Antimony resistance in Leishmania, focusing on experimental research

Journal of Tropical Medicine

Volumn , Issue , 2011, Pages

  Jeddi, Fakhri ^a   Piarroux, Renaud ^a   Mary, Charles ^a  

^a TIMONE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY DERIVATIVE; CHLOROCRESOL; GLYCOPROTEIN P; MEGLUMINE ANTIMONATE; METHOTREXATE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN A; ORNITHINE DECARBOXYLASE; OXIDOREDUCTASE; PROTOZOAL DNA; PROTOZOAL PROTEIN; PROTOZOAL RNA; STIBOGLUCONATE SODIUM; THIOL DEPENDENT REDUCTASE 1; TRYPANOTHIONE REDUCTASE; UNCLASSIFIED DRUG;

AMASTIGOTE; ANTIBIOTIC RESISTANCE; ANTIPROTOZOAL RESISTANCE; APOPTOSIS; CHROMOSOME; CLONING; CULTURE MEDIUM; CULTURE TECHNIQUE; DISEASE MODEL; DNA POLYMORPHISM; FLOW CYTOMETRY; GENE AMPLIFICATION; GENE DELETION; GENE OVEREXPRESSION; GENETIC RESISTANCE; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IC 50; IMMUNOBLOTTING; IN VITRO STUDY; INJECTION COUPLED MASS SPECTROMETRY; LEISHMANIA; LEISHMANIA DONOVANI; LEISHMANIA INFANTUM; LEISHMANIA MAJOR; LEISHMANIA TARENTOLAE; LEISHMANIASIS; MACROPHAGE; MASS SPECTROMETRY; MUTANT; NONHUMAN; PARASITE ISOLATION; PRIORITY JOURNAL; PROMASTIGOTE; PULSED FIELD GEL ELECTROPHORESIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW;

EID: 84855601851     PISSN: 16879686     EISSN: 16879694     Source Type: Journal    
DOI: 10.1155/2011/695382     Document Type: Review

References (124)

1. World Health Organization, Control of the leishmaniases World Health Organization Technical Report Series 2010 949 1 186
2. Palatnik-de-Sousa C. B., Vaccines for leishmaniasis in the fore coming 25 years Vaccine 2008 26 14 1709 1724
3. Desjeux P., The increase in risk factors for leishmaniasis worldwide Transactions of the Royal Society of Tropical Medicine and Hygiene 2001 95 3 239 243 (Pubitemid 33713068)
4. Chappuis F., Sundar S., Hailu A., Ghalib H., Rijal S., Peeling R. W., Alvar J., Boelaert M., Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nature Reviews Microbiology 2007 5 11 873 882 (Pubitemid 47578388)
5. Hadighi R., Mohebali M., Boucher P., Hajjaran H., Khamesipour A., Ouellette M., Unresponsiveness to glucantime treatment in Iranian cutaneous Leishmaniasis due to drug-resistant Leishmania tropica parasites Plos Medicine 2006 3 5 e162
6. Lira R., Sundar S., Makharia A., Kenney R., Gam A., Saraiva E., Sacks D., Evidence that the high incidence of treatment failures in Indian kala-azar is due to the emergence of antimony-resistant strains of Leishmania donovani Journal of Infectious Diseases 1999 180 2 564 567 (Pubitemid 30256350)
7. Sundar S., More D. K., Singh M. K., Singh V. P., Sharma S., Makharia A., Kumar P. C. K., Murray H. W., Failure of pentavalent antimony in visceral leishmaniasis in India: report from the center of the Indian epidemic Clinical Infectious Diseases 2000 31 4 1104 1107 (Pubitemid 32299375)
8. Abdo M. G., Elamin W. M., Khalil E. A., Mukhtar M. M., Antimony-resistant Leishmania donovani in eastern Sudan: incidence and In vitro correlation Eastern Mediterranean Health Journal 2003 9 4 837 843 (Pubitemid 40485321)
9. Faraut-Gambarelli F., Piarroux R., Deniau M., Giusiano B., Marty P., Michel G., Faugre B., Dumon H., In vitro and in vivo resistance of Leishmania infantum to meglumine antimoniate: a study of 37 strains collected from patients with visceral leishmaniasis Antimicrobial Agents and Chemotherapy 1997 41 4 827 830 (Pubitemid 27150540)
10. Gramiccia M., Gradoni L., Orsini S., Decreased sensitivity to meglumine antimoniate (Glucantime) of Leishmania infantum isolated from dogs after several courses of drug treatment Annals of Tropical Medicine and Parasitology 1992 86 6 613 620 (Pubitemid 23090621)
11. Gradoni L., Soteriadou K., Louzir H., Dakkak A., Toz S. O., Jaffe C., Dedet J. P., Campino L., Caavate C., Dujardin J. C., Drug regimens for visceral leishmaniasis in Mediterranean countries Tropical Medicine and International Health 2008 13 10 1272 1276
