A novel ABCG-like transporter of Trypanosoma cruzi is involved in natural resistance to benznidazole

Memorias do Instituto Oswaldo Cruz

Volumn 110, Issue 3, 2015, Pages 433-444

  Zingales, Bianca ^a   Araujo, Rafael Gomes Aquino ^a   Moreno, Margoth ^a   Franco, Jaques ^a   Aguiar, Pedro Henrique Nascimento ^b   Nunes, Solange Lessa ^a   Silva, Marcelo Nunes ^a   Ienne, Susan ^a   Machado, Carlos Renato ^b   Brandão, Adeilton ^c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

ABCG transporter; Benznidazole resistance; Chagas disease; Single nucleotide polymorphisms; T. cruzi strains; Transcript abundance

Indexed keywords

TRYPANOSOMA CRUZI;

ABC TRANSPORTER; ANTITRYPANOSOMAL AGENT; BENZNIDAZOLE; CARRIER PROTEIN; NITROIMIDAZOLE DERIVATIVE; PROTOZOAL DNA;

ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SENSITIVITY; GENETICS; GENOTYPE; HUMAN; PHYLOGENY; TRYPANOSOMA CRUZI;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; DNA, PROTOZOAN; DRUG RESISTANCE; GENOTYPE; HUMANS; MEMBRANE TRANSPORT PROTEINS; NITROIMIDAZOLES; PARASITIC SENSITIVITY TESTS; PHYLOGENY; TRYPANOCIDAL AGENTS; TRYPANOSOMA CRUZI;

EID: 84928159538     PISSN: 00740276     EISSN: 16788060     Source Type: Journal    
DOI: 10.1590/0074-02760140407     Document Type: Article

References (50)

1. Bailey TL, Bodén M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208.
2. Baptista CS, Vêncio RZN, Abdala S, Valadares MP, Martins CAO, Zingales B 2004. DNA microarrays for comparative genomics and analysis of gene expression in Trypanosoma cruzi. Mol Biochem Parasitol 138: 183-194.
3. Baptista CS, Vêncio RZN, Abdala SB, Carranza JC, Westenberger SJ, Silva MN, Pereira CAB, Galvão LMC, Gontijo ED, Chiari E, Sturm NR, Zingales B 2006. Differential transcription profiles in Trypanosoma cruzi associated with clinical forms of Chagas disease: maxicircle NADH dehydrogenase subunit 7 gene truncation in asymptomatic patient isolates. Mol Biochem Parasitol 150: 236-248.
4. BoseDasgupta S, Ganguly A, Roy A, Mukherjee T, Majumder HK 2008. A novel ATP-binding cassette transporter, ABCG6, is involved in chemoresistance of Leishmania. Mol Biochem Parasitol 158: 176-188.
5. Brandão A 2006. The untranslated regions of genes from Trypanosoma cruzi: perspectives for functional characterization of strains and isolates. Mem Inst Oswaldo Cruz 101: 775-777.
6. Brandão A, Jiang T 2009. The composition of untranslated regions in Trypanosoma cruzi genes. Parasitol Int 58: 215-219.
7. Campos PC, Bartholomeu DC, DaRocha WD, Cerqueira GC, Teixeira SMR 2008. Sequences involved in mRNA processing in Trypanosoma cruzi. Int J Parasitol 38: 1383-1389.
8. Campos-Salinas J, León-Guerrero D, González-Rey E, Delgado M, Castanys S, Pérez-Victoria JM, Gamarro F 2013. LABCG2, a new ABC transporter implicated in phosphatidylserine exposure is involved in the infectivity and pathogenicity of Leishmania. PLoS Negl Trop Dis 7: e2179.
9. Castanys-Muñoz E, Alder-Baerens N, Pomorski T, Gamarro F, Castanys S 2007. A novel ATP-binding cassette transporter from Leishmania is involved in transport of phosphatidylcholine analogues and resistance to alkyl-phospholipids. Mol Microbiol 64: 1141-1153.
10. Castanys-Muñoz E, Pérez-Victoria JM, Gamarro F, Castanys S 2008. Characterization of an ABCG-like transporter from the protozoan parasite Leishmania with a role in drug resistance and transbilayer lipid movement. Antimicrob Agents Chemother 52: 3573-3579.
11. Clayton C, Shapira M 2007. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101.
12. Clayton CE 2014. Networks of gene expression regulation in Trypanosoma brucei. Mol Biochem Parasitol 195: 96-106.
13. Dallagiovanna B, Gamarro F, Castanys S 1996. Molecular characterization of a P-glycoprotein-related tcpgp2 gene in Trypanosoma cruzi. Mol Biochem Parasitol 75: 145-157.
14. DaRocha WD, Silva RA, Bartholomeu DC, Pires SF, Freitas JM, Macedo AM, Vazquez MP, Levin MJ, Teixeira SMR 2004. Expression of exogenous genes in Trypanosoma cruzi: improving vectors and electroporation protocols. Parasitol Res 92: 113-120.
15. Doyle LA, Yang W, Abruzzo LV, Krogmann T, Gao Y, Rishi AK, Ross DD 1998. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 95: 15665-15670.
16. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou L, Huang Y, Kindlund E, Klingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarleton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
17. Filardi LS, Brener Z 1987. Susceptibility and natural resistance of Trypanosoma cruzi strains to drugs used clinically in Chagas disease. Trans R Soc Trop Med Hyg 81: 755-759.
18. Gordon D, Abajian C, Green P 1998. Consed: a graphical tool for sequence finishing. Genome Res 8: 195-202.
19. Higgins CF 1992. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8: 67-113.
20. Higgins CF 2007. Multiple molecular mechanisms for multidrug resistance transporters. Nature 446: 749-757.
21. Igarashi KF, Aoki H, Mamitsuka K, Kuma M, Kanehisa M 2004. The evolutionary repertoires of the eukaryotic-type ABC transporters in terms of the phylogeny of ATP-binding domains in eukaryotes and prokaryotes. Mol Biol Evol 21: 2149-2160.
22. Klokouzas A, Shahi S, Hladky SB, Barrand MA, van Veen HW 2003. ABC transporters and drug resistance in parasitic protozoa. Int J Antimocrob Agents 22: 301-317.
23. Kondo C, Suzuki H, Itoda M, Ozawa S, Sawada J, Kobayashi D, Ieiri I, Mine K, Ohtsubo K, Sugiyama Y 2004. Functional analysis of SNPs variants of BCRP/ABCG2. Pharm Res 21: 1895-1903.
24. Lai D, Proctor JR, Zhu JYA, Meyer IM 2012. R-chie: a web server and R package for visualizing RNA secondary structures. Nucleic Acids Res 40: e95.
25. Lara FA, Sant’anna C, Lemos D, Laranja GA, Coelho MG, Salles IR, Michel A, Oliveira PL, Cunha-E-Silva N, Salmon D, Paes MC 2007. Heme requirement and intracellular trafficking in Trypanosoma cruzi epimastigotes. Biochem Biophys Res Commun 355: 16-22.
26. Leprohon P, Legare D, Girard I, Papadopoulou B, Ouellette M 2006. Modulation of Leishmania ABC protein gene expression through life stages and among drug-resistant parasites. Eukaryot Cell 5: 1713-1725.
27. Maingon R, Gerke R, Rodriguez M, Urbina J, Hoenicka J, Negri S, Aguirre T, Nehlin J, Knapp T, Crampton J 1988. The tubulin genes of Trypanosoma cruzi. Eur J Biochem 171: 285-291.
28. Miles MA, Llewellyn MS, Lewis MD, Yeo M, Baleela R, Fitzpatrick S, Gaunt MW, Mauricio IL 2009. The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future. Parasitology 136: 1509-1528.
29. Moncayo A, Silveira AC 2009. Current epidemiological trends for Chagas disease in Latin America and future challenges in epidemiology, surveillance and health policy. Mem Inst Oswaldo Cruz 104 (Suppl. I): 17-30.
30. Moreno M, D’ávila DA, Silva MN, Galvão LMC, Macedo AM, Chiari E, Gontijo ED, Zingales B 2010. Trypanosoma cruzi benznidazole susceptibility in vitro does not predict the therapeutic outcome of human Chagas disease. Mem Inst Oswaldo Cruz 105: 918-924.
31. Murta SM, dos Santos WG, Anacleto C, Nirdé P, Moreira ES, Romanha AJ 2001. Drug resistance in Trypanosoma cruzi is not associated with amplification or overexpression of P-glycoprotein (PGP) genes. Mol Biochem Parasitol 117: 223-228.
32. Murta SM, Gazzinelli RT, Brener Z, Romanha AJ 1998. Molecular characterization of susceptible and naturally resistant strains of Trypanosoma cruzi to benznidazole and nifurtimox. Mol Biochem Parasitol 93: 203-214.
33. Rassi Jr A, Rassi A, de Rezende JM 2012. American trypanosomiasis (Chagas disease). Infect Dis Clin N Am 26: 275-291.
34. Reuter JS, Mathews DH 2010. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11: 129.
35. Sauvage V, Aubert D, Escotte-Binet S, Villena I 2009. The role of ATP-binding cassette (ABC) proteins in protozoan parasites. Mol Biochem Parasitol 167: 81-94.
36. Sharom FJ 2008. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 9: 105-127.
37. Siegel TN, Gunasekera K, Cross GAM, Ochsenreiter T 2011. Gene expression in Trypanosoma brucei: lessons from high-throughput RNA sequencing. Trends Parasitol 27: 434-441.
38. Sosa-Estani S, Viotti R, Segura EL 2009. Therapy, diagnosis and prognosis of chronic Chagas disease: insight gained in Argentina. Mem Inst Oswaldo Cruz 104 (Suppl. I): 167-180.
39. Torres C, Barreiro L, Dallagiovanna B, Gamarro F, Castanys S 1999. Characterization of a new ATP-binding cassette transporter in Trypanosoma cruzi associated to a L1Tc retrotransposon. Biochim Biophys Acta 1489: 428-432.
40. Torres C, Pérez-Victoria FJ, Parodi-Talice A, Castanys S, Gamarro F 2004. Characterization of an ABCA-like transporter involved in vesicular trafficking in the protozoan parasite Trypanosoma cruzi. Mol Microbiol 54: 632-646.
41. Urbina JA 2010. Specific chemotherapy of Chagas disease: relevance, current limitations and new approaches. Acta Trop 115: 55-68.
42. Velamakanni S, Wei SL, Janvilisri T, van Veen HW 2007. ABCG transporters: structure, substrate specificities and physiological roles: a brief overview. J Bioenerg Biomembr 239: 465-471.
43. Villarreal D, Barnabé C, Sereno D, Tibayrenc M 2004. Lack of correlation between in vitro susceptibility to benznidazole and phylogenetic diversity of Trypanosoma cruzi, the agent of Chagas disease. Exp Parasitol 108: 24-31.
44. Weatherly DB, Boehlke C, Tarleton RL 2009. Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10: 255.
45. WHO-World Health Organization 2012. Research priorities for Chagas disease, human African trypanosomiasis and leishmaniasis. Available from: Httpapps.who.int/iris/bitstream/10665/77472/1/WHO_TRS_975_eng.pdf.
46. Yanase K, Tsukahara S, Mitsuhashi J, Sugimoto Y 2006. Functional SNPs of the breast cancer resistance protein-therapeutic effects and inhibitor development. Cancer Lett 234: 73-80.
47. Yao Z, Weinberg Z, Ruzzo W 2006. CMfinder-a covariance model based RNA motif finding algorithm. Bioinformatics 22: 445-452.
48. Zingales B, Andrade SG, Briones MRS, Campbell DA, Chiari E, Fernandes O, Guhl F, Lages-Silva E, Macedo AM, Machado CR, Miles MA, Romanha AJ, Sturm NR, Tibayrenc M, Schijman AG 2009. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz 104: 1051-1054.
49. Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM, Teixeira MMG, Schijman AG, Llewelly MS, Lages-Silva E, Machado CR, Andrade SG, Sturm NR 2012. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect Genet Evol 12: 240-253.
50. Zingales B, Miles MA, Moraes CB, Luquetti A, Guhl F, Schijman AG, Ribeiro I 2014. Drug discovery for Chagas disease should consider Trypanosoma cruzi strain diversity. Mem Inst Oswaldo Cruz 109: 828-833.