Make it or take it: Fatty acid metabolism of apicomplexan parasites

Eukaryotic Cell

Volumn 6, Issue 10, 2007, Pages 1727-1735

  Mazumdar, Jolly ^a,b   Striepen, Boris ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID SYNTHASE; POLYKETIDE SYNTHASE;

ANIMAL; APICOMPLEXA; ENDOPLASMIC RETICULUM; ENZYMOLOGY; LIPID METABOLISM; METABOLISM; PARASITE; SHORT SURVEY;

ANIMALS; APICOMPLEXA; ENDOPLASMIC RETICULUM; FATTY ACID SYNTHETASE COMPLEX; LIPID METABOLISM; PARASITES; POLYKETIDE SYNTHASES;

EID: 35348837375     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00255-07     Document Type: Short Survey

References (84)

1. Abrahamsen, M. S., T. J. Templeton, S. Enomoto, J. E. Abrahante, G. Zhu, C. A. Lancto, M. Deng, C. Liu, G. Widmer, S. Tzipori, G. A. Buck, P. Xu, A. T. Bankier, P. H. Dear, B. A. Konfortov, H. F. Spriggs, L. Iyer, V. Anantharaman, L. Aravind, and V. Kapur. 2004. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441-445.
2. Allary, M., J. Z. Lu, L. Zhu, and S. T. Prigge. 2007. Scavenging of the cofactor lipoate is essential for the survival of the malaria parasite Plasmodium falciparum. Mol. Microbiol. 63:1331-1344.
3. Bano, N., J. D. Romano, B. Jayabalasingham, and I. Coppens. 2007. Cellular interactions of Plasmodium liver stage with its host mammalian cell. Int. J. Parasitol. 37:1329-1341.
4. Bethke, L. L., M. Zilversmit, K. Nielsen, J. Daily, S. K. Volkman, D. Ndiaye, E. R. Lozovsky, D. L. Hartl, and D. F. Wirth. 2006. Duplication, gene conversion, and genetic diversity in the species-specific acyl-CoA synthetase gene family of Plasmodium falciparum. Mol. Biochem. Parasitol. 150:10-24.
5. Bisanz, C., O. Bastion, D. Grando, J. Jouhet, E. Marechal, and M. F. Cesbron-Delauw. 2006. Toxoplasma gondii acyl-lipid metabolism: de novo synthesis from apicoplast-generated fatty acids versus scavenging of host cell precursors. Biochem. J. 394:197-205.
6. Cai, X., D. Herschap, and G. Zhu. 2005. Functional characterization of an evolutionarily distinct phosphopantetheinyl transferase in the apicomplexan Cryptosporidium parvum. Eukaryot. Cell 4:1211-1220.
7. Charron, A. J., and L. D. Sibley. 2002. Host cells: mobilizable lipid resources for the intracellular parasite Toxoplasma gondii. J. Cell Sci. 115:3049-3059.
8. Chhibber, M., G. Kumar, P. Parasuraman, T. N. Ramya, N. Surolia, and A. Surolia. 2006. Novel diphenyl ethers: design, docking studies, synthesis and inhibition of enoyl ACP reductase of Plasmodium falciparum and Escherichia coli. Bioorg. Med. Chem. 14:8086-8098.
9. Coppens, I. 2006. Contribution of host lipids to Toxoplasma pathogenesis. Cell. Microbiol. 8:1-9.
10. Coppens, I., J. D. Dunn, J. D. Romano, M. Pypaert, H. Zhang, J. C. Boothroyd, and K. A. Joiner. 2006. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell 125:261-274.
11. Coppens, I., A. P. Sinai, and K. A. Joiner. 2000. Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J. Cell Biol. 149:167-180.
12. Crawford, M. J., N. Thomsen-Zieger, M. Ray, J. Schachtner, D. S. Roos, and F. Seeber. 2006. Toxoplasma gondii scavenges host-derived lipoic acid despite its de novo synthesis in the apicoplast. EMBO J. 25:3214-3222.
13. Crawford, M. J., G. Zhu, and D. S. Roos. 2003. Both type I and type II fatty acid synthases in Toxoplasma gondii, abstr. 14C. Mol. Parasitol. Meet. XIV.
14. Cronan, J. E., X. Zhao, and Y. Jiang. 2005. Function, attachment and synthesis of lipoic acid in Escherichia coli. Adv. Microb. Physiol. 50:103-146.
