Acyl-CoA synthetase activity in Plasmodium knowlesi-infected erythrocytes displays peculiar substrate specificities.

In its blood stages the malaria parasite, Plasmodium, displays very high lipid metabolism. We present evidence for an abundant long-chain acyl-CoA synthetase (EC 6.2.1.3) activity in Plasmodium knowlesi-infected simian erythrocytes. The activity was found to be 20-fold higher in the schizont-infected (the last parasite stage) than in control erythrocytes. The cosubstrate requirements of the enzyme were similar to those previously reported for acyl-CoA synthetases from other sources. Among the separated reaction products of oleyl-CoA synthetase, only PPi and oleyl-CoA were inhibitory, with Ki over 350 microM. The fatty acid specificity of the parasite acyl-CoA synthetase activity was fairly marked and depended on the unsaturation state of the substrate. The tested fatty acids displayed similar Vmax, whereas their Km ranged from 11 (palmitate) to 59 microM (arachidonate). Finally, experiments involving heat inactivation and separation on hydroxyapatite excluded the presence of a specific arachidonyl-CoA synthetase identical to those present in other cells. On the other hand, fatty acid competition experiments evidenced the existence of at least two distinct enzymatic sites for fatty acid activation in P. knowlesi-infected simian erythrocytes: one is specific for saturated fatty acids and the other for polyunsaturated species, whereas oleate could be activated at both sites.

[1]  J. Folch,et al.  A simple method for the isolation and purification of total lipides from animal tissues. , 1957, The Journal of biological chemistry.

[2]  Saitoh Yasushi,et al.  Synthesis and metabolism of arachidonyl- and eicosapentaenoyl-CoA in rat aorta. , 1983 .

[3]  J. Kaufman,et al.  Cysteines in the transmembrane region of major histocompatibility complex antigens are fatty acylated via thioester bonds. , 1984, The Journal of biological chemistry.

[4]  M. Vaughan,et al.  INCORPORATION OF FATTY ACIDS INTO PHOSPHOLIPIDS OF ERYTHROCYTE MEMBRANES. , 1964, Journal of lipid research.

[5]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[6]  F. Gunstone,et al.  Selective transfer of cyclopropane acids by acyl coenzyme A: phospholipid acyltransferases. , 1969, The Journal of biological chemistry.

[7]  D. F. Wallach,et al.  A reevaluation of the status of cholesterol in erythrocytes infected by Plasmodium knowlesi and P. falciparum. , 1984, Molecular and biochemical parasitology.

[8]  H. Vial,et al.  Phospholipid Biosynthesis in Synchronous Plasmodium falciparum Cultures1 , 1982 .

[9]  T. Flatmark,et al.  Acyl-CoA synthetase activity of rat liver microsomes. Substrate specificity with special reference to very-long-chain and isomeric fatty acids. , 1981, Biochimica et biophysica acta.

[10]  I. Singh,et al.  Characterization of rat brain microsomal acyl-coenzyme A ligases: different enzymes for the synthesis of palmitoyl-coenzyme A and lignoceroyl-coenzyme A. , 1986, Archives of biochemistry and biophysics.

[11]  T. Tanaka,et al.  Purification and properties of long-chain acyl-coenzyme-A synthetase from rat liver. , 1979, European journal of biochemistry.

[12]  M. Mishina,et al.  Separation and characterization of two long-chain acyl-CoA synthetases from Candida lipolytica. , 1978, European journal of biochemistry.

[13]  I. Rosenfeld,et al.  Identification and quantitation of acyl thioesters by thin-layer chromatography of hydroxamic acid derivatives. , 1975, Analytical biochemistry.

[14]  W. Lands,et al.  Effects of ethylenic bond position upon acyltransferase activity with isomeric cis,cis-octadecadienoyl coenzyme A thiol esters. , 1968, The Journal of biological chemistry.

[15]  R. Ledeen,et al.  Long‐chain acyl‐coenzyme a synthetase in rat brain myelin , 1987, Journal of neuroscience research.