12. Petrela R., Kuneshka L., Foto E., Zavalani F., Gradoni L., Pediatric visceral leishmaniasis in Albania: a retrospective analysis of 1,210 consecutive hospitalized patients (19952009) Plos Neglected Tropical Diseases 2010 4 9, article e814
13. Grogl M., Thomason T. N., Franke E. D., Drug resistance in leishmaniasis: its implication in systemic chemotherapy of cutaneous and mucocutaneous disease American Journal of Tropical Medicine and Hygiene 1992 47 1 117 126
14. Carri J., Riera C., Gllego M., Ports M., In vitro activity of pentavalent antimony derivatives on promastigotes and intracellular amastigotes of Leishmania infantum strains from humans and dogs in Spain Acta Tropica 2001 79 2 179 183 (Pubitemid 32441789)
15. Haimeur A., Ouellette M., Gene amplification in Leishmania tarentolae selected for resistance to sodium stibogluconate Antimicrobial Agents and Chemotherapy 1998 42 7 1689 1694 (Pubitemid 28311563)
16. Ouellette M., Haimeur A., Grondin K., Légaré D., Papadopoulou B., Amplification of ABC transporter gene pgpA and of other heavy metal resistance genes in Leishmania tarentolae and their study by gene transfection and gene disruption Methods in Enzymology 1998 292 182 193 (Pubitemid 29343887)
17. Grondin K., Haimeur A., Mukhopadhyay R., Rosen B. P., Ouellette M., Co-amplification of the -glutamylcysteine synthetase gene gsh1 and of the ABC transporter gene pgpA in arsenite-resistant Leishmania tarentolae Embo Journal 1997 16 11 3057 3065 (Pubitemid 27234945)
18. Papadopoulou B., Roy G., Dey S., Rosen B. P., Olivier M., Ouellette M., Gene disruption of the p-glycoprotein related gene pgpA of leishmania tarentolae Biochemical and Biophysical Research Communications 1996 224 3 772 778 (Pubitemid 26278660)
19. Grondin K., Roy G., Ouellette M., Formation of extrachromosomal circular amplicons with direct or inverted duplications in drug-resistant Leishmania tarentolae Molecular and Cellular Biology 1996 16 7 3587 3595 (Pubitemid 26199878)
20. Dey S., Papadopoulou B., Haimeur A., Roy G., Grondin K., Dou D., Rosen B. P., Ouellette M., High level arsenite resistance in Leishmania tarentolae is mediated by an active extrusion system Molecular and Biochemical Parasitology 1994 67 1 49 57 (Pubitemid 24287310)
21. El Fadili K., Messier N., Leprohon P., Roy G., Guimond C., Trudel N., Saravia N. G., Papadopoulou B., Légaré D., Ouellette M., Role of the ABC transporter MRPA (PGPA) in antimony resistance in Leishmania infantum axenic and intracellular amastigotes Antimicrobial Agents and Chemotherapy 2005 49 5 1988 1993 (Pubitemid 40631616)
22. Roberts W. L., Berman J. D., Rainey P. M., In vitro antileishmanial properties of triand pentavalent antimonial preparations Antimicrobial Agents and Chemotherapy 1995 39 6 1234 1239
23. Roberts W. L., Rainey P. M., Antileishmanial activity of sodium stibogluconate fractions Antimicrobial Agents and Chemotherapy 1993 37 9 1842 1846 (Pubitemid 23265539)
24. Ephros M., Waldman E., Zilberstein D., Pentostam induces resistance to antimony and the preservative chlorocresol in Leishmania donovani promastigotes and axenically grown amastigotes Antimicrobial Agents and Chemotherapy 1997 41 5 1064 1068 (Pubitemid 27194186)
25. Ephros M., Bitnun A., Shaked P., Waldman E., Zilberstein D., Stage-specific activity of pentavalent antimony against Leishmania donovani axenic amastigotes Antimicrobial Agents and Chemotherapy 1999 43 2 278 282 (Pubitemid 29079158)
26. Ariyanayagam M. R., Fairlamb A. H., Ovothiol and trypanothione as antioxidants in trypanosomatids Molecular and Biochemical Parasitology 2001 115 2 189 198 (Pubitemid 32566228)
27. Carri J., Ports M., In vitro susceptibility to pentavalent antimony in Leishmania infantum strains is not modified during In vitro or in vivo passages but is modified after host treatment with meglumine antimoniate BMC Pharmacology 2002 2 2 11
