The antitumoral depsipeptide IB-01212 kills Leishmania through an apoptosis-like process involving intracellular targets

Molecular Pharmaceutics

Volumn 7, Issue 5, 2010, Pages 1608-1617

  Luque Ortega, Juan R ^a   Cruz, Luis J ^b,c   Albericio, Fernando ^c   Rivas, Luis ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

antibiotic peptide; apoptosis; Leishmania; Marine depsipeptide; mitochondria

Indexed keywords

CLONOSTACHYS; DEPSIPEPTIDE; IB 01212; UNCLASSIFIED DRUG;

AMASTIGOTE; ANTIPROTOZOAL ACTIVITY; APOPTOSIS; ARTICLE; DRUG MECHANISM; DRUG SYNTHESIS; DRUG TARGETING; FUNGUS; LEISHMANIA; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROMASTIGOTE;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTIPROTOZOAL AGENTS; APOPTOSIS; CELL MEMBRANE; DEPSIPEPTIDES; FUNGAL PROTEINS; LEISHMANIA; MACROPHAGES, PERITONEAL; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED BALB C;

EID: 77957739105     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp100035f     Document Type: Article

References (43)

1. Morales, M. A.; Cruz, I.; Rubio, J. M.; Chicharro, C.; Canavate, C.; Laguna, F.; Alvar, J. Relapses versus reinfections in patients coinfected with Leishmania infantum and human immunodeficiency virus type 1 J. Infect. Dis. 2002, 185, 1533-1537
2. Palatnik-de-Sousa, C. B. Vaccines for leishmaniasis in the fore coming 25 years Vaccine 2008, 26, 1709-1724
3. Croft, S. L.; Sundar, S.; Fairlamb, A. H. Drug resistance in leishmaniasis Clin. Microbiol. Rev. 2006, 19, 111-126
4. Mishra, J.; Saxena, A.; Singh, S. Chemotherapy of leishmaniasis: past, present and future Curr. Med. Chem. 2007, 14, 1153-1169
5. Golenser, J.; Domb, A. New formulations and derivatives of amphotericin B for treatment of leishmaniasis Mini-Rev. Med. Chem. 2006, 6, 153-162
6. Sundar, S.; Chakravarty, J. Paromomycin in the treatment of leishmaniasis Expert Opin. Invest. Drugs 2008, 17, 787-794
7. Croft, S. L.; Engel, J. Miltefosine - discovery of the antileishmanial activity of phospholipid derivatives Trans. R. Soc. Trop. Med. Hyg. 2006, 100 (1) S4-8
8. Fuertes, M. A.; Nguewa, P. A.; Castilla, J.; Alonso, C.; Perez, J. M. Anticancer compounds as leishmanicidal drugs: challenges in chemotherapy and future perspectives Curr. Med. Chem. 2008, 15, 433-439
9. Mayer, A. M.; Gustafson, K. R. Marine pharmacology in 2005-2006: antitumour and cytotoxic compounds Eur. J. Cancer 2008, 44, 2357-2387
10. Molinski, T. F.; Dalisay, D. S.; Lievens, S. L.; Saludes, J. P. Drug development from marine natural products Nat. Rev. Drug Discovery 2009, 8, 69-85
11. Azumi, K.; Yokosawa, H.; Ishii, S. Halocyamines: novel antimicrobial tetrapeptide-like substances isolated from the hemocytes of the solitary ascidian Halocynthia roretzi Biochemistry 1990, 29, 159-165
12. Kamiya, H.; Sakai, R.; Jimbo, M. Bioactive molecules from sea hares Prog. Mol. Subcell. Biol. 2006, 43, 215-239
13. Tincu, J. A.; Taylor, S. W. Antimicrobial peptides from marine invertebrates Antimicrob. Agents Chemother. 2004, 48, 3645-3654
