The role of ABC transporters in drug-resistant leishmania

Drug Resistance in Leishmania Parasites: Consequences, Molecular Mechanisms and Possible Treatments

Volumn , Issue , 2013, Pages 237-258

  Coelho, Adriano C ^a   Cotrim, Paulo C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84880253692     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-7091-1125-3_12     Document Type: Chapter

References (127)

1. Akopyants NS et al. (2009) Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324:265-268
2. Albrecht C, Viturro E (2007) The ABCA subfamily-gene and protein structures, functions and associated hereditary diseases. Pflugers Arch 453:581-589
3. Allikmets R et al. (1996) Characterization of the human ABC superfamily: isolation and mapping of 21 new genes using the expressed sequence tags database. Hum Mol Genet 5:1649-1655
4. Arana FE et al. (1998) Involvement of thiol metabolism in resistance to Glucantime in Leishmania tropica. Biochem Pharmacol 56:1201-1208
5. Araujo-Santos JM et al. (2005) The overexpression of an intracellular ABCA-like transporter alters phospholipid trafficking in Leishmania. Biochem Biophys Res Commun 330:349-355
6. Basselin M et al. (2002) Resistance to pentamidine in Leishmania mexicana involves exclusion of the drug from the mitochondrion. Antimicrob Agents Chemother 46:3731-3738
7. Beverley SM (1991) Gene amplification in Leishmania. Annu Rev Microbiol 45:417-444
8. Beverley SM (2003) Protozomics: trypanosomatid parasite genetics comes of age. Nat Rev Genet 4:11-19
9. Bitonti AJ et al. (1988) Reversal of chloroquine resistance in malaria parasite Plasmodium falciparum by desipramine. Science 242:1301-1303
10. Bories C et al. (2008) Selection and phenotype characterisation of sitamaquine-resistant promastigotes of Leishmania donovani. Biomed Pharmacother 62:164-167
11. Borst P, Ouellette M (1995) New mechanisms of drug resistance in parasitic protozoa. Annu Rev Microbiol 49:427-460
12. Borst P et al. (2000) A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 92:1295-1302
13. BoseDasgupta S et al. (2008) A novel ATP-binding cassette transporter, ABCG6 is involved in chemoresistance of Leishmania. Mol Biochem Parasitol 158:176-188
14. Callahan HL, Beverley SM (1991) Heavy metal resistance: a new role for P-glycoproteins in Leishmania. J Biol Chem 266:18427-18430
15. Callahan HL, Beverley SM (1992) A member of the aldoketo reductase family confers methotrexate resistance in Leishmania. J Biol Chem 267:24165-24168
16. Castanys-Munoz E et al. (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
17. Castanys-Munoz E et al. (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
18. Chen ZQ et al. (2006) The essential vertebrate ABCE1 protein interacts with eukaryotic initiation factors. J Biol Chem 281:7452-7457
19. Chiquero MJ et al. (1998) Altered drug membrane permeability in a multidrug-resistant Leishmania tropica line. Biochem Pharmacol 55:131-139
20. Chow LM et al. (1993) Cloning and functional analysis of an extrachromosomally amplified multidrug resistance-like gene in Leishmania enriettii. Mol Biochem Parasitol 60(2):195-208
21. Clayton CE (1999) Genetic manipulation of kinetoplastida. Parasitol Today 15:372-378
22. Clayton C, Shapira M (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156:93-101
23. 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
24. Coelho AC et al. (2006) Intracellular location of the ABC transporter PRP1 related to pentamidine resistance in Leishmania major. Mol Biochem Parasitol 150:378-383
25. Coelho AC et al. (2007) Role of the ABC transporter PRP1 (ABCC7) in pentamidine resistance in Leishmania amastigotes. Antimicrob Agents Chemother 51:3030-3032
26. Coelho AC et al. (2008) Characterization of Leishmania (Leishmania) amazonensis promastigotes resistant to pentamidine. Exp Parasitol 120:98-102
27. Croft SL, Sundar S, Fairlamb AH (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19:111-126
28. 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
29. Dean M, Annilo T (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet 6:123-142
30. Dean M, Rzhetsky A, Allikmets R (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11:1156-1166
31. V resistance in Leishmania donovani isolates from Nepal. Antimicrob Agents Chemother 49:4616-4621
32. Deeley RG, Westlake C, Cole SP (2006) Transmembrane transport of endo-and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 86:849-899