28. Carri J., De Colmenares M., Riera C., Gllego M., Arboix M., Ports M., Leishmania infantum stage-specific activity of pentavalent antimony related with the assay conditions Experimental Parasitology 2000 95 3 209 214
29. Grogl M., Oduola A. M. J., Cordero L. D. C., Kyle D. E., Leishmania spp.: development of pentostam-resistant clones In vitro by discontinuous drug exposure Experimental Parasitology 1989 69 1 78 90 (Pubitemid 19187902)
30. Garin Y. J. F., Sulahian A., Pratlong F., Meneceur P., Gangneux J. P., Prina E., Dedet J. P., Derouin F., Virulence of Leishmania infantum is expressed as a clonal and dominant phenotype in experimental infections Infection and Immunity 2001 69 12 7365 7373 (Pubitemid 33086560)
31. Dube A., Singh N., Sundar S., Singh N., Refractoriness to the treatment of sodium stibogluconate in Indian kala-azar field isolates persist in in vitro and in vivo experimental models Parasitology Research 2005 96 4 216 223 (Pubitemid 40933669)
32. Légaré D., Richard D., Mukhopadhyay R., Stierhof Y. D., Rosen B. P., Haimeur A., Papadopoulou B., Ouellette M., The Leishmania ATP-binding cassette protein PGPA is an intracellular metal-thiol transporter ATPase Journal of Biological Chemistry 2001 276 28 26301 26307
33. Mukhopadhyay R., Dey S., Xu N., Gage D., Lightbody J., Ouellette M., Rosen B. P., Trypanothione overproduction and resistance to antimonials and arsenicals in Leishmania Proceedings of the National Academy of Sciences of the United States of America 1996 93 19 10383 10387 (Pubitemid 26314631)
34. Mehta A., Shaha C., Mechanism of metalloid-induced death in Leishmania spp. role of iron, reactive oxygen species, Ca2+, and glutathione Free Radical Biology and Medicine 2006 40 10 1857 1868
35. Sereno D., Cavaleyra M., Zemzoumi K., Maquaire S., Ouaissi A., Lemesre J. L., Axenically grown amastigotes of Leishmania infantum used as an in vitro model to investigate the pentavalent antimony mode of action Antimicrobial Agents and Chemotherapy 1998 42 12 3097 3102 (Pubitemid 28553724)
36. Borst P., Ouellette M., New mechanisms of drug resistance in parasitic protozoa Annual Review of Microbiology 1995 49 427 460
37. Goyeneche-Patino D. A., Valderrama L., Walker J., Saravia N. G., Antimony resistance and trypanothione in experimentally selected and clinical strains of Leishmania panamensis Antimicrobial Agents and Chemotherapy 2008 52 12 4503 4506
38. Launois P., Conceiao-Silva F., Himmerlich H., Parra-Lopez C., Tacchini-Cottier F., Louis J. A., Setting in motion the immune mechanisms underlying genetically determined resistance and susceptibility to infection with Leishmania major Parasite Immunology 1998 20 5 223 230 (Pubitemid 28255395)
39. Carter K. C., Sundar S., Spickett C., Pereira O. C., Mullen A. B., The in vivo susceptibility of Leishmania donovani to sodium stibogluconate is drug specific and can be reversed by inhibiting glutathione biosynthesis Antimicrobial Agents and Chemotherapy 2003 47 5 1529 1535 (Pubitemid 36548533)
40. Croft S. L., Monitoring drug resistance in leishmaniasis Tropical Medicine and International Health 2001 6 11 899 905 (Pubitemid 33010876)
41. Seifert K., Escobar P., Croft S. L., In vitro activity of anti-leishmanial drugs against Leishmania donovani is host cell dependent Journal of Antimicrobial Chemotherapy 2010 65 3 508 511
42. Gupta N., Goyal N., Rastogi A. K., In vitro cultivation and characterization of axenic amastigotes of Leishmania Trends in Parasitology 2001 17 3 150 153 (Pubitemid 32422185)
43. Vermeersch M., Da Luz R. I., Toté K., Timmermans J. P., Cos P., Maes L., In vitro susceptibilities of Leishmania donovani promastigote and amastigote stages to antileishmanial reference drugs: practical relevance of stage-specific differences Antimicrobial Agents and Chemotherapy 2009 53 9 3855 3859
44. Pan A. A., Duboise S. M., Eperon S., Rivas L., Hodgkinson V., Traub-Cseko Y., McMahon-Pratt D., Developmental life cycle of Leishmania cultivation and characterization of cultured extracellular amastigotes The Journal of Eukaryotic Microbiology 1993 40 2 213 223
