Down regulation of KMP-11 in Leishmania infantum axenic antimony resistant amastigotes as revealed by a proteomic screen

Experimental Parasitology

Volumn 123, Issue 1, 2009, Pages 51-57

  El Fadili, Karima ^a   Drummelsmith, Jolyne ^a   Roy, Gaétan ^a   Jardim, Armando ^b   Ouellette, Marc ^a  

^a LAVAL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Drug resistance; Leishmania; Proteomics

Indexed keywords

ANTIMONY; ARGININOSUCCINATE SYNTHASE; MEMBRANE PROTEIN;

AMASTIGOTE; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG RESISTANCE; DRUG SENSITIVITY; FLAGELLATE; GENE EXPRESSION; LEISHMANIA INFANTUM; MASS SPECTROMETRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN EXPRESSION; PROTEOMICS;

ANIMALS; ANTIMONY SODIUM GLUCONATE; ANTIPROTOZOAL AGENTS; ARGININOSUCCINATE SYNTHASE; BLOTTING, NORTHERN; BLOTTING, WESTERN; DOWN-REGULATION; DRUG RESISTANCE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION; LEISHMANIA INFANTUM; MEMBRANE GLYCOPROTEINS; OPEN READING FRAMES; PROTEOMICS; PROTOZOAN PROTEINS; RNA, PROTOZOAN;

KINETOPLASTIDA; LEISHMANIA INFANTUM; PROTOZOA;

EID: 68049132858     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2009.05.013     Document Type: Article

References (51)

