Analogs of natural aminoacyl-tRNA synthetase inhibitors clear malaria in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 51, 2014, Pages E5508-E5517

  Novoa, Eva Maria ^a,j   Camacho, Noelia ^a   Tor, Anna ^a   Wilkinson, Barrie ^b,c,k   Moss, Steven ^b,c   Marín García, Patricia ^d,e   Azcárate, Isabel G ^d   Bautista, José M ^d   Mirando, Adam C ^f   Francklyn, Christopher S ^f   Varon, Sònia ^g   Royo, Miriam ^g,h   Cortés, Alfred ^a,g,i   De Pouplana, Lluís Ribas ^a,i  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b BIOTICA TECHNOLOGY LTD   (United Kingdom)

^c Isomerase Therapeutics Ltd   (United Kingdom)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e UNIVERSIDAD REY JUAN CARLOS   (Spain)

^f UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF BARCELONA   (Spain)

^h CIBER in Bioengineering Biomaterials and Nanomedicine   (Spain)

ⁱ INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^j MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^k JOHN INNES CENTRE   (United Kingdom)

more..

Author keywords

Aminoacyl tRNA synthetase; Borrelidin; Drug design; Malaria; Plasmodium

Indexed keywords

2 AMINOCYCLOPENTANECARBOXYLIC ACID; AMINO ACID TRANSFER RNA LIGASE; AMINO ACID TRANSFER RNA LIGASE INHIBITOR; ANTIMALARIAL AGENT; BC 194; BC 195; BC 196; BC 220; BC 240; BORRELIDIN; GLUTAMATE TRANSFER RNA LIGASE; GLUTAMINE TRANSFER RNA LIGASE; ISOLEUCINE TRANSFER RNA LIGASE; LEUCINE TRANSFER RNA LIGASE; LIGASE INHIBITOR; LYSINE TRANSFER RNA LIGASE; PROLINE TRANSFER RNA; PSEUDOMONIC ACID; SERINE TRANSFER RNA LIGASE; THREONINE TRANSFER RNA; TYROSINE TRANSFER RNA LIGASE; UNCLASSIFIED DRUG; ENZYME INHIBITOR;

AMINOACYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL ACTIVITY; APICOPLAST; ARTICLE; CONTROLLED STUDY; HEK293 CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; IN VIVO STUDY; LIMIT OF DETECTION; MALARIA; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; POLYACRYLAMIDE GEL ELECTROPHORESIS; RNA TRANSLATION; STRUCTURE ACTIVITY RELATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; MALARIA, FALCIPARUM;

MUS; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII;

AMINO ACYL-TRNA SYNTHETASES; ANIMALS; ANTIMALARIALS; ENZYME INHIBITORS; HUMANS; MALARIA, FALCIPARUM; MICE; PLASMODIUM FALCIPARUM;

EID: 84919930151     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1405994111     Document Type: Article

References (71)