45. Mittal M. K., Rai S., Ashutosh, Ravinder, Gupta S., Sundar S., Goyal N., Characterization of natural antimony resistance in Leishmania donovani isolates American Journal of Tropical Medicine and Hygiene 2007 76 4 681 688 (Pubitemid 351627707)
46. Thakur C. P., Thakur S., Narayan S., Sinha A., Comparison of treament regimens of kala-azar based on culture and sensitivity amastigotes to sodium antimony gluconate Indian Journal of Medical Research 2008 127 6 582 588
47. Rijal S., Yardley V., Chappuis F., Decuypere S., Khanal B., Singh R., Boelaert M., De Doncker S., Croft S., Dujardin J. C., Antimonial treatment of visceral leishmaniasis: are current in vitro susceptibility assays adequate for prognosis of in vivo therapy outcome? Microbes and Infection 2007 9 4 529 535 (Pubitemid 46442794)
48. Rojas R., Valderrama L., Valderrama M., Varona M. X., Ouellette M., Saravia N., Resistance to antimony and treatment failure in human Leishmania (Viannia) infection Journal of Infectious Diseases 2006 193 10 1375 1383 (Pubitemid 43673385)
49. Coderre J. A., Beverley S. M., Schimke R. T., Santi D. V., Overproduction of a bifunctional thymidylate synthetase-dihydrofolate reductase and DNA amplification in methotrexate-resistant Leishmania tropica Proceedings of the National Academy of Sciences of the United States of America 1983 80 8 I 2132 2136 (Pubitemid 13097149)
50. Ellenberger T. E., Beverley S. M., Multiple drug resistance and conservative amplification of the H region in Leishmania major Journal of Biological Chemistry 1989 264 25 15094 15103 (Pubitemid 19237343)
51. Katakura K., Chang K. P., H DNA amplification in Leishmania resistant to both arsenite and methotrexate Molecular and Biochemical Parasitology 1989 34 2 189 191 (Pubitemid 19098383)
52. White T. C., Fase-Fowler F., van Luenen H., Calafat J., Borst P., The H circles of Leishmania tarentolae are a unique amplifiable system of oligomeric DNAs associated with drug resistance Journal of Biological Chemistry 1988 263 32 16977 16983 (Pubitemid 18268882)
53. Ouellette M., Hettema E., Wst D., Fase-Fowler F., Borst P., Direct and inverted DNA repeats associated with P-glycoprotein gene amplification in drug resistant Leishmania Embo Journal 1991 10 4 1009 1016 (Pubitemid 21905560)
54. Marchini J. F., Cruz A. K., Beverley S. M., Tosi L. R., The H region HTBF gene mediates terbinafine resistance in Leishmania major Molecular and Biochemical Parasitology 2003 131 1 77 81 (Pubitemid 37101181)
55. Callahan H. L., Beverley S. M., A member of the aldoketo reductase family confers methotrexate resistance in Leishmania Journal of Biological Chemistry 1992 267 34 24165 24168
56. Mary C., Faraut F., Deniau M., Dereure J., Aoun K., Ranque S., Piarroux R., Frequency of drug resistance gene amplification in clinical Leishmania strains International Journal of Microbiology 2010 2010 8
57. Mukherjee A., Padmanabhan P. K., Singh S., Role of ABC transporter MRPA, -glutamylcysteine synthetase and ornithine decarboxylase in natural antimony-resistant isolates of Leishmania donovani Journal of Antimicrobial Chemotherapy 2007 59 204 211 (Pubitemid 47072058)
58. Singh N., Singh R. T., Sundar S., Novel mechanism of drug resistance in kala azar field isolates Journal of Infectious Diseases 2003 188 4 600 607 (Pubitemid 37011815)
59. Leprohon P., Légaré D., Girard I., Papadopoulou B., Ouellette M., Modulation of Leishmania ABC protein gene expression through life stages and among drug-resistant parasites Eukaryotic Cell 2006 5 10 1713 1725 (Pubitemid 44641711)
60. Leprohon P., Légaré D., Raymond F., Madore.., Hardiman G., Corbeil J., Ouellette M., Gene expression modulation is associated with gene amplification, supernumerary chromosomes and chromosome loss in antimony-resistant Leishmania infantum Nucleic Acids Research 2009 37 5 1387 1399
