The heat shock protein HSP70 and heat shock cognate protein HSC70 contribute to antimony tolerance in the protozoan parasite Leishmania

Cell Stress and Chaperones

Volumn 9, Issue 3, 2004, Pages 294-303

  Brochu, Christian ^a   Halmeur, Anass ^a,b   Ouellette, Marc ^a  

^a LAVAL UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY; ANTIMONY TARTRATE; ARSENIC TRIOXIDE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 70;

AMASTIGOTE; ANIMAL CELL; ARTICLE; COSMID; DRUG MECHANISM; DRUG TOLERANCE; GENE OVEREXPRESSION; LEISHMANIA TARENTOLAE; LEISHMANIASIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN SYNTHESIS;

ANIMALS; ANTIMONY; ANTIMONY POTASSIUM TARTRATE; COSMIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE; GENE EXPRESSION; HSC70 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; LEISHMANIA; LEISHMANIASIS; STRESS; TRANSFECTION;

ANIMALIA; LEISHMANIA TARENTOLAE; PROTOZOA;

EID: 7644219918     PISSN: 13558145     EISSN: None     Source Type: Journal    
DOI: 10.1379/CSC-15R1.1     Document Type: Article

References (49)

1. Argaman M, Aly R, Shapira M. 1994. Expression of heat shock protein 83 in Leishmania is regulated post-transcriptionally. Mol Biochem Parasitol 64: 95-110.
2. Berman J. 2003. Current treatment approaches to leishmaniasis. Curr Opin Infect Dis 16: 397-401.
3. Brandau S, Dresel A, Clos J. 1995. High constitutive levels of heat-shock proteins in human-pathogenic parasites of the genus Leishmania. Biochem J 310: 225-232.
4. Brochu C, Wang J, Roy G, Messier N, Wang XY, Saravia NG, Ouellette M. 2003. Antimony uptake systems in the protozoan parasite Leishmania and accumulation differences in antimony-resistant parasites. Antimicrob Agents Chemother 47: 3073-3079.
5. Brun R, Schonenberger M. 1979. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop 36: 289-292.
6. Chou CC, Forouhar F, Yeh YH, Shr HL, Wang C, Hsiao CD. 2003. Crystal structure of the C-terminal 10-kDa subdomain of Hsc70. J Biol Chem 278: 30311-30316.
7. Cotrim PC, Garrity LK, Beverley SM. 1999. Isolation of genes mediating resistance to inhibitors of nucleoside and ergosterol metabolism in Leishmania by overexpression/selection. J Biol Chem 274: 37723-37730.
8. Del Razo LM, Quintanilla-Vega B, Brambila-Colombres E, Calderon-Aranda ES, Manno M, Albores A. 2001. Stress proteins induced by arsenic. Toxicol Appl Pharmacol 177: 132-148.
9. Dey S, Ouellette M, Lightbody J, Papadopoulou B, Rosen BP. 1996. An ATP-dependent As(III)-glutathione transport system in membrane vesicles of Leishmania tarentolae. Proc Natl Acad Sci U S A 93: 2192-2197.
10. Dey S, Papadopoulou B, Haimeur A, Roy G, Grondin K, Dou D, Rosen BP, Ouellette M. 1994. High level arsenite resistance in Leishmania tarentolae is mediated by an active extrusion system. Mol Biochem Parasitol 67: 49-57.
11. Fairlamb AH, Cerami A. 1992. Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 46: 695-729.
12. Grondin K, Haimeur A, Mukhopadhyay R, Rosen BP, 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.
13. 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.
14. Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, Wasunna MK, Bryceson AD. 2002. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect Dis 2: 494-501.
15. Guimond C, Trudel N, Brochu C, et al. 2003. Modulation of gene expression in Leishmania drug resistant mutants as determined by targeted DNA microarrays. Nucleic Acids Res 31: 5886-5896.
16. Haimeur A, Brochu C, Genest P, Papadopoulou B, 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.
17. Haimeur A, Guimond C, Pilote S, Mukhopadhyay R, Rosen BP, Poulin R, 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.
18. Haimeur A, Ouellette M. 1998. Gene amplification in Leishmania tarentolae selected for resistance to sodium stibogluconate. Antimicrob Agents Chemother 42: 1689-1694.
19. Harlow E, Lane D. 1988. Antibodies, a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Hartl FU, Hayer-Hartl M. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858.
21. Herwaldt BL. 1999. Leishmaniasis. Lancet 354: 1191-1199.
22. Hunter KW, Cook CL, Hayunga EG. 1984. Leishmanial differentiation in vitro: induction of heat shock proteins. Biochem Biophys Res Commun 125: 755-760.
23. Kiang JG, Tsokos GC. 1998. Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 80: 183-201.
24. Kündig C, Haimeur A, Légaré D, Papadopoulou B, Ouellette M. 1999. Increased transport of pteridines compensates for mutations in the high affinity folate transporter and contributes to methotrexate resistance in the protozoan parasite Leishmania tarentolae. Embo J 18: 2342-2351.