15. Ferguson, D. J., S. A. Campbell, F. L. Henriquez, L. Phan, E. Mui, T. A. Richards, S. P. Muench, M. Allary, J. Z. Lu, S. T. Prigge, F. Tomley, M. W. Shirley, D. W. Rice, R. McLeod, and C. W. Roberts. 2007. Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in Eimeria tenella. Int. J. Parasitol. 37:33-51.
16. Fleige, T., K. Fischer, D. J. Ferguson, U. Gross, and W. Bohne. 2007. Carbohydrate metabolism in the Toxoplasma gondii apicoplast: localization of three glycolytic isoenzymes, the single pyruvate dehydrogenase complex, and a plastid phosphate translocator. Eukaryot. Cell 6:984-996.
17. Foth, B. J., L. M. Stimmler, E. Handman, B. S. Crabb, A. N. Hodder, and G. I. McFadden. 2005. The malaria parasite Plasmodium falciparum has only one pyruvate dehydrogenase complex, which is located in the apicoplast. Mol. Microbiol. 55:39-53.
18. Fritzler, J. M., and G. Zhu. 2007. Functional characterization of the acyl-[acyl carrier protein] ligase in the Cryptosporidium parvum giant polyketide synthase. Int. J. Parasitol. 37:307-316.
19. Gardner, M. J., R. Bishop, T. Shah, E. P. de Villiers, J. M. Carlton, N. Hall, Q. Ren, I. T. Paulsen, A. Pain, M. Berriman, R. J. Wilson, S. Sato, S. A. Ralph, D. J. Mann, Z. Xiong, S. J. Shallom, J. Weidman, L. Jiang, J. Lynn, B. Weaver, A. Shoaibi, A. R. Domingo, D. Wasawo, J. Crabtree, J. R. Wortman, B. Haas, S. V. Angiuoli, T. H. Creasy, C. Lu, B. Suh, J. C. Silva, T. R. Utterback, T. V. Feldblyum, M. Pertea, J. Allen, W. C. Nierman, E. L. Taracha, S. L. Salzberg, O. R. White, H. A. Fitzhugh, S. Morzaria, J. C. Venter, C. M. Fraser, and V. Nene. 2005. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309:134-137.
20. Gerold, P., A. Dieckmann-Schuppert, and R. T. Schwarz. 1994. Glycosylphosphatidylinositols synthesized by asexual erythrocytic stages of the malarial parasite, Plasmodium falciparum. Candidates for plasmodial glycosylphosphatidylinositol membrane anchor precursors and pathogenicity factors. J. Biol. Chem. 269:2597-2606.
21. Goodman, C. D., and G. I. McFadden. 2007. Fatty acid biosynthesis as a drug target in apicomplexan parasites. Curr. Drug Targets 8:15-30.
22. Gueguen, V., D. Macherel, M. Jaquinod, R. Douce, and J. Bourguignon. 2000. Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J. Biol. Chem. 275:5016-5025.
23. Jelenska, J., M. J. Crawford, O. S. Harb, E. Zuther, R. Haselkorn, D. S. Roos, and P. Gornicki. 2001. Subcellular localization of acetyl-CoA carboxylase in the apicomplexan parasite Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 98:2723-2728.
24. Jelenska, J., A. Sirikhachornkit, R. Haselkorn, and P. Gornicki. 2002. The carboxyltransferase activity of the apicoplast acetyl-CoA carboxylase of Toxoplasma gondii is the target of aryloxyphenoxypropionate inhibitors. J. Biol. Chem. 277:23208-23215.
25. Joiner, K. A., S. A. Fuhrman, H. M. Miettinen, L. H. Kasper, and I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249:641-646.
26. Jomaa, H., J. Wiesner, S. Sanderbrand, B. Altincicek, C. Weidemeyer, M. Hintz, I. Turbachova, M. Eberl, J. Zeidler, H. K. Lichtenthaler, D. Soldati, and E. Beck. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285:1573-1576.
27. Jones, S. M., J. E. Urch, M. Kaiser, R. Brun, J. L. Harwood, C. Berry, and I. H. Gilbert. 2005. Analogues of thiolactomycin as potential antimalarial agents. J. Med. Chem. 48:5932-5941.
28. Kaiser, K., K. Matuschewski, N. Camargo, J. Ross, and S. H. Kappe. 2004. Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins. Mol. Microbiol. 51:1221-1232.
