Gene Amplification and Point Mutations in Pyrimidine Metabolic Genes in 5-Fluorouracil Resistant Leishmania infantum

PLoS Neglected Tropical Diseases

Volumn 7, Issue 11, 2013, Pages

  Ritt, Jean François ^a   Raymond, Frédéric ^a   Leprohon, Philippe ^a   Légaré, Danielle ^a   Corbeil, Jacques ^a   Ouellette, Marc ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FLUOROURACIL; THYMIDINE KINASE; URIDINE PHOSPHORYLASE;

ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; GENE AMPLIFICATION; GENETIC TRANSFECTION; GENETIC VARIABILITY; LEISHMANIA INFANTUM; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHENOTYPIC VARIATION; POINT MUTATION; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; SOUTHERN BLOTTING;

ANTIPROTOZOAL AGENTS; BIOSYNTHETIC PATHWAYS; COMPARATIVE GENOMIC HYBRIDIZATION; DNA MUTATIONAL ANALYSIS; DRUG RESISTANCE; FLUOROURACIL; LEISHMANIA INFANTUM; MUTATION; PROTOZOAN PROTEINS; PYRIMIDINES; SEQUENCE ANALYSIS, DNA; TRANSFECTION;

EID: 84888229717     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002564     Document Type: Article

References (59)