[16]  J. Russell,et al.  Characterization of an arachidonic acid-selective acyl-CoA synthetase from murine T lymphocytes. , 1985, Biochimica et biophysica acta.

[17]  J. Bar-Tana,et al.  The purification and properties of microsomal palmitoyl-coenzyme A synthetase. , 1971, The Biochemical journal.

[18]  P. Myler,et al.  Purification of mature schizonts of Plasmodium falciparum on colloidal silica gradients. , 1982, Bulletin of the World Health Organization.

[19]  G. Marinetti,et al.  Tightly (covalently) bound fatty acids in cell membrane proteins. , 1982, Biochimica et biophysica acta.

[20]  J. Mead,et al.  Long chain fatty acid activation in subcellular preparations from rat liver. , 1968, The Journal of biological chemistry.

[21]  Y. Marcel,et al.  Kinetic studies on the chain length specificity of long chain acyl coenzyme A synthetase from rat liver microsomes. , 1972, The Journal of biological chemistry.

[22]  D. Clark,et al.  Effects of diabetes mellitus on renal fatty acid activation and desaturation. , 1985, Biochemical pharmacology.

[23]  G. Holz,et al.  Lipids and the malarial parasite. , 1977, Bulletin of the World Health Organization.

[24]  H. Vial,et al.  Modification of the fatty acid composition of individual phospholipids and neutral lipids after infection of the simian erythrocyte by Plasmodium knowlesi. , 1986, Biochimica et biophysica acta.

[25]  N. Bazan,et al.  Kinetic properties of arachidonoyl-coenzyme A synthetase in rat brain microsomes. , 1983, Archives of biochemistry and biophysics.

[26]  H. Vial,et al.  Phospholipid biosynthesis by Plasmodium knowlesi-infected erythrocytes: the incorporation of phospohlipid precursors and the identification of previously undetected metabolic pathways. , 1982, The Journal of parasitology.

[27]  H. Vial,et al.  Cholinephosphotransferase and ethanolaminephosphotransferase activities in Plasmodium knowlesi-infected erythrocytes. Their use as parasite-specific markers. , 1984, Biochimica et biophysica acta.

[28]  S. Ōmura,et al.  Triacsins, new inhibitors of acyl-CoA synthetase produced by Streptomyces sp. , 1986, The Journal of antibiotics.

[29]  L. van Deenen,et al.  Metabolism of red-cell lipids. I. Incorporation in vitro of fatty acids into phospholipids from mature erythrocytes. , 1965, Biochimica et biophysica acta.

[30]  C. Homewood,et al.  A comparison of methods used for the removal of white cells from malaria-infected blood. , 1976, Annals of tropical medicine and parasitology.

[31]  P. Majerus,et al.  Arachidonoyl-CoA synthetase. Separation from nonspecific acyl-CoA synthetase and distribution in various cells and tissues. , 1985, The Journal of biological chemistry.

[32]  L. van Deenen,et al.  Metabolism of red-cell lipids. II. Conversions of lysophosphoglycerides. , 1965, Biochimica et biophysica acta.

[33]  D. Evered,et al.  Malaria and the red cell. (Ciba Foundation Symposium 94, held 27-29 April 1982, London, UK.). , 1983 .

[34]  K. Haldar,et al.  Acylation of a Plasmodium falciparum merozoite surface antigen via sn-1,2-diacyl glycerol. , 1985, The Journal of biological chemistry.

[35]  W. Renooij,et al.  Topological asymmetry of phospholipid metabolism in rat erythrocyte membranes. Evidence for flip-flop of lecithin. , 1976, European journal of biochemistry.

[36]  D. Riendeau,et al.  ATP- and coenzyme A-dependent fatty acid incorporation into proteins of cell-free extracts from mouse tissues. , 1986, The Journal of biological chemistry.

[37]  W. D. Nunn,et al.  Purification and characterization of acyl coenzyme A synthetase from Escherichia coli. , 1981, The Journal of biological chemistry.

[38]  P. Majerus,et al.  Discovery of an arachidonoyl coenzyme A synthetase in human platelets. , 1982, The Journal of biological chemistry.