29. Kapoor, M., J. Gopalakrishnapai, N. Surolia, and A. Surolia. 2004. Mutational analysis of the triclosan-binding region of enoyl-ACP (acyl-carrier protein) reductase from Plasmodium falciparum. Biochem. J. 381:735-741.
30. Karnataki, A., A. Derocher, I. Coppens, C. Nash, J. E. Feagin, and M. Parsons. 2007. Cell cycle-regulated vesicular trafficking of Toxoplasma APT1, a protein localized to multiple apicoplast membranes. Mol. Microbiol. 63:1653-1668.
31. Knappe, S., U. I. Flugge, and K. Fischer. 2003. Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol. 131:1178-1190.
32. Kohler, S., C. F. Delwiche, P. W. Denny, L. G. Tilney, P. Webster, R. J. Wilson, J. D. Palmer, and D. S. Roos. 1997. A plastid of probable green algal origin in Apicomplexan parasites. Science 275:1485-1489.
33. Lack, G., E. Homberger-Zizzari, G. Folkers, L. Scapozza, and R. Perozzo. 2006. Recombinant expression and biochemical characterization of the unique elongating beta-ketoacyl-acyl carrier protein synthase involved in fatty acid biosynthesis of Plasmodium falciparum using natural and artificial substrates. J. Biol. Chem. 281:9538-9546.
34. Lee, S. H., J. L. Stephens, and P. T. Englund. 2007. A fatty-acid synthesis mechanism specialized for parasitism. Nat. Rev. Microbiol. 5:287-297.
35. Lee, S. H., J. L. Stephens, K. S. Paul, and P. T. Englund. 2006. Fatty acid synthesis by elongases in trypanosomes. Cell 126:691-699.
36. Leonard, A. E., S. L. Pereira, H. Sprecher, and Y. S. Huang. 2004. Elongation of long-chain fatty acids. Prog. Lipid Res. 43:36-54.
37. Mazumdar, J., E. Wilson, K. Masarek, C. Hunter, and B. Striepen. 2006. Apicoplast fatty acid synthesis is essential for organelle biogenesis and parasite survival in Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 103:13192-13197.
38. McFadden, G. I., M. E. Reith, J. Munholland, and N. Lang-Unnasch. 1996. Plastid in human parasites. Nature 381:482.
39. McLeod, R., S. P. Muench, J. B. Rafferty, D. E. Kyle, E. J. Mui, M. J. Kirisits, D. G. Mack, C. W. Roberts, B. U. Samuel, R. E. Lyons, M. Dorris, W. K. Milhous, and D. W. Rice. 2001. Triclosan inhibits the growth of Plasmodium falciparum and Toxoplasma gondii by inhibition of apicomplexan Fab I. Int. J. Parasitol. 31:109-113.
40. McMillan, P. J., L. M. Stimmler, B. J. Foth, G. I. McFadden, and S. Muller. 2005. The human malaria parasite Plasmodium falciparum possesses two distinct dihydrolipoamide dehydrogenases. Mol. Microbiol. 55:27-38.
41. Mikolajczak, S. A., V. Jacobs-Lorena, D. C. MacKellar, N. Camargo, and S. H. Kappe. 2007. L-FABP is a critical host factor for successful malaria liver stage development. Int. J. Parasitol. 37:483-489.
42. Mordue, D. G., S. Hakansson, I. Niesman, and L. D. Sibley. 1999. Toxoplasma gondii resides in a vacuole that avoids fusion with host cell endocytic and exocytic vesicular trafficking pathways. Exp. Parasitol. 92:87-99.
43. Mordue, D. G., and L. D. Sibley. 1997. Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J. Immunol. 159:4452-4459.
44. Mueller, A. K., N. Camargo, K. Kaiser, C. Andorfer, U. Frevert, K. Matuschewski, and S. H. Kappe. 2005. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc. Natl. Acad. Sci. USA 102:3022-3027.
45. Mueller, A. K., M. Labaied, S. H. Kappe, and K. Matuschewski. 2005. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433:164-167.
46. Muench, S. P., S. T. Prigge, R. McLeod, J. B. Rafferty, M. J. Kirisits, C. W. Roberts, E. J. Mui, and D. W. Rice. 2007. Studies of Toxoplasma gondii and Plasmodium falciparum enoyl acyl carrier protein reductase and implications for the development of antiparasitic agents. Acta Crystallogr. D 63:328-338.
