Drug resistance in human African trypanosomiasis

Future Microbiology

Volumn 6, Issue 9, 2011, Pages 1037-1047

  Barrett, Michael P ^a   Vincent, Isabel M ^a   Burchmore, Richard Js ^a   Kazibwe, Anne Jn ^b   Matovu, Enock ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b MAKERERE UNIVERSITY   (Uganda)

Author keywords

drug resistance; eflornithine transporter; HAPT1; human African trypanosomiasis; nitroreductase; P2 transporter; sleeping sickness; treatment failure

Indexed keywords

2 AMINOPURINE; AMINO ACID TRANSPORTER; CARRIER PROTEIN; EFLORNITHINE; MELARSOPROL; NIFURTIMOX; PENTAMIDINE; SURAMIN;

AFRICAN TRYPANOSOMIASIS; CELL MEMBRANE; DRUG TREATMENT FAILURE; HUMAN; NONHUMAN; PARASITE INCIDENCE; PRIORITY JOURNAL; PROTOZOAL GENETICS; REVIEW; TREATMENT DURATION; TRYPANOSOMA BRUCEI;

ANIMALS; DRUG RESISTANCE; EFLORNITHINE; HUMANS; MEMBRANE TRANSPORT PROTEINS; NIFURTIMOX; PENTAMIDINE; PROTOZOAN PROTEINS; TREATMENT FAILURE; TRYPANOCIDAL AGENTS; TRYPANOSOMA; TRYPANOSOMIASIS, AFRICAN;

TRYPANOSOMA BRUCEI;

EID: 80053517353     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.11.88     Document Type: Review

References (53)

