'FAS't inhibition of malaria

Biochemical Journal

Volumn 383, Issue 3, 2004, Pages 401-412

  Surolia, Avadhesha ^a   Ramya, T N C ^a   Ramya, V ^a   Surolia, Namita ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

Antimalarial; Apicoplast; Fatty acid biosynthesis pathway; Malaria; Plasmodium falciparum; Triclosan

Indexed keywords

BIOSYNTHESIS; DRUG DOSAGE; ENZYME INHIBITION; ENZYME KINETICS; VACCINES;

FATTY ACID BIOSYNTHESIS SYSTEM; MORTALITY RATE; PLASMODIUM SP.;

MALARIA CONTROL;

1,2 DITHIOLE 3 ONE; 2,2 DIHYDROXYPHENYL ETHER; 3 DECYNOYL N ACETYLCYSTEAMINE; ANTIMALARIAL AGENT; CERULETIDE; CHLORAMPHENICOL; CHLOROQUINE; CLINDAMYCIN; DIAZOBORINE; FATTY ACID; GENZ 10850; GENZ 8575; HEXACHLOROPHENE; ISONIAZID; MALARIA VACCINE; NAS 21; NAS 91; RIFAMPICIN; THIOLACTOMYCIN; TRICLOSAN; UNCLASSIFIED DRUG;

APICOPLAST; CELL ORGANELLE; DICLOFOP; DRUG SYNTHESIS; DRUG TARGETING; ENZYME INHIBITION; FATTY ACID SYNTHESIS; FENOXAPROP; MALARIA; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE SURVIVAL; PHENOTYPE; PLASMODIUM; PLASMODIUM FALCIPARUM; PLASTID; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME;

ANIMALS; ENZYME INHIBITORS; FATTY ACID SYNTHETASE COMPLEX; FATTY ACIDS; HUMANS; MALARIA; PLASMODIUM;

PLASMODIUM FALCIPARUM; PLASMODIUM SP.; PROTOZOA;

EID: 9144226932     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041051     Document Type: Review

References (80)

1. World Health Organization (2002) The World Health Report 2002: reducing risks, promoting healthy life.
2. World Health Organization (1995) The World Health Report 1995.
3. Ramya, T. N. C., Surolia, N. and Surolia, A. (2002) Survival strategies of the malarial parasite Plasmodium falciparum. Curr. Sci. 83, 818-825
4. Baird, J. K. (1995) Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitai. Today 11, 105-111
5. Robert, A., Benoit-Vical, F, Dechy-Cabaret, O. and Meunier, B. (2001) From classical antimalarial drugs to new compounds based on the mechanism of action of artemisinin. Pure Appl. Chem. 73, 1173-1188
6. Eckstein-Ludwig, U., Webb, R. J., van Goethem, I. D. A., East, J. M., Lee, A. G., Kimura, M., O'Neill, P. M., Bray, P. G., Ward, S. A. and Krishna, S. (2003) Artemisinins target the SERCA of Plasmodium falciparum. Nature (London) 424, 957-961
7. Nontprasert, A., Nosten-Bertrand, M., Pukrittayakamee, S., Vanijanonta, S., Angus, B. J. and White, N. J. (1998) Assessment of the neurotoxicity of parenteral artemisinin derivatives in mice. Am. J. Trop. Med. Hyg. 59, 519-522
8. Nontprasert, A., Pukrittayakamee, S., Nosten-Bertrand, M., Vanijanonta, S. and White, N. J. (2000) Studies of the neurotoxicity of oral artemisinin derivatives in mice. Am. J. Trop. Med. Hyg. 62, 409-412
9. Waller, R. F., Keeling, P. J., Donald, R. G. K., Striepen, B., Handman, E., Lang-Unnasch, N., Cowman, A. F., Besra, G. S., Roos, D. S. and McFadden, G. I. (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 95, 12352-12357
10. Surolia, N. and Surolia, A. (2001) Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat. Med. 7, 167-173
11. Sharma, S. K., Kapoor, M., Ramya, T. N. C., Kumar, S., Kumar, G., Modak, R., Sharma, S., Surolia, N. and Surolia, A. (2003) Identification, characterization and inhibition of Plasmodium falciparum β-hydroxyacyl-acyl carrier protein dehydratase (FabZ). J. Biol. Chem. 278, 45661-45671
12. Pillai, S., Rajagopal, C., Kapoor, M., Kumar, G., Gupta, A. and Surolia, N. (2003) Functional characterization of β-ketoacyl-ACP reductase (FabG) from Plasmodium falciparum. Biochem. Biophys. Res. Commun. 303, 387-392
13. McMurry, L. M., Oethinger, M. and Levy, S. B. (1998) Triclosan targets lipid synthesis. Nature (London) 394, 531-532
14. Zuther, E., Johnson, J. J., Haselkorn, R., McLeod, R. and Gornicki, P. (1999) Growth of Toxoplasma gondii is inhibited by aryloxyphenoxypropionate herbicides targeting acetyl-CoA carboxylase. Proc. Natl. Acad. Sci. U.S.A. 96, 13387-13392
15. Waller, R. F., Ralph, S. A., Reed, M. B., Su, V., Douglas, J. D., Minnikin, D. E., Cowman, A. F., Besra, G. S. and McFadden, G. I. (2003) A type II pathway for fatty acid biosynthesis presents drug targets in Plasmodium falciparum. Antimicrob. Agents Chemother. 47, 297-301
16. Verwoert, I. I., Verhagen, E. F., van der Linden, K. H., Verbree, E. C., Nijkamp, H. J. and Stuitje, A. R. (1994) Molecular characterization of an Escherichia coli mutant with a temperature-sensitive malonyl coenzyme A-acyl carrier protein transacylase. FEBS Lett. 348, 311-316
17. Zhang, Y. and Cronan, Jr, J. E. (1998) Transcriptional analysis of essential genes of the Escherichia coli fatty acid biosynthesis gene cluster by functional replacement with the analogous Salmonella typhimurium gene cluster. J. Bacteriol. 180, 3295-3303
18. Kutchma, A. J., Hoang, T. T. and Schweizer, H. P. (1999) Characterization of a Pseudomonas aeruginosa fatty acid biosynthetic gene cluster: purification of acyl carrier protein (ACP) and malonyl-coenzyme A:ACP transacylase (FabD). J. Bacteriol. 181, 5498-5504
19. Verwoert, I. I., Verbree, E. C., van der Linden, K. H., Nijkamp, H. J. and Stuitje, A. R. (1992) Cloning, nucleotide sequence, and expression of the Escherichia coli fabD gene, encoding malonyl coenzyme A-acyl carrier protein transacylase. J. Bacteriol. 174, 2851-2857
20. Magnuson, K., Oh, W., Larson, T. J. and Cronan, Jr, J. E. (1992) Cloning and nucleotide sequence of the fabD gene encoding malonyl coenzyme A-acyl carrier protein transacylase of Escherichia coli. FEBS Lett. 299, 262-266
21. Serre, L., Verbree, E. C., Dauter, Z., Stuitje, A. R. and Derewenda, Z. S. (1995) The Escherichia coli malonyl-CoA:acyl carrier protein transacylase at 1.5-Å resolution: crystal structure of a fatty acid synthase component. J. Biol. Chem. 270, 12961-12964
22. Prigge, S. T., He, X., Gerena, L., Waters, N. C. and Reynolds, K. A. (2003) The initiating steps of a type II fatty acid synthase in Plasmodium falciparum are catalyzed by PfACP, PfMCAT and PfKASIII. Biochemistry 42, 1160-1169
23. Waters, N. C., Kopydlowski, K. M., Guszczynski, T., Wei, L., Sellers, P., Ferlan, J. T., Lee, P. J., Li, Z., Woodard, C. L., Shallom, S. et al. (2002) Functional characterization of the acyl carrier protein (PfACP) and β-ketoacyl ACP synthase III (PfKASIII) from Plasmodium falciparum. Mol. Biochem. Parasitol. 123, 85-94
24. Tsay, J. T., Oh, W, Larson, T. J., Jackowski, S. and Rock, C. O. (1992) Isolation and characterization of the β-ketoacyl-acyl carrier protein synthase III gene (fabH) from Escherichia coli K-12. J. Biol. Chem. 267, 6807-6814
25. Fisher, M., Kroon, J. T. M., Martindale, W., Stuitje, A. R., Slabas, A. R. and Rafferty, J. B. (2000) The X-ray structure of Brassica napus β-ketoacyl-acyl carrier protein reductase and its implications for substrate binding and catalysis. Structure 8, 339-347
26. Zhang, Y.-M. and Rock, C. O. (2004) Evaluation of epigallocatechin gallate and related plant polyphenols as inhibitors of the FabG and FabI reductases of bacterial type II fatty acid synthase. J. Biol. Chem. 279, 30994-31001
27. Clark, D. P., de Mendoza, D., Polacco, M. L. and Cronan, Jr, J. E. (1983) β-Hydroxydecanoyl thio ester dehydrase does not catalyze a rate-limiting step in Escherichia coli unsaturated fatty acid synthesis. Biochemistry 22, 5897-5902
28. Heath, R. J. and Rock, C. O. (1996) Roles of the FabA and FabZ β-hydroxyacyl-acyl carrier protein dehydratases in Escherichia coli fatty acid biosynthesis. J. Biol. Chem. 271, 27795-27801
29. Helmkamp, Jr, G. M., Brock, D. J. H. and Bloch, K. (1968) β-Hydroxydecanoyl thioester dehydrase: specificity of substrates and acetylenic inhibitors. J. Biol. Chem. 243, 3229-3232
30. Leesong, M., Henderson, B. S., Gillig, J. R., Schwab, J. M. and Smith, J. L. (1996) Structure of a dehydratase-isomerase from the bacterial pathway for biosynthesis of unsaturated fatty acids: two catalytic activities in one active site. Structure 4, 253-264
31. Swarna Mukhi, P. L., Sharma, S. K., Kapoor, M., Surolia, IM., Surolia, A. and Suguna, K. (2004) Crystallization and preliminary crystallographic analysis of β-hydroxyacyl ACP dehydratase (FabZ) from Plasmodium falciparum. Acta Crystallogr. D Biol. Crystallogr. 60, 120-121
32. Egan, A. F. and Russell, R. R. B. (1973) Conditional mutants affecting the cell envelope of Escherichia coli. Genet. Res. 21, 3603-3611
33. Heath, R. J. and Rock, C. O. (1995) Enoyl-acyl carrier protein reductase (fabl) plays a determinant role in completing cycles of fatty acid elongation in Escherichia coli. J. Biol. Chem. 270, 26538-26542
34. Heath, R. J., Yu, Y.-T., Shapiro, M. A., Olson, E. and Rock, C. O. (1998) Broad spectrum antimicrobial biocides target the Fabl component of fatty acid synthesis. J. Biol. Chem. 273, 30316-30321
35. Heath, R. J., Rubin, J. R., Holland, D. R., Zhang, E., Snow, M. E. and Rock, C. O. (1999) Mechanism of triclosan inhibition of bacterial fatty acid synthesis. J. Biol. Chem. 274, 11110-11114
36. Suguna, K., Surolia, A. and Surolia, N. (2001) Structural basis for triclosan and NAD binding to enoyl-ACP reductase of Plasmodium falciparum. Biochem. Biophys. Res. Commun. 283, 224-228
37. Kapoor, M., Dar, M. J., Surolia, A. and Surolia, N. (2001) Kinetic determinants of the interaction of enoyl-ACP reductase from Plasmodium falciparum with its substrates and inhibitors. Biochem. Biophys. Res. Commun. 289, 832-837
38. Ward, W. H. J., Holdgate, G. A., Rowsell, S., McLean, E. G., Pauptit, R. A., Clayton, E., Nichols, W. W., Minshull, C. A., Jude, D. A., Mistry, A. et al. (1999) Kinetic and structural characteristics of the inhibition of anoyl (acyl carrier protein) reductase by triclosan. Biochemistry 38, 12514-12525
39. Kapoor, M., Reddy, C. C., Krishnasastry, M. V., Surolia, N. and Surolia, A. (2004) Slow-tight binding inhibition of enoyl-acyl carrier protein reductase from Plasmodium falciparum by triclosan. Biochem. J. 381, 735-741
40. Kapoor, M. (2003) Kinetic studies on enoyl-ACP reductase from Plasmodium falciparum: a potent target of antimalarials. Ph.D. Thesis, Indian Institute of Science, Bangalore, India
41. Kapoor, M., Mukhi, P. L., Surolia, N., Suguna, K. and Surolia, A. (2004) Kinetic and structural analysis of the increased affinity of enoyl-ACP reductase for triclosan in the presence of NAD+. Biochem. J. 381, 725-733
42. Heath, R. J., Li, J., Ronald, G. E. and Rock, C. O. (2000) Inhibition of the Staphylococcus aureus NADPH-dependent enoyl-acyl carrier protein reductase by triclosan and hexachlorophene, J. Biol. Chem. 275, 4654-659
43. Seefeld, M. A., Miller, W. H., Newlander, K. A., Burgess, W. J., Payne, D. J., Rittenhouse, S. F., Moore, T. D., DeWolf, Jr, W. E., Keller, P. M., Qiu, X. et al. (2001) Inhibitors of bacterial enoyl acyl carrier protein reductase (Fabl): 2,9-disubstituted 1,2,3,4-tetrahydropyrido[3,4-b]indoles as potential antibacterial agents. Bioorg. Med. Chem. Lett. 11, 2241-2244
44. Miller, W. H., Seefeld, M. A., Newlander, K. A., Uzinskas, I. N., Burgess, W. J., Heerding, D. A., Yuan, C. C. K., Head, M. S., Payne, D. J., Rittenhouse, S. F. et al. (2002) Discovery of aminopyridine-based inhibitors of bacterial enoyl-ACP reductase (Fabl). J. Med. Chem. 45, 3246-3256
45. Seefeid, M. A., Miller, W. H., Newlander, K. A., Burgess, W. J., DeWoll, Jr, W. E., Elkins, P. A., Head, M. S., Jakas, D. R., Janson, C. A., Keller, P. M. et al. (2003) Indole naphthyridinones as inhibitors of bacterial enoyl-ACP reductases Fabl and FabK. J. Med. Chem. 46, 1627-1635
46. Heerding, D. A., Chan, G., DeWolf, Jr, W. E., Fosberry, A. P., Janson, C. A., Jaworski, D. D., McManus, E., Miller, W. H., Moore, T. D., Payne, D. J. et al. (2001) 1,4-Disubstituted imidazoles are potential antibacterial agents functioning as inhibitors of enoyl acyl carrier protein reductase (Fabl). Bioorg. Med. Chem. Lett. 11, 2061-2065
47. Parikh, S. L., Xiao, G. and Tonge, P. J. (2000) Inhibition of InhA, the enoyl reductase from Mycobacterium tuberculosis, by triclosan and isoniazid. Biochemistry 39, 7645-7650
48. Kuo, M. R., Morbidoni, H. R., Alland, D., Sneddon, S. F., Gourlie, B. B., Slaveski, M. M., Leonard, M., Gregory, J. S., Janjigian, A. D., Yee, C. et al. (2003) Targeting tuberculosis and malaria through inhibition of enoyl reductase. J. Biol. Chem. 278, 20851-20859
49. Goerg, H., Ochola, S. A. and Goerg, R. (1999) Treatment of malaria tropica with a fixed combination of rifampicin, co-trimoxazole and isoniazid: a clinical study. Chemotherapy 45, 68-76
50. Rosenfeld, I. S., D'Agnolo, G. and Vagelos, P. R. (1973) Synthesis of unsaturated fatty acids and the lesion in fabB mutants. J. Biol. Chem. 248, 2452-2460
51. D'Agnolo, G., Rosenfeld, I. S. and Vagelos, P. R. (1975) Multiple forms of β-ketoacyl-acyl carrier protein synthetase in Escherichia coli J. Biol. Chem. 250, 5289-5294
52. Garwin, J. L., Klages, A. L. and Cronan, Jr, J. E. (1980) β-Ketoacyl-acyl carrier protein synthase II of Escherichia coli evidence for function in the thermal regulation of fatty acid synthesis. J. Biol. Chem. 255, 3263-3265
53. Vance, D. E., Goldberg, I., Mitsuhashi, O., Bloch, K., Omura, S. and Nomura, S. (1972) Inhibition of fatty acid synthetases by the antibiotic cerulenin. Biochem. Biophys. Res. Commun. 48, 649-656
54. Kawaguchi, A., Tomoda, H., Nozoe, S., Omura, S. and Okuda, S. (1982) Mechanism of action of cerulenin on fatty acid synthetase: effect of cerulenin on iodotacetamide-induced malonyl-CoA decarboxylase activity. J. Biochem. (Tokyo) 92, 7-12
55. Kauppinen, S., Siggaard-Anderson, M. and van Wettstein-Knowles, P. (1988) β-Ketoacyl-ACP synthase I of Escherichia coli: nucleotide sequence of the fabB gene and identification of the cerulenin binding residue. Carlsberg Res. Commun. 53, 357-370
56. Heath, R. J. White, S. W. and Rock, C. Q. (2002) Inhibitors of fatty acid synthesis as antimicrobial chemotherapeutics. Appl. Microbiol. Biotechnol. 58, 695-703
