Abstract
To study the mechanism of lipoprotein lipase (LPL) regulation by exercise, we recruited 16 healthy athletes to undergo a 2-wk period of detraining. Fasting fat and muscle biopsies were performed both before and after the detraining period. In muscle, detraining resulted in a decrease in LPL activity in both the heparin-releasable (HR) (-45%, P < 0.05) and cellular (extractable [EXT]) (-75%, P < 0.005) fractions, with no significant changes in LPL immunoreactive mass and mRNA levels. However, several subjects demonstrated parallel decreases in LPL mass and mRNA levels with detraining, suggesting that there is some degree of heterogeneity in response. In adipose tissue, detraining had the opposite effects on LPL activity. In the HR fraction, detraining resulted in an 86% increase (P < 0.005) in LPL activity, which was paralleled by a 100% (P = 0.02) increase in HR mass. However, there was no significant change in EXT LPL activity or EXT LPL mass. There were no changes in adipose LPL synthetic rate or LPL mRNA levels with detraining. The ratio of adipose tissue/muscle LPL, which may be an important indicator of the tendency for storage of circulating lipids in adipose tissue, increased significantly after detraining. The adipose/muscle LPL ratio was 0.51 +/- 0.17 in the exercising runners, and 4.45 +/- 2.46 in the same runners after detraining (P < 0.05). Thus, detraining of athletes resulted in a decrease in muscle LPL that occurred through post-translational mechanisms, whereas adipose tissue LPL increased, also due to posttranslational changes. This decrease in muscle LPL, coupled with an increase in adipose LPL, yielded a condition favoring adipose tissue storage.
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- Belfrage P., Vaughan M. Simple liquid-liquid partition system for isolation of labeled oleic acid from mixtures with glycerides. J Lipid Res. 1969 May;10(3):341–344. [PubMed] [Google Scholar]
- Borensztajn J., Rone M. S., Babirak S. P., McGarr J. A., Oscai L. B. Effect of exercise on lipoprotein lipase activity in rat heart and skeletal muscle. Am J Physiol. 1975 Aug;229(2):394–397. doi: 10.1152/ajplegacy.1975.229.2.394. [DOI] [PubMed] [Google Scholar]
- Ch'ng J. L., Mulligan R. C., Schimmel P., Holmes E. W. Antisense RNA complementary to 3' coding and noncoding sequences of creatine kinase is a potent inhibitor of translation in vivo. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10006–10010. doi: 10.1073/pnas.86.24.10006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Costill D. L., Cleary P., Fink W. J., Foster C., Ivy J. L., Witzmann F. Training adaptations in skeletal muscle of juvenile diabetics. Diabetes. 1979 Sep;28(9):818–822. doi: 10.2337/diab.28.9.818. [DOI] [PubMed] [Google Scholar]
- Davis R. C., Ben-Zeev O., Martin D., Doolittle M. H. Combined lipase deficiency in the mouse. Evidence of impaired lipase processing and secretion. J Biol Chem. 1990 Oct 15;265(29):17960–17966. [PubMed] [Google Scholar]
- Doolittle M. H., Ben-Zeev O., Elovson J., Martin D., Kirchgessner T. G. The response of lipoprotein lipase to feeding and fasting. Evidence for posttranslational regulation. J Biol Chem. 1990 Mar 15;265(8):4570–4577. [PubMed] [Google Scholar]
- Eckel R. H. Lipoprotein lipase. A multifunctional enzyme relevant to common metabolic diseases. N Engl J Med. 1989 Apr 20;320(16):1060–1068. doi: 10.1056/NEJM198904203201607. [DOI] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
- Fried S. K., Zechner R. Cachectin/tumor necrosis factor decreases human adipose tissue lipoprotein lipase mRNA levels, synthesis, and activity. J Lipid Res. 1989 Dec;30(12):1917–1923. [PubMed] [Google Scholar]
- Friedman G., Ben-Naim M., Halimi O., Etienne J., Stein O., Stein Y. The expression of lipoprotein lipase activity and mRNA in mesenchymal rat heart cell cultures is modulated by bFGF. Biochim Biophys Acta. 1991 Feb 26;1082(1):27–32. doi: 10.1016/0005-2760(91)90295-s. [DOI] [PubMed] [Google Scholar]
- Giralt M., Martin I., Vilaró S., Villarroya F., Mampel T., Iglesias R., Viñas O. Lipoprotein lipase mRNA expression in brown adipose tissue: translational and/or posttranslational events are involved in the modulation of enzyme activity. Biochim Biophys Acta. 1990 Apr 6;1048(2-3):270–273. doi: 10.1016/0167-4781(90)90066-b. [DOI] [PubMed] [Google Scholar]
- Goers J. W., Pedersen M. E., Kern P. A., Ong J., Schotz M. C. An enzyme-linked immunoassay for lipoprotein lipase. Anal Biochem. 1987 Oct;166(1):27–35. doi: 10.1016/0003-2697(87)90541-0. [DOI] [PubMed] [Google Scholar]