1. Herwaldt BL, (1999) Leishmaniasis. The Lancet 354: 1191-1199.
2. Murray HW, Berman JD, Davies CR, Saravia NG, (2005) Advances in leishmaniasis. Lancet 366: 1561-1577.
3. Singh N, Kumar M, Singh RK, (2012) Leishmaniasis: current status of available drugs and new potential drug targets. Asian Pac J Trop Med 5: 485-497.
4. Sundar S, Chakravarty J, (2013) Leishmaniasis: an update of current pharmacotherapy. Expert Opin Pharmacother 14: 53-63.
5. Croft SL, Sundar S, Fairlamb AH, (2006) Drug Resistance in Leishmaniasis. Clinical Microbiology Reviews 19: 111-126.
6. Ali JAM, Creek DJ, Burgess K, Allison HC, Field MC, et al. (2013) Pyrimidine Salvage in Trypanosoma brucei Bloodstream Forms and the Trypanocidal Action of Halogenated Pyrimidines. Molecular Pharmacology 83: 439-453.
7. Papageorgiou IG, Yakob L, Al Salabi MI, Diallinas G, Soteriadou KP, et al. (2005) Identification of the first pyrimidine nucleobase transporter in Leishmania: similarities with the Trypanosoma brucei U1 transporter and antileishmanial activity of uracil analogues. Parasitology 130: 275-283.
8. Wilson ZN, Gilroy CA, Boitz JM, Ullman B, Yates PA, (2012) Genetic dissection of pyrimidine biosynthesis and salvage in Leishmania donovani. J Biol Chem 287: 12759-12770.
9. Gutteridge WE, Coombs GH (1977) Biochemistry of parasitic protozoa.: MacMillan Press, London. 172 p.
10. Hassan HF, Coombs GH, (1988) Purine and pyrimidine metabolism in parasitic protozoa. FEMS Microbiol Rev 4: 47-83.
11. de Koning HP, Bridges DJ, Burchmore RJ, (2005) Purine and pyrimidine transport in pathogenic protozoa: from biology to therapy. FEMS Microbiol Rev 29: 987-1020.
12. de Koning HP, Jarvis SM, (1998) A highly selective, high-affinity transporter for uracil in Trypanosoma brucei brucei: evidence for proton-dependent transport. Biochemistry and Cell Biology 76: 853-858.
13. Ali JA, Tagoe DN, Munday JC, Donachie A, Morrison LJ, et al. (2013) Pyrimidine biosynthesis is not an essential function for Trypanosoma brucei bloodstream forms. PLoS One 8: e58034.
14. Nare B, Luba J, Hardy LW, Beverley S, (1997) New approaches to Leishmania chemotherapy: pteridine reductase 1 (PTR1) as a target and modulator of antifolate sensitivity. Parasitology 114 Suppl: S101-110.
15. 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.
16. Ouellette M, Drummelsmith J, El-Fadili A, Kundig C, Richard D, et al. (2002) Pterin transport and metabolism in Leishmania and related trypanosomatid parasites. Int J Parasitol 32: 385-398.
17. Cunningham ML, Beverley SM, (2001) Pteridine salvage throughout the Leishmania infectious cycle: implications for antifolate chemotherapy. Mol Biochem Parasitol 113: 199-213.
18. Richard D, Kundig C, Ouellette M, (2002) A new type of high affinity folic acid transporter in the protozoan parasite Leishmania and deletion of its gene in methotrexate-resistant cells. J Biol Chem 277: 29460-29467.
19. Richard D, Leprohon P, Drummelsmith J, Ouellette M, (2004) Growth phase regulation of the main folate transporter of Leishmania infantum and its role in methotrexate resistance. J Biol Chem 279: 54494-54501.
20. Vickers TJ, Beverley SM, (2011) Folate metabolic pathways in Leishmania. Essays Biochem 51: 63-80.
21. Dridi L, Ahmed Ouameur A, Ouellette M, (2010) High Affinity S-Adenosylmethionine Plasma Membrane Transporter of Leishmania Is a Member of the Folate Biopterin Transporter (FBT) Family. Journal of Biological Chemistry 285: 19767-19775.
22. Katakura K, Fujise H, Takeda K, Kaneko O, Torii M, et al. (2004) Overexpression of LaMDR2, a novel multidrug resistance ATP-binding cassette transporter, causes 5-fluorouracil resistance in Leishmania amazonensis. FEBS Letters 561: 207-212.
23. Peters GJ, Backus HH, Freemantle S, van Triest B, Codacci-Pisanelli G, et al. (2002) Induction of thymidylate synthase as a 5-fluorouracil resistance mechanism. Biochim Biophys Acta 1587: 194-205.
24. Zhao X, Yu YT, (2007) Incorporation of 5-fluorouracil into U2 snRNA blocks pseudouridylation and pre-mRNA splicing in vivo. Nucleic Acids Res 35: 550-558.
25. Kammler S, Lykke-Andersen S, Jensen TH, (2008) The RNA exosome component hRrp6 is a target for 5-fluorouracil in human cells. Mol Cancer Res 6: 990-995.
26. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
27. El Fadili A, Kündig C, Ouellette M, (2002) Characterization of the folylpolyglutamate synthetase gene and polyglutamylation of folates in the protozoan parasite Leishmania. Molecular and Biochemical Parasitology 124: 63-71.
28. Papadopoulou B, Roy G, Ouellette M, (1992) A novel antifolate resistance gene on the amplified H circle of Leishmania. EMBO J 11: 3601-3608.
