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Intraerythrocytic Plasmodium falciparum utilize a broad range of serum-derived fatty acids with limited modification for their growth

Published online by Cambridge University Press:  19 June 2006

F. MI-ICHI
Affiliation:
Department of Molecular Protozoology, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan Department of Biomedical Chemistry, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyou-ku, Tokyo 113-0033, Japan
K. KITA
Affiliation:
Department of Biomedical Chemistry, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyou-ku, Tokyo 113-0033, Japan
T. MITAMURA
Affiliation:
Department of Molecular Protozoology, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan

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).

Type
Research Article
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Asahi, H., Kanazawa, T., Hirayama, N. and Kajihara, Y. ( 2005). Investigating serum factors promoting erythrocytic growth of Plasmodium falciparum. Experimental Parasitology 109, 715.CrossRefGoogle Scholar
Bligh, E. G. and Dyer, W. J. ( 1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911917.CrossRefGoogle Scholar
Grellier, P., Rigomier, D., Clavey, V., Fruchart, J.-C. and Schrevel, J. ( 1991). Lipid traffic between high density proteins and Plasmodium falciparum-infected red blood cells. Journal of Cell Biology 112, 267277.CrossRefGoogle Scholar
Hanada, K., Mitamura, T., Fukasawa, M., Magistrado, P. A., Horii, T. and Nishijima, M. ( 2000). Neutral sphingomyelinase activity dependent on Mg2+ and anionic phospholipids in the intraerythrocytic malaria parasite Plasmodium falciparum. The Biochemical Journal 346, 671677.CrossRefGoogle Scholar
Heusser, D. ( 1968). Thin-layer chromatography of fatty acids on silanized silica gel. Journal of Chromatography 33, 6269.CrossRefGoogle Scholar
Holz, G. G. ( 1977). Lipids and the malaria parasite. Bulletin of the World Health Organization 55, 237248.Google Scholar
Hsiao, L. L., Howard, R. J., Aikawa, M. and Taraschi, T. F. ( 1991). Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum. The Biochemical Journal 274, 121132.CrossRefGoogle Scholar
Kaluzny, M. A., Duncan, L. A., Merritt, M. V. and Epps, D. E. ( 1985). Rapid separation of lipid classes in high yield and purity using bonded phase columns. Journal of Lipid Research 26, 135140.Google Scholar
Khunyoshyeng, S., Cheevadhanarak, S., Rachdawong, S. and Tanticharoen, 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, 1321.CrossRefGoogle Scholar
Krishnegowda, G. and Gowda, D. C. ( 2003). Intraerythrocytic Plasmodium falciparum incorporates extraneous fatty acids to its lipids without any structural modification. Molecular and Biochemical Parasitology 132, 5558.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. and Yamada, N. ( 2002). Cloning and characterization of a mammalian fatty acyl-CoA elongase as a lipogenic enzyme regulated by SREBPs. Journal of Lipid Research 43, 911920.Google Scholar
Mitamura, T., Hanada, K., Ko-Mitamura, E. P., Nishijima, M. and Horii, T. ( 2000). Serum factors governing intraerythrocytic development and cell cycle progression of Plasmodium falciparum. Parasitology International 49, 219229.CrossRefGoogle Scholar
Mitamura, T. and Palacpac, N. M. Q. ( 2003). Lipid metabolism in Plasmodium falciparum-infected erythrocyte: possible new targets for malaria chemotherapy. Microbes and Infections 5, 545552.CrossRefGoogle Scholar
Ofulla, A. V. O., Okaoye, V. C. N., Khan, B., Githure, J. I., Roberts, C. R., Johnson, A. J. and Martin, S. K. ( 1993). Cultivation of Plasmodium falciparum parasites in a serum-free medium. American Journal of Tropical Medicine and Hygiene 49, 335340.CrossRefGoogle Scholar
Palacpac, N. M. Q., Hiramine, Y., Mi-ichi, F., Torii, M., Kita, K., Hiramatsu, R., Horii, T. and Mitamura, T. ( 2004). Developmental stage-specific triacylglycerol biosynthesis, degradation and trafficking as lipid bodies in Plasmodium falciparum-infected erythrocyte. Journal of Cell Science 117, 14691480.CrossRefGoogle Scholar
Surolia, N. and Surolia, A. ( 2001). Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nature, Medicine 7, 167173.CrossRefGoogle Scholar
Trager, W. and Jensen, J. B. ( 1976). Human malaria parasites in continuous culture. Science 193, 673675.CrossRefGoogle Scholar
Vial, H. J. and Ancelin, M. L. ( 1998). Malarial lipids. In Parasite Biology, Pathogenesis, and Protection ( ed. Sherman, I. W.), pp. 159175. ASM Press, Washington, D.C.
Vial, H. J., Thuet, M. J. and Philippot, J. R. ( 1982). Phospholipid biosynthesis in synchronous Plasmodium falciparum cultures. Journal of Protozoology 29, 258263.CrossRefGoogle Scholar