- Gunning P., Ponte P., Okayama H., Engel J., Blau H., Kedes L. Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gamma-actin mRNAs: skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. Mol Cell Biol. 1983 May;3(5):787–795. doi: 10.1128/mcb.3.5.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heath G. W., Gavin J. R., 3rd, Hinderliter J. M., Hagberg J. M., Bloomfield S. A., Holloszy J. O. Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity. J Appl Physiol Respir Environ Exerc Physiol. 1983 Aug;55(2):512–517. doi: 10.1152/jappl.1983.55.2.512. [DOI] [PubMed] [Google Scholar]
- Hollenberg C. H. The origin and glyceride distribution of fatty acids in rat adipose tissue. J Clin Invest. 1966 Feb;45(2):205–216. doi: 10.1172/JCI105333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horton E. S. Exercise and physical training: effects on insulin sensitivity and glucose metabolism. Diabetes Metab Rev. 1986;2(1-2):1–17. doi: 10.1002/dmr.5610020101. [DOI] [PubMed] [Google Scholar]
- Kern P. A., Ong J. M., Goers J. W., Pedersen M. E. Regulation of lipoprotein lipase immunoreactive mass in isolated human adipocytes. J Clin Invest. 1988 Feb;81(2):398–406. doi: 10.1172/JCI113332. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kern P. A., Ong J. M., Saffari B., Carty J. The effects of weight loss on the activity and expression of adipose-tissue lipoprotein lipase in very obese humans. N Engl J Med. 1990 Apr 12;322(15):1053–1059. doi: 10.1056/NEJM199004123221506. [DOI] [PubMed] [Google Scholar]
- Kiens B., Lithell H., Mikines K. J., Richter E. A. Effects of insulin and exercise on muscle lipoprotein lipase activity in man and its relation to insulin action. J Clin Invest. 1989 Oct;84(4):1124–1129. doi: 10.1172/JCI114275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kruys V., Wathelet M., Poupart P., Contreras R., Fiers W., Content J., Huez G. The 3' untranslated region of the human interferon-beta mRNA has an inhibitory effect on translation. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6030–6034. doi: 10.1073/pnas.84.17.6030. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lithell H., Cedermark M., Fröberg J., Tesch P., Karlsson J. Increase of lipoprotein-lipase activity in skeletal muscle during heavy exercise. Relation to epinephrine excretion. Metabolism. 1981 Nov;30(11):1130–1134. doi: 10.1016/0026-0495(81)90059-7. [DOI] [PubMed] [Google Scholar]
- Lithell H., Schéle R., Vessby B., Jacobs I. Lipoproteins, lipoprotein lipase, and glycogen after prolonged physical activity. J Appl Physiol Respir Environ Exerc Physiol. 1984 Sep;57(3):698–702. doi: 10.1152/jappl.1984.57.3.698. [DOI] [PubMed] [Google Scholar]
- Lukaski H. C., Bolonchuk W. W., Hall C. B., Siders W. A. Validation of tetrapolar bioelectrical impedance method to assess human body composition. J Appl Physiol (1985) 1986 Apr;60(4):1327–1332. doi: 10.1152/jappl.1986.60.4.1327. [DOI] [PubMed] [Google Scholar]
- Nilsson-Ehle P., Schotz M. C. A stable, radioactive substrate emulsion for assay of lipoprotein lipase. J Lipid Res. 1976 Sep;17(5):536–541. [PubMed] [Google Scholar]
- Ong J. M., Kern P. A. Effect of feeding and obesity on lipoprotein lipase activity, immunoreactive protein, and messenger RNA levels in human adipose tissue. J Clin Invest. 1989 Jul;84(1):305–311. doi: 10.1172/JCI114155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ong J. M., Kern P. A. The role of glucose and glycosylation in the regulation of lipoprotein lipase synthesis and secretion in rat adipocytes. J Biol Chem. 1989 Feb 25;264(6):3177–3182. [PubMed] [Google Scholar]
- Ong J. M., Kirchgessner T. G., Schotz M. C., Kern P. A. Insulin increases the synthetic rate and messenger RNA level of lipoprotein lipase in isolated rat adipocytes. J Biol Chem. 1988 Sep 15;263(26):12933–12938. [PubMed] [Google Scholar]
- Ong J. M., Saffari B., Simsolo R. B., Kern P. A. Epinephrine inhibits lipoprotein lipase gene expression in rat adipocytes through multiple steps in posttranscriptional processing. Mol Endocrinol. 1992 Jan;6(1):61–69. doi: 10.1210/mend.6.1.1738372. [DOI] [PubMed] [Google Scholar]
- Ong J. M., Simsolo R. B., Saffari B., Kern P. A. The regulation of lipoprotein lipase gene expression by dexamethasone in isolated rat adipocytes. Endocrinology. 1992 Apr;130(4):2310–2316. doi: 10.1210/endo.130.4.1547742. [DOI] [PubMed] [Google Scholar]
- Oscai L. B., Caruso R. A., Wergeles A. C. Lipoprotein lipase hydrolyzes endogenous triacylglycerols in muscle of exercised rats. J Appl Physiol Respir Environ Exerc Physiol. 1982 Apr;52(4):1059–1063. doi: 10.1152/jappl.1982.52.4.1059. [DOI] [PubMed] [Google Scholar]
- Peltonen P., Marniemi J., Hietanen E., Vuori I., Ehnholm C. Changes in serum lipids, lipoproