Gene expression modulation is associated with gene amplification, supernumerary chromosomes and chromosome loss in antimony-resistant Leishmania infantum

Nucleic Acids Research

Volumn 37, Issue 5, 2009, Pages 1387-1399

  Leprohon, Philippe ^a   Légaré, Danielle ^a   Raymond, Frédéric ^a   Madore, Éric ^a   Hardiman, Gary ^b   Corbeil, Jacques ^a   Ouellette, Marc ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY;

ANEUPLOIDY; ARTICLE; CHROMOSOME; CHROMOSOME 23; CHROMOSOME LOSS; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; GENE AMPLIFICATION; GENE CASSETTE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE NUMBER; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC RESISTANCE; GENOME ANALYSIS; HAPLOIDY; LEISHMANIA INFANTUM; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SOUTHERN BLOTTING; STRAIN DIFFERENCE; SUPERNUMERARY CHROMOSOME;

ANEUPLOIDY; ANIMALS; ANTIMONY; DRUG RESISTANCE; GENE AMPLIFICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LEISHMANIA INFANTUM; MONOSOMY; MUTATION; TRYPANOCIDAL AGENTS;

LEISHMANIA INFANTUM; PROTOZOA;

EID: 63249133197     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn1069     Document Type: Article

References (70)

1. Murray,H.W., Berman,J.D., Davies,C.R. and Saravia,N.G. (2005) Advances in leishmaniasis. Lancet., 366, 1561-1577.
2. Hadighi,R., Mohebali,M., Boucher,P., Hajjaran,H., Khamesipour,A. and Ouellette,M. (2006) Unresponsiveness to glucantime treatment in Iranian cutaneous leishmaniasis due to drug-resistant Leishmania tropica parasites. PLoS Med., 3, e162.
3. Lira,R., Sundar,S., Makharia,A., Kenney,R., Gam,A., Saraiva,E. and Sacks,D. (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.
4. Rojas,R., Valderrama,L., Valderrama,M., Varona,M.X., Ouellette,M. and Saravia,N.G. (2006) Resistance to antimony and treatment failure in human Leishmania (Viannia) infection. J. Infect. Dis., 193, 1375-1383.
5. Croft,S.L., Sundar,S. and Fairlamb,A.H. (2006) Drug resistance in leishmaniasis. Clin. Microbiol. Rev., 19, 111-126.
6. Jha,T.K., Olliaro,P., Thakur,C.P., Kanyok,T.P., Singhania,B.L., Singh,I.J., Singh,N.K., Akhoury,S. and Jha,S. (1998) Randomised controlled trial of aminosidine (paromomycin) v sodium stibogluconate for treating visceral leishmaniasis in North Bihar, India. Br. Med. J., 316, 1200-1205.
7. Perez-Victoria,F.J., Gamarro,F., Ouellette,M. and Castanys,S., (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.
8. Ouellette,M., Drummelsmith,J. and Papadopoulou,B. (2004) Leishmaniasis: drugs in the clinic, resistance and new developments. Drug Resist. Updat., 7, 257-266.
9. Sundar,S. and Rai,M. (2005) Treatment of visceral leishmaniasis. Expert Opin. Pharmacother., 6, 2821-2829.
10. Berman,J. (2003) Current treatment approaches to leishmaniasis. Curr. Opin. Infect. Dis., 16, 397-401.
11. Croft,S.L. and Coombs,G.H. (2003) Leishmaniasis - current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol. 19, 502-508.
12. Shaked-Mishan,P., Ulrich,N., Ephros,M. and Zilberstein,D. (2001) Novel Intracellular SbV reducing activity correlates with antimony susceptibility in Leishmania donovani. J. Biol. Chem., 276, 3971-3976.
13. Gourbal,B., Sonuc,N., Bhattacharjee,H., Legare,D., Sundar,S., Ouellette,M., Rosen,B.P. and Mukhopadhyay,R. (2004) Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. J. Biol. Chem., 279, 31010-31017.
14. Marquis,N., Gourbal,B., Rosen,B.P., Mukhopadhyay,R. and Ouellette,M. (2005) Modulation in aquaglyceroporin AQP1 gene transcript levels in drug-resistant Leishmania. Mol. Microbiol., 57, 1690-1699.
15. Fairlamb,A.H. and Cerami,A. (1992) Metabolism and functions of trypanothione in the Kinetoplastida. Annu. Rev. Microbiol., 46 695-729.