33. Dey S et al. (1996) An ATP-dependent As(III)-glutathione transport system in membrane vesicles of Leishmania tarentolae. Proc Natl Acad Sci USA 93:2192-2197
34. Dias FC 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
35. Dodge MA et al. (2004) Localization and activity of multidrug resistance protein 1 in the secretory pathway of Leishmania parasites. Mol Microbiol 51:1563-1575
36. Ejendal KF, Hrycyna CA (2002) Multidrug resistance and cancer: the role of the human ABC transporter ABCG2. Curr Protein Pept Sci 3:503-511
37. El Fadili K 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
38. Ellenberger TE, Beverley SM (1989) Multiple drug resistance and conservative amplification of the H region in Leishmania major. J Biol Chem 264:15094-15103
39. Endicott JA, Ling V (1989) The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu Rev Biochem 58:137-171
40. Estevez AM et al. (2004) Effects of depletion and overexpression of the Trypanosoma brucei ribonuclease L inhibitor homologue. Mol Biochem Parasitol 133:137-141
41. Fairlamb AH, Cerami A (1992) Metabolism and functions of trypanothione in the kinetoplastida.Annu Rev Microbiol 46:695-729
42. Ghedin E et al. (2001) Secretory and endocytic pathways converge in a dynamic endosomal system in a primitive protozoan. Traffic 2:175-188
43. Gottesman MM, Pastan I (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 62:385-427
44. Gottesman MM, Fojo T, Bates SE (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2:48-58
45. Grondin K, Papadopoulou B, Ouellette M (1993) Homologous recombination between direct repeat sequences yields P-glycoprotein containing amplicons in arsenite resistant Leishmania. Nucleic Acids Res 21:1895-1901
46. Grondin K et al. (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
47. Gueiros-Filho FJ et al. (1995) Leishmania amazonensis: multidrug resistance in vinblastine-resistant promastigotes is associated with rhodamine 123 efflux, DNA amplification, and RNA overexpression of a Leishmania mdr1 gene. Exp Parasitol 81:480-490
48. Haimeur A 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
49. III resistant Leishmania tarentolae. Mol Biochem Parasitol 108:131-135
50. Henderson DM et al. (1992) Multidrug resistance in Leishmania donovani is conferred by amplification of a gene homologous to the mammalian mdr1 gene. Mol Cell Biol 12:2855-2865
51. Hendrickson N et al. (1993) Molecular characterization of the ldmdr1 multidrug resistance gene from Leishmania donovani. Mol Biochem Parasitol 60:53-64
52. Herget M, Tampe R (2007) Intracellular peptide transporters in human-compartmentalization of the “peptidome”. Pflugers Arch 453:591-600
53. Hettema EH et al (1996) The ABC transporter proteins Pat1 and Pat2 are required for import of long-chain fatty acids into peroxisomes of Saccharomyces cerevisiae. EMBO J 15:3813-3822
54. Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67-113
55. Ivens AC et al. (1998) A physical map of the Leishmania major Friedlin genome. Genome Res 8:135-145
56. Ivens AC et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309:436-442
57. Jha TK et al. (1999) Miltefosine, an oral agent, for the treatment of Indian visceral leishmaniasis.N Engl J Med 341:1795-1800
58. Kapler GM, Beverley SM (1989) Transcriptional mapping of the amplified region encoding the dihydrofolate reductase-thymidylate synthase of Leishmania major reveals a high density of transcripts, including overlapping and antisense RNAs. Mol Cell Biol 9:3959-3972
59. Katakura K et al. (1999) Structural and functional analysis of the LaMDR1 multidrug resistance gene in Leishmania amazonensis. Biochem Biophys Res Commun 255:289-294
60. Katakura K et al. (2004) Overexpression of LaMDR2, a novel multidrug resistance ATP-binding cassette transporter, causes 5-fluorouracil resistance in Leishmania amazonensis. FEBS Lett 561:207-212
61. Kerr ID (2004) Sequence analysis of twin ATP binding cassette proteins involved in translational control, antibiotic resistance, and ribonuclease L inhibition. Biochem Biophys Res Commun 315:166-173
62. Kispal G et al. (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18:3981-3989
63. Klokouzas A et al. (2003) ABC transporters and drug resistance in parasitic protozoa. Int J Antimicrob Agents 22:301-317
64. Lee JS et al. (1994) Rhodamine efflux patterns predict P-glycoprotein substrates in the National Cancer Institute drug screen. Mol Pharmacol 46:627-638
65. Legare D, Hettema E, Ouellette M (1994) The P-glycoprotein-related gene family in Leishmania. Mol Biochem Parasitol 68:81-91
