Gene expression profiling and molecular characterization of antimony resistance in Leishmania amazonensis

PLoS Neglected Tropical Diseases

Volumn 5, Issue 5, 2011, Pages

  do Monte Neto, Rubens L ^a,b   Coelho, Adriano C ^b   Raymond, Frédéric ^b,c   Légaré, Danielle ^b   Corbeil, Jacques ^b,c   Melo, Maria N ^a   Frézard, Frédéric ^a   Ouellette, Marc ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY; MILTEFOSINE; MULTIDRUG RESISTANCE PROTEIN A; PROTOZOAL PROTEIN; THIOL; UNCLASSIFIED DRUG; ANTIPROTOZOAL AGENT;

AMPLICON; ANTIBIOTIC RESISTANCE; ANTIFUNGAL RESISTANCE; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; DRUG RESISTANCE; GENE; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; LEISHMANIA; MOLECULAR MECHANICS; MULTIDRUG RESISTANCE PROTEIN A GENE; NONHUMAN; PHENOTYPE; PROMASTIGOTE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SUPERNUMERARY CHROMOSOME; VALIDATION PROCESS; ANIMAL; DRUG EFFECT; GENETICS; HUMAN; LEISHMANIA MEXICANA; METABOLISM; MICROARRAY ANALYSIS;

ANIMALS; ANTIMONY; ANTIPROTOZOAL AGENTS; DRUG RESISTANCE; GENE EXPRESSION PROFILING; HUMANS; LEISHMANIA MEXICANA; METABOLIC NETWORKS AND PATHWAYS; MICROARRAY ANALYSIS;

EID: 79957990836     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001167     Document Type: Article

References (63)

