Intraerythrocytic Plasmodium falciparum utilize a broad range of serum-derived fatty acids with limited modification for their growth | Parasitology | Cambridge Core (original) (raw)

Abstract

Plasmodium falciparum causes the most severe form of malaria. Utilization of fatty acids in serum is thought to be necessary for survival of this parasite in erythrocytes, and thus characterization of the parasite fatty acid metabolism is important in developing a new strategy for controlling malaria. Here, we examined which combinations of fatty acids present in human serum support the continuous culture of P. falciparum in serum-free medium. Metabolic labelling and gas chromatography analyses revealed that, despite the need for particular fatty acids for the growth of intraerythrocytic P. falciparum, it can metabolize a broad range of serum-derived fatty acids into the major lipid species of their membranes and lipid bodies. In addition, these analyses showed that the parasite's overall fatty acid composition reflects that of the medium, although the parasite has a limited capacity to desaturate and elongate serum-derived fatty acids. These results indicate that the Plasmodium parasite is distinct from most cells, which maintain their fatty acid composition by coordinating de novo biosynthesis, scavenging, and modification (desaturation and elongation).

References

Asahi, H.,Kanazawa, T.,Hirayama, N. andKajihara, Y. (2005).Investigating serum factors promoting erythrocytic growth of Plasmodium falciparum.Experimental Parasitology 109,7–15.CrossRefGoogle Scholar

Bligh, E. G. andDyer, W. J. (1959).A rapid method of total lipid extraction and purification.Canadian Journal of Biochemistry and Physiology 37,911–917.CrossRefGoogle Scholar

Grellier, P.,Rigomier, D.,Clavey, V.,Fruchart, J.-C. andSchrevel, J. (1991).Lipid traffic between high density proteins and _Plasmodium falciparum_-infected red blood cells.Journal of Cell Biology 112,267–277.CrossRefGoogle Scholar

Hanada, K.,Mitamura, T.,Fukasawa, M.,Magistrado, P. A.,Horii, T. andNishijima, M. (2000).Neutral sphingomyelinase activity dependent on Mg2+ and anionic phospholipids in the intraerythrocytic malaria parasite Plasmodium falciparum.The Biochemical Journal 346,671–677.CrossRefGoogle Scholar

Heusser, D. (1968).Thin-layer chromatography of fatty acids on silanized silica gel.Journal of Chromatography 33,62–69.CrossRefGoogle Scholar

Holz, G. G. (1977).Lipids and the malaria parasite.Bulletin of the World Health Organization 55,237–248.Google Scholar

Hsiao, L. L.,Howard, R. J.,Aikawa, M. andTaraschi, T. F. (1991).Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum.The Biochemical Journal 274,121–132.CrossRefGoogle Scholar

Kaluzny, M. A.,Duncan, L. A.,Merritt, M. V. andEpps, D. E. (1985).Rapid separation of lipid classes in high yield and purity using bonded phase columns.Journal of Lipid Research 26,135–140.Google Scholar

Khunyoshyeng, S.,Cheevadhanarak, S.,Rachdawong, S. andTanticharoen, M. (2002).Differential expression of desaturases and changes in fatty acid composition during sporangiospore germination and development in Mucor rouxii.Fungal Genetics and Biology 37,13–21.CrossRefGoogle Scholar

Krishnegowda, G. andGowda, D. C. (2003).Intraerythrocytic Plasmodium falciparum incorporates extraneous fatty acids to its lipids without any structural modification.Molecular and Biochemical Parasitology 132,55–58.CrossRefGoogle Scholar

Matsuzaka, T.,Shimano, H.,Yahagi, N.,Yoshikawa, T.,Amemiya-Kudo, M.,Hasty, A. H.,Okazaki, H.,Tamura, Y.,Iizuka, Y.,Ohashi, K.,Osuga, J.,Takahashi, A.,Yato, S.,Sone, H.,Ishibashi, S. andYamada, N. (2002).Cloning and characterization of a mammalian fatty acyl-CoA elongase as a lipogenic enzyme regulated by SREBPs.Journal of Lipid Research 43,911–920.Google Scholar

Mitamura, T.,Hanada, K.,Ko-Mitamura, E. P.,Nishijima, M. andHorii, T. (2000).Serum factors governing intraerythrocytic development and cell cycle progression of Plasmodium falciparum.Parasitology International 49,219–229.CrossRefGoogle Scholar

Mitamura, T. andPalacpac, N. M. Q. (2003).Lipid metabolism in _Plasmodium falciparum_-infected erythrocyte: possible new targets for malaria chemotherapy.Microbes and Infections 5,545–552.CrossRefGoogle Scholar

Ofulla, A. V. O.,Okaoye, V. C. N.,Khan, B.,Githure, J. I.,Roberts, C. R.,Johnson, A. J. andMartin, S. K. (1993).Cultivation of Plasmodium falciparum parasites in a serum-free medium.American Journal of Tropical Medicine and Hygiene 49,335–340.CrossRefGoogle Scholar

Palacpac, N. M. Q.,Hiramine, Y.,Mi-ichi, F.,Torii, M.,Kita, K.,Hiramatsu, R.,Horii, T. andMitamura, T. (2004).Developmental stage-specific triacylglycerol biosynthesis, degradation and trafficking as lipid bodies in _Plasmodium falciparum_-infected erythrocyte.Journal of Cell Science 117,1469–1480.CrossRefGoogle Scholar

Surolia, N. andSurolia, A. (2001).Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum.Nature, Medicine 7,167–173.CrossRefGoogle Scholar

Trager, W. andJensen, J. B. (1976).Human malaria parasites in continuous culture.Science 193,673–675.CrossRefGoogle Scholar

Vial, H. J. andAncelin, M. L. (1998).Malarial lipids. In_Parasite Biology, Pathogenesis, and Protection_ ( ed. Sherman, I. W.), pp.159–175.ASM Press,Washington, D.C.

Vial, H. J.,Thuet, M. J. andPhilippot, J. R. (1982).Phospholipid biosynthesis in synchronous Plasmodium falciparum cultures.Journal of Protozoology 29,258–263.CrossRefGoogle Scholar