1. Brun R, Blum J, Chappuis F, Burri C. Human African trypanosomiasis. Lancet 375(9709), 148-159 (2010).
2. Brun R, Don R, Jacobs RT, Wang MZ, Barrett MP. Development of novel drugs for human African trypanosomiasis. Future Microbiol. 6(6), 677-691 (2011).
3. Sternberg JM, Maclean L. A spectrum of disease in human African trypanosomiasis: the host and parasite genetics of virulence. Parasitol. 137(14), 2007-2015 (2010).
4. Welburn SC, Maudlin I, Simarro PP. Controlling sleeping sickness -a review. Parasitology. 136(14), 1943-1949 (2009).
5. Simarro PP, Diarra A, Ruiz Postigo JA, Franco JR, Jannin JG. The human African trypanosomiasis control and surveillance programme of the World Health Organization 2000-2009: the way forward. PLoS Negl Trop Dis. 5(2), e1007 (2011).
6. Giroud C, Ottones F, Coustou V, et al. Murine Models for Trypanosoma brucei gambiense disease progression -from silent to chronic infections and early brain tropism. PLoS Negl. Trop. Dis. 3(9), e509 (2009).
7. Schlagenhauf P, Petersen E. Antimalaria drug resistance: the mono-combi-counterfeit triangle. Expert Rev. Anti Infect. Ther. 7(9), 1039-1042 (2009).
8. Schad GJ, Allanson A, Mackay SP, Cannavan A, Tettey JN. Development and validation of an improved HPLC method for the control of potentially counterfeit isometamidium products. J. Pharm. Biomed. Anal. 46(1), 45-51 (2008). (Pubitemid 350216323)
9. Barrett MP, Boykin DW, Brun R, Tidwell RR. Human African trypanosomiasis: pharmacological re-engagement with a neglected disease. Br. J. Pharmacol. 152(8), 1155-1171 (2007). (Pubitemid 350242432)
10. Sanderson L, Dogruel M, Rodgers J, De Koning HP, Thomas SA. Pentamidine movement across the murine blood-brain and blood-cerebrospinal fluid barriers: effect of trypanosome infection, combination therapy, P-glycoprotein, and multidrug resistance-associated protein. J. Pharmacol. Exp. Ther. 329(3), 967-977 (2009).
11. Sanderson L, Khan A, Thomas S. Distribution of suramin, an antitrypanosomal drug, across the blood-brain and blood-cerebrospinal fluid interfaces in wild-type and P-glycoprotein transporter-deficient mice. Antimicrob. Agents Chemother. 51(9), 3136-3146 (2007). (Pubitemid 350067520)
12. Sanderson L, Dogruel M, Rodgers J, Bradley B, Thomas SA. The blood-brain barrier significantly limits eflornithine entry into Trypanosoma brucei brucei infected mouse brain. J. Neurochem. 107(4), 1136-1146 (2008).
13. Lejon V, Legros D, Savignoni A, Etchegorry MG, Mbulamberi D, Büscher P. Neuro-inflammatory risk factors for treatment failure in "early second stage" sleeping sickness patients treated with pentamidine. J. Neuroimmunol. 144(1-2), 132-138 (2003). (Pubitemid 37329938)
14. Balasegaram M, Harris S, Checchi F, Hamel C, Karunakara U. Treatment outcomes and risk factors for relapse in patients with early-stage human African trypanosomiasis (HAT) in the Republic of the Congo. Bull. World Health Organ. 84(10), 777-782 (2006). (Pubitemid 44610112)
15. Brun R, Schumacher R, Schmid C, Kunz C, Burri C. The phenomenon of treatment failures in Human African Trypanosomiasis. Trop. Med. Int. Health 6(11), 906-914 (2001). (Pubitemid 33010877)
16. Matovu E, Geiser F, Schneider V, et al. Genetic variants of the TbAT1 adenosine transporter from African trypanosomes in relapse infections following melarsoprol therapy. Mol. Biochem. Parasitol. 117(1), 73-81 (2001). (Pubitemid 32823484)
17. AJ, Nerima B, de Koning HP, Mäser P, Barrett MP, Matovu E. Genotypic status of the TbAT1/P2 adenosine transporter of Trypanosoma brucei gambiense isolates from Northwestern Uganda following melarsoprol withdrawal. PLoS Negl. Trop. Dis. 3(9), e523 (2009).
18. Maina N, Maina KJ, Mäser P, Brun R. Genotypic and phenotypic characterization of Trypanosoma brucei gambiense isolates from Ibba, South Sudan, an area of high melarsoprol treatment failure rate. Acta Trop. 104(2-3), 84-90 (2007). (Pubitemid 47592836)
19. Balasegaram M, Harris S, Checchi F, Ghorashian S, Hamel C, Karunakara U. Melarsoprol versus eflornithine for treating late-stage Gambian trypanosomiasis in the Republic of the Congo. Bull. World Health Organ. 84(10), 783-791 (2006). (Pubitemid 44610113)
20. Pépin J, Khonde N, Maiso F, et al. Short-course eflornithine in Gambian trypanosomiasis: a multicentre randomized controlled trial. Bull. World Health Organ. 78(11), 1284-1295 (2000).
21. Carter NS, Fairlamb AH. Arsenical-resistant trypanosomes lack an unusual adenosine transporter. Nature 361(6408), 173-176 (1993). (Pubitemid 23031354)
22. Mäser P, Sütterlin C, Kralli A, Kaminsky R. A nucleoside transporter from Trypanosoma brucei involved in drug resistance. Science 285(5425), 242-244 (1999). (Pubitemid 29329994)
23. Matovu E, Stewart ML, Geiser F, et al. Mechanisms of arsenical and diamidine uptake and resistance in Trypanosoma brucei. Eukaryot. Cell 2(5), 1003-1008 (2003). (Pubitemid 37298713)
24. Bridges DJ, Gould MK, Nerima B, Mäser P, Burchmore RJ, de Koning HP. Loss of the high-affinity pentamidine transporter is responsible for high levels of cross-resistance between arsenical and diamidine drugs in African trypanosomes. Mol. Pharmacol. 71(4), 1098-1108 (2007). (Pubitemid 46457013)
25. de Koning HP. Ever-increasing complexities of diamidine and arsenical crossresistance in African trypanosomes. Trends Parasitol. 24(8), 345-349 (2008).