16. Grondin,K., Haimeur,A., Mukhopadhyay,R., Rosen,B.P. and 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.
17. Guimond,C., Trudel,N., Brochu,C., Marquis,N., El Fadili,A., Peytavi,R., Briand,G., Richard,D., Messier,N., Papadopoulou,B. et al. (2003) Modulation of gene expression in Leishmania drug resistant mutants as determined by targeted DNA microarrays. Nucleic Acids Res., 31 5886-5896.
18. Haimeur,A., Brochu,C., Genest,P., Papadopoulou,B. and Ouellette,M. (2000) Amplification of the ABC transporter gene PGPA and increased trypanothione levels in potassium antimonyl tartrate (SbIII) resistant Leishmania tarentolae. Mol. Biochem. Parasitol., 108, 131-135.
19. Haimeur,A., Guimond,C., Pilote,S., Mukhopadhyay,R., Rosen,B.P., Poulin,R. and Ouellette,M. (1999) Elevated levels of polyamines and trypanothione resulting from overexpression of the ornithine decarboxylase gene in arsenite-resistant Leishmania. Mol. Microbiol. 34, 726-735.
20. Legare,D., Papadopoulou,B., Roy,G., Mukhopadhyay,R., Haimeur,A., Dey,S., Grondin,K., Brochu,C., Rosen,B.P. and Ouellette,M. (1997) Efflux systems and increased trypanothione levels in arsenite-resistant Leishmania. Exp. Parasitol., 87, 275-282.
21. Mukhopadhyay,R., Dey,S., Xu,N., Gage,D., Lightbody,J., Ouellette,M. and Rosen,B.P. (1996) Trypanothione overproduction and resistance to antimonials and arsenicals in Leishmania. Proc. Natl Acad. Sci. USA 93, 10383-10387.
22. Mandal,G., Wyllie,S., Singh,N., Sundar,S., Fairlamb,A.H. and Chatterjee,M. (2007) Increased levels of thiols protect antimony unresponsive Leishmania donovani field isolates against reactive oxygen species generated by trivalent antimony. Parasitology, 134, 1679-1687.
23. Wyllie,S., Cunningham,M.L. and Fairlamb,A.H. (2004) Dual action of antimonial drugs on thiol redox metabolism in the human pathogen Leishmania donovani. J. Biol. Chem., 279, 39925-39932.
24. Grondin,K., Papadopoulou,B. and Ouellette,M. (1993) Homologous recombination between direct repeat sequences yields P-glycoprotein containing amplicons in arsenite resistant Leishmania. Nucleic Acids Res., 21, 1895-1901.
25. Ouellette,M., Hettema,E., Wust,D., Fase-Fowler,F. and Borst,P. (1991) Direct and inverted DNA repeats associated with P-glycoprotein gene amplification in drug resistant Leishmania. EMBO J., 10, 1009-1016.
26. Brochu,C., Haimeur,A. and Ouellette,M. (2004) The heat shock protein HSP70 and heat shock cognate protein HSC70 contribute to antimony tolerance in the protozoan parasite leishmania. Cell Stress Chaperones, 9, 294-303.
27. Vergnes,B., Gourbal,B., Gitard,I., Sundar,S., Drummelsmith,J. and Ouellette,M. (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.
28. Genest,P.A., Haimeur,A., Legare,D., Seteno,D., Roy,G., Messier,N., Papadopoulou,B. and Ouellette,M. (2008) A protein of the leucine-rich repeats (LRRs) superfamily is implicated in antimony resistance in Leishmania infanturn amastigotes. Mol. Biochem. Parasitol., 158 95-99.
29. Singh,N., Singh,R.T. and Sundar,S. (2003) Novel mechanism of drug resistance in kala azar field isolates. J. Infect. Dis., 188 600-607.
30. Wyllie,S., Vickers,T.J. and Fairlamb,A.H. (2008) Roles of trypanothione S-transferase and tryparedoxin peroxidase in resistance to antimonials. Antimicrob. Agents Chemother., 52, 1359-1365.
31. Choudhury,K., Zander,D., Kube,M., Reinhardt,R. and Clos,J. (2008) Identification of a Leishmania infantum gene mediating resistance to miltefosine and SbIII. Int. J. Parasitol., 38, 1411-1423.
