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Activation of free fatty acids in subcellular fractions of human skeletal muscle

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Abstract

In human pathology littel is known about the activating enzymes for fatty acids of different carbon chain length. In order to have a better insight into disorders of lipid metabolism in human skeletal muscle, we studied the distribution of acyl-CoA synthetases in muscular subcellular fractions. We find that in muscle mainly long chain fatty acids are activated to CoA esters. Distribution of palmityl-CoA synthetase in subcellular fractions compared with marker enzymes suggested that this enzymatic activity is located only in the outer mitochondrial membrane, in contrast to human liver, where this enzyme is also located in the microsomes. In human skeletal muscle we also found low butyryl-CoA formation, which was limited to the mitochondrial matrix. This site of activation implies that short chain fatty acids may not depend on carnitine for their oxidation in the mitochondrial matrix, in contrast to long chain fatty acids activated in the outer mitochondrial membrane.

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References

  1. Aas, M., andBremer, J. 1968. Short chain fatty acid activation in rat liver. A new assay procedure for the enzymes and studies on their intracellular localization. Biochim. Biophys. Acta 164:157–166.

    Google Scholar 

  2. Aas, M., andBremer, J. 1969. Activation of propionate in rat kidney. FEBS Letters 5:57–59.

    Google Scholar 

  3. Aas, M. 1971. Organ and subcellular distribution of fatty acid activating enzymes in the rat. Biochim. Biophys. Acta 231:32–47.

    Google Scholar 

  4. Banis, R.J., andTove, S. B. 1974. Solubilization of long chain fatty acyl-CoA synthetase from chicken adipose tissue microsomes. Biochim. Biophys. Acta 348:210–220.

    Google Scholar 

  5. Bar Tana, J., Rose, C., andShapiro, B. 1968. Studies on medium chain fatty acylcoenzyme A synthetase, purification and properties. Biochem. J. 109:269–282.

    Google Scholar 

  6. Bar Tana, J., Rose, G., andShapiro, B. 1971. The purification and properties of microsomal palmitoyl-coenzyme A synthetase. Biochem. J. 122:353–362.

    Google Scholar 

  7. Berge, R. K., Vollet, S. E., andFarstad, M. 1980. Intracellular localization of palmitoyl-CoA hydrolase and palmitoyl-CoA synthetase in human blood platelets and liver. Scand. J. Clin. Lab. Invest. 40:271–278.

    Google Scholar 

  8. Bremer, J., Bjerve, K. S., Christopherson, B. O., Daae, L. N. W., Solberg, H. E., andAas, M. 1974. Factors controlling the metabolism of fatty acids in the liver. Pages 159–176,in Lundquist, F., andTygstrup, N. (eds.), Regulation of Hepatic Metabolism. Academic Press, New York.

    Google Scholar 

  9. Campagnari, F., andWebster, L. T. 1963. Purification and properties of acetyl coenzyme A synthetase from bovine heart mitochondria. J. Biol. Chem. 238:1628–1633.

    Google Scholar 

  10. Choi, Y. R., Fogle, P. J., Clarke, P. R. H., andBieber, L. L. 1977. Quantification of water-soluble acyl-carnitines and carnitine acyltransferases in rat tissue. J. Biol. Chem. 252:7930–7931.

    Google Scholar 

  11. DiMauro, S., Trevisan, C., andHays, A. 1980. Disorders of lipid metabolism in muscle. Muscle and Nerve 3:369–388.

    Google Scholar 

  12. Farstad, M., Aas, M., andSander, J. 1973. Long-chain acyl-CoA synthetase activity in blood platelets and some human tissues. Scand. J. Clin. Invest. 31:205–211.

    Google Scholar 

  13. Felig, P., andWharen, J. 1975. Fuel homeostasis in exercise. N. Engl. J. Med. 293:1078–1084.

    Google Scholar 

  14. Fritz, I. B., andYue, K. T. N. 1963. Long chain carnitine acyltransferase and the role of acylcarnitine derivatives in the catalytic increase of fatty acid oxidation induced by carnitine. J. Lipid. Res. 4:279–288.

    Google Scholar 

  15. Fritz, I. B., Kopec, B., andBrosnan, J. T. 1974. Localization of carnitine palmitoyl-transferases on inner membranes of mitochondria, and their possible role in the regulation of fatty acyl group translocation. Pages 482–497,in Lundquist, F., andTygstrup, N. (eds.), Regulation of Hepatic Metabolism. Academic Press, New York.

    Google Scholar 

  16. Groot, P. H. E., andHulsmann, W. C. 1973. The activation and oxidation of octanoate and palmitate by rat skeletal muscle mitochondria. Biochim. Biophys. Acta 316:124–135.

    Google Scholar 

  17. Groot, P. H. E., andVan Loon, C. M. I. 1975. The activation of short chain fatty acids by the soluble fraction of guinea-pig heart and liver mitochondria. Biochim. Biophys. Acta 380:12–20.

    Google Scholar 

  18. Hele, H. 1954. The acetate activating enzyme of beef heart. J. Biol. Chem. 206:671–676.

    Google Scholar 

  19. Hosaka, K., Mishina, M., Tanaka, T., Kamiryo, T., andNuma, S. 1979. Acyl-CoA synthetase I from Candida Lipolytica, purification properties and immunochemical studies. Eur. J. Biochem. 93:197–203.

    Google Scholar 

  20. Hryb, D. J., andHogg, J. F. 1979. Chain length specificities of peroxisomal and mitochondrial β-oxidation in rat liver. Biochem. Biophys. Res. Commun. 87:1200–1206.

    Google Scholar 

  21. Johnston, R. W., Osmundsen, H., andPark, M. V. 1979. Associative properties of butyryl-coenzyme A synthetase from ox liver mitochondria. Biochim. Biophys. Acta 569:70–81.

    Google Scholar 

  22. Lazarow, P. B. 1978. Rat liver peroxisomes catalyze the oxidation of fatty acids. J. Biol. Chem. 253:1522–1528.

    Google Scholar 

  23. Lippel, K., Robinson, J., andTrams, E. G. 1970. Intracellular distribution of palmitoyl-CoA synthetase in rat liver. Biochim. Biophys. Acta 206:173–177.

    Google Scholar 

  24. Londesborough, J. C., Yuan, S.L., andWebster, L. T. 1973. The molecular weight and thiol residues of acetyl-coenzyme A synthetase from ox heart mitochondria. Biochem. J. 133:23–36.

    Google Scholar 

  25. Maes, E., andBar Tana, J. 1977. Rat liver microsomal palmitoyl-CoA synthetase: Subunit structure. Biochim. Biophys. Acta 480:527–530.

    Google Scholar 

  26. Mahler, H. R., Wakil, S. J., andBock, R. M. 1953. Studies on fatty acid oxidation, enzymatic activation of fatty acids. J. Biol. Chem. 204:453–468.

    Google Scholar 

  27. Martin, P. A., Temple, N. J., andConnock, M. J. 1979. Zonal rotor study of the subcellular distribution of acyl-CoA synthetases, carnitine-acyl-transferases and phosphatidate phosphatase in the guinea pig small intestine. Eur. J. Cell. Biol. 19:3–10.

    Google Scholar 

  28. Matlib, M. A., Shannon, W. A., andSrere, P. A. 1977. Measurement of matrix enzyme activity in isolated mitochondria made permeable with toluene. Arch. Biochem. Biophys. 178:396–407.

    Google Scholar 

  29. McCaman, R. E., McCaman, M. W., Hunt, J. M., andSmith, M. S. 1965. Microdetermination of monoamineoxidase and 5-hydroxytryptophan decarboxilase activity in nervous tissues. J. Neurochem. 12:15–23.

    Google Scholar 

  30. Mishima, M., Kamiryo, T., Tashiro, S., andNuma, S. 1978. Separation and characterization of two long-chain acyl-CoA synthetases from Candida Lipolytica. Eur. J. Biochem. 82:347–354.