14. Cruz, L. J.; Luque-Ortega, J. R.; Rivas, L.; Albericio, F.; Kahalalide, F an antitumor depsipeptide in clinical trials, and its analogues as effective antileishmanial agents Mol. Pharmaceutics 2009, 6, 813-824
15. Fennell, B. J.; Carolan, S.; Pettit, G. R.; Bell, A. Effects of the antimitotic natural product dolastatin 10, and related peptides, on the human malarial parasite Plasmodium falciparum J. Antimicrob. Chemother. 2003, 51, 833-841
16. Otoguro, K.; Ishiyama, A.; Namatame, M.; Nishihara, A.; Furusawa, T.; Masuma, R.; Shiomi, K.; Takahashi, Y.; Yamada, H.; Omura, S. Selective and potent in vitro antitrypanosomal activities of ten microbial metabolites J. Antibiot. (Tokyo) 2008, 61, 372-378
17. Cruz, L. J.; Insua, M. M.; Baz, J. P.; Trujillo, M.; Rodriguez-Mias, R. A.; Oliveira, E.; Giralt, E.; Albericio, F.; Canedo, L. M. IB-01212, a new cytotoxic cyclodepsipeptide isolated from the marine fungus Clonostachys sp. ESNA-A009 J. Org. Chem. 2006, 71, 3335-3338
18. Cruz, L. J.; Cuevas, C.; Canedo, L. M.; Giralt, E.; Albericio, F. Total solid-phase synthesis of marine cyclodepsipeptide IB-01212 J. Org. Chem. 2006, 71, 3339-3344
19. Cruz, L. J.; Francesch, A.; Cuevas, C.; Albericio, F. Synthesis and structure-activity relationship of cytotoxic marine cyclodepsipeptide IB-01212 analogues ChemMedChem 2007, 2, 1076-1084
20. Chicharro, C.; Granata, C.; Lozano, R.; Andreu, D.; Rivas, L. N-terminal fatty acid substitution increases the leishmanicidal activity of CA(1-7)M(2-9), a cecropin-melittin hybrid peptide Antimicrob. Agents Chemother. 2001, 45, 2441-2449
21. Luque-Ortega, J. R.; Martinez, S.; Saugar, J. M.; Izquierdo, L. R.; Abad, T.; Luis, J. G.; Pinero, J.; Valladares, B.; Rivas, L. 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. 2004, 48, 1534-1540
22. Paris, C.; Loiseau, P. M.; Bories, C.; Breard, J. Miltefosine induces apoptosis-like death in Leishmania donovani promastigotes Antimicrob. Agents Chemother. 2004, 48, 852-859
23. Diaz-Achirica, P.; Ubach, J.; Guinea, A.; Andreu, D.; Rivas, L. 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. 1998, 330 (Pt 1) 453-460
24. Bayo-Puxan, N.; Fernandez, A.; Tulla-Puche, J.; Riego, E.; Cuevas, C.; Alvarez, M.; Albericio, F. Total solid-phase synthesis of the azathiocoraline class of symmetric bicyclic peptides Chemistry 2006, 12, 9001-9009
25. Tulla-Puche, J.; Marcucci, E.; Fermin, M.; Bayo-Puxan, N.; Albericio, F. Protection by conformationally restricted mobility: first solid-phase synthesis of triostin A Chemistry 2008, 14, 4475-4478
26. Huang, H. W. Molecular mechanism of antimicrobial peptides: the origin of cooperativity Biochim. Biophys. Acta 2006, 1758, 1292-1302
27. Luque-Ortega, J. R.; Saugar, J. M.; Chiva, C.; Andreu, D.; Rivas, L. Identification of new leishmanicidal peptide lead structures by automated real-time monitoring of changes in intracellular ATP Biochem. J. 2003, 375, 221-230
28. Hale, J. D.; Hancock, R. E. Alternative mechanisms of action of cationic antimicrobial peptides on bacteria Expert Rev. Anti-Infect. Ther. 2007, 5, 951-959
29. Garcia-Martin, F.; Cruz, L. J.; Rodriguez-Mias, R. A.; Giralt, E.; Albericio, F. Design and synthesis of FAJANU: a de novo C(2) symmetric cyclopeptide family J. Med. Chem. 2008, 51, 3194-202