1. Jomaa H, et al. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285(5433):1573-1576.
2. Ralph SA, D'Ombrain MC, McFadden GI (2001) The apicoplast as an antimalarial drug target. Drug Resist Updat 4(3):145-151.
3. Seeber F (2003) Biosynthetic pathways of plastid-derived organelles as potential drug targets against parasitic apicomplexa. Curr Drug Targets Immune Endocr Metabol Disord 3(2):99-109.
4. Surolia N, Surolia A (2001) Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat Med 7(2):167-173.
5. Borrmann S, et al. (2004) Fosmidomycin-clindamycin for the treatment of Plasmodium falciparum malaria. J Infect Dis 190(9):1534-1540.
6. Miller LH, et al. (1974) Evaluation of clindamycin in combination with quinine against multidrug-resistant strains of Plasmodium falciparum. Am J Trop Med Hyg 23(4):565-569.
7. Ariey F, et al. (2014) A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505(7481):50-55.
8. Goldberg DE, Siliciano RF, Jacobs WR, Jr (2012) Outwitting evolution: Fighting drug-resistant TB, malaria, and HIV. Cell 148(6):1271-1283.
9. Andriantsoanirina V, et al. (2009) Plasmodium falciparum drug resistance in Madagascar: Facing the spread of unusual pfdhfr and pfmdr-1 haplotypes and the decrease of dihydroartemisinin susceptibility. Antimicrob Agents Chemother 53(11):4588-4597.
10. Bonnet M, et al. (2009) Varying efficacy of artesunate+amodiaquine and artesunate+ sulphadoxine-pyrimethamine for the treatment of uncomplicated falciparum malaria in the Democratic Republic of Congo: A report of two in-vivo studies. Malar J 8:192.
11. Carrara VI, et al. (2009) Changes in the treatment responses to artesunate-mefloquine on the northwestern border of Thailand during 13 years of continuous deployment. PLoS ONE 4(2):e4551.
12. Hurdle JG, O'Neill AJ, Chopra I (2005) Prospects for aminoacyl-tRNA synthetase inhibitors as new antimicrobial agents. Antimicrob Agents Chemother 49(12):4821-4833.
13. Kim S, Lee SW, Choi EC, Choi SY (2003) Aminoacyl-tRNA synthetases and their inhibitors as a novel family of antibiotics. Appl Microbiol Biotechnol 61(4):278-288.
14. Bennett I, et al. (1999) Synthesis and antibacterial properties of beta-diketone acrylate bioisosteres of pseudomonic acid A. Bioorg Med Chem Lett 9(13):1847-1852.
15. Schimmel P, Tao J, Hill J (1998) Aminoacyl tRNA synthetases as targets for new anti-infectives. FASEB J 12(15):1599-1609.
16. Hoepfner D, et al. (2012) Selective and specific inhibition of the plasmodium falciparum lysyl-tRNA synthetase by the fungal secondary metabolite cladosporin. Cell Host Microbe 11(6):654-663.
17. Istvan ES, et al. (2011) Validation of isoleucine utilization targets in Plasmodium falciparum. Proc Natl Acad Sci USA 108(4):1627-1632.
18. Hoen R, et al. (2013) Selective inhibition of an apicoplastic aminoacyl-tRNA synthetase from Plasmodium falciparum. ChemBioChem 14(4):499-509.
19. Guiguemde WA, Guy RK (2012) An all-purpose antimalarial drug target. Cell Host Microbe 11(6):555-557.
20. Azcárate IG, et al. (2013) Insights into the preclinical treatment of blood-stage malaria by the antibiotic borrelidin. Br J Pharmacol 169(3):645-658.
21. Otoguro K, et al. (2003) In vitro and in vivo antimalarial activities of a non-glycosidic 18-membered macrolide antibiotic, borrelidin, against drug-resistant strains of Plasmodia. J Antibiot (Tokyo) 56(8):727-729.
22. Ishiyama A, et al. (2011) Borrelidin, a potent antimalarial: Stage-specific inhibition profile of synchronized cultures of Plasmodium falciparum. J Antibiot (Tokyo) 64(5):381-384.
23. Ruan B, et al. (2005) A unique hydrophobic cluster near the active site contributes to differences in borrelidin inhibition among threonyl-tRNA synthetases. J Biol Chem 280(1):571-577.
24. Moss SJ, et al. (2006) Biosynthesis of the angiogenesis inhibitor borrelidin: Directed biosynthesis of novel analogues. Chem Commun (Camb) (22):2341-2343.
25. Kawamura T, et al. (2003) Anti-angiogenesis effects of borrelidin are mediated through distinct pathways: Threonyl-tRNA synthetase and caspases are independently involved in suppression of proliferation and induction of apoptosis in endothelial cells. J Antibiot (Tokyo) 56(8):709-715.
26. Williams TF, Mirando AC, Wilkinson B, Francklyn CS, Lounsbury KM (2013) Secreted Threonyl-tRNA synthetase stimulates endothelial cell migration and angiogenesis. Sci Rep 3:1317.
27. Nass G, Poralla K, Zähner H (1969) Effect of the antibiotic Borrelidin on the regulation of threonine biosynthetic enzymes in E. coli. Biochem Biophys Res Commun 34(1):84-91.
28. Jackson KE, et al. (2012) Dual targeting of aminoacyl-tRNA synthetases to the apicoplast and cytosol in Plasmodium falciparum. Int J Parasitol 42(2):177-186.
29. Wilkinson B, et al. (2006) Separation of anti-angiogenic and cytotoxic activities of borrelidin by modification at the C17 side chain. Bioorg Med Chem Lett 16(22):5814-5817.
30. Sugawara A, et al. (2013) Borrelidin analogues with antimalarial activity: Design, synthesis and biological evaluation against Plasmodium falciparum parasites. Bioorg Med Chem Lett 23(8):2302-2305.
31. Dahl EL, Rosenthal PJ (2007) Multiple antibiotics exert delayed effects against the Plasmodium falciparum apicoplast. Antimicrob Agents Chemother 51(10):3485-3490.
32. Goodman CD, Su V, McFadden GI (2007) The effects of anti-bacterials on the malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 152(2):181-191.