26. Lüscher A, Nerima B, Mäser P. Combined contribution of TbAT1 and TbMRPA to drug resistance in Trypanosoma brucei. Mol. Biochem. Parasitol. 150(2), 364-366 (2006). (Pubitemid 44691943)
27. Paine MF, Wang MZ, Generaux CN. Diamidines for human African trypanosomiasis. Curr. Opin. Investig. Drugs 11(8), 876-883 (2010).
28. Carter NS, Berger BJ, Fairlamb AH. Uptake of diamidine drugs by the P2 nucleoside transporter in melarsen-sensitive and -resistant Trypanosoma brucei brucei. J. Biol. Chem. 270(47), 28153-28157 (2011)
29. Bernhard SC, Nerima B, Mäser P, Brun R. Melarsoprol-and pentamidine-resistant Trypanosoma brucei rhodesiense populations and their cross-resistance. Int. J Parasitol. 37 (Pubitemid 47417979)
30. Teka IA, Kazibwe AJ, El-Sabbagh N, et al. The diamidine diminazene aceturate is a substrate for the high affinity pentamidine transporter: implications for the development of high resistance levels in trypanosomes. Mol. Pharmacol. 80(1), 110-116 (2011)
31. Lanteri CA, Stewart ML, Brock JM, et al. Roles for the Trypanosoma brucei P2 transporter in DB75 uptake and resistance. Mol. Pharmacol. 70(5), 1585-1592 (2006).
32. Ward CP, Wong PE, Burchmore RJ, de Koning HP, Barrett MP. Trypanocidal furamidine analogues: influence of pyridine nitrogens on trypanocidal activity, transport kinetics, and resistance patterns. Antimicrob. Agents Chemother. 55(5), 2352-2361 (2011).
33. Stewart ML, Burchmore RJ, Clucas C, et al. Multiple genetic mechanisms lead to loss of functional TbAT1 expression in drug-resistant trypanosomes. Eukaryot. Cell. 9(2), 336-343 (2010).
34. Stewart ML, Krishna S, Burchmore RJ, et al. Detection of arsenical drug resistance in Trypanosoma brucei with a simple fluorescence test. Lancet 366(9484), 486-487 (2005). (Pubitemid 41111697)
35. Jones D, Nyalwidhe J, Tetley L, Barrett MP. McArthur revisited: fluorescence microscopes for field diagnostics. Trends Parasitol. 23(10), 468-469 (2007). (Pubitemid 47465092)
36. Ortiz D, Sanchez MA, Quecke P, Landfear SM. Two novel nucleobase/ pentamidine transporters from Trypanosoma brucei. Mol. Biochem. Parasitol. 163(2), 67-76 (2009).
37. Bacchi CJ, Garofalo J, Ciminelli M, et al. Resistance to DL-alpha-difluoromethylornithine by clinical isolates of Trypanosoma brucei rhodesiense. Role of S-adenosylmethionine. Biochem. Pharmacol. 46(3), 471-481 (1993). (Pubitemid 23239998)
38. Xiao Y, McCloskey DE, Phillips MA. RNA interference-mediated silencing of ornithine decarboxylase and spermidine synthase genes in Trypanosoma brucei provides insight into regulation of polyamine biosynthesis. Eukaryot. Cell. 8(5), 747-755 (2009).
39. Iten M, Matovu E, Brun R, Kaminsky R. Innate lack of susceptibility of Ugandan Trypanosoma brucei rhodesiense to DL-alpha-difluoromethylornithine (DFMO). Trop. Med. Parasitol. 46(3), 190-194 (1995).
40. Bitonti AJ, Bacchi CJ, McCann PP, Sjoerdsma A. Uptake of alpha-difluoromethylornithine by Trypanosoma brucei brucei. Biochem. Pharmacol. 35(2), 351-354 (1986).
41. Bellofatto V, Fairlamb AH, Henderson GB, Cross GA. Biochemical changes associated with alpha-difluoromethylornithine uptake and resistance in Trypanosoma brucei. Mol. Biochem. Parasitol. 25(3), 227-238 (1987).
42. Phillips MA, Wang CC. A Trypanosoma brucei mutant resistant to alpha-difluoromethylornithine. Mol. Biochem. Parasitol. 22(1), 9-17 (1987). (Pubitemid 17225810)
43. Vincent IM, Creek D, Watson DG, et al. A molecular mechanism for eflornithine resistance in African trypanosomes. PLoS Pathog. 6(11), e1001204 (2010).
44. Schumann Burkard G, Jutzi P, Roditi I. Genome-wide RNAi screens in bloodstream form trypanosomes identify drug transporters. Mol. Biochem. Parasitol. 175(1), 91-94 (2011).
45. Baker N, Alsford S, Horn D. Genome-wide RNAi screens in African trypanosomes identify the nifurtimox activator NTR and the eflornithine transporter AAT6. Mol. Biochem. Parasitol. 176 1, 55-57 (2011).
46. Priotto G, Kasparian S, Mutombo W, et al. Nifurtimox-eflornithine combination therapy for second-stage African Trypanosoma brucei gambiense trypanosomiasis: a multicentre, randomised, Phase III, non-inferiority trial. Lancet. 374(9683), 56-64 (2009).
47. Wilkinson SR, Kelly JM. Trypanocidal drugs: mechanisms, resistance and new targets. Expert Rev. Mol. Med. 11, e31 (2009).
48. Jeganathan S, Sanderson L, Dogruel M, Rodgers J, Croft S, Thomas SA. The distribution of nifurtimox across the healthy and trypanosome-infected murine blood-brain and blood-cerebrospinal fluid barriers. J. Pharmacol. Exp. Ther. 336(2), 506-515 (2011).
49. Wilkinson SR, Taylor MC, Horn D, Kelly JM, Cheeseman I. A mechanism for cross-resistance to nifurtimox and benznidazole in trypanosomes. Proc. Natl Acad. Sci. USA 105(13), 5022-5027 (2008). (Pubitemid 351738503)
50. Hall BS, Bot C, Wilkinson SR. Nifurtimox activation by trypanosomal type I nitroreductases generates cytotoxic nitrile metabolites. J. Biol. Chem. 286(15), 13088-13095 (2011).
51. Sokolova AY, Wyllie S, Patterson S, Oza SL, Read KD, Fairlamb AH. Cross-resistance to nitro drugs and implications for treatment of human African trypanosomiasis. Antimicrob. Agents Chemother. 54(7), 2893-2900 (2010).
52. Torreele E, Bourdin Trunz B, Tweats D, et al. Fexinidazole -a new oral nitroimidazole drug candidate entering clinical development for the treatment of sleeping sickness. PLoS Negl. Trop. Dis. 4(12), e923 (2010).
53. Alsford S, Turner DJ, Obado SO, et al. High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res. 21(6), 915-924 (2011).