    Google Scholar 

  31. Nimmo, H. G. 1979. The location of glycerol-phosphate acyltransferase and fatty acyl-CoA synthetases on inner surface of the mitochondrial outer membrane. FEBS Letters 101:262–264.

    Google Scholar 

  32. Norum, K. R. 1964. Palmityl-CoA: carnitine palmityl-transferase. Purification from calf liver mitochondria and some properties of the enzyme. Biochim. Biophys. Acta 89:95–108.

    Google Scholar 

  33. Pande, S. V. 1972. Some properties of microsomal fatty acid activating enzyme of rat liver. Biochim. Biophys. Acta 270:197–208.

    Google Scholar 

  34. Paul, H. S., andAdibi, S. 1978. Effect of carnitine on branched-chain aminoacid oxidation by liver and skeletal muscle. Am. J. Physiol. 234:E 494-E 499.

    Google Scholar 

  35. Philipp, D. P., andParsons, P. 1979. Isolation and purification of long chain fatty acyl coenzyme-A ligase from rat liver mitochondria. J. Biol. Chem. 254:10776–10784.

    Google Scholar 

  36. Philipp, D. P., andParsons, P. 1979b. Kinetic characterization of long chain fatty acyl coenzyme A ligase from liver mitochondria. J. Biol. Chem. 254:10785–10790.

    Google Scholar 

  37. Racker, E., andProctor, H. 1970. Reconstitution of the outer mitochondrial membrane with monoamine oxidase. Biochim. Biophys. Res. Commun. 39:1120–1125.

    Google Scholar 

  38. Scholte, H. R. 1973. The separation and enzymatic characterization of inner and outer membranes of rat heart mitochondria. Biochim. Biophys. Acta 330:283–293.

    Google Scholar 

  39. Schnaitman, C., Erwin, V. G., andGreenawalt, J. W. 1967. The submitochondrial localization of monoamino axidase, an enzymatic marker for the outer membrane of rat liver mitochondria. J. Cell Biol. 32:719–735.

    Google Scholar 

  40. Solberg, H. E. 1972. Different carnitine acyl-transferases in calf liver. Biochim. Biophys. Acta 280:422–433.

    Google Scholar 

  41. Srere, P. A. 1963. Citryl-CoA and the citrate condensing enzyme. Biochim. Biophys. Acta 77:693–696.

    Google Scholar 

  42. Suzue, G., andMarcel, Y. 1972. Kinetic studies on the chain length specificity of long chain acyl-coenzyme A synthetase from rat liver microsomes. J. Biol. Chem. 247:6781–6783.

    Google Scholar 

  43. Tanaka, T., Hosaka, K., Hoshimaru, M., andNuma, S. 1979. Purification and properties of long-chain acyl-coenzyme-A synthetase from rat liver. Eur. J. Biochem. 98:165–172.

    Google Scholar 

  44. Webster, L. T., Gerowin, L. D., andRakita, L. 1965. Purification and characteristics of a butyryl coenzyme A synthetase from bovine heart mitochondria. J. Biol. Chem. 240:29–33.

    Google Scholar 

  45. Webster, L. T. 1965. Studies of the acetyl coenzyme A synthetase reaction. J. Biol. Biochem. 240:4158–4163.

    Google Scholar 

  46. Wharen, J. 1977. Glucose turnover during exercise in man. Ann. N. Y. Acad. Sci. 301:45–55.

    Google Scholar 

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Authors and Affiliations

  1. H. Houston Merritt Clinical Research Center for Muscular Dystrophy and Related Diseases Department of Neurology, Columbia University, 630 W. 168th Street, 10032, New York, New York

    Carlo Trevisan & Salvatore DiMauro

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  1. Carlo Trevisan
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  2. Salvatore DiMauro
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Dr. Trevisan is the recipient of a posdoctoral fellowship from the Muscular Dystrophy Association.

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Trevisan, C., DiMauro, S. Activation of free fatty acids in subcellular fractions of human skeletal muscle. Neurochem Res 8, 551–561 (1983). https://doi.org/10.1007/BF00964696

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