47. Mulliri, K. A., L. Lim, S. A. Ralph, T. P. Spurck, E. Handman, and G. I. McFadden. 2006. Membrane transporters in the relict plastid of malaria parasites. Proc. Natl. Acad. Sci. USA 103:9572-9577.
48. Nicola, G., C. A. Smith, E. Lucumi, M. R. Kuo, L. Karagyozov, D. A. Fidock, J. C. Sacchettini, and R. Abagyan. 2007. Discovery of novel inhibitors targeting enoyl-acyl carrier protein reductase in Plasmodium falciparum by structure-based virtual screening. Biochem. Biophys. Res. Commun. 358:686-691.
49. Perozzo, R., M. Kuo, A. S. Sidhu, J. T. Valiyaveettil, R. Bittman, W. R. Jacobs, Jr., D. A. Fidock, and J. C. Sacchettini. 2002. Structural elucidation of the specificity of the antibacterial agent triclosan for malarial enoyl acyl carrier protein reductase. J. Biol. Chem. 277:13106-13114.
50. Quittnat, F., Y. Nishikawa, T. T. Stedman, D. R. Voelker, J. Y. Choi, M. M. Zahn, R. C. Murphy, R. M. Barkley, M. Pypaert, K. A. Joiner, and I. Coppens. 2004. On the biogenesis of lipid bodies in ancient eukaryotes: synthesis of triacylglycerols by a Toxoplasma DGAT1-related enzyme. Mol. Biochem. Parasitol. 138:107-122.
51. Ralph, S. A., G. G. Van Dooren, R. F. Waller, M. J. Crawford, M. J. Fraunholz, B. J. Foth, C. J. Tonkin, D. S. Roos, and G. I. McFadden. 2004. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2:203-216.
52. Rawsthorne, S. 2002. Carbon flux and fatty acid synthesis in plants. Prog. Lipid Res. 41:182-196.
53. Rein, K. S., and R. V. Snyder. 2006. The biosynthesis of polyketide metabolites by dinoflagellates. Adv. Appl. Microbiol. 59:93-125.
54. Salcedo, S. P., and D. W. Holden. 2005. Bacterial interactions with the eukaryotic secretory pathway. Curr. Opin. Microbiol. 8:92-98.
55. Sato, S., B. Clough, L. Coates, and R. J. Wilson. 2004. Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist 155:117-125.
56. Sharma, S. K., M. Kapoor, T. N. Ramya, S. Kumar, G. Kumar, R. Modak, S. Sharma, N. Surolia, and A. Surolia. 2003. Identification, characterization, and inhibition of Plasmodium falciparum beta-hydroxyacyl-acyl carrier protein dehydratase (FabZ). J. Biol. Chem. 278:45661-45671.
57. Shaw, M. K. 2003. Cell invasion by Theileria sporozoites. Trends Parasitol. 19:2-6.
58. Sinai, A. P., and K. A. Joiner. 1997. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51:415-462.
59. Sinai, A. P., P. Webster, and K. A. Joiner. 1997. Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J. Cell Sci. 110:2117-2128.
60. Snyder, R. V., M. A. Guerrero, C. D. Sinigalliano, J. Winshell, R. Perez, J. V. Lopez, and K. S. Rein. 2005. Localization of polyketide synthase encoding genes to the toxic dinoflagellate Karenia brevis. Phytochemistry 66:1767-1780.
61. Stephens, J. L., S. H. Lee, K. S. Paul, and P. T. Englund. 2007. Mitochondrial fatty acid synthesis in Trypanosoma brucei. J. Biol. Chem. 282:4427-4436.
62. Surolia, A., T. N. Ramya, V. Ramya, and N. Surolia. 2004. 'FAS't inhibition of malaria. Biochem. J. 383:401-412.
63. Surolia, N., and A. Surolia. 2001. Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat. Med. 7:167-173.
64. Swarnamukhi, P. L., S. K. Sharma, P. Bajaj, N. Surolia, A. Surolia, and K. Suguna. 2006. Crystal structure of dimeric FabZ of Plasmodium falciparum reveals conformational switching to active hexamers by peptide flips. FEBS Lett. 580:2653-2660.
65. Thomsen-Zieger, N., J. Schachtner, and F. Seeber. 2003. Apicomplexan parasites contain a single lipoic acid synthase located in the plastid. FEBS Lett. 547:80-86.