25. Lawrence F, Robert-Gero M. 1985. Induction of heat shock and stress proteins in promastigotes of three Leishmania species. Proc Natl Acad Sci USA 82: 4414-4417.
26. Lee MG. 1998. The 3′ untranslated region of the hsp 70 genes maintains the level of steady state mRNA in Trypanosoma brucei upon heat shock. Nucleic Acids Res 26: 4025-4033.
27. Légaré D, Richard D, Mukhopadhyay R, Stierhof YD, Rosen BP, Haimeur A, Papadopoulou B, Ouellette M. 2001. The Leishmania ABC protein PGPA is an intracellular metal-thiol transporter ATPase. J Biol Chem 276: 26301-26307.
28. Miller MA, McGowan SE, Gantt KR, et al. 2000. Inducible resistance to oxidant stress in the protozoan Leishmania chagasi. J Biol Chem 275: 33883-33889.
29. Morimoto RI, Santoro MG. 1998. Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat Biotechnol 16: 833-838.
30. Murray HW. 2001. Clinical and experimental advances in treatment of visceral leishmaniasis. Antimicrob Agents Chemother 45: 2185-2197.
31. Ouellette M, Hettema E, Wust D, Fase-Fowler F, Borst P. 1991. Direct and inverted DNA repeats associated with P-glycoprotein gene amplification in drug resistant Leishmania. Embo J 10: 1009-1016.
32. Papadopoulou B, Roy G, Dey S, Rosen BP, Ouellette M. 1994. Contribution of the Leishmania P-glycoprotein-related gene ItpgpA to oxyanion resistance. J Biol Chem 269: 11980-11986.
33. Papadopoulou B, Roy G, Ouellette M. 1992. A novel antifolate resistance gene on the amplified H circle of Leishmania. Embo J 11: 3601-3608.
34. Perez-Victoria FJ, Gamarro F, Ouellette M, 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.
35. Quijada L, Requena JM, Soto M, Alonso C. 1998. Analysis of the antigenic properties of the L. infantum Hsp70: design of synthetic peptides for specific serodiagnosis of human leishmaniasis. Immunol Lett 63: 169-174.
36. Quijada L, Soto M, Alonso C, Requena JM. 1997. Analysis of post-transcriptional regulation operating on transcription products of the tandemly linked Leishmania infantum hsp70 genes. J Biol Chem 272: 4493-4499.
37. Quijada L, Soto M, Alonso C, Requena JM. 2000. Identification of a putative regulatory element in the 3′-untranslated region that controls expression of HSP70 in Leishmania infantum. Mol Biochem Parasitol 110: 79-91.
38. Ryan KA, Dasgupta S, Beverley SM. 1993. Shuttle cosmid vectors for the trypanosomatid parasite Leishmania. Gene 131: 145-150.
39. Sereno D, Cavaleyra M, Zemzoumi K, Maquaire S, Ouaissi A, Lemesre JL. 1998. Axenically grown amastigotes of Leishmania infantum used as an in vitro model to investigate the pentavalent antimony mode of action. Antimicrob Agents Chemother 42: 3097-3102.
40. Shaked-Mishan P, Ulrich N, Ephros M, Zilberstein D. 2001. Novel intracellular SbV reducing activity correlates with antimony susceptibility in Leishmania donovani. J Biol Chem 276: 3971-3976.
41. Singh N, Singh RT, Sundar S. 2003. Novel mechanism of drug resistance in kala azar field isolates. J Infect Dis 188: 600-607.
42. Snawder JE, Tirmenstein MA, Mathias PI, Toraason M. 1999. Induction of stress proteins in rat cardiac myocytes by antimony. Toxicol Appl Pharmacol 159: 91-97.
43. Swofford DL. 2003. PAUP* Phylogenetic Analysis Using Parsimony* and Other Methods, Version 4. Sinauer Associates, Sunderland, MA.
44. Tamar S, 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.
45. Vasudevan G, Carter NS, Drew ME, Beverley SM, Sanchez MA, Seyfang A, Ullman B, Landfear SM. 1998. Cloning of Leishmania nucleoside transporter genes by rescue of a transport-deficient mutant. Proc Natl Acad Sci U S A 95: 9873-9878.
46. White TC, Fase-Fowler F, van Luenen H, Calafat J, Borst P. 1988. The H circles of Leishmania tarentolae are a unique amplifiable system of oligomeric DNAs associated with drug resistance. J Biol Chem 263: 16977-16983.
47. Wiesgigl M, Clos J. 2001. Heat shock protein 90 homeostasis controls stage differentiation in Leishmania donovani. Mol Biol Cell 12: 3307-3316.
48. Zilberstein D, Shapira M. 1994. The role of pH and temperature in the development of Leishmania parasites. Annu Rev Microbiol 48: 449-470.
49. Zurita AI, Rodriguez J, Pinero JE, Pacheco R, Carmelo E, del Castllo A, Valladares B. 2003. Cloning and characterization of the Leishmania (Viannia) braziliensis Hsp70 gene. Diagnostic use of the C-terminal fragment rLb70(513-663). J Parasitol 89: 372-378.