1. Murray HW, Berman JD, Davies CR, Saravia NG, (2005) Advances in leishmaniasis. Lancet 366: 1561-1577.
2. Marzochi MC, Marzochi KB, (1994) Tegumentary and visceral leishmaniases in Brazil: emerging anthropozoonosis and possibilities for their control. Cad Saude Publica 10 (Suppl 2): 359-375.
3. Sundar S, (2001) Drug resistance in Indian visceral leishmaniasis. Trop Med Int Health 6: 849-854.
4. Sundar S, Thakur BB, Tandon AK, Agrawal NR, Mishra CP, et al. (1994) Clinicoepidemiological study of drug resistance in Indian kala-azar. Bmj 308: 307.
5. Croft SL, Sundar S, Fairlamb AH, (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19: 111-126.
6. Frezard F, Demicheli C, Ferreira CS, Costa MA, (2001) Glutathione-induced conversion of pentavalent antimony to trivalent antimony in meglumine antimoniate. Antimicrob Agents Chemother 45: 913-916.
7. Shaked-Mishan P, Ulrich N, Ephros M, Zilberstein D, (2001) Novel Intracellular SbV reducing activity correlates with antimony susceptibility in Leishmania donovani. J Biol Chem 276: 3971-3976.
8. Zhou Y, Messier N, Ouellette M, Rosen BP, Mukhopadhyay R, (2004) Leishmania major LmACR2 is a pentavalent antimony reductase that confers sensitivity to the drug pentostam. J Biol Chem 279: 37445-37451.
9. Denton H, McGregor JC, Coombs GH, (2004) Reduction of anti-leishmanial pentavalent antimonial drugs by a parasite-specific thiol-dependent reductase, TDR1. Biochem J 381: 405-412.
10. Yan S, Li F, Ding K, Sun H, (2003) Reduction of pentavalent antimony by trypanothione and formation of a binary and ternary complex of antimony(III) and trypanothione. J Biol Inorg Chem 8: 689-697.
11. Ferreira Cdos S, Martins PS, Demicheli C, Brochu C, Ouellette M, et al. (2003) Thiol-induced reduction of antimony(V) into antimony(III): a comparative study with trypanothione, cysteinyl-glycine, cysteine and glutathione. Biometals 16: 441-446.
12. Gourbal B, Sonuc N, Bhattacharjee H, Legare D, Sundar S, et al. (2004) Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. J Biol Chem 279: 31010-31017.
13. Marquis N, Gourbal B, Rosen BP, Mukhopadhyay R, Ouellette M, (2005) Modulation in aquaglyceroporin AQP1 gene transcript levels in drug-resistant Leishmania. Mol Microbiol 57: 1690-1699.
14. Mukhopadhyay R, Dey S, Xu N, Gage D, Lightbody J, et al. (1996) Trypanothione overproduction and resistance to antimonials and arsenicals in Leishmania. Proc Natl Acad Sci U S A 93: 10383-10387.
15. Grondin K, Haimeur A, Mukhopadhyay R, Rosen BP, Ouellette M, (1997) Co-amplification of the gamma-glutamylcysteine synthetase gene gsh1 and of the ABC transporter gene pgpA in arsenite-resistant Leishmania tarentolae. Embo J 16: 3057-3065.
16. Haimeur A, Guimond C, Pilote S, Mukhopadhyay R, Rosen BP, et al. (1999) Elevated levels of polyamines and trypanothione resulting from overexpression of the ornithine decarboxylase gene in arsenite-resistant Leishmania. Mol Microbiol 34: 726-735.
17. Ouellette M, Legare D, Haimeur A, Grondin K, Roy G, et al. (1998) ABC transporters in Leishmania and their role in drug resistance. Drug Resist Updat 1: 43-48.
18. Legare D, Richard D, Mukhopadhyay R, Stierhof YD, Rosen BP, et al. (2001) The Leishmania ATP-binding cassette protein PGPA is an intracellular metal-thiol transporter ATPase. J Biol Chem 276: 26301-26307.
19. Ouellette M, Borst P, (1991) Drug resistance and P-glycoprotein gene amplification in the protozoan parasite Leishmania. Res Microbiol 142: 737-746.
20. Mukherjee A, Padmanabhan PK, Singh S, Roy G, Girard I, et al. (2007) Role of ABC transporter MRPA, gamma-glutamylcysteine synthetase and ornithine decarboxylase in natural antimony-resistant isolates of Leishmania donovani. J Antimicrob Chemother 59: 204-211.
21. Callahan HL, Beverley SM, (1991) Heavy metal resistance: a new role for P-glycoproteins in Leishmania. J Biol Chem 266: 18427-18430.
22. Ouellette M, Fase-Fowler F, Borst P, (1990) The amplified H circle of methotrexate-resistant leishmania tarentolae contains a novel P-glycoprotein gene. Embo J 9: 1027-1033.