29. 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.
30. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
31. Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, et al. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39: 839-847.
32. Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, et al. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Research 38: D457-D462.
33. Li H, Durbin R, (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595.
34. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
35. Lassmann T, Hayashizaki Y, Daub CO, (2011) SAMStat: monitoring biases in next generation sequencing data. Bioinformatics 27: 130-131.
36. Papadopoulou B, Roy G, Ouellette M, (1993) Frequent amplification of a short chain dehydrogenase gene as part of circular and linear amplicons in methotrexate resistant Leishmania. Nucleic Acids Res 21: 4305-4312.
37. Beverley SM, (1991) Gene Amplification in Leishmania. Annual Review of Microbiology 45: 417-444.
38. Borst P, Ouellette M, (1995) New Mechanisms of Drug Resistance in Parasitic Protozoa. Annual Review of Microbiology 49: 427-460.
39. Coderre JA, Beverley SM, Schimke RT, Santi DV, (1983) Overproduction of a bifunctional thymidylate synthetase-dihydrofolate reductase and DNA amplification in methotrexate-resistant Leishmania tropica. Proceedings of the National Academy of Sciences 80: 2132-2136.
40. Ellenberger TE, Beverley SM, (1987) Reductions in methotrexate and folate influx in methotrexate-resistant lines of Leishmania major are independent of R or H region amplification. Journal of Biological Chemistry 262: 13501-13506.
41. Downing T, Imamura H, Decuypere S, Clark TG, Coombs GH, et al. (2011) Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome Res 21: 2143-2156.
42. Coelho AC, Boisvert S, Mukherjee A, Leprohon P, Corbeil J, et al. (2012) Multiple mutations in heterogeneous miltefosine-resistant Leishmania major population as determined by whole genome sequencing. PLoS Negl Trop Dis 6: e1512.
43. Mukherjee A, Boisvert S, do Monte-Neto RL, Coelho AC, Raymond F, et al. (2013) Telomeric gene deletion and intrachromosomal amplification in antimony resistant Leishmania. Mol Microbiol.
44. Hammond DJ, Gutteridge WE, (1982) UMP synthesis in the kinetoplastida. Biochimica et Biophysica Acta (BBA)- General Subjects 718: 1-10.
45. 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.
46. Vasudevan G, Carter NS, Drew ME, Beverley SM, Sanchez MA, et al. (1998) Cloning of Leishmania nucleoside transporter genes by rescue of a transport-deficient mutant. Proc Natl Acad Sci U S A 95: 9873-9878.
47. Carter NS, Drew ME, Sanchez M, Vasudevan G, Landfear SM, et al. (2000) Cloning of a novel inosine-guanosine transporter gene from Leishmania donovani by functional rescue of a transport-deficient mutant. J Biol Chem 275: 20935-20941.
48. Cruz A, Beverley SM, (1990) Gene replacement in parasitic protozoa. Nature 348: 171-173.
49. 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.
50. Longley DB, Harkin DP, Johnston PG, (2003) 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 3: 330-338.
51. Zhang N, Yin Y, Xu SJ, Chen WS, (2008) 5-Fluorouracil: mechanisms of resistance and reversal strategies. Molecules 13: 1551-1569.
52. Longley DB, Johnston PG, (2005) Molecular mechanisms of drug resistance. Journal of Pathology 205: 275-292.
53. Wang W, Marsh S, Cassidy J, McLeod HL, (2001) Pharmacogenomic dissection of resistance to thymidylate synthase inhibitors. Cancer Res 61: 5505-5510.
54. Naumov DG, (2012) [Furanosidase superfamily: search of homologues]. Mol Biol (Mosk) 46: 354-360.
55. Burchmore RJS, Wallace LJM, Candlish D, Al-Salabi MI, Beal PR, et al. (2003) Cloning, Heterologous Expression, and in Situ Characterization of the First High Affinity Nucleobase Transporter from a Protozoan. Journal of Biological Chemistry 278: 23502-23507.
56. Sanchez MA, Tryon R, Pierce S, Vasudevan G, Landfear SM, (2004) Functional expression and characterization of a purine nucleobase transporter gene from Leishmania major. Mol Membr Biol 21: 11-18.
57. Henriques C, Sanchez MA, Tryon R, Landfear SM, (2003) Molecular and functional characterization of the first nucleobase transporter gene from African trypanosomes. Mol Biochem Parasitol 130: 101-110.
58. Gudin S, Quashie NB, Candlish D, Al-Salabi MI, Jarvis SM, et al. (2006) Trypanosoma brucei: a survey of pyrimidine transport activities. Exp Parasitol 114: 118-125.
59. Fernandes JF, Castellani O, (1959) Nucleotide and polynucleotide synthesis in Trypanosoma cruzi. II. In vitro effect of tioguanine and of the aminonucleoside of stylomycin. Exp Parasitol 8: 480-485.