Farnesyl diphosphate synthase is a cytosolic enzyme in Leishmania major promastigotes and its overexpression confers resistance to risedronate

Eukaryotic Cell

Volumn 5, Issue 7, 2006, Pages 1057-1064

  Ortiz Gómez, Aurora ^a   Jiménez, Carmen ^a   Estévez, Antonio M ^a   Carrero Lérida, Juana ^a   Ruiz Pérez, Luis M ^a   González Pacanowska, Dolores ^a  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG DERIVATIVE; ETIDRONIC ACID; GERANYLTRANSFERASE; RECOMBINANT PROTEIN; RISEDRONIC ACID;

ANIMAL; ARTICLE; CHEMISTRY; CYTOSOL; DRUG RESISTANCE; ENZYMOLOGY; GENETIC SELECTION; GENETIC TRANSFECTION; LEISHMANIA MAJOR; PHYSIOLOGY; TISSUE DISTRIBUTION;

ANIMALS; CYTOSOL; DRUG RESISTANCE; ETIDRONIC ACID; GERANYLTRANSTRANSFERASE; LEISHMANIA MAJOR; RECOMBINANT PROTEINS; SELECTION (GENETICS); TISSUE DISTRIBUTION; TRANSFECTION;

LEISHMANIA MAJOR;

EID: 33746218929     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00034-06     Document Type: Article

References (58)