23. Callahan HL, Roberts WL, Rainey PM, Beverley SM, (1994) The PGPA gene of Leishmania major mediates antimony (SbIII) resistance by decreasing influx and not by increasing efflux. Mol Biochem Parasitol 68: 145-149.
24. Coelho AC, Beverley SM, Cotrim PC, (2003) Functional genetic identification of PRP1, an ABC transporter superfamily member conferring pentamidine resistance in Leishmania major. Mol Biochem Parasitol 130: 83-90.
25. Gamarro F, Chiquero MJ, Amador MV, Legare D, Ouellette M, et al. (1994) P-glycoprotein overexpression in methotrexate-resistant Leishmania tropica. Biochem Pharmacol 47: 1939-1947.
26. Carter KC, Hutchison S, Henriquez FL, Legare D, Ouellette M, et al. (2006) Resistance of Leishmania donovani to sodium stibogluconate is related to the expression of host and parasite gamma-glutamylcysteine synthetase. Antimicrob Agents Chemother 50: 88-95.
27. Sereno D, Guilvard E, Maquaire S, Cavaleyra M, Holzmuller P, et al. (2001) Experimental studies on the evolution of antimony-resistant phenotype during the in vitro life cycle of Leishmania infantum: implications for the spread of chemoresistance in endemic areas. Acta Trop 80: 195-205.
28. Liarte DB, Murta SM, (2010) Selection and phenotype characterization of potassium antimony tartrate-resistant populations of four New World Leishmania species. Parasitol Res 107: 205-212.
29. Zauli-Nascimento RC, Miguel DC, Yokoyama-Yasunaka JK, Pereira LI, Pelli de Oliveira MA, et al. (2010) In vitro sensitivity of Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis Brazilian isolates to meglumine antimoniate and amphotericin B. Trop Med Int Health 15: 68-76.
30. Dias FC, Ruiz JC, Lopes WC, Squina FM, Renzi A, et al. (2007) Organization of H locus conserved repeats in Leishmania (Viannia) braziliensis correlates with lack of gene amplification and drug resistance. Parasitol Res 101: 667-676.
31. Ubeda JM, Legare D, Raymond F, Ouameur AA, Boisvert S, et al. (2008) Modulation of gene expression in drug resistant Leishmania is associated with gene amplification, gene deletion and chromosome aneuploidy. Genome Biol 9: R115.
32. Leprohon P, Legare D, Raymond F, Madore E, Hardiman G, et al. (2009) Gene expression modulation is associated with gene amplification, supernumerary chromosomes and chromosome loss in antimony-resistant Leishmania infantum. Nucleic Acids Res 37: 1387-1399.
33. de Oliveira JP, Fernandes F, Cruz AK, Trombela V, Monteiro E, et al. (2007) Genetic diversity of Leishmania amazonensis strains isolated in northeastern Brazil as revealed by DNA sequencing, PCR-based analyses and molecular karyotyping. Kinetoplastid Biol Dis 6: 5.
34. Dey S, Papadopoulou B, Haimeur A, Roy G, Grondin K, et al. (1994) High level arsenite resistance in Leishmania tarentolae is mediated by an active extrusion system. Mol Biochem Parasitol 67: 49-57.
35. Rochette A, Raymond F, Ubeda JM, Smith M, Messier N, et al. (2008) Genome-wide gene expression profiling analysis of Leishmania major and Leishmania infantum developmental stages reveals substantial differences between the two species. BMC Genomics 9: 255.
36. Smyth GK, Speed T, (2003) Normalization of cDNA microarray data. Methods 31: 265-273.
37. Smyth GK, Michaud J, Scott HS, (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075.
38. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
39. Fairlamb AH, Henderson GB, Bacchi CJ, Cerami A, (1987) In vivo effects of difluoromethylornithine on trypanothione and polyamine levels in bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 24: 185-191.
40. El Fadili K, Messier N, Leprohon P, Roy G, Guimond C, et al. (2005) Role of the ABC transporter MRPA (PGPA) in antimony resistance in Leishmania infantum axenic and intracellular amastigotes. Antimicrob Agents Chemother 49: 1988-1993.
41. 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.
42. Ouellette M, Drummelsmith J, Papadopoulou B, (2004) Leishmaniasis: drugs in the clinic, resistance and new developments. Drug Resist Updat 7: 257-266.
43. Beverley SM, (1991) Gene amplification in Leishmania. Annu Rev Microbiol 45: 417-444.
