Gene expression study using real-time PCR identifies an NTR gene as a major marker of resistance to benznidazole in Trypanosoma cruzi

Parasites and Vectors

Volumn 4, Issue 1, 2011, Pages

  Mejía Jaramillo, Ana M ^a   Fernández, Geysson J ^a   Palacio, Lina ^a   Triana Chávez, Omar ^a  

^a UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

BENZNIDAZOLE; MESSENGER RNA; NIFURTIMOX; NITROREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; ANTITRYPANOSOMAL AGENT; NITROIMIDAZOLE DERIVATIVE; PROTOZOAL PROTEIN;

ARTICLE; ENZYME ACTIVITY; GENE EXPRESSION; IC 50; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; RANDOM AMPLIFIED POLYMORPHIC DNA; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; TRYPANOSOMA CRUZI; CHAGAS DISEASE; DRUG EFFECT; DRUG RESISTANCE; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MULTIGENE FAMILY; PARASITOLOGY;

TRYPANOSOMA CRUZI;

CHAGAS DISEASE; DRUG RESISTANCE; GENE EXPRESSION; HUMANS; MULTIGENE FAMILY; NITROIMIDAZOLES; NITROREDUCTASES; PROTOZOAN PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; TRYPANOCIDAL AGENTS; TRYPANOSOMA CRUZI;

EID: 80052559869     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-4-169     Document Type: Article

References (63)