61. Gourbal B., Sonuc N., Bhattacharjee H., Legare D., Sundar S., Ouellette M., Rosen B. P., Mukhopadhyay R., Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin Journal of Biological Chemistry 2004 279 30 31010 31017 (Pubitemid 39037760)
62. Marquis N., Gourbal B., Rosen B. P., Mukhopadhyay R., Ouellette M., Modulation in aquaglyceroporin AQP1 gene transcript levels in drug-resistant Leishmania Molecular Microbiology 2005 57 6 1690 1699 (Pubitemid 41337396)
63. Zhou Y., Messier N., Ouellette M., Rosen B. P., Mukhopadhyay R., Leishmania major LmACR2 is a pentavalent antimony reductase that confers sensitivity to the drug Pentostam Journal of Biological Chemistry 2004 279 36 37445 37451 (Pubitemid 39195454)
64. Leprohon P., Légaré D., Ouellette M., Intracellular localization of the ABCC proteins of Leishmania and their role in resistance to antimonials Antimicrobial Agents and Chemotherapy 2009 53 6 2646 2649
65. Kumar A., Boggula V. R., Sundar S., Shasany A. K., Dube A., Identification of genetic markers in Sodium Antimony Gluconate (SAG) sensitive and resistant Indian clinical isolates of Leishmania donovani through amplified fragment length polymorphism (AFLP) Acta Tropica 2009 110 1 80 85
66. Vergnes B., Gourbal B., Girard I., Sundar S., Drummelsmith J., Ouellette M., A proteomics screen implicates HSP83 and a small kinetoplastid calpain-related protein in drug resistance in Leishmania donovani clinical field isolates by modulating drug-induced programmed cell death Molecular and Cellular Proteomics 2007 6 1 88 101 (Pubitemid 46152694)
67. Brochu C., Wang J., Roy G., Messier N., Wang X. Y., Saravia N. G., Ouellette M., Antimony uptake systems in the protozoan parasite Leishmania and accumulation differences in antimony-resistant parasites Antimicrobial Agents and Chemotherapy 2003 47 10 3073 3079 (Pubitemid 37229559)
68. Shaked-Mishant P., Ulrich N., Ephros M., Zilberstein D., Novel intracellular Sbv reducing activity correlates with antimony susceptibility in Leishmania donovani Journal of Biological Chemistry 2001 276 6 3971 3976
69. Decuypere S., Rijal S., Yardley V., De Doncker S., Laurent T., Khanal B., Chappuis F., Dujardin J. C., Gene expression analysis of the mechanism of natural Sb(V) resistance in Leishmania donovani isolates from Nepal Antimicrobial Agents and Chemotherapy 2005 49 11 4616 4621 (Pubitemid 41552591)
70. Mukhopadhyay R., Mandal G., Atluri V. S., Figarella K., Uzcategui N. L., Zhou Y., Beitz E., Ajees A. A., Bhattacharjee H., The role of alanine 163 in solute permeability of Leishmania major aquaglyceroporin LmAQP1 Molecular and Biochemical Parasitology 2011 175 1 83 90
71. Uzcategui N. L., Zhou Y., Figarella K., Ye J., Mukhopadhyay R., Bhattacharjee H., Alteration in glycerol and metalloid permeability by a single mutation in the extracellular C-loop of Leishmania major aquaglyceroporin LmAQP1 Molecular Microbiology 2008 70 6 1477 1486
72. Mandal S., Maharjan M., Singh S., Chatterjee M., Madhubala R., Assessing aquaglyceroporin gene status and expression profile in antimony-susceptible andresistant clinical isolates of Leishmania donovani from India Journal of Antimicrobial Chemotherapy 2010 65 3 496 507
73. Goodwin L. G., Pentostam (sodium stibogluconate); a 50-year personal reminiscence Transactions of the Royal Society of Tropical Medicine and Hygiene 1995 89 3 339 341
74. Mottram J. C., Coombs G. H., Leishmania mexicana enzyme activities of amastigotes and promastigotes and their inhibition by antimonials and arsenicals Experimental Parasitology 1985 59 2 151 160 (Pubitemid 15110104)
75. Sereno D., Lemesre J. L., Axenically cultured amastigote forms as an In vitro model for investigation of antileishmanial agents Antimicrobial Agents and Chemotherapy 1997 41 5 972 976 (Pubitemid 27194170)
76. Frézard F., Demicheli C., Ferreira C. S., Costa M. A., Glutathione-induced conversion of pentavalent antimony to trivalent antimony in meglumine antimoniate Antimicrobial Agents and Chemotherapy 2001 45 3 913 916 (Pubitemid 32182044)