33. Ward A, Campoli-Richards DM (1986) Mupirocin. A review of its antibacterial activity, pharmacokinetic properties and therapeutic use. Drugs 32(5):425-444.
34. Parenti MA, Hatfield SM, Leyden JJ (1987) Mupirocin: A topical antibiotic with a unique structure and mechanism of action. Clin Pharm 6(10):761-770.
35. Oki T, Hirano M, Tomatsu K, Numata K, Kamei H (1989) Cispentacin, a new antifungal antibiotic. II. In vitro and in vivo antifungal activities. J Antibiot (Tokyo) 42(12):1756-1762.
36. Capobianco JO, Zakula D, Coen ML, Goldman RC (1993) Anti-Candida activity of cis-pentacin: The active transport by amino acid permeases and possible mechanisms of action. Biochem Biophys Res Commun 190(3):1037-1044.
37. Jacobs RT, Plattner JJ, Keenan M (2011) Boron-based drugs as antiprotozoals. Curr Opin Infect Dis 24(6):586-592.
38. Rock FL, et al. (2007) An antifungal agent inhibits an aminoacyl-tRNA synthetase by trapping tRNA in the editing site. Science 316(5832):1759-1761.
39. Barak O, Loo DS (2007) AN-2690, a novel antifungal for the topical treatment of onychomycosis. Curr Opin Investig Drugs 8(8):662-668.
40. Gerken SC, Arfin SM (1984) Chinese hamster ovary cells resistant to borrelidin overproduce threonyl-tRNA synthetase. J Biol Chem 259(14):9202-9206.
41. Vong BG, Kim SH, Abraham S, Theodorakis EA (2004) Stereoselective total synthesis of (-)-borrelidin. Angew Chem Int Ed Engl 43(30):3947-3951.
42. Moss S, Wilkinson B, Zhang M (2007) Patent Cooperation Treaty Int Appl WO2007135078 (May 17, 2007).
43. Gardner MJ, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419(6906):498-511.
44. Schlitzer M (2008) Antimalarial drugs: What is in use and what is in the pipeline. Arch Pharm (Weinheim) 341(3):149-163.
45. Flannery EL, Chatterjee AK, Winzeler EA (2013) Antimalarial drug discovery - approaches and progress towards new medicines. Nat Rev Microbiol 11(12):849-862.
46. White NJ, et al. (2014) Malaria. Lancet 383(9918):723-735.
47. Garcia-Bustos JF, Gamo FJ (2013) Antimalarial drug resistance and early drug discovery. Curr Pharm Des 19(2):270-281.
48. Dahl EL, et al. (2006) Tetracyclines specifically target the apicoplast of the malaria parasite Plasmodium falciparum. Antimicrob Agents Chemother 50(9):3124-3131.
49. Wells TN (2013) Discovering and developing new medicines for malaria control and elimination. Infect Disord Drug Targets 13(4):292-302.
50. Gamo FJ, et al. (2010) Thousands of chemical starting points for antimalarial lead identification. Nature 465(7296):305-310.
51. Guiguemde WA, et al. (2010) Chemical genetics of Plasmodium falciparum. Nature 465(7296):311-315.
52. Plouffe D, et al. (2008) In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc Natl Acad Sci USA 105(26):9059-9064.
53. Hoffmann F (1900) US Patent 644,077.
54. Desai SA (2012) Ion and nutrient uptake by malaria parasite-infected erythrocytes. Cell Microbiol 14(7):1003-1009.
55. Desai SA (2014) Why do malaria parasites increase host erythrocyte permeability? Trends Parasitol 30(3):151-159.
56. Biagini GA, et al. (2003) Heme binding contributes to antimalarial activity of bisquaternary ammoniums. Antimicrob Agents Chemother 47(8):2584-2589.
57. Stead AM, et al. (2001) Diamidine compounds: Selective uptake and targeting in Plasmodium falciparum. Mol Pharmacol 59(5):1298-1306.
58. Woolard J, et al. (2011) Borrelidin modulates the alternative splicing of VEGF in favour of anti-angiogenic isoforms. Chem Sci 2011(2):273-278.
59. Urbán P, Estelrich J, Cortés A, Fernàndez-Busquets X (2011) A nanovector with complete discrimination for targeted delivery to Plasmodium falciparum-infected versus non-infected red blood cells in vitro. J Control Release 151(2):202-211.
60. Francklyn CS, First EA, Perona JJ, Hou YM (2008) Methods for kinetic and thermodynamic analysis of aminoacyl-tRNA synthetases. Methods 44(2):100-118.
61. Peters W, Robinson B (1999) Handbook of Animal Models of Infection, eds Zak O, Sande M (Academic Press, San Diego, CA), pp 757-773.
62. Moneriz C, et al. (2011) Parasitostatic effect of maslinic acid. I. Growth arrest of Plasmodium falciparum intraerythrocytic stages. Malar J 10:82.
63. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG; NC3Rs Reporting Guidelines Working Group (2010) Animal research: Reporting in vivo experiments: The ARRIVE guidelines. Br J Pharmacol 160(7):1577-1579.
64. Fidock DA, Rosenthal PJ, Croft SL, Brun R, Nwaka S (2004) Antimalarial drug discovery: Efficacy models for compound screening. Nat Rev Drug Discov 3(6):509-520.
65. Kicska GA, Ting LM, Schramm VL, Kim K (2003) Effect of dietary p-aminobenzoic acid on murine Plasmodium yoelii infection. J Infect Dis 188(11):1776-1781.
66. Sali A (1995) Comparative protein modeling by satisfaction of spatial restraints. Mol Med Today 1(6):270-277.
67. Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292(2):195-202.
68. Wiederstein M, Sippl MJ (2007) ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35(Web Server issue):W407-W410.
69. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8(4):477-486.
70. Russell RB, Barton GJ (1992) Multiple protein sequence alignment from tertiary structure comparison: Assignment of global and residue confidence levels. Proteins 14(2):309-323.
71. Friesner RA, et al. (2004) Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J Med Chem 47(7):1739-1749.