1. Social and Medical Aspects: Morbidity and Mortality in General Population. Pinto-Dias J, Schofield C, American Trypanosomiasis Chagas disease: one hundred years of research, Telleria J, Tibayrenc M, First 2010 45 54
2. Geographical Distribution of Chagas Disease. Patterson J, Guhl F, American Trypanosomiasis Chagas disease: one hundred years of research, Telleria J, Tibayrenc M, First 2010 83 114
3. A critical review on Chagas disease chemoterapy. Coura JR, Castro SLd, Mem Inst Oswaldo Cruz 2002 97 3 24 11992141 (Pubitemid 135746197)
4. Trypanosomiasis vector control in Africa and Latin America. Schofield CJ, Kabayo JP, Parasit Vectors 2008 1 24 10.1186/1756-3305-1-24 18673535
5. Trypanocidal drugs: mechanisms, resistance and new targets. Wilkinson SR, Kelly JM, Expert Rev Mol Med 2009 11 31 19863838
6. Mode of action of natural and synthetic drugs against Trypanosoma cruzi and their interaction with the mammalian host. Maya JD, Cassels BK, Iturriaga-Vasquez P, Ferreira J, Faundez M, Galanti N, Ferreira A, Morello A, Comp Biochem Physiol A Mol Integr Physiol 2007 146 601 620 10.1016/j.cbpa.2006. 03.004 16626984 (Pubitemid 46341910)
7. Peroxiredoxins play a major role in protecting Trypanosoma cruzi against macrophage- and endogenously-derived peroxynitrite. Piacenza L, Peluffo G, Alvarez MN, Kelly JM, Wilkinson SR, Radi R, Biochem J 2008 410 359 368 10.1042/BJ20071138 17973627 (Pubitemid 351346194)
8. The role of glutathione peroxidases in trypanosomatids. Wilkinson SR, Kelly JM, Biol Chem 2003 384 517 525 10.1515/BC.2003.060 12751782 (Pubitemid 36609168)
9. Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum. Wilkinson SR, Obado SO, Mauricio IL, Kelly JM, Proc Natl Acad Sci USA 2002 99 13453 13458 10.1073/pnas.202422899 12351682 (Pubitemid 35215402)
10. Distinct mitochondrial and cytosolic enzymes mediate trypanothione- dependent peroxide metabolism in Trypanosoma cruzi. Wilkinson SR, Temperton NJ, Mondragon A, Kelly JM, J Biol Chem 2000 275 8220 8225 10.1074/jbc.275.11.8220 10713147 (Pubitemid 30159739)
11. The iron-containing superoxide dismutases of trypanosomatidae. Turrens JF, McCord JM, Free Radic Biol Med 2006 40 193 195 10.1016/j.freeradbiomed.2005. 11.018 16413401 (Pubitemid 43069344)
12. Nifurtimox activation by trypanosomal type I nitroreductases generates cytotoxic nitrile metabolites. Hall BS, Bot C, Wilkinson SR, J Biol Chem 2011 286 13088 13095 10.1074/jbc.M111.230847 21345801
13. A key role for old yellow enzyme in the metabolism of drugs by Trypanosoma cruzi. Kubata BK, Kabututu Z, Nozaki T, Munday CJ, Fukuzumi S, Ohkubo K, Lazarus M, Maruyama T, Martin SK, Duszenko M, Urade Y, J Exp Med 2002 196 1241 1251 10.1084/jem.20020885 12417633 (Pubitemid 35304189)
14. Exploiting the drug-activating properties of a novel trypanosomal nitroreductase. Hall BS, Wu X, Hu L, Wilkinson SR, Antimicrob Agents Chemother 2010 54 1193 1199 10.1128/AAC.01213-09 20028822
15. A mechanism for cross-resistance to nifurtimox and benznidazole in trypanosomes. Wilkinson SR, Taylor MC, Horn D, Kelly JM, Cheeseman I, Proc Natl Acad Sci USA 2008 105 5022 5027 10.1073/pnas.0711014105 18367671 (Pubitemid 351738503)
16. Biochemical and molecular mechanisms of drug resistance in parasites. Ouellette M, Trop Med Int Health 2001 6 874 882 10.1046/j.1365-3156.2001.00777.x 11703841 (Pubitemid 33010873)
17. New mechanism of drug resistance in parasitic protozoa. Borst P, Oullette M, Annu Rev Microbiol 1995 49 427 460 10.1146/annurev.mi.49.100195.002235 8561467
18. Molecular mechanisms of drug resistance. Hayes JD, Wolf CR, Biochem J 1990 272 281 295 1980062