77. dos Santos Ferreira C., Silveira Martins P., Demicheli C., Brochu C., Ouellette M., Frézard F., Thiol-induced reduction of antimony(V) into antimony(III): a comparative study with trypanothione, cysteinyl-glycine, cysteine and glutathione BioMetals 2003 16 3 441 446 (Pubitemid 36356775)
78. Hansen C., Hansen E. W., Hansen H. R., Reduction of Sb(V) in a human macrophage cell line measured by HPLC-ICP-MS. Biological Trace Element Research. In press
79. Denton H., McGregor J. C., Coombs G. H., Reduction of anti-leishmanial pentavalent antimonial drugs by a parasite-specific thiol-dependent reductase, TDR1 Biochemical Journal 2004 381 2 405 412 (Pubitemid 38969684)
80. Fairlamb A. H., Cerami A., Metabolism and functions of trypanothione in the kinetoplastida Annual Review of Microbiology 1992 46 695 729
81. Cunningham M. L., Zvelebil M. J., Fairlamb A. H., Mechanism of inhibition of trypanothione reductase and glutathione reductase by trivalent organic arsenicals European Journal of Biochemistry 1994 221 1 285 295 (Pubitemid 24120573)
82. Wyllie S., Fairlamb A. H., Differential toxicity of antimonial compounds and their effects on glutathione homeostasis in a human leukaemia monocyte cell line Biochemical Pharmacology 2006 71 3 257 267 (Pubitemid 41817286)
83. Guimond C., Trudel N., Brochu C., Marquis N., El Fadili A., Peytavi R., Briand G., Richard D., Messier N., Papadopoulou B., Corbeil J., Bergeron M. G., Légaré D., Ouellette M., Modulation of gene expression in Leishmania drug resistant mutants as determined by targeted DNA microarrays Nucleic Acids Research 2003 31 20 5886 5896 (Pubitemid 37442315)
84. Mandal G., Wyllie S., Singh N., Sundar S., Fairlamb A. H., Chatterjee M., Increased levels of thiols protect antimony unresponsive Leishmania donovani field isolates against reactive oxygen species generated by trivalent antimony Parasitology 2007 134 12 1679 1687 (Pubitemid 47530771)
85. Haimeur A., Guimond C., Pilote S., Mukhopadhyay R., Rosen B. P., Poulin R., Ouellette M., Elevated levels of polyamines and trypanothione resulting from overexpression of the ornithine decarboxylase gene in arsenite-resistant Leishmania Molecular Microbiology 1999 34 4 726 735
86. Adaui V., Schnorbusch K., Zimic M., Gutirrez A., Decuypere S., Vanaerschot M., De Doncker S., Maes I., Llanos-Cuentas A., Chappuis F., Arvalo J., Dujardin J. -C., Comparison of gene expression patterns among Leishmania braziliensis clinical isolates showing a different in vitro susceptibility to pentavalent antimony Parasitology 2011 138 2 183 193
87. Carter K. C., Hutchison S., Henriquez F. L., Légaré D., Ouellette M., Roberts C. W., Mullen A. B., Resistance of Leishmania donovani to sodium stibogluconate is related to the expression of host and parasite -glutamylcysteine synthetase Antimicrobial Agents and Chemotherapy 2006 50 1 88 95 (Pubitemid 43042907)
88. Légaré D., Hettema E., Ouellette M., The P-glycoprotein-related gene family in Leishmania Molecular and Biochemical Parasitology 1994 68 1 81 91 (Pubitemid 24358619)
89. Henderson D. M., Sifri C. D., Rodgers M., Wirth D. F., Hendrickson N., Ullman B., Multidrug resistance in Leishmania donovani is conferred by amplification of a gene homologous to the mammalian mdr1 gene Molecular and Cellular Biology 1992 12 6 2855 2865
90. Chow L. M., Wong A. K., Ullman B., Wirth D. F., Cloning and functional analysis of an extrachromosomally amplified multidrug resistance-like gene in Leishmania enriettii Molecular and Biochemical Parasitology 1993 60 2 195 208
91. Gueiros-Filho F. J., Viola J. P., Gomes F. C., Leishmania amazonensis: multidrug resistance in vinblastine-resistant promastigotes is associated with rhodamine 123 efflux, DNA amplification, and RNA overexpression of a Leishmania mdr1 gene Experimental Parasitology 1995 81 4 480 490