30. Van Hellemond, J. J.; Tielens, A. G. Inhibition of the respiratory chain results in a reversible metabolic arrest in Leishmania promastigotes Mol. Biochem. Parasitol. 1997, 85, 135-138
31. Menna-Barreto, R. F.; Salomao, K.; Dantas, A. P.; Santa-Rita, R. M.; Soares, M. J.; Barbosa, H. S.; de Castro, S. L. Different cell death pathways induced by drugs in Trypanosoma cruzi: an ultrastructural study Micron 2009, 40, 157-168
32. Shaha, C. Apoptosis in Leishmania species & its relevance to disease pathogenesis Indian J. Med. Res. 2006, 123, 233-244
33. Luque-Ortega, J. R.; van't Hof, W.; Veerman, E. C.; Saugar, J. M.; Rivas, L. Human antimicrobial peptide histatin 5 is a cell-penetrating peptide targeting mitochondrial ATP synthesis in Leishmania FASEB J. 2008, 22, 1817-1828
34. Luque-Ortega, J. R.; Reuther, P.; Rivas, L.; Dardonville, C. New benzophenone-derived bisphosphonium salts as leishmanicidal leads targeting mitochondria through inhibition of respiratory complex II J. Med. Chem. 2010, 53, 1788-1798
35. Glaser, T. A.; Utz, G. L.; Mukkada, A. J. The plasma membrane electrical gradient (membrane potential) in Leishmania donovani promastigotes and amastigotes Mol. Biochem. Parasitol. 1992, 51, 9-15
36. Zilberstein, D.; Philosoph, H.; Gepstein, A. Maintenance of cytoplasmic pH and proton motive force in promastigotes of Leishmania donovani Mol. Biochem. Parasitol. 1989, 36, 109-117
37. Besteiro, S.; Williams, R. A.; Coombs, G. H.; Mottram, J. C. Protein turnover and differentiation in Leishmania Int. J. Parasitol. 2007, 37, 1063-1075
38. Rosenzweig, D.; Smith, D.; Myler, P. J.; Olafson, R. W.; Zilberstein, D. Post-translational modification of cellular proteins during Leishmania donovani differentiation Proteomics 2008, 8, 1843-1850
39. Rosenzweig, D.; Smith, D.; Opperdoes, F.; Stern, S.; Olafson, R. W.; Zilberstein, D. Retooling Leishmania metabolism: from sand fly gut to human macrophage FASEB J. 2008, 22, 590-602
40. Jelokhani-Niaraki, M.; Kondejewski, L. H.; Wheaton, L. C.; Hodges, R. S. Effect of ring size on conformation and biological activity of cyclic cationic antimicrobial peptides J. Med. Chem. 2009, 52, 2090-2097
41. Kiricsi, M.; Prenner, E. J.; Jelokhani-Niaraki, M.; Lewis, R. N.; Hodges, R. S.; McElhaney, R. N. The effects of ring-size analogs of the antimicrobial peptide gramicidin S on phospholipid bilayer model membranes and on the growth of Acholeplasma laidlawii B Eur. J. Biochem. 2002, 269, 5911-5920
42. van der Knaap, M.; Engels, E.; Busscher, H. J.; Otero, J. M.; Llamas-Saiz, A. L.; van Raaij, M. J.; Mars-Groenendijk, R. H.; Noort, D.; van der Marel, G. A.; Overkleeft, H. S.; Overhand, M. Synthesis and biological evaluation of asymmetric gramicidin S analogues containing modified D-phenylalanine residues Bioorg. Med. Chem. 2009, 17, 6318-6328
43. Krauth-Siegel, R. L.; Comini, M. A. Redox control in trypanosomatids, parasitic protozoa with trypanothione-based thiol metabolism Biochim. Biophys. Acta 2008, 1780, 1236-1248