19. Differential gene expression in benznidazole-resistant Trypanosoma cruzi parasites. Villarreal D, Nirde P, Hide M, Barnabe C, Tibayrenc M, Antimicrob Agents Chemother 2005 49 2701 2709 10.1128/AAC.49.7.2701-2709.2005 15980339 (Pubitemid 40917581)
20. Characterization of a gene encoding alcohol dehydrogenase in benznidazole-susceptible and -resistant populations of Trypanosoma cruzi. Campos FM, Liarte DB, Mortara RA, Romanha AJ, Murta SM, Acta Trop 2009 111 56 63 10.1016/j.actatropica.2009.02.007 19426664
21. Molecular characterization of cytosolic and mitochondrial tryparedoxin peroxidase in Trypanosoma cruzi populations susceptible and resistant to benznidazole. Nogueira FB, Ruiz JC, Robello C, Romanha AJ, Murta SM, Parasitol Res 2009 104 835 844 10.1007/s00436-008-1264-1 19018566
22. Proteomic analysis of Trypanosoma cruzi resistance to Benznidazole. Andrade HM, Murta SM, Chapeaurouge A, Perales J, Nirdé P, Romanha AJ, J Proteome Res 2008 7 2357 2367 10.1021/pr700659m 18435557
23. Differential gene expression in Trypanosoma cruzi populations susceptible and resistant to benznidazole. Murta SM, Nogueira FB, dos Santos PF, Campos FF, Volpe C, Liarte DB, Nirde P, Probst CM, Krieger MA, Goldenberg S, Romanha AJ, Acta Trop 2008 107 59 65 10.1016/j.actatropica.2008.04.011 18501872
24. Trypanosoma cruzi: characterisation of the gene encoding tyrosine aminotransferase in benznidazole-resistant and susceptible populations. Rego JV, Murta SM, Nirde P, Nogueira FB, de Andrade HM, Romanha AJ, Exp Parasitol 2008 118 111 117 10.1016/j.exppara.2007.05.013 17678649 (Pubitemid 350299335)
25. Deletion of copies of the gene encoding old yellow enzyme (TcOYE), a NAD(P)H flavin oxidoreductase, associates with in vitro-induced benznidazole resistance in Trypanosoma cruzi. Murta SM, Krieger MA, Montenegro LR, Campos FF, Probst CM, Avila AR, Muto NH, de Oliveira RC, Nunes LR, Nirde P, et al. Mol Biochem Parasitol 2006 146 151 162 10.1016/j.molbiopara.2005.12.001 16442642 (Pubitemid 43356356)
26. Increased expression of iron-containing superoxide dismutase-A (TcFeSOD-A) enzyme in Trypanosoma cruzi population with in vitro-induced resistance to benznidazole. Nogueira FB, Krieger MA, Nirde P, Goldenberg S, Romanha AJ, Murta SM, Acta Trop 2006 100 119 132 10.1016/j.actatropica.2006.10. 004 17113553 (Pubitemid 44821036)
27. Growth and Differentiation in Trypanosoma cruzi. I. Origin of Metacyclic Trypanosomes in Liquid Media. Camargo EP, Rev Inst Med Trop Sao Paulo 1964 12 93 100
28. Drug-resistant epimastigotes of Trypanosoma cruzi and persistence of this phenotype after differentiation into amastigotes. Nirdé P, Larroque C, Barnabé C, C R Acad Sci Ser 1995 318 1239 1244 (Pubitemid 26019870)
29. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Mosmann T, J Immunol Methods 1983 65 55 63 10.1016/0022-1759(83)90303-4 6606682 (Pubitemid 14203433)
30. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Pfaffl MW, Horgan GW, Dempfle L, Nucleic Acids Res 2002 30 36 10.1093/nar/30.9.e36 11972351
31. A new mathematical model for relative quantification in real-time RT-PCR. Pfaffl MW, Nucleic Acids Res 2001 29 45 10.1093/nar/29.9.e45 11328886
32. Detection of exon deletions within an entire gene (CFTR) by relative quantification on the LightCycler. Schneider M, Joncourt F, Sanz J, von Känel T, Gallati S, Clin Chem 2006 52 2005 2012 10.1373/clinchem.2005. 065136 16990428 (Pubitemid 44658200)
33. Phosphate inhibition of the copper- and zinc-containing superoxide dismutase: a reexamination. Beyer WF, Wang Y, Fridovich I, Biochemistry 1986 25 6084 6088 10.1021/bi00368a037 3024700 (Pubitemid 17204044)