44. Ouellette M, Hettema E, Wust D, Fase-Fowler F, Borst P, (1991) Direct and inverted DNA repeats associated with P-glycoprotein gene amplification in drug resistant Leishmania. Embo J 10: 1009-1016.
45. Decuypere S, Rijal S, Yardley V, De Doncker S, Laurent T, et al. (2005) Gene expression analysis of the mechanism of natural Sb(V) resistance in Leishmania donovani isolates from Nepal. Antimicrob Agents Chemother 49: 4616-4621.
46. Lira R, Sundar S, Makharia A, Kenney R, Gam A, et al. (1999) Evidence that the high incidence of treatment failures in Indian kala-azar is due to the emergence of antimony-resistant strains of Leishmania donovani. J Infect Dis 180: 564-567.
47. Hadighi R, Mohebali M, Boucher P, Hajjaran H, Khamesipour A, et al. (2006) Unresponsiveness to Glucantime treatment in Iranian cutaneous leishmaniasis due to drug-resistant Leishmania tropica parasites. PLoS Med 3: e162.
48. Rojas R, Valderrama L, Valderrama M, Varona MX, Ouellette M, et al. (2006) Resistance to antimony and treatment failure in human Leishmania (Viannia) infection. J Infect Dis 193: 1375-1383.
49. Yardley V, Ortuno N, Llanos-Cuentas A, Chappuis F, Doncker SD, et al. (2006) American tegumentary leishmaniasis: Is antimonial treatment outcome related to parasite drug susceptibility? J Infect Dis 194: 1168-1175.
50. Guimond C, Trudel N, Brochu C, Marquis N, El Fadili A, et al. (2003) Modulation of gene expression in Leishmania drug resistant mutants as determined by targeted DNA microarrays. Nucleic Acids Res 31: 5886-5896.
51. Machuca C, Rodriguez A, Herrera M, Silva S, Ponte-Sucre A, (2006) Leishmania amazonensis: metabolic adaptations induced by resistance to an ABC transporter blocker. Exp Parasitol 114: 1-9.
52. Haile S, Papadopoulou B, (2007) Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr Opin Microbiol 10: 569-577.
53. Clayton C, Shapira M, (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101.
54. Lye LF, Owens K, Shi H, Murta SM, Vieira AC, et al. (2010) Retention and loss of RNA interference pathways in trypanosomatid protozoans. PLoS Pathog 6: e1001161.
55. Anacleto C, Abdo MC, Ferreira AV, Murta SM, Romanha AJ, et al. (2003) Structural and functional analysis of an amplification containing a PGPA gene in a glucantime-resistant Leishmania (Viannia) guyanensis cell line. Parasitol Res 90: 110-118.
56. Detke S, Katakura K, Chang KP, (1989) DNA amplification in arsenite-resistant Leishmania. Exp Cell Res 180: 161-170.
57. Liu X, Chang KP, (1992) The 63-kilobase circular amplicon of tunicamycin-resistant Leishmania amazonensis contains a functional N-acetylglucosamine-1-phosphate transferase gene that can be used as a dominant selectable marker in transfection. Mol Cell Biol 12: 4112-4122.
58. Legare D, Papadopoulou B, Roy G, Mukhopadhyay R, Haimeur A, et al. (1997) Efflux systems and increased trypanothione levels in arsenite-resistant Leishmania. Exp Parasitol 87: 275-282.
59. Moreira ES, Anacleto C, Petrillo-Peixoto ML, (1998) Effect of glucantime on field and patient isolates of New World Leishmania: use of growth parameters of promastigotes to assess antimony susceptibility. Parasitol Res 84: 720-726.
60. Grondin K, Roy G, Ouellette M, (1996) Formation of extrachromosomal circular amplicons with direct or inverted duplications in drug-resistant Leishmania tarentolae. Mol Cell Biol 16: 3587-3595.
61. Mittal MK, Rai S, Ashutosh, Ravinder, Gupta S, et al. (2007) Characterization of natural antimony resistance in Leishmania donovani isolates. Am J Trop Med Hyg 76: 681-688.
62. Mandal S, Maharjan M, Singh S, Chatterjee M, Madhubala R, (2010) Assessing aquaglyceroporin gene status and expression profile in antimony-susceptible and-resistant clinical isolates of Leishmania donovani from India. J Antimicrob Chemother 65: 496-507.
63. Mandal G, Wyllie S, Singh N, Sundar S, Fairlamb AH, et al. (2007) Increased levels of thiols protect antimony unresponsive Leishmania donovani field isolates against reactive oxygen species generated by trivalent antimony. Parasitology 134: 1679-1687.