Oleic acid biosynthesis in Plasmodium falciparum: Characterization of the stearoyl-CoA desaturase and investigation as a potential therapeutic target

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Gratraud, Paul ^a   Huws, Enlli ^b   Falkard, Brie ^c   Adjalley, Sophie ^c   Fidock, David A ^c   Berry, Laurence ^a   Jacobs Jr , William R ^d   Baird, Mark S ^b   Vial, Henri ^a   Kremer, Laurent ^a  

^a UNIVERSITÉ DE MONTPELLIER   (France)

^b BANGOR UNIVERSITY   (United Kingdom)

^c Columbia University ^*  (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE; ACYL COENZYME A DESATURASE INHIBITOR; ANTIMALARIAL AGENT; ENZYME INHIBITOR; METHYL STERCULATE; OLEIC ACID; PALMITIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; STEARIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL LABELING; CELL LYSATE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ERYTHROCYTE; FATTY ACID SYNTHESIS; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSGENIC ORGANISM;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIMALARIALS; CYCLOPROPANES; ERYTHROCYTES; ESCHERICHIA COLI; FATTY ACIDS; GREEN FLUORESCENT PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; OLEIC ACID; PLASMODIUM FALCIPARUM; SEQUENCE HOMOLOGY, AMINO ACID; STEAROYL-COA DESATURASE;

MAMMALIA; PLASMODIUM FALCIPARUM;

EID: 70249092571     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006889     Document Type: Article

References (68)

1. Greenwood BM, Fidock DA, Kyle DE, Kappe SH, Alonso PL, et al. (2008) Malaria: progress, perils, and prospects for eradication. J Clin Invest 118: 1266-1276.
2. Mitamura T, Hanada K, Ko-Mitamura EP, Nishijima M, Horii T (2000) Serum factors governing intraerythrocytic development and cell cycle progression of Plasmodium falciparum. Parasitol Int 49: 219-229.
3. Vial HJ, Thuet MJ, Broussal JL, Philippot JR (1982) Phospholipid biosynthesis by Plasmodium knowlesi-infected erythrocytes: the incorporation of phospohlipid precursors and the identification of previously undetected metabolic pathways. J Parasitol 68: 379-391.
4. Vial HJ, Ancelin ML (1992) Malarial lipids. An overview. Subcell Biochem 18: 259-306.
5. Vial HJ, Ben Mamoun C (2005) In: Molecular Approaches to Malaria. Sherman IW, ed. Washington D. C.: ASM Press. pp 327-352. pp 327-352.
6. Mitamura T, Palacpac NM (2003) Lipid metabolism in Plasmodium falciparum-infected erythrocytes: possible new targets for malaria chemotherapy. Microbes Infect 5: 545-552.
7. Mazumdar J, Striepen B (2007) Make it or take it: fatty acid metabolism of apicomplexan parasites. Eukaryot Cell 6: 1727-1735.
8. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, et al. (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci U S A 95: 12352-12357.
9. Surolia N, Surolia A (2001) Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat Med 7: 167-173.
10. Yu M, Kumar TR, Nkrumah LJ, Coppi A, Retzlaff S, et al. (2008) The fatty acid biosynthesis enzyme FabI plays a key role in the development of liver-stage malarial parasites. Cell Host Microbe 4: 567-578.
11. Vaughan AM, O'Neill MT, Tarun AS, Camargo N, Phuong TM, et al. (2009) Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell Microbiol 11: 506-520.
12. Krishnegowda G, Gowda DC (2003) Intraerythrocytic Plasmodium falciparum incorporates extraneous fatty acids to its lipids without any structural modification. Mol Biochem Parasitol 132: 55-58.
13. Shanklin J, Whittle E, Fox BG (1994) Eight histidine residues are catalytically essential in a membrane-associated iron enzyme, stearoyl-CoA desaturase, and are conserved in alkane hydroxylase and xylene monooxygenase. Biochemistry 33: 12787-12794.
14. Miyazaki M, Kim YC, Gray-Keller MP, Attie AD, Ntambi JM (2000) The biosynthesis of hepatic cholesterol esters and triglycerides is impaired in mice with a disruption of the gene for stearoyl-CoA desaturase 1. J Biol Chem 275: 30132-30138.
15. Phetsuksiri B, Jackson M, Scherman H, McNeil M, Besra GS, et al. (2003) Unique mechanism of action of the thiourea drug isoxyl on Mycobacterium tuberculosis. J Biol Chem 278: 53123-53130.
16. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
17. Nkrumah LJ, Muhle RA, Moura PA, Ghosh P, Hatfull GF, et al. (2006) Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat Methods 3: 615-621.
18. Lambros C, Vanderberg JP (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
19. Fidock DA, Nomura T, Wellems TE (1998) Cycloguanil and its parent compound proguanil demonstrate distinct activities against Plasmodium falciparum malaria parasites transformed with human dihydrofolate reductase. Mol Pharmacol 54: 1140-1147.
20. Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, et al. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137: 13-21.
21. Kyes S, Pinches R, Newbold C (2000) A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol Biochem Parasitol 105: 311-315.
22. Kremer L, Guerardel Y, Gurcha SS, Locht C, Besra GS (2002) Temperature-induced changes in the cell-wall components of Mycobacterium thermoresistibile. Microbiology 148: 3145-3154.
23. Baird MS, Dale CM, Lytollis W, Simpson MJ (1992) Tetrahedron Letts 33: 1521-1522.
24. Baird MS, Grehan B (1993) J Chem Soc Perkin Trans 1: 1547-1548.
25. Fulco AJ, Bloch K (1964) Cofactor Requirements for the Formation of Delta-9-Unsaturated Fatty Acids in Mycobacterium Phlei. J Biol Chem 239: 993-997.
26. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
27. Desjardins RE, Canfield CJ, Haynes JD, Chulay JD (1979) Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother 16: 710-718.
28. Trang DT, Huy NT, Kariu T, Tajima K, Kamei K (2004) One-step concentration of malarial parasite-infected red blood cells and removal of contaminating white blood cells. Malar J 3: 7.
29. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
30. Strittmatter P, Spatz L, Corcoran D, Rogers MJ, Setlow B, et al. (1974) Purification and properties of rat liver microsomal stearyl coenzyme A desaturase. Proc Natl Acad Sci U S A 71: 4565-4569.
31. Martin CE, Oh CS, Jiang Y (2007) Regulation of long chain unsaturated fatty acid synthesis in yeast. Biochim Biophys Acta 1771: 271-285.
32. Stukey JE, McDonough VM, Martin CE (1990) The OLE1 gene of Saccharomyces cerevisiae encodes the delta 9 fatty acid desaturase and can be functionally replaced by the rat stearoyl-CoA desaturase gene. J Biol Chem 265: 20144-20149.
33. Wicker-Thomas C, Henriet C, Dallerac R (1997) Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochem Mol Biol 27: 963-972.
34. Man WC, Miyazaki M, Chu K, Ntambi JM (2006) Membrane topology of mouse stearoyl-CoA desaturase 1. J Biol Chem 281: 1251-1260.
35. Mi-Ichi F, Kita K, Mitamura T (2006) Intraerythrocytic Plasmodium falciparum utilize a broad range of serum-derived fatty acids with limited modification for their growth. Parasitology 133: 399-410.
36. Heinemann FS, Ozols J (2003) Stearoyl-CoA desaturase, a short-lived protein of endoplasmic reticulum with multiple control mechanisms. Prostaglandins Leukot Essent Fatty Acids 68: 123-133.
37. Wang J, Yu L, Schmidt RE, Su C, Huang X, et al. (2005) Characterization of HSCD5, a novel human stearoyl-CoA desaturase unique to primates. Biochem Biophys Res Commun 332: 735-742.
38. Flowers MT, Ntambi JM (2008) Role of stearoyl-coenzyme A desaturase in regulating lipid metabolism. Curr Opin Lipidol 19: 248-256.
39. Enoch HG, Catala A, Strittmatter P (1976) Mechanism of rat liver microsomal stearyl-CoA desaturase. Studies of the substrate specificity, enzyme-substrate interactions, and the function of lipid. J Biol Chem 251: 5095-5103.
40. Miyazaki M, Bruggink SM, Ntambi JM (2006) Identification of mouse palmitoyl-coenzyme A Delta9-desaturase. J Lipid Res 47: 700-704.
41. Kumar N, Koski G, Harada M, Aikawa M, Zheng H (1991) Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family. Mol Biochem Parasitol 48: 47-58.
42. van Dooren GG, Marti M, Tonkin CJ, Stimmler LM, Cowman AF, et al. (2005) Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol 57: 405-419.
43. Mouray E, Moutiez M, Girault S, Sergheraert C, Florent I, et al. (2007) Biochemical properties and cellular localization of Plasmodium falciparum protein disulfide isomerase. Biochimie 89: 337-346.
44. Elmendorf HG, Haldar K (1993) Identification and localization of ERD2 in the malaria parasite Plasmodium falciparum: separation from sites of sphingomyelin synthesis and implications for organization of the Golgi. Embo J 12: 4763-4773.
45. Tilley L, McFadden G, Cowman A, Klonis N (2007) Illuminating Plasmodium falciparum-infected red blood cells. Trends Parasitol 23: 268-277.
46. Munro S, Pelham HR (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48: 899-907.
47. Haldar K, Holder AA (1993) Export of parasite proteins to the erythrocyte in Plasmodium falciparum-infected cells. Semin Cell Biol 4: 345-353.
48. Jeffcoat R, Pollard MR (1977) Studies on the inhibition of the desaturases by cyclopropenoid fatty acids. Lipids 12: 480-485.
49. Johnson AR, Pearson JA, Shenstone FS, Fogerty AC (1967) Inhibition of the desaturation of stearic to oleic acid by cyclopropene fatty acids. Nature 214: 1244-1245.
50. Vial HJ, Thuet MJ, Philippot JR (1982) Phospholipid biosynthesis in synchronous Plasmodium falciparum cultures. J Protozool 29: 258-263.
51. Hsiao LL, Howard RJ, Aikawa M, Taraschi TF (1991) Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum. Biochem J 274 (Pt 1): 121-132.
52. Beaumelle BD, Vial HJ (1986) Modification of the fatty acid composition of individual phospholipids and neutral lipids after infection of the simian erythrocyte by Plasmodium knowlesi. Biochim Biophys Acta 877: 262-270.
53. Berenbaum MC (1978) A method for testing for synergy with any number of agents. J Infect Dis 137: 122-130.
54. Gupta S, Thapar MM, Wernsdorfer WH, Bjorkman A (2002) In vitro interactions of artemisinin with atovaquone, quinine, and mefloquine against Plasmodium falciparum. Antimicrob Agents Chemother 46: 1510-1515.
55. Krugliak M, Deharo E, Shalmiev G, Sauvain M, Moretti C, et al. (1995) Antimalarial effects of C18 fatty acids on Plasmodium falciparum in culture and on Plasmodium vinckei petteri and Plasmodium yoelii nigeriensis in vivo. Exp Parasitol 81: 97-105.
56. Moll GN, Vial HJ, Ancelin ML, Op den Kamp JA, Roelofsen B, et al. (1988) Phospholipid uptake by Plasmodium knowlesi infected erythrocytes. FEBS Lett 232: 341-346.
57. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, et al. (2004) Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216.
58. Lee SH, Stephens JL, Paul KS, Englund PT (2006) Fatty acid synthesis by elongases in trypanosomes. Cell 126: 691-699.
59. Lee SH, Stephens JL, Englund PT (2007) A fatty-acid synthesis mechanism specialized for parasitism. Nat Rev Microbiol 5: 287-297.
60. Santiago TC, Zufferey R, Mehra RS, Coleman RA, Mamoun CB (2004) The Plasmodium falciparum PfGatp is an endoplasmic reticulum membrane protein important for the initial step of malarial glycerolipid synthesis. J Biol Chem 279: 9222-9232.
61. Naik RS, Branch OH, Woods AS, Vijaykumar M, Perkins DJ, et al. (2000) Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. J Exp Med 192: 1563-1576.
62. Jackson KE, Klonis N, Ferguson DJ, Adisa A, Dogovski C, et al. (2004) Food vacuole-associated lipid bodies and heterogeneous lipid environments in the malaria parasite, Plasmodium falciparum. Mol Microbiol 54: 109-122.
63. Skinner TS, Manning LS, Johnston WA, Davis TM (1996) In vitro stage-specific sensitivity of Plasmodium falciparum to quinine and artemisinin drugs. Int J Parasitol 26: 519-525.
64. Waller RF, Ralph SA, Reed MB, Su V, Douglas JD, et al. (2003) A type II pathway for fatty acid biosynthesis presents drug targets in Plasmodium falciparum. Antimicrob Agents Chemother 47: 297-301.
65. Vial HJ, Wein S, Farenc C, Kocken C, Nicolas O, et al. (2004) Prodrugs of bisthiazolium salts are orally potent antimalarials. Proc Natl Acad Sci U S A 101: 15458-15463.
66. Chimanuka B, Francois G, Timperman G, Heyden YV, Holenz J, et al. (2001) A comparison of the stage-specific efficacy of chloroquine, artemether and dioncophylline B against the rodent malaria parasite Plasmodium chabaudi chabaudi in vivo. Parasitol Res 87: 795-803.
67. Dieckmann A, Jung A (1986) Stage-specific sensitivity of Plasmodium falciparum to antifolates. Z Parasitenkd 72: 591-594.
68. Fogerty AC, Johnson AR, Pearson JA (1972) Ring position in cyclopropene fatty acids and stearic acid desaturation in hen liver. Lipids 7: 335-338.