Tafenoquine, an antiplasmodial 8-aminoquinoline, targets Leishmania respiratory complex III and induces apoptosis

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 12, 2010, Pages 5344-5351

  Carvalho, Luis ^a   Luque Ortega, Juan Román ^b   Manzano, José Ignacio ^a   Castanys, Santiago ^a   Rivas, Luis ^b   Gamarro, Francisco ^a  

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

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; TAFENOQUINE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; DNA FRAGMENTATION; DRUG MECHANISM; IN VITRO STUDY; LEISHMANIA; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROMASTIGOTE;

ADENOSINE TRIPHOSPHATE; AMINOQUINOLINES; ANTIMALARIALS; APOPTOSIS; CALCIUM; CELL MEMBRANE; DNA FRAGMENTATION; ELECTRON TRANSPORT COMPLEX III; LEISHMANIA; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES;

EID: 78649644451     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00790-10     Document Type: Article

References (41)

1. Alvarez-Fortes, E., L. M. Ruiz-Perez, F. Bouillaud, E. Rial, and L. Rivas. 1998. Expression and regulation of mitochondrial uncoupling protein 1 from brown adipose tissue in Leishmania major promastigotes. Mol. Biochem. Parasitol. 93:191-202.
2. Besteiro, S., D. Tonn, L. Tetley, G. H. Coombs, and J. C. Mottram. 2008. The AP3 adaptor is involved in the transport of membrane proteins to acidocalcisomes of Leishmania. J. Cell Sci. 121:561-570.
3. Besteiro, S., R. A. Williams, L. S. Morrison, G. H. Coombs, and J. C. Mottram. 2006. Endosome sorting and autophagy are essential for differentiation and virulence of Leishmania major. J. Biol. Chem. 281:11384-11396.
4. Chappuis, F., S. Sundar, A. Hailu, H. Ghalib, S. Rijal, R. W. Peeling, J. Alvar, and M. Boelaert. 2007. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat. Rev. Microbiol. 5:873-882.
5. Chen, M., L. Zhai, S. B. Christensen, T. G. Theander, and A. Kharazmi. 2001. Inhibition of fumarate reductase in Leishmania major and L. donovani by chalcones. Antimicrob. Agents Chemother. 45:2023-2029.
6. Das, M., S. B. Mukherjee, and C. Shaha. 2001. Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J. Cell Sci. 114:2461-2469.
7. Das, R., A. Roy, N. Dutta, and H. K. Majumder. 2008. Reactive oxygen species and imbalance of calcium homeostasis contributes to curcumin induced programmed cell death in Leishmania donovani. Apoptosis 13:867-882.
8. den Boer, M. L., J. Alvar, R. N. Davidson, K. Ritmeijer, and M. Balasegaram. 2009. Developments in the treatment of visceral leishmaniasis. Expert Opin. Emerg. Drugs 14:395-410.
9. Diaz-Achirica, P., J. Ubach, A. Guinea, D. Andreu, and L. Rivas. 1998. The plasma membrane of Leishmania donovani promastigotes is the main target for CA(1-8)M(1-18), a synthetic cecropin A-melittin hybrid peptide. Biochem. J. 330:453-460.
10. Docampo, R., W. de Souza, K. Miranda, P. Rohloff, and S. N. Moreno. 2005. Acidocalcisomes - conserved from bacteria to man. Nat. Rev. Microbiol. 3:251-261.
11. Dolai, S., R. K. Yadav, S. Pal, and S. Adak. 2009. Overexpression of mitochondrial Leishmania major ascorbate peroxidase enhances tolerance to oxidative stress-induced programmed cell death and protein damage. Eukaryot. Cell 8:1721-1731.
12. Drose, S., and U. Brandt. 2008. The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J. Biol. Chem. 283:21649-21654.
13. Guerra, D. G., A. Decottignies, B. M. Bakker, and P. A. Michels. 2006. The mitochondrial FAD-dependent glycerol-3-phosphate dehydrogenase of Trypanosomatidae and the glycosomal redox balance of insect stages of Trypanosoma brucei and Leishmania spp. Mol. Biochem. Parasitol. 149:155-169.
14. Halliwell, B., and J. M. Gutteridge. 1990. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186:1-85.
15. Kennedy, M. L., F. Cortes-Selva, J. M. Perez-Victoria, I. A. Jimenez, A. G. Gonzalez, O. M. Munoz, F. Gamarro, S. Castanys, and A. G. Ravelo. 2001. Chemosensitization of a multidrug-resistant Leishmania tropica line by new sesquiterpenes from Maytenus magellanica and Maytenus chubutensis. J. Med. Chem. 44:4668-4676.
16. Lanners, H. N. 1991. Effect of the 8-aminoquinoline primaquine on culture-derived gametocytes of the malaria parasite Plasmodium falciparum. Parasitol. Res. 77:478-481.
17. Lopez-Martin, C., J. M. Perez-Victoria, L. Carvalho, S. Castanys, and F. Gamarro. 2008. Sitamaquine sensitivity in Leishmania species is not mediated by drug accumulation in acidocalcisomes. Antimicrob. Agents Chemother. 52:4030-4036.
18. 2+ pool content and signaling and expression of a calcium pump are linked to virulence in Leishmania mexicana amazonesis amastigotes. J. Biol. Chem. 272:9464-9473.
19. Luque-Ortega, J. R., S. Martinez, J. M. Saugar, L. R. Izquierdo, T. Abad, J. G. Luis, J. Pinero, B. Valladares, and L. Rivas. 2004. Fungus-elicited metabolites from plants as an enriched source for new leishmanicidal agents: antifungal phenyl-phenalenone phytoalexins from the banana plant (Musa acuminata) target mitochondria of Leishmania donovani promastigotes. Antimicrob. Agents Chemother. 48:1534-1540.
20. Luque-Ortega, J. R., and L. Rivas. 2007. Miltefosine (hexadecylphosphocholine) inhibits cytochrome c oxidase in Leishmania donovani promastigotes. Antimicrob. Agents Chemother. 51:1327-1332.
21. Luque-Ortega, J. R., O. M. Rivero-Lezcano, S. L. Croft, and L. Rivas. 2001. In vivo monitoring of intracellular ATP levels in Leishmania donovani promastigotes as a rapid method to screen drugs targeting bioenergetic metabolism. Antimicrob. Agents Chemother. 45:1121-1125.
22. Luque-Ortega, J. R., J. M. Saugar, C. Chiva, D. Andreu, and L. Rivas. 2003. Identification of new leishmanicidal peptide lead structures by automated real-time monitoring of changes in intracellular ATP. Biochem. J. 375:221-230.
23. Luque-Ortega, J. R., W. van't Hof, E. C. Veerman, J. M. Saugar, and L. Rivas. 2008. Human antimicrobial peptide histatin 5 is a cell-penetrating peptide targeting mitochondrial ATP synthesis in Leishmania. FASEB J. 22:1817-1828.
24. Mehta, A., and C. Shaha. 2004. Apoptotic death in Leishmania donovani promastigotes in response to respiratory chain inhibition: complex II inhibition results in increased pentamidine cytotoxicity. J. Biol. Chem. 279:11798-11813.
25. Menna-Barreto, R. F., K. Salomao, A. P. Dantas, R. M. Santa-Rita, M. J. Soares, H. S. Barbosa, and S. L. de Castro. 2009. Different cell death pathways induced by drugs in Trypanosoma cruzi: an ultrastructural study. Micron 40:157-168.
26. Moreno, S. N., and R. Docampo. 2003. Calcium regulation in protozoan parasites. Curr. Opin. Microbiol. 6:359-364.
27. Mukherjee, A., P. K. Padmanabhan, M. H. Sahani, M. P. Barrett, and R. Madhubala. 2006. Roles for mitochondria in pentamidine susceptibility and resistance in Leishmania donovani. Mol. Biochem. Parasitol. 145:1-10.
28. 2+ levels through the activation of non-selective cation channels induced by oxidative stress causes mitochondrial depolarization leading to apoptosis-like death in Leishmania donovani promastigotes. J. Biol. Chem. 277:24717-24727.
29. Nanayakkara, N. P., A. L. Ager, Jr., M. S. Bartlett, V. Yardley, S. L. Croft, I. A. Khan, J. D. McChesney, and L. A. Walker. 2008. Antiparasitic activities and toxicities of individual enantiomers of the 8-aminoquinoline 8-[(4-amino-1-methylbutyl)amino]-6-methoxy-4-methyl-5-[3,4-dichlorophenoxy] quinoline succinate. Antimicrob. Agents Chemother. 52:2130-2137.
30. Opperdoes, F. R., and P. A. Michels. 2008. Complex I of Trypanosomatidae: does it exist? Trends Parasitol. 24:310-317.
31. Perez-Victoria, F. J., F. Gamarro, M. Ouellette, and S. Castanys. 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.
32. Piacenza, L., F. Irigoin, M. N. Alvarez, G. Peluffo, M. C. Taylor, J. M. Kelly, S. R. Wilkinson, and R. Radi. 2007. Mitochondrial superoxide radicals mediate programmed cell death in Trypanosoma cruzi: cytoprotective action of mitochondrial iron superoxide dismutase overexpression. Biochem. J. 403:323-334.
33. Sen, N., B. B. Das, A. Ganguly, T. Mukherjee, S. Bandyopadhyay, and H. K. Majumder. 2004. Camptothecin-induced imbalance in intracellular cation homeostasis regulates programmed cell death in unicellular hemoflagellate Leishmania donovani. J. Biol. Chem. 279:52366-52375.
34. Sottocasa, G. L., B. Kuylenstierna, L. Ernster, and A. Bergstrand. 1967. An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J. Cell Biol. 32:415-438.
35. Sundar, S., and M. Chatterjee. 2006. Visceral leishmaniasis - current therapeutic modalities. Indian J. Med. Res. 123:345-352.
36. Tekwani, B. L., and L. A. Walker. 2006. 8-Aminoquinolines: future role as antiprotozoal drugs. Curr. Opin. Infect. Dis. 19:623-631.
37. Van Hellemond, J. J., and A. G. Tielens. 1997. Inhibition of the respiratory chain results in a reversible metabolic arrest in Leishmania promastigotes. Mol. Biochem. Parasitol. 85:135-138.
38. Vercesi, A. E., C. F. Bernardes, M. E. Hoffmann, F. R. Gadelha, and R. Docampo. 1991. Digitonin permeabilization does not affect mitochondrial function and allows the determination of the mitochondrial membrane potential of Trypanosoma cruzi in situ. J. Biol. Chem. 266:14431-14434.
39. 2+, pentamidine and WR-6026 on mitochondrial membrane potential in situ. Biochem. J. 284:463-467.
40. Vergnes, B., B. Gourbal, I. Girard, S. Sundar, J. Drummelsmith, and M. Ouellette. 2007. A proteomics screen implicates HSP83 and a small kineto-plastid 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.
41. Yardley, V., F. Gamarro, and S. L. Croft. 2010. Antileishmanial and antitrypanosomal activities of the 8-aminoquinoline tafenoquine. Antimicrob. Agents Chemother. 54:XXX-XXX.