zimmer EA, Martin SL, Beverly SM, Kan YM, Wilson AC. Rapid duplication and loss of genes coding for the a chain of haemoglobin. Proc Natl Acad Sci USA 1980;77:2158-62.
51. Lynch M, Conery LM. The evolutionary fate and consequences of duplicate genes. Science 2000;290:1151-5.
52. Hurles M. Gene duplication: the genomic trade in spare parts. PloS Biol 2004;2:E206.
53. Saravia NG, Holguín AF, Cibulskis RE, D´Alessandro A. Divergent isoenzyme profiles of sylvatic and domiciliary Trypanosoma cruzi in the Eastern plains, piedmont, and highlands of Colombia. Am J Trop Med Hyg 1987;36:59-69.
54. Cuervo P, Cupolillo E, Segura I, Saravia N, Fernandes O. Genetic diversity of Colombian sylvatic Trypanosoma cruzi isolates revealed by the ribosomal DNA. Mem Inst Oswaldo Cruz 2002;97:877-80.
55. Jaramillo N, Moreno J, Triana O, Arcos-Burgos M, Muñoz S, Solari A. Genetic structure and phylogenetic relationships of Colombian Trypanosoma cruzi populations as determined by schizodeme and
isoenzyme markers. Am J Trop Med Hyg 1999;61:986-93.
56. Moncayo A. Chagas disease: current epidemiological trends after the interruption of vectorial and transfusional transmission in the Southern Cone countries. Mem Inst Oswaldo Cruz 2003;98:577-91.
57. Guhl F, Restrepo M, Angulo VM, Antunes CMF, Campbell-Lendrum D, Davies CR. Lessons from a national survey of Chagas disease transmission risk in Colombia. Trends Parasitol 2005;21:259-62.
58. Hartl CL, Clark AG. Principles of population genetics. Sunderland, Massachusetts; Sinauer Associate: 1997.
59. Garcia ES, Gonzalez MS, Azambuja P. Biological factors involving Trypanosoma cruzi life cycle in the invertebrate vector, Rhodnius prolixus. Mem Inst Oswaldo Cruz 1999;94(Suppl. 1):213-6.
60. Azambuja P, Garcia ES, Ratcliffe NA. Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 2005;21:568-72.
61. Rodríguez P, Escalante M, Díez H, Cuervo C, Montilla M, Nicholls RS, et al. Estudio de la variabilidad de seis cepas colombianas de Trypanosoma cruzi mediante polimorfismos de longitud de los fragmentos de restricción (RFLP) y amplificación aleatoria de ADN polimórfico (RAPD). Biomédica 2002;22:263-71.
Cómo citar
1.
Rojas W, Caro MA, Lopera JG, Triana O, Dib JC, Bedoya G. Análisis de polimorfismos en los genes tripanotión reductasa y cruzipaína en cepas colombianas de Trypanosoma cruzi. biomedica [Internet]. 1 de enero de 2007 [citado 23 de abril de 2024];27(1esp):50-63. Disponible en: https://revistabiomedica.org/index.php/biomedica/article/view/248
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