57. Price, A. C., Choi, K.-H., Heath, R. J., Li, Z., White, S. W. and Rock, C. O. (2001) Inhibition of β-ketoacyl-acyl carrier protein syntheses by thiolactomycin and cerulenin. J. Biol. Chem. 276, 6551-6559
58. Tsay, J.-T., Rock, C. O. and Jackowski, S. (1992) Overproduction of β-ketoacyl-acyl carrier protein synthase I imparts thiolactomycin resistance to Escherichia coli K-12. J. Bacteriol. 174, 508-513
59. Jackowski, S., Murphy, C. M., Cronan, Jr, J. E. and Rock, C. O. (1989) Acetoacetyl-acyl carrier protein synthase: a target for the antibiotic thiolactomycin. J. Biol. Chem. 264, 7624-7629
60. Hayashi, I., Yamamoto, O., Sasaki, H., Kawaguchi, A. and Okazaki, H. (1983) Mechanism of action of the antibiotic thiolactomycin inhibition of fatty acid synthesis of Escherichia coli. Biochem. Biophys. Res. Commun. 115, 1108-1113
61. Waller, R. F., Reed, M. B., Cowman, A. F. and McFadden, G. I. (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19, 1794-1802
62. Bozdech, Z., Llinas, M., Pulliam, B. L., Wong, E. D., Zhu, J. and DeRisi, J. L. (2003) The transcriptome of the Intraerythrocytic developmental cycle of Plasmodium. PLoS Biol. 1, E5
63. LeRoch, K. G., Zhou, Y., Blair, P. L., Grainger, M., Moch, J. K., Haynes, J. D., De La Vega, P., Holder, A. A., Batalov, S., Carucci, D. J. and Winzeler, E. A. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 1503-1508
64. Maréchal, E. and Cesbron-Delauw, M.-F. (2001) The apicoplast: a new member of the plastid family. Trends Plant Sci. 6, 200-205
65. Gleeson, M. T. (2000) The plastid in Apicomplexa: what use is it? Int. J. Parasitol. 30, 1053-1070
66. McFadden, G. I., Reith, M., Munholland, J. and Lang-Unnasch, N. (1996) Plastid in human parasites. Nature (London) 381, 482
67. Wilson, R. J. M. (1993) Plastids better red than dead. Nature (London) 366, 638
68. McFadden, G. I. and Gilson, P. (1995) Something borrowed, something green: lateral transfer of chloroplasts by secondary endosymbiosis. Trends Ecol. Evol. 10, 12-17
69. Martin, W., Stoebe, B., Goremykin, V., Hapsmann, S., Hasegawa, M. and Kowallik, K. V. (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature (London) 14, 162-165
70. McFadden, G. I. (2001) Chloroplast origin and integration. Plant Physiol. 125, 50-53
71. Gardner, M. J., Shallom, S. J., Carlton, J. M., Salzberg, S. L., Nene, V., Shoaibi, A., Ciecko, A., Lynn, J., Rizzo, M., Weaver, B. et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature (London) 418, 498-511
72. Sato, S., Tews, I. and Wilson, R. (2000) Impact of a plastid-bearing endocytobiont on apicomplexan genomes. Int. J. Parasitol. 30, 427-439
73. Ralph, S. A., van Dooren, G. G., Waller, R. F., Crawford, M. J., Fraunholz, M. J., Foth, B. J., Tonkin, C. J., Roos, D. S. and McFadden, G. I. (2004) Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2, 203-216
74. Kubis, S. E. and Rawsthorne, S. (2000) The role of plastidial transporters in developing embryos of oilseed rape (Brassica napus L.) for fatty acid synthesis. Biochem. Soc. Trans. 28, 665-666
75. Furet, Y. X. and Pechere, J. C. (1991) Newly documented antimicrobial activity of quinolines. Eur. J. Clin. Microbiol. Infect. Dis. 10, 249-254
76. Cundliffe, E. (1990) Recognition sites for antibiotics within rRNA. In The Ribosome: Structure, Function and Evolution (Hill, W. H. et al., eds.), pp. 479-490, American Society of Microbiology, Washington
77. Fichera, M. E., Bhopale, M. K. and Roos, D. S. (1995) In vitro assays elucidate peculiar kinetics of clindamycin action against Toxoplasma gondii. Antimicrob. Agents Chemother. 39, 1530-1537
78. He, C. Y., Shaw, M. K., Pletcher, C. H., Striepen, B., Tilney, L. G. and Roos, D. S. (2001) A plastid segregation defect in the protozoan parasite Toxoplasma gondii. EMBO J. 20, 330-339
79. McFadden, G. I. and Roos, D. S. (1999) Apicomplexan plastids as drug targets. Trends Microbiol. 7, 328-333
80. Bhattacharjee, A. K., Hartell, M. G., Nichols, D. A., Hicks, R. P., Stanton, B., van Hamont, J. E. and Milhous, W. K. (2004) Structure-activity relationship study of antimalarial indolo[2,1-o]quinazoline-6,12-diones (tryptanthrins): three dimensional pharmacophore modeling and identification of new antimalarial candidates. Eur. J. Med. Chem. 39, 59-67