92. Chiquero M. J., Perez-Victoria J. M., O'Valle F., Gonzalez-Ros J. M., Del Moral R. G., Ferragut J. A., Castanys S., Gamarro F., Altered drug membrane permeability in a multidrug-resistant Leishmania tropica line Biochemical Pharmacology 1998 55 2 131 139 (Pubitemid 28006179)
93. Quellette M., Fase-Fowler F., Borst P., The amplified H circle of methotrexate-resistant Leishmania tarentolae contains a novel P-glycoprotein gene Embo Journal 1990 9 4 1027 1033
94. Haimeur A., Brochu C., Genest P., Papadopoulou B., Ouellette M., Amplification of the ABC transporter gene PGPA and increased trypanothione levels in potassium antimonyl tartrate (SbIII) resistant Leishmania tarentolae Molecular and Biochemical Parasitology 2000 108 1 131 135 (Pubitemid 30236323)
95. Légaré D., Papadopoulou B., Roy G., Mukhopadhyay R., Haimeur A., Dey S., Grondin K., Brochu C., Rosen B. P., Ouellette M., Efflux systems and increased trypanothione levels in arsenite-resistant Leishmania Experimental Parasitology 1997 87 3 275 282 (Pubitemid 27494332)
96. Dias F. C., Ruiz J. C., Lopes W. C., Squina F. M., Renzi A., Cruz A. K., Tosi L. R. O., Organization of H locus conserved repeats in Leishmania (Viannia) braziliensis correlates with lack of gene amplification and drug resistance Parasitology Research 2007 101 3 667 676 (Pubitemid 47101426)
97. Callahan H. L., Beverley S. M., Heavy metal resistance: a new role for P-glycoproteins in Leishmania Journal of Biological Chemistry 1991 266 28 18427 18430 (Pubitemid 21908099)
98. Papadopoulou B., Roy G., Dey S., Rosen B. P., Ouellette M., Contribution of the Leishmania P-glycoprotein-related gene ltpgpA to oxyanion resistance Journal of Biological Chemistry 1994 269 16 11980 11986 (Pubitemid 24196691)
99. Callahan H. L., Roberts W. L., Rainey P. M., Beverley S. M., The PGPA gene of Leishmania major mediates antimony (SbIII) resistance by decreasing influx and not by increasing efflux Molecular and Biochemical Parasitology 1994 68 1 145 149 (Pubitemid 24358624)
100. Dey S., Ouellette M., Lightbody J., Papadopoulou B., Rosen B. P., An ATP-dependent as(III)-glutathione transport system in membrane vesicles of Leishmania tarentolae Proceedings of the National Academy of Sciences of the United States of America 1996 93 5 2192 2197 (Pubitemid 26079904)
101. Mandal G., Sarkar A., Saha P., Singh N., Sundar S., Chatterjee M., Functionality of drug efflux pumps in antimonial resistant Leishmania donovani field isolates Indian Journal of Biochemistry and Biophysics 2009 46 1 86 92
102. Dzamitika S. A., Falco C. A., de Oliveira F. B., Marbeuf C., Garnier-Suillerot A., Demicheli C., Rossi-Bergmann B., Frézard F., Role of residual Sb(III) in meglumine antimoniate cytotoxicity and MRP1-mediated resistance Chemico-Biological Interactions 2006 160 3 217 224
103. Torres C., Perez-Victoria F. J., Parodi-Talice A., Castanys S., Gamarro F., Characterization of an ABCA-like transporter involved in vesicular trafficking in the protozoan parasite Trypanosoma cruzi Molecular Microbiology 2004 54 632 664
104. Arana F. E., Perez-Victoria J. M., Repetto Y., Involvement of thiol metabolism in resistance to glucantime in Leishmania tropica Biochemical Pharmacology 1998 56 1201 1208 (Pubitemid 28511244)
105. Iyer J. P., Kaprakkaden A., Choudhary M. L., Shaha C., Crucial role of cytosolic tryparedoxin peroxidase in Leishmania donovani survival, drug response and virulence Molecular Microbiology 2008 68 2 372 391 (Pubitemid 351422957)
106. Wyllie S., Mandal G., Singh N., Sundar S., Fairlamb A. H., Chatterjee M., Elevated levels of tryparedoxin peroxidase in antimony unresponsive Leishmania donovani field isolates Molecular and Biochemical Parasitology 2010 173 2 162 164
107. Wyllie S., Vickers T. J., Fairlamb A. H., Roles of trypanothione S-transferase and tryparedoxin peroxidase in resistance to antimonials Antimicrobial Agents and Chemotherapy 2008 52 4 1359 1365 (Pubitemid 351521999)