66. Legare D et al. (1997) Efflux systems and increased trypanothione levels in arsenite-resistant Leishmania. Exp Parasitol 87:275-282
67. Legare D et al. (2001) The Leishmania ATP-binding cassette protein PGPA is an intracellular metal-thiol transporter ATPase. J Biol Chem 276:26301-26307
68. Leprohon P et al. (2006) Modulation of Leishmania ABC protein gene expression through life stages and among drug-resistant parasites. Eukaryot Cell 5:1713-1725
69. Leprohon P, Legare D, Ouellette M (2009a) Intracellular localization of the ABCC proteins of Leishmania and their role in resistance to antimonials. Antimicrob Agents Chemother 53:2646-2649
70. Leprohon P et al. (2009b) Gene expression modulation is associated with gene amplification, supernumerary chromosomes and chromosome loss in antimony-resistant Leishmania infantum. Nucleic Acids Res 37:1387-1399
71. Leslie EM, Deeley RG, Cole SP (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216-237
72. Lux H et al (2000) Ether-lipid (alkyl-phospholipid) metabolism and the mechanism of action of ether-lipid analogues in Leishmania. Mol Biochem Parasitol 111:1-14
73. Lye LF et al. (2010) Retention and loss of RNA interference pathways in trypanosomatid protozoans. PLoS Pathog 6:e1001-161
74. Marton MJ et al. (1997) Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2alpha kinase GCN2. Mol Cell Biol 17:4474-4489
75. Mary C et al. (2010) Frequency of drug resistance gene amplification in clinical Leishmania strains. Int J Microbiol 2010:819060. doi:10.1155/2010/819060
76. McConville MJ et al. (2002) Secretory pathway of trypanosomatid parasites. Microbiol Mol Biol Rev 66:122-154
77. Michels PA et al. (2006) Metabolic functions of glycosomes in trypanosomatids. Biochim Biophys Acta 1763:1463-1477
78. Mitsuhashi N et al. (2000) MTABC3, a novel mitochondrial ATP-binding cassette protein involved in iron homeostasis. J Biol Chem 275:17536-17540
79. Mittal MK et al. (2007) Characterization of natural antimony resistance in Leishmania donovani isolates. Am J Trop Med Hyg 76:681-688
80. Momen H (2001) Some current problems in the systematics of Trypanosomatids. Int J Parasitol 31:640-642
81. Mookerjee Basu J et al. (2008) Inhibition of ABC transporters abolishes antimony resistance in Leishmania infection. Antimicrob Agents Chemother 52:1080-1093
82. Mukherjee A et al. (2006) Roles for mitochondria in pentamidine susceptibility and resistance in Leishmania donovani. Mol Biochem Parasitol 145:1-10
83. Mukherjee A 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
84. Mukhopadhyay R et al. (1996) Trypanothione overproduction and resistance to antimonials and arsenicals in Leishmania. Proc Natl Acad Sci USA 93:10383-10387
85. Mullin KA et al. (2001) Regulated degradation of an endoplasmic reticulum membrane protein in a tubular lysosome in Leishmania mexicana. Mol Biol Cell 12:2364-2377
86. Murta SM et al. (2001) Drug resistance in Trypanosoma cruzi is not associated with amplification or overexpression of P-glycoprotein (PGP) genes. Mol Biochem Parasitol 117:223-228
87. 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
88. Ouellette M et al. (1991) Direct and inverted DNA repeats associated with P-glycoprotein gene amplification in drug resistant Leishmania. EMBO J 10:1009-1016
89. Ouellette M et al. (1998) ABC transporters in Leishmania and their role in drug resistance. Drug Resist Updat 1:43-48
90. Padron-Nieves M et al. (2009) Glibenclamide modulates Glucantime activity and disposition in Leishmania major. Exp Parasitol 121:331-337
91. Papadopoulou B, Roy G, Ouellette M (1992) A novel antifolate resistance gene on the amplified H circle of Leishmania. EMBO J 11:3601-3608
92. Papadopoulou B et al. (1994) Contribution of the Leishmania P-glycoprotein-related gene ltpgpA to oxyanion resistance. J Biol Chem 269:11980-11986
93. Papadopoulou B et al. (1996) Gene disruption of the P-glycoprotein related gene pgpa of Leishmania tarentolae. Biochem Biophys Res Commun 224:772-778
94. Parodi-Talice A et al. (2003) The overexpression of a new ABC transporter in Leishmania is related to phospholipid trafficking and reduced infectivity. Biochim Biophys Acta 1612:195-207
95. Peacock CS et al. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39:839-847
96. Perez-Victoria JM et al. (2001a) ABC transporters in the protozoan parasite Leishmania. Int Microbiol 4:159-166
97. Perez-Victoria JM et al. (2001b) Alkyl-lysophospholipid resistance in multidrug-resistant Leish-mania tropica and chemosensitization by a novel P-glycoprotein-like transporter modulator. Antimicrob Agents Chemother 45:2468-2474