34. Multiple NADPH-cytochrome P450 reductases from Trypanosoma cruzi suggested role on drug resistance. Portal P, Villamil SF, Alonso GD, De Vas MG, Flawiá MM, Torres HN, Paveto C, Mol Biochem Parasitol 2008 160 42 51 10.1016/j.molbiopara.2008.03.007 18455247 (Pubitemid 351699263)
35. Geographical clustering of Trypanosoma cruzi I groups from Colombia revealed by low-stringency single specific primer-PCR of the intergenic regions of spliced-leader genes. Mejía-Jaramillo AM, Arboleda-Sánchez S, Rodríguez IB, Cura C, Salazar A, Del Mazo J, Triana-Chávez O, Schijman AG, Parasitol Res 2009 104 399 410 10.1007/s00436-008-1212-0 18850114
36. Random amplified polymorphic DNA analysis of Trypanosoma cruzi strains. Steindel M, Dias Neto E, de Menezes CL, Romanha AJ, Simpson AJ, Mol Biochem Parasitol 1993 60 71 79 10.1016/0166-6851(93)90030-2 8366896
37. A Critical Review on Chagas Disease Chemotherapy. Rodrigues J, Castro S, Mem Inst Oswaldo Cruz 2002 97 3 24 11992141 (Pubitemid 135746197)
38. Advances in Chagas disease drug development: 2009-2010. Buckner FS, Navabi N, Curr Opin Infect Dis 2010 23 609 616 10.1097/QCO.0b013e3283402956 20885320
39. Specific chemotherapy of Chagas disease: relevance, current limitations and new approaches. Urbina JA, Acta Trop 2010 115 55 68 10.1016/j.actatropica. 2009.10.023 19900395
40. Mode of action of nifurtimox and N-oxide-containing heterocycles against Trypanosoma cruzi: is oxidative stress involved? Boiani M, Piacenza L, Hernández P, Boiani L, Cerecetto H, González M, Denicola A, Biochem Pharmacol 2010 79 1736 1745 10.1016/j.bcp.2010.02.009 20178775
41. Trypanosoma cruzi: effect and mode of action of nitroimidazole and nitrofuran derivatives. Maya JD, Bollo S, Nũez-Vergara LJ, Squella JA, Repetto Y, Morello A, Périé J, Chauvière G, Biochem Pharmacol 2003 65 999 1006 10.1016/S0006-2952(02)01663-5 12623132 (Pubitemid 36293683)
42. "Activation" of nitrofurazone in animal tissues. McCalla DR, Reuvers A, Kaiser C, Biochem Pharmacol 1971 20 3532 3537 10.1016/0006-2952(71) 90459-X 4399895
43. Evaluation of nitroreductase and acetyltransferase participation in N-nitrosodiethylamine genotoxicity. Aiub CA, Mazzei JL, Pinto LF, Felzenszwalb I, Chem Biol Interact 2006 161 146 154 10.1016/j.cbi.2006.03.012 16720019 (Pubitemid 43776626)
44. Nitroreductase: a prodrug-activating enzyme for cancer gene therapy. Searle PF, Chen MJ, Hu L, Race PR, Lovering AL, Grove JI, Guise C, Jaberipour M, James ND, Mautner V, et al. Clin Exp Pharmacol Physiol 2004 31 811 816 10.1111/j.1440-1681.2004.04085.x 15566399 (Pubitemid 39556859)
45. Structural and mechanistic studies of Escherichia coli nitroreductase with the antibiotic nitrofurazone. Reversed binding orientations in different redox states of the enzyme. Race PR, Lovering AL, Green RM, Ossor A, White SA, Searle PF, Wrighton CJ, Hyde EI, J Biol Chem 2005 280 13256 13264 10.1074/jbc.M409652200 15684426 (Pubitemid 40517209)
46. Genetics of nitrofurazone resistance in Escherichia coli. McCalla DR, Kaiser C, Green MH, J Bacteriol 1978 133 10 16 338576 (Pubitemid 8259417)
47. Oxygen-insensitive nitroreductases: analysis of the roles of nfsA and nfsB in development of resistance to 5-nitrofuran derivatives in Escherichia coli. Whiteway J, Koziarz P, Veall J, Sandhu N, Kumar P, Hoecher B, Lambert IB, J Bacteriol 1998 180 5529 5539 9791100 (Pubitemid 28489842)
48. Metronidazole resistance in the protozoan parasite Entamoeba histolytica is associated with increased expression of iron-containing superoxide dismutase and peroxiredoxin and decreased expression of ferredoxin 1 and flavin reductase. Wassmann C, Hellberg A, Tannich E, Bruchhaus I, J Biol Chem 1999 274 26051 26056 10.1074/jbc.274.37.26051 10473552 (Pubitemid 29437046)