32. Decuypere,S., Rijal,S., Yardley,V., De Doncker,S., Laurent,T., Khanal,B., Chappuis,F., and Dujardin,J.C. (2005) Gene expression analysis of the mechanism of natural Sb(V) resistance in Leishmania donovani isolates from Nepal. Antimicrob. Agents Chemother., 49 4616-4621.
33. Mukherjee,A., Padmanabhahan,P.K., Singh,S., Roy,G., Girard,I., Chatterjee,M., Ouellette,M. and Madhubala,R. (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.
34. Goyeneche-Patino,D.A., Valderrama,L., Walker,J. and Saravia,N.G. (2008) Antimony resistance and trypanothione in experimentally selected and clinical strains of Leishmania panamensis. Antimicrob. Agents Chemother., 52, 4503-4506.
35. Mittal,M.K., Rai,S., Ashutosh, Ravinder, Gupta,S., Sundar,S. and Goyal,N. (2007) Characterization of natural antimony resistance in Leishmania donovani isolates. Am. J. Trop. Med. Hyg., 76, 681-688.
36. Singh,N., Almeida,R., Kothari,H., Kumar,P., Mandal,G., Chatterjee,M., Venkatachalam,S., Govind,M.K., Mandal,S.K. and Sundar,S. (2007) Differential gene expression analysis in antimony-unresponsive Indian kala azar (visceral leishmaniasis) clinical isolates by DNA microarray. Parasitology, 134, 777-787.
37. El-Fadili,K., Messier,N., Leprohon,P., Roy,G., Guimond,C., Trudel,N., Saravia,N.G., Papadopoulou,B., Legare,D. and Ouellette,M. (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. Leprohon,P., Legare,D., Girard,I., Papadopoulou,B. and Ouellette,M. (2006) Modulation of Leishmania ABC protein gene, expression through life stages and among drug-resistant parasites. Eukaryot. Cell, 5, 1713-1725.
39. Rochette,A., Raymond,F., Ubeda,J.M., Smith,M., Messier,N., Boisvert,S., Rigault,P., Corbeil,J., Ouellette,M. and Papadopoulou,B. (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.
40. Ubeda,J.M., Legare,D., Raymond,F., Ouameur,A.A., Boisvert,S., Rigault,P., Corbeil,J., Tremblay,M.J., Olivier,M., Papadopoulou,B. et al. (2008) Modulation of gene expression in drug resistant Leishmama is associated with gene amplification, gene deletion and chromosome aneuploidy. Genome Biol., 9, R115.
41. Papadopoulou,B., Roy,G. and Ouellette,M. (1992) A novel antifolate resistance gene on the amplified H circle of Leishmania. EMBO J., 11, 3601-3608.
42. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning Cold Spring Harbor Laboratory Press, New York.
43. Papadopoulou,B., Roy,G., Dey,S., Rosen,B.P. and Ouellette,M. (1994) Contribution of the Leishmania P-glycoprotein-related gene ltpgpA to oxyanion resistance. J. Biol. Chem., 269, 11980-11986.
44. Ivens,A.C., Peacock,C.S., Worthey,E.A., Murphy,L., Aggarwal,G., Berriman,M., Sisk,E., Rajandream,M.A., Adlem,E., Aert,R. et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science, 309, 436-442.
45. Peacock,C.S., Seeger,K., Harris,D., Murphy,L., Ruiz,J.C., Quail,M.A., Peters,N., Adlem,E., Tivey,A., Aslett,M. et al. (2007), Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat. Genet., 39, 839-847.
46. Smyth,G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, Article 3.
47. Smyth,G.K., Michaud,J. and Scott,H.S. (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics, 21, 2067-2075.
48. Smyth,G.K. and Speed,T. (2003) Normalization of cDNA microarray data. Methods, 31, 265-273.
49. Grondin,K., Roy,G. and Ouellette,M. (1996) Formation of extra-chromosomal circular amplicons with direct or inverted duplications in drug-resistant Leishmania tarentolae. Mol. Cell. Biol., 16, 3587-3595.
50. Beverley,S.M, (1991) Gene amplification in Leishmania, Annu. Rev. Microbiol., 45, 417-444.
51. Selmecki,A., Forche,A. and Berman,J. (2006) Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science, 313, 367-370.