1. Bergstrom, J. D., R. G. Bostedor, P. J. Masarachia, A. A. Reszka, and G. Rodan. 2000. Alendronate is a specific, nanomolar inhibitor of farnesyl diphosphate synthase. Arch. Biochem. Biophys. 373:231-241.
2. Biardi, L., and S. K. Krisans. 1996. Compartmentalization of cholesterol biosynthesis. Conversion of mevalonate to farnesyl diphosphate occurs in the peroxisomes. J. Biol. Chem. 271:1784-1788.
3. Bora, D. 1999. Epidemiology of visceral leishmaniasis in India. Natl. Med. J. India 12:62-68.
4. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
5. Brown, D. L., and R. Robbins. 1999. Developments in the therapeutic applications of bisphosphonates. J. Clin. Pharmacol. 39:651-660.
6. Brown, R. J., E. van Beek, D. J. Watts, C. W. Lowik, and S. E. Papapoulos. 1998. Differential effects of aminosubstituted analogs of hydroxy bisphosphonates on the growth of Dictyostelium discoideum. J. Bone Miner. Res. 13:253-258.
7. Callens, M., D. A. Kuntz, and F. R. Opperdoes. 1991. Characterization of pyruvate kinase of Trypanosoma brucei and its role in the regulation of carbohydrate metabolism. Mol. Biochem. Parasitol. 47:19-29.
8. Camacho, A., R. Arrebola, J. Pena-Diaz, L. M. Ruiz-Perez, and D. Gonzalez-Pacanowska. 1997. Description of a novel eukaryotic deoxyuridine 5′-triphosphate nucleotidohydrolase in Leishmania major. Biochem. J. 325:441-447.
9. Chudzik, D. M., P. A. Michels, S. de Walque, and W. G. Hol. 2000. Structures of type 2 peroxisomal targeting signals in two trypanosomatid aldolases. J. Mol. Biol. 300:697-707.
10. Concepcion, J. L., D. Gonzalez-Pacanowska, and J. A. Urbina. 1998. 3-Hydroxy-3-methyl-glutaryl-CoA reductase in Trypanosoma (Schizotrypanum) cruzi: subcellular localization and kinetic properties. Arch. Biochem. Biophys. 352:114-120.
11. Croft, S. L., and G. H. Coombs. 2003. Leishmaniasis-current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol. 19:502-508.
12. Cromartie, T. H., K. J. Fisher, and J. N. Grossman. 1999. The discovery of a novel site of action for herbicidal bisphosphonates. Pestic. Biochem. Physiol. 63:114-126.
13. Cunillera, N., A. Boronat, and A. Ferrer. 1997. The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J. Biol. Chem. 272:15381-15388.
14. Desjeux, P. 2004. Leishmaniasis: current situation and new perspectives. Comp. Immunol. Microbiol. Infect. Dis. 27:305-318.
15. 2+ storage compartment in trypanosomatids and apicomplexan parasites. Parasitol. Today 15:443-448.
16. Dunford, J. E., K. Thompson, F. P. Coxon, S. P. Luckman, F. M. Hahn, C. D. Poulter, F. H. Ebetino, and M. J. Rogers. 2001. Structure-activity relationships for inhibition of farnesyl diphosphate synthase in vitro and inhibition of bone resorption in vivo by nitrogen-containing bisphosphonates. J. Pharmacol. Exp. Ther. 296:235-242.
17. Gabelli, S. B., J. S. McLellan, A. Montalvetti, E. Oldfield, R. Docampo, and L. M. Amzel. 2006. Structure and mechanism of the farnesyl diphosphate synthase from Trypanosoma cruzi: implications for drug design. Proteins 62:80-88.
18. Ginger, M. L., M. L. Chance, I. H. Sadler, and L. J. Goad. 2001. The biosynthetic incorporation of the intact leucine skeleton into sterol by the trypanosomatid Leishmania mexicana. J. Biol. Chem. 276:11674-11682.
19. Grove, J. E., R. J. Brown, and D. J. Watts. 2000. The intracellular target for the antiresorptive aminobisphosphonate drugs in Dictyostelium discoideum is the enzyme farnesyl diphosphate synthase. J. Bone Miner. Res. 15:971-981.
20. Guerra-Giraldez, C., L. Quijada, and C. E. Clayton. 2002. Compartmentation of enzymes in a microbody, the glycosome, is essential in Trypanosoma brucei. J. Cell Sci. 115:2651-2658.
21. Hogenboom, S., J. J. Tuyp, M. Espeel, J. Koster, R. J. Wanders, and H. R. Waterham. 2004. Mevalonate kinase is a cytosolic enzyme in humans. J. Cell Sci. 117:631-539.
22. Hogenboom, S., J. J. Tuyp, M. Espeel, J. Koster, R. J. Wanders, and H. R. Waterham. 2004. Phosphomevalonate kinase is a cytosolic protein in humans. J. Lipid Res. 45:697-705.
23. Hudock, M. P., C. E. Sanz-Rodriguez, Y. Song, J. M. Chan, Y. Zhang, S. Odeh, T. Kosztowski, A. Leon-Rossell, J. L. Concepcion, V. Yardley, S. L. Croft, J. A. Urbina, and E. Oldfield. 2006. Inhibition of Trypanosoma cruzi hexokinase by bisphosphonates. J. Med. Chem. 49:215-223.
24. Hugueney, P., F. Bouvier, A. Badillo, J. Quennemet, A. d'Harlingue, and B. Camara. 1996. Developmental and stress regulation of gene expression for plastid and cytosolic isoprenoid pathways in pepper fruits. Plant Physiol. 111:619-626.
25. Keller, R. K., and S. J. Fliesler. 1999. Mechanism of aminobisphosphonate action: characterization of alendronate inhibition of the isoprenoid pathway. Biochem. Biophys. Res. Commun. 266:560-563.
26. Kotsikorou, E., Y. Song, J. M. Chan, S. Faelens, Z. Tovian, E. Broderick, N. Bakalara, R. Docampo, and E. Oldfield. 2005. Bisphosphonate inhibition of the exopolyphosphatase activity of the Trypanosoma brucei soluble vacuolar pyrophosphatase. J. Med. Chem. 48:6128-6139.
27. Kovacs, W. J., and S. Krisans. 2003. Cholesterol biosynthesis and regulation: role of peroxisomes. Adv. Exp. Med. Biol. 544:315-327.
28. Koyama, T. 1999. Molecular analysis of prenyl chain elongating enzymes. Biosci. Biotechnol. Biochem. 63:1671-1676.
29. Kunzmann, V., E. Bauer, J. Feurle, F. Weissinger, H. P. Tony, and M. Wilhelm. 2000. Stimulation of gammadelta T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood 96:384-392.
30. LeBowitz, J. H., C. M. Coburn, D. McMahon-Pratt, and S. M. Beverley. 1990. Development of a stable Leishmania expression vector and application to the study of parasite surface antigen genes. Proc. Natl. Acad. Sci. USA 87:9736-9740.
31. Ling, Y., G. Sahota, S. Odeh, J. M. Chan, F. G. Araujo, S. N. Moreno, and E. Oldfield. 2005. Bisphosphonate inhibitors of Toxoplasma gondii growth: in vitro, QSAR, and in vivo investigations. J. Med. Chem. 48:3130-3140.
32. Marchesini, N., F. A. Ruiz, M. Vieira, and R. Docampo. 2002. Acidocalcisomes are functionally linked to the contractile vacuole of Dictyostelium discoideum. J. Biol. Chem. 277:8146-8153.
33. Martin, M. B., J. S. Grimley, J. C. Lewis, H. T. Heath III, B. N. Bailey, H. Kendrick, V. Yardley, A. Caldera, R. Lira, J. A. Urbina, S. N. Moreno, R. Docampo, S. L. Croft, and E. Oldfield. 2001. Bisphosphonates inhibit the growth of Trypanosoma brucei, Trypanosoma cruzi, Leishmania donovani, Toxoplasma gondii, and Plasmodium falciparum: a potential route to chemotherapy. J. Med. Chem. 44:909-916.
34. Massarini, E., and J. J. Cazzulo. 1975. Two forms of citrate synthase in a marine pseudomonad. FEBS Lett. 57:134-138.
35. Montalvetti, A., B. N. Bailey, M. B. Martin, G. W. Severin, E. Oldfield, and R. Docampo. 2001. Bisphosphonates are potent inhibitors of Trypanosoma cruzi farnesyl pyrophosphate synthase. J. Biol. Chem. 276:33930-33937.
36. Montalvetti, A., A. Fernandez, J. M. Sanders, S. Ghosh, E. Van Brussel, E. Oldfield, and R. Docampo. 2003. Farnesyl pyrophosphate synthase is an essential enzyme in Trypanosoma brucei. In vitro RNA interference and in vivo inhibition studies. J. Biol. Chem. 278:17075-17083.
37. Nakai, K., and P. Horton. 1999. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24:34-36.
38. Olivier, L. M., W. Kovacs, K. Masuda, G. A. Keller, and S. K. Krisans. 2000. Identification of peroxisomal targeting signals in cholesterol biosynthetic enzymes. AA-CoA thiolase, hmg-coa synthase, MPPD, and FPP synthase. J. Lipid Res. 41:1921-1935.
39. Opperdoes, F. R., and J. P. Szikora. 2006. In silico prediction of the glycosomal enzymes of Leishmania major and trypanosomes. Mol. Biochem. Parasitol. 147:193-206.
40. Pena-Diaz, J., A. Montalvetti, C. L. Flores, A. Constan, R. Hurtado-Guerrero, W. De Souza, C. Gancedo, L. M. Ruiz-Perez, and D. Gonzalez-Pacanowska. 2004. Mitochondrial localization of the mevalonate pathway enzyme 3-hydroxy-3-methyl-glutaryl-CoA reductase in the Trypanosomatidae. Mol. Biol. Cell 15:1356-1363.
41. Racagni, G. E., and E. E. Machado de Domenech. 1983. Characterization of Trypanosoma cruzi hexokinase. Mol. Biochem. Parasitol. 9:181-188.
42. Rodan, G. A. 1998. Mechanisms of action of bisphosphonates. Annu. Rev. Pharmacol. Toxicol. 38:375-388.
43. Rodan, G. A., and T. J. Martin. 2000. Therapeutic approaches to bone diseases. Science 289:1508-1514.
44. Rodriguez, N., B. N. Bailey, M. B. Martin, E. Oldfield, J. A. Urbina, and R. Docampo. 2002. Radical cure of experimental cutaneous leishmaniasis by the bisphosphonate pamidronate. J. Infect. Dis. 186:138-140.
45. Rogers, M. J., D. J. Watts, and R. G. Russell. 1997. Overview of bisphosphonates. Cancer 80:1652-1660.
46. Rogers, M. J., D. J. Watts, R. G. Russell, X. Ji, X. Xiong, G. M. Blackburn, A. V. Bayless, and F. H. Ebetino. 1994. Inhibitory effects of bisphosphonates on growth of amoebae of the cellular slime mold Dictyostelium discoideum. J. Bone Miner. Res. 9:1029-1039.
47. Rogers, M. J., X. Xiong, R. J. Brown, D. J. Watts, R. G. Russell, A. V. Bayless, and F. H. Ebetino. 1995. Structure-activity relationships of new heterocycle-containing bisphosphonates as inhibitors of bone resorption and as inhibitors of growth of Dictyostelium discoideum amoebae. Mol. Pharmacol. 47:398-402.
48. Sanders, J. M., A. O. Gomez, J. Mao, G. A. Meints, E. M. Van Brussel, A. Burzynska, P. Kafarski, D. Gonzalez-Pacanowska, and E. Oldfield. 2003. 3-D QSAR investigations of the inhibition of Leishmania major farnesyl pyrophosphate synthase by bisphosphonates. J. Med. Chem. 46:5171-5183.
49. Sanmiya, K., O. Ueno, M. Matsuoka, and N. Yamamoto. 1999. Localization of farnesyl diphosphate synthase in chloroplasts. Plant Cell Physiol. 40:348-354.
50. Schlatterer, C., S. Buravkov, K. Zierold, and G. Knoll. 1994. Calcium-sequestering organelles of Dictyostelium discoideum: changes in element content during early development as measured by electron probe X-ray microanalysis. Cell Calcium 16:101-111.
51. Tarshis, L. C., M. Yan, C. D. Poulter, and J. C. Sacchettini. 1994. Crystal structure of recombinant farnesyl diphosphate synthase at 2.6-A resolution. Biochemistry 33:10871-10877.
52. Urbina, J. A., J. L. Concepcion, S. Rangel, G. Visbal, and R. Lira. 2002. Squalene synthase as a chemotherapeutic target in Trypanosoma cruzi and Leishmania mexicana. Mol. Biochem. Parasitol. 125:35-45.
53. Urbina, J. A., B. Moreno, S. Vierkotter, E. Oldfield, G. Payares, C. Sanoja, B. N. Bailey, W. Yan, D. A. Scott, S. N. Moreno, and R. Docampo. 1999. Trypanosoma cruzi contains major pyrophosphate stores, and its growth in vitro and in vivo is blocked by pyrophosphate analogs. J. Biol. Chem. 274:33609-33615.
54. van Beek, E., E. Pieterman, L. Cohen, C. Lowik, and S. Papapoulos. 1999. Nitrogen-containing bisphosphonates inhibit isopentenyl pyrophosphate isomerase/farnesyl pyrophosphate synthase activity with relative potencies corresponding to their antiresorptive potencies in vitro and in vivo. Biochem. Biophys. Res. Commun. 255:491-494.
55. Wilkin, D. J., S. Y. Kutsunai, and P. A. Edwards. 1990. Isolation and sequence of the human farnesyl pyrophosphate synthetase cDNA. Coordinate regulation of the mRNAs for farnesyl pyrophosphate synthetase, 3-hydroxy-3-methylglutaryl coenzyme A reductase, and 3-hydroxy-3-methylglutaryl coenzyme A synthase by phorbol ester. J. Biol. Chem. 265:4607-4614.
56. Yardley, V., A. A. Khan, M. B. Martin, T. R. Slifer, F. G. Araujo, S. N. Moreno, R. Docampo, S. L. Croft, and E. Oldfield. 2002. In vivo activities of farnesyl pyrophosphate synthase inhibitors against Leishmania donovani and Toxoplasma gondii. Antimicrob. Agents Chemother. 46:929-931.
57. Yokoyama, K., P. Trobridge, F. S. Buckner, J. Scholten, K. D. Stuart, W. C. Van Voorhis, and M. H. Gelb. 1998. The effects of protein faraesyltransferase inhibitors on trypanosomatids: inhibition of protein farnesylation and cell growth. Mol. Biochem. Parasitol. 94:87-97.
58. Yokoyama, K., P. Trobridge, F. S. Buckner, W. C. Van Voorhis, K. D. Stuart, and M. H. Gelb. 1998. Protein farnesyltransferase from Trypanosoma brucei. A heterodimer of 61- and 65-kDa subunits as a new target for antiparasite therapeutics. J. Biol. Chem. 273:26497-26505.