1. Berberich C., Machado G., Morales G., Carrillo G., Jimenez-Ruiz A., and Alonso C. The expression of the Leishmania infantum KMP-11 protein is developmentally regulated and stage specific. Biochimica et Biophysica Acta 1442 (1998) 230-237
2. Brochu C., Wang J., Roy G., Messier N., Wang X.Y., Saravia N.G., and Ouellette M. Antimony uptake systems in the protozoan parasite Leishmania and accumulation differences in antimony-resistant parasites. Antimicrobial Agents and Chemotherapy 47 (2003) 3073-3079
3. Croft S.L., Sundar S., and Fairlamb A.H. Drug resistance in leishmaniasis. Clinical Microbiology Reviews 19 (2006) 111-126
4. Cruz A.K., Titus R., and Beverley S.M. Plasticity in chromosome number and testing of essential genes in Leishmania by targeting. Proceedings of the National Academy of Sciences USA 90 (1993) 1599-1603
5. Decuypere S., Rijal S., Yardley V., De Doncker S., Laurent T., Khanal B., Chappuis F., and Dujardin J.C. Gene expression analysis of the mechanism of natural Sb(V) resistance in Leishmania donovani isolates from Nepal. Antimicrobial Agents and Chemotherapy 49 (2005) 4616-4621
6. Denton H., McGregor J.C., and Coombs G.H. Reduction of antileishmanial pentavalent antimonial drugs by a parasite-specific thiol dependent reductase TDR1. Biochemical Journal 381 (2004) 405-412
7. Dey S., Ouellette M., Lightbody J., Papadopoulou B., and Rosen B.P. An ATP-dependent As(III)-glutathione transport system in membrane vesicles of Leishmania tarentolae. Proceedings of the National Academy of Sciences USA 93 (1996) 2192-2197
8. Drummelsmith J., Brochu V., Girard I., Messier N., and Ouellette M. Proteome mapping of the protozoan parasite Leishmania and application to the study of drug targets and resistance mechanisms. Molecular and Cellular Proteomics 2 (2003) 146-155
9. Drummelsmith J., Girard I., Trudel N., and Ouellette M. Differential protein expression analysis of Leishmania major reveals novel roles for methionine adenosyltransferase and S-adenosylmethionine in methotrexate resistance. Journal of Biological Chemistry 279 (2004) 33273-33280
10. Dumas C., Ouellette M., Tovar J., Cunningham M.L., Fairlamb A.H., Tamar S., Olivier M., and Papadopoulou B. Disruption of the trypanothione reductase gene of Leishmania decreases its ability to survive oxidative stress in macrophages. EMBO Journal 16 (1997) 2590-2598
11. El Fadili K., Messier N., Leprohon P., Roy G., Guimond C., Trudel N., Saravia N.G., Papadopoulou B., Legare D., and Ouellette M. Role of the ABC transporter MRPA (PGPA) in antimony resistance in Leishmania infantum axenic and intracellular amastigotes. Antimicrobial Agents and Chemotherapy 49 (2005) 1988-1993
12. Fairlamb A.H., and Cerami A. Metabolism and functions of trypanothione in the Kinetoplastida. Annual Review of Microbiology 46 (1992) 695-729
13. Faraut-Gambarelli F., Piarroux R., Deniau M., Giusiano B., Marty P., Michel G., Faugere B., and 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 41 (1997) 827-830
14. Foucher A.L., Papadopoulou B., and Ouellette M. Prefractionation by digitonin extraction increases representation of the cytosolic and intracellular proteome of Leishmania infantum. Journal of Proteome Research 5 (2006) 1741-1750
15. Fuertes M.A., Berberich C., Lozano R.M., Gimenez-Gallego G., and Alonso C. Folding stability of the kinetoplastid membrane protein-11 (KMP-11) from Leishmania infantum. European Journal of Biochemistry 260 (1999) 559-567
16. Gourbal B., Sonuc N., Bhattacharjee H., Legare D., Sundar S., Ouellette M., Rosen B.P., and Mukhopadhyay R. Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. Journal of Biological Chemistry 279 (2004) 31010-31017
17. Goyeneche-Patino D.A., Valderrama L., Walker J., and Saravia N.G. Antimony resistance and trypanothione in experimentally selected and clinical strains of Leishmania panamensis. Antimicrobial Agents and Chemotherapy 52 (2008) 4503-4506
18. Grondin K., Haimeur A., Mukhopadhyay R., Rosen B.P., and Ouellette M. Co-amplification of the gamma-glutamylcysteine synthetase gene gsh1 and of the ABC transporter gene pgpA in arsenite-resistant Leishmania tarentolae. EMBO Journal 16 (1997) 3057-3065
19. Hadighi R., Mohebali M., Boucher P., Hajjaran H., Khamesipour A., and Ouellette M. Unresponsiveness to glucantime treatment in Iranian cutaneous leishmaniasis due to drug-resistant Leishmania tropica parasites. PLoS Medicine 3 (2006) e162
20. Haimeur A., Brochu C., Genest P., Papadopoulou B., and 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 108 (2000) 131-135
21. Haimeur A., Guimond C., Pilote S., Mukhopadhyay R., Rosen B.P., Poulin R., and Ouellette M. Elevated levels of polyamines and trypanothione resulting from overexpression of the ornithine decarboxylase gene in arsenite-resistant Leishmania. Molecular Microbiology 34 (1999) 726-735
22. Herwaldt B.L. Leishmaniasis. Lancet 354 (1999) 1191-1199
23. Jardim A., Funk V., Caprioli R.M., and Olafson R.W. Isolation and structural characterization of the Leishmania donovani kinetoplastid membrane protein-11, a major immunoreactive membrane glycoprotein. Biochemical Journal 305 (1995) 307-313
24. Jardim A., Hanson S., Ullman B., McCubbin W.D., Kay C.M., and Olafson R.W. Cloning and structure-function analysis of the Leishmania donovani kinetoplastid membrane protein-11. Biochemical Journal 305 (1995) 315-320