52. Holzer,T.R., McMaster,W.R. and Forney,J.D. (2006) Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. Mol. Biochem. Parasitol., 146, 198-218.
53. Leifso,K., Cohen-Freue,G., Dogra,N., Murray,A. and McMaster,W.R. (2007) Genomic and proteomic expression analysis of Leishmania promastigote and amastigote life stages: The Leishmania genome is constitutively expressed. Mol. Biochem. Parasitol., 152, 35-46.
54. Saxena,A., Lahav,T., Holland,N., Aggarwal,G., Anupama,A., Huang,Y., Volpin,H., Myler,P.J. and Zilberstein,D. (2007) Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation. Mol. Biochem. Parasitol., 152, 53-65.
55. Liu,X. and Chang,K.P. (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.
56. Chow,L.M., Wong,A.K., Ullman,B. and Wirth,D.F. (1993) Cloning and functional analysis of an extrachromosomally amplified multi-drug resistance-like gene in Leishmania enriettii. Mol. Biochem. Parasitol., 60, 195-208.
57. Clayton,C.E. (2002) Life without transcriptional control? From fly to man and back again. EMBO J., 21, 1881-1888.
58. Lukes,J., Mauricio,I.L., Schonian,G., Dujardin,J.C., Soteriadou,K., Dedet,J.P., Kuhls,K., Tintaya,K.W., Jirku,M., Chocholova,E. et al. (2007) Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proc. Natl Acad. Sci. USA, 104, 9375-9380.
59. Cruz,A.K., Titus,R. and Beverley,S.M. (1993) Plasticity in chromosome number and testing of essential genes in Leishmania by targeting. Proc. Natl Acad. Sci. USA, 90, 1599-1603.
60. Martinez-Calvillo, S., Stuart,K. and Myler,P.J. (2005) Ploidy changes associated with disruption of two adjacent genes on Leishmania major chromosome 1. Int. J. Parasitol., 35, 419-429.
61. Coste,A., Selmecki,A., Forche,A., Diogo,D., Bougnoux,M.E., d'Enfert,C., Berman,J. and Sanglard,D. (2007) Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot. Cell 6, 1889-1904.
62. Doubre,H., Cesari,D., Mairovitz,A., Benac,C., Chantot-Bastaraud,S., Dagnon,K., Antoine,M., Danel,C., Bernaudin,J.F. and Fleury-Feith,J. (2005) Multidrug resistance-associated protein (MRP1) is overexpressed in DNA aneuploid carcinomatous cells in non-small cell lung cancer (NSCLC). Int. J. Cancer, 113, 568-574.
63. Tamar,S. and Papadopoulou,B. (2001) A telomere-mediated chromosome fragmentation approach to assess mitotic stability and ploidy alterations of Leishmania chromosomes. J. Biol. Chem., 276, 11662-11673.
64. Yih,L.H., Ho,I.C. and Lee,T.C. (1997) Sodium arsenite disturbs mitosis and induces chromosome loss in human fibroblasts. Cancer Res., 57, 5051-5059.
65. Wang,Y., O'Brate,A., Zhou,W. and Giannakakou,P. (2005) Resistance to microtubule-stabilizing drugs involves two events: Beta-tubulin mutation in one allele followed by loss of the second allele. Cell Cycle, 4, 1847-1853.
66. Tseng,Y.Y., Yu,C.W. and Liao,V.H. (2007) Caenorhabditis elegans expresses a functional ArsA. FEBS J., 274, 2566-2572.
67. McNicoll,F., Muller,M., Cloutier,S., Boilard,N., Rochette,A., Dube,M. and Papadopoulou,B. (2005) Distinct, 3′-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J. Biol. Chem., 280, 35238-35246.
68. Bringaud,F., Muller,M., Cerqueira,G.C., Smith,M., Rochette,A., El-Sayed,N.M., Papadopoulou,B. and Ghedin,E. (2007) Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog., 3, 1291-1307.
69. Subhi,A.L., Diegelman,P., Porter,C.W., Tang,B., Lu,Z.J., Markham,G.D. and Kruger,W.D. (2003) Methylthioadenosine phosphorylase regulates ornithine decarboxylase by production of downstream metabolites. J. Biol. Chem., 278, 49868-49873.
70. Hughes,T.R., Roberts,C.J., Dai,H., Jones,A.R., Meyer,M.R., Slade, D., Burchard,J., Dow,S., Ward,T.R., Kidd,M.J. et al. (2000) Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet., 25, 333-337.