108. Coelho A. C., Gentil L. G., da Silveira J. F., Cotrim P. C., Characterization of Leishmania (Leishmania) amazonensis promastigotes resistant to pentamidine Experimental Parasitology 2008 120 98 102
109. Thaithong S., Ranford-Cartwright L. C., Siripoon N., Harnyuttanakorn P., Kanchanakhan N. S., Seugorn A., Rungsihirunrat K., Cravo P. V. L., Beale G. H., Plasmodium falciparum gene mutations and amplification of dihydrofolate reductase genes in parasites grown In vitro in presence of pyrimethamine Experimental Parasitology 2001 98 2 59 70 (Pubitemid 32692295)
110. Rakotomanga M., Loiseau P. M., Saint-Pierre-Chazalet M., Hexadecylphosphocholine interaction with lipid monolayers Biochimica et Biophysica Acta 2004 1661 212 218 (Pubitemid 38296745)
111. Kothari H., Kumar P., Sundar S., Singh N., Possibility of membrane modification as a mechanism of antimony resistance in Leishmania donovani Parasitology International 2007 56 1 77 80 (Pubitemid 46274490)
112. Kumar D., Kulshrestha A., Singh R., Salotra P., In vitro susceptibility of field isolates of Leishmania donovani to miltefosine and amphotericin B: correlation with sodium antimony gluconate susceptibility and implications for treatment in areas of endemicity Antimicrobial Agents and Chemotherapy 2009 53 2 835 838
113. Dougherty M. K., Morrison D. K., Unlocking the code of 14-3-3 Journal of Cell Science 2004 117 10 1875 1884 (Pubitemid 38745122)
114. Beere H. M., The stress of dying: the role of heat shock proteins in the regulation of apoptosis Journal of Cell Science 2004 117 13 2641 2651 (Pubitemid 38997248)
115. Brochu C., Halmeur A., Ouellette M., The heat shock protein HSP70 and heat shock cognate protein HSC70 contribute to antimony tolerance in the protozoan parasite Leishmania Cell Stress and Chaperones 2004 9 3 294 303 (Pubitemid 39457433)
116. Neffe A. T., Abell A. D., Developments in the design and synthesis of calpain inhibitors Current Opinion in Drug Discovery and Development 2005 8 6 684 700 (Pubitemid 41659398)
117. Singh R., Kumar D., Duncan R. C., Nakhasi H. L., Salotra P., Overexpression of histone H2A modulates drug susceptibility in Leishmania parasites International Journal of Antimicrobial Agents 2010 36 1 50 57
118. Wiese M., A mitogen-activated protein (MAP) kinase homologue of Leishmania mexicana is essential for parasite survival in the infected host Embo Journal 1998 17 9 2619 2628 (Pubitemid 28221197)
119. Erdmann M., Scholz A., Melzer I. M., Schmetz C., Wiese M., Interacting protein kinases involved in the regulation of flagellar length Molecular Biology of the Cell 2006 17 4 2035 2045 (Pubitemid 44011616)
120. Samant M., Sahasrabuddhe A. A., Singh N., Gupta S. K., Sundar S., Dube A., Proteophosphoglycan is differentially expressed in sodium stibogluconate-sensitive and resistant Indian clinical isolates of Leishmania donovani Parasitology 2007 134 9 1175 1184 (Pubitemid 47174067)
121. El Fadili K., Drummelsmith J., Roy G., Jardim A., Ouellette M., Down regulation of KMP-11 in Leishmania infantum axenic antimony resistant amastigotes as revealed by a proteomic screen Experimental Parasitology 2009 123 1 51 57
122. Genest P. A., Haimeur A., Légaré D., Sereno D., Roy G., Messier N., Papadopoulou B., Ouellette M., A protein of the leucine-rich repeats (LRRs) superfamily is implicated in antimony resistance in Leishmania infantum amastigotes Molecular and Biochemical Parasitology 2008 158 1 95 99 (Pubitemid 351181236)
123. Yardley V., Ortuno N., Llanos-Cuentas A., American tegumentary leishmaniasis: is antimonial treatment outcome related to parasite drug susceptibility? Journal of Infectious Diseases 2006 194 1168 1175 (Pubitemid 44547658)
124. Torres D. C., Adaui V., Ribeiro-Alves M., Romero G. A. S., Arévalo J., Cupolillo E., Dujardin J. C., Targeted gene expression profiling in Leishmania braziliensi and Leishmania guyanensis parasites isolated from Brazilian patients with different antimonial treatment outcomes Infection, Genetics and Evolution 2010 10 6 727 733