66. Tomavo, S. , J. F. Dubremetz, and R. T. Schwarz. 1992. A family of glycolipids from Toxoplasma gondii. Identification of candidate glycolipid precursor(s) for Toxoplasma gondii glycosylphosphatidylinositol membrane anchors. J. Biol. Chem. 267:11721-11728.
67. Tomova, C. , W. J. Geerts, T. Muller-Reichert, R. Entzeroth, and B. M. Humbel. 2006. New comprehension of the apicoplast of sarcocystis by transmission electron tomography. Biol. Cell 98:535-545.
68. Trenkamp, S., W. Martin, and K. Tietjen. 2004. Specific and differential inhibition of very-long-chain fatty acid elongases from Arabidopsis thaliana by different herbicides. Proc. Natl. Acad. Sci. USA 101:11903-11908.
69. van Dooren, G. G., M. Marti, C. J. Tonkin, L. M. Stimmler, A. F. Cowman, and G. I. McFadden. 2005. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol. Microbiol. 57:405-419.
70. van Dooren, G. G., L. M. Stimmler, and G. I. McFadden. 2006. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol. Rev. 30:596-630.
71. Vial, H. J., and M. L. Ancelin. 1992. Malarial lipids. An overview. Subcell. Biochem. 18:259-306.
72. Vielemeyer, O., M. T. McIntosh, K. A. Joiner, and I. Coppens. 2004. Neutral lipid synthesis and storage in the intraerythrocytic stages of Plasmodium falciparum. Mol. Biochem. Parasitol. 135:197-209.
73. Waller, R. F., P. J. Keeling, R. G. Donald, B. Striepen, E. Handman, N. Lang-Unnasch, A. F. Cowman, G. S. Besra, D. S. Roos, and G. I. McFadden. 1998. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 95:12352-12357.
74. Waller, R. F., S. A. Ralph, M. B. Reed, V. Su, J. D. Douglas, D. E. Minnikin, A. F. Cowman, G. S. Besra, and G. I. McFadden. 2003. A type II pathway for fatty acid biosynthesis presents drug targets in Plasmodium falciparum. Antimicrob. Agents Chemother. 47:297-301.
75. Wickramasinghe, S. R., K. A. Inglis, J. E. Urch, S. Muller, D. M. van Aalten, and A. H. Fairlamb. 2006. Kinetic, inhibition and structural studies on 3-oxoacyl-ACP reductase from Plasmodium falciparum, a key enzyme in fatty acid biosynthesis. Biochem. J. 393:447-457.
76. Wilson, R. J., P. W. Denny, P. R. Preiser, K. Rangachari, K. Roberts, A. Roy, A. Whyte, M. Strath, D. J. Moore, P. W. Moore, and D. H. Williamson. 1996. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 261:155-172.
77. Wrenger, C., and S. Muller. 2004. The human malaria parasite Plasmodium falciparum has distinct organelle-specific lipoylation pathways. Mol. Microbiol. 53:103-113.
78. Zeng, B., X. Cai, and G. Zhu. 2006. Functional characterization of a fatty acyl-CoA-binding protein (ACBP) from the apicomplexan Cryptosporidium parvum. Microbiology 152:2355-2363.
79. Zeng, B., and G. Zhu. 2006. Two distinct oxysterol binding protein-related proteins in the parasitic protist Cryptosporidium parvum (Apicomplexa). Biochem. Biophys. Res. Commun. 346:591-599.
80. Zhu, G. 2004. Current progress in the fatty acid metabolism in Cryptosporidium parvum. J. Eukaryot. Microbiol. 51:381-388.
81. Zhu, G., M. J. LaGier, F. Stejskal, J. J. Millership, X. Cai, and J. S. Keithly. 2002. Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase. Gene 298:79-89.
82. Zhu, G., Y. Li, X. Cai, J. J. Millership, M. J. Marchewka, and J. S. Keithly. 2004. Expression and functional characterization of a giant type I fatty acid synthase (CpFAS1) gene from Cryptosporidium parvum. Mol. Biochem. Parasitol. 134:127-135.
83. Zhu, G., M. J. Marchewka, and J. S. Keithly. 2000. Cryptosporidium parvum appears to lack a plastid genome. Microbiology 146:315-321.
84. Zhu, G., M. J. Marchewka, K. M. Woods, S. J. Upton, and J. S. Keithly. 2000. Molecular analysis of a type I fatty acid synthase in Cryptosporidium parvum. Mol. Biochem. Parasitol. 105:253-260.