25. Jardim A., Tolson D.L., Turco S.J., Pearson T.W., and Olafson R.W. The Leishmania donovani lipophosphoglycan T lymphocyte-reactive component is a tightly associated protein complex. Journal of Immunology 147 (1991) 3538-3544
26. Jayanarayan K.G., and Dey C.S. Resistance to arsenite modulates expression of beta- and gamma-tubulin and sensitivity to paclitaxel during differentiation of Leishmania donovani. Parasitology Research 88 (2002) 754-759
27. Légaré D., Richard D., Mukhopadhyay R., Stierhof Y.D., Rosen B.P., Haimeur A., Papadopoulou B., and Ouellette M. The Leishmania ABC protein PGPA is an intracellular metal-thiol transporter ATPase. Journal of Biological Chemistry 276 (2001) 26301-26307
28. Leprohon P., Légaré D., Raymond F., Hardiman G., Corbeil J., and Ouellette M. Gene expression modulation is associated with gene amplification, supernumerary chromosomes and chromosome loss in antimony-resistant Leishmania infantum. Nucleic Acids Research 37 (2009) 1387-1399
29. Li Z., and Wang C.C. KMP-11, a basal body and flagellar protein, is required for cell division in Trypanosoma brucei. Eukaryotic Cell 7 (2008) 1941-1950
30. Lira R., Sundar S., Makharia A., Kenney R., Gam A., Saraiva E., and 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 180 (1999) 564-567
31. Maisnier-Patin S., and Andersson D.I. Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Research Microbiology 155 (2004) 360-369
32. Marquis N., Gourbal B., Rosen B.P., Mukhopadhyay R., and Ouellette M. Modulation in aquaglyceroporin AQP1 gene transcript levels in drug-resistant Leishmania. Molecular Microbiology 57 (2005) 1690-1699
33. Mittal M.K., Rai S., Ashutosh R., Gupta S., Sundar S., and Goyal N. Characterization of natural antimony resistance in Leishmania donovani isolates. American Journal of Tropical Medicine and Hygiene 76 (2007) 681-688
34. Mukherjee A., Padmanabhan P.K., Singh S., Roy G., Girard I., Chatterjee M., Ouellette M., and Madhubala R. Role of ABC transporter MRPA, gamma-glutamylcysteine synthetase and ornithine decarboxylase in natural antimony-resistant isolates of Leishmania donovani. Journal of Antimicrobial Chemotherapy 59 (2007) 204-211
35. Murray H.W., Berman J., Davies C.R., and Saravia N.G. Advances in leishmaniasis. Lancet 366 (2005) 1561-1577
36. Ouellette M., Drummelsmith J., and Papadopoulou B. Leishmaniasis: drugs in the clinic, resistance and new developments. Drug Resistance Updates 7 (2004) 257-266
37. Polevoda B., and Sherman F. Nalpha-terminal acetylation of eukaryotic proteins. Journal of Biological Chemistry 275 (2000) 36479-36482
38. Rosenzweig D., Smith D., Myler P.J., Olafson R.W., and Zilberstein D. Post-translational modification of cellular proteins during Leishmania donovani differentiation. Proteomics 8 (2008) 1843-1850
39. Rosenzweig D., Smith D., Opperdoes F., Stern S., Olafson R.W., and Zilberstein D. Retooling Leishmania metabolism: from sand fly gut to human macrophage. FASEB Journal 22 (2008) 590-602
40. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning (1989), Cold Spring Harbour laboratory, New York
41. Sereno D., Cavaleyra M., Zemzoumi K., Maquaire S., Ouaissi A., and 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 42 (1998) 3097-3102
42. Sereno D., and Lemesre J.L. Axenically cultured amastigote forms as an in vitro model for investigation of antileishmanial agents. Antimicrobial Agents and Chemotherapy 41 (1997) 972-976
43. Sereno D., Roy G., Lemesre J.L., Papadopoulou B., and Ouellette M. DNA transformation of Leishmania infantum axenic amastigotes and their use in drug screening. Antimicrobial Agents and Chemotherapy 45 (2001) 1168-1173
44. Shaked-Mishan P., Ulrich N., Ephros M., and Zilberstein D. Novel intracellular SbV reducing activity correlates with antimony susceptibility in Leishmania donovani. Journal of Biological Chemistry 276 (2001) 3971-3976
45. Singh N., Almeida R., Kothari H., Kumar P., Mandal G., Chatterjee M., Venkatachalam S., Govind M.K., Mandal S.K., and Sundar S. Differential gene expression analysis in antimony-unresponsive Indian kala azar (visceral leishmaniasis) clinical isolates by DNA microarray. Parasitology 134 (2007) 777-787
46. Stebeck C.E., Baron G.S., Beecroft R.P., and Pearson T.W. Molecular characterization of the kinetoplastid membrane protein-11 from African trypanosomes. Molecular and Biochemical Parasitology 81 (1996) 81-88
47. Stebeck C.E., Beecroft R.P., Singh B.N., Jardim A., Olafson R.W., Tuckey C., Prenevost K.D., and Pearson T.W. Kinetoplastid membrane protein-11 (KMP-11) is differentially expressed during the life cycle of African trypanosomes and is found in a wide variety of kinetoplastid parasites. Molecular and Biochemical Parasitology 71 (1995) 1-13
48. Sundar S. Drug resistance in Indian visceral leishmaniasis. Tropical Medicine and International Health 6 (2001) 849-854
49. Thakur C.P., Narayan S., and Ranjan A. Epidemiological, clinical & pharmacological study of antimony-resistant visceral leishmaniasis in Bihar, India. Indian Journal of Medical Research 120 (2004) 166-172
50. Vergnes B., Gourbal B., Girard I., Sundar S., Drummelsmith J., and 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 6 (2007) 88-101
51. Zhou Y., Messier N., Ouellette M., Rosen B.P., and Mukhopadhyay R. Leishmania major LmACR2 is a pentavalent antimony reductase that confers sensitivity to the drug pentostam. Journal of Biological Chemistry 279 (2004) 37445-37451