98. Perez-Victoria FJ et al. (2003) Functional cloning of the Miltefosine transporter. A novel P-type phospholipid translocase from Leishmania involved in drug resistance. J Biol Chem 278:49965-49971
99. Perez-Victoria FJ et al. (2006) Phospholipid translocation and Miltefosine potency require both L. donovani Miltefosine transporter and the new protein LdRos3 in Leishmania parasites. J Biol Chem 281:23766-23775
100. Petriv OI et al (2002) RNA interference of peroxisome-related genes in C. elegans: a new model for human peroxisomal disorders. Physiol Genomics 10:79-91
101. Pompella A et al. (2003) The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol 66:1499-1503
102. Ponte-Sucre A (2007) Availability and applications of ATP-binding cassette (ABC) transporter blockers. Appl Microbiol Biotechnol 76:279-286
103. Rougeron V et al. (2009) Extreme inbreeding in Leishmania braziliensis. Proc Natl Acad Sci USA 106:10224-10229
104. Sanchez-Canete MP et al. (2009) Low plasma membrane expression of the Miltefosine transport complex renders Leishmania braziliensis refractory to the drug. Antimicrob Agents Chemother 53:1305-1313
105. Saurin W, Hofnung M, Dassa E (1999) Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J Mol Evol 48:22-41
106. Sauvage V et al. (2009) The role of ATP-binding cassette (ABC) proteins in protozoan parasites Mol Biochem Parasitol 167:81-94
107. Seifert K et al. (2003) Characterisation of Leishmania donovani promastigotes resistant to hexadecylphosphocholine (Miltefosine). Int J Antimicrob Agents 22:380-387
108. Serrano-Martin X, Payares G, Mendoza-Leon A (2006) Glibenclamide, a blocker of K + (ATP) channels, shows antileishmanial activity in experimental murine cutaneous leishmaniasis. Antimicrob Agents Chemother 50:4214-4216
109. Shahi SK, Krauth-Siegel RL, Clayton CE (2002) Overexpression of the putative thiol conjugate transporter TbMRPA causes melarsoprol resistance in Trypanosoma brucei. Mol Microbiol 43:1129-1138
110. Shani N, Valle D (1998) Peroxisomal ABC transporters. Methods Enzymol 292:753-776
111. Silva N et al. (2004) Cell differentiation and infectivity of Leishmania mexicana are inhibited in a strain resistant to an ABC-transporter blocker. Parasitology 128:629-634
112. Singh N, Singh RT, Sundar S (2003) Novel mechanism of drug resistance in kala azar field isolates. J Infect Dis 188:600-607
113. Soto J et al. (2001) Treatment of American cutaneous leishmaniasis with Miltefosine, an oral agent. Clin Infect Dis 33:E57-E61
114. Stevens JR et al. (2001) The molecular evolution of Trypanosomatidae. Adv Parasitol 48:1-56
115. Sundaram P et al. (2006) ATP-binding cassette transporters are required for efficient RNA interference in Caenorhabditis elegans. Mol Biol Cell 17:3678-3688
116. Theodoulou FL, Holdsworth M, Baker A (2006) Peroxisomal ABC transporters. FEBS Lett 580:1139-1155
117. Torres C et al. (1999) Characterization of a new ATP-binding cassette transporter in Trypanosoma cruzi associated to aL1Tc retrotransposon. Biochim Biophys Acta 1489:428-432
118. Torres C et al. (2004) Characterization of an ABCA-like transporter involved in vesicular trafficking in the protozoan parasite Trypanosoma cruzi. Mol Microbiol 54:632-646
119. Tyzack JK et al. (2000) ABC50 interacts with eukaryotic initiation factor 2 and associates with the ribosome in an ATP-dependent manner. J Biol Chem 275:34131-34139
120. Ubeda JM 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
121. van Helvoort A et al. (1996) MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 87:507-517
122. Velamakanni S et al. (2007) ABCG transporters: structure, substrate specificities and physiological roles: a brief overview. J Bioenerg Biomembr 39:465-471
123. Vergnes B et al. (2007) 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. Mol Cell Proteomics 6:88-101
124. Walker JE et al. (1982) Distantly related sequences in the alpha-and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945-951
125. Wong IL, Chow LM (2006) The role of Leishmania enriettii multidrug resistance protein 1 (LeMDR1) in mediating drug resistance is iron-dependent. Mol Biochem Parasitol 150:278-287
126. Zhou A, Hassel BA, Silverman RH (1993) Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell 72:753-765
127. Zhou SF et al. (2008) Substrates and inhibitors of human multidrug resistance associated proteins and the implications in drug development. Curr Med Chem 15:1981-2039