49. Quantitative RT-PCR analysis of multiple genes encoding putative metronidazole nitroreductases from Helicobacter pylori. Kwon DH, Osato MS, Graham DY, El-Zaatari FA, Int J Antimicrob Agents 2000 15 31 36 10.1016/S0924-8579(00)00122-9 10856674 (Pubitemid 30336368)
50. Frameshift mutations in rdxA and metronidazole resistance in North American Helicobacter pylori isolates. Kwon DH, Pẽa JA, Osato MS, Fox JG, Graham DY, Versalovic J, J Antimicrob Chemother 2000 46 793 796 10.1093/jac/46.5.793 11062200
51. Frame-shift mutations in NAD(P)H flavin oxidoreductase encoding gene (frxA) from metronidazole resistant Helicobacter pylori ATCC43504 and its involvement in metronidazole resistance. Kwon DH, Kato M, El-Zaatari FA, Osato MS, Graham DY, FEMS Microbiol Lett 2000 188 197 202 10.1111/j.1574-6968.2000. tb09193.x 10913705 (Pubitemid 30412099)
52. Genome-wide RNAi screens in African trypanosomes identify the nifurtimox activator NTR and the eflornithine transporter AAT6. Baker N, Alsford S, Horn D, Mol Biochem Parasitol 2011 176 55 57 10.1016/j.molbiopara.2010.11.010 21093499
53. Divergence of trypanothione-dependent tryparedoxin cascade into cytosolic and mitochondrial pathways in arsenite-resistant variants of Leishmania amazonensis. Hsu JY, Lin YC, Chiang SC, Lee ST, Mol Biochem Parasitol 2008 157 193 204 10.1016/j.molbiopara.2007.11.002 18083246
54. Induction of resistance to azole drugs in Trypanosoma cruzi. Buckner FS, Wilson AJ, White TC, Van Voorhis WC, Antimicrob Agents Chemother 1998 42 3245 3250 9835521 (Pubitemid 28553748)
55. Deletion of the Trypanosoma brucei superoxide dismutase gene sodb1 increases sensitivity to nifurtimox and benznidazole. Prathalingham SR, Wilkinson SR, Horn D, Kelly JM, Antimicrob Agents Chemother 2007 51 755 758 10.1128/AAC.01360-06 17145786 (Pubitemid 46185302)
56. Phenotype of recombinant Leishmania donovani and Trypanosoma cruzi which over-express trypanothione reductase. Sensitivity towards agents that are thought to induceoxidative stress. Kelly J, Taylor M, Smith K, Hunter K, Fairlamb A, Eur J Biochem 1993 218 9
57. Mechanisms of action of aminoglycoside antibiotics in eucaryotic protein synthesis. Eustice DC, Wilhelm JM, Antimicrob Agents Chemother 1984 26 53 60 6433789 (Pubitemid 14086724)
58. Drug resistance mechanisms in clinical isolates of Leishmania donovani. Singh N, Indian J Med Res 2006 123 411 422 16778320 (Pubitemid 43905579)
59. Changes in Trypanosoma cruzi kinetoplast DNA minicircles induced by environmental conditions and subcloning. Alves A, Almeida Dd, Von Kruger W, J Euk Microbiol 1994 41 415 419 10.1111/j.1550-7408.1994.tb06099.x 8087110 (Pubitemid 2130959)
60. Genetic variability of Trypanosoma cruzi in blood and organs of infected mice determined by LSSP-PCR. Mejia AM, Triana O, Biomedica 2005 25 76 86 15962904
61. Kinetoplast DNA signatures of Trypanosoma cruzi strains obtained directly from infected tissues. Vago AR, Macedo AM, Oliveira RP, Andrade LO, Chiari E, Galvao LM, Reis D, Pereira ME, Simpson AJ, Tostes S, Pena SD, Am J Pathol 1996 149 2153 2159 8952547 (Pubitemid 26415231)
62. Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic Chagas disease: differential distribution of genetic types into diverse organs. Vago AR, Andrade LO, Leite AA, d'Avila Reis D, Macedo AM, Adad SJ, Tostes S Jr, Moreira MC, Filho GB, Pena SD, Am J Pathol 2000 156 1805 1809 10.1016/S0002-9440(10)65052-3 10793092 (Pubitemid 30646718)
63. Reflections on the population dynamics of Trypanosoma cruzi: heterogeneity versus plasticity. Pacheco RS, Brito CM, Mem Inst Oswaldo Cruz 1999 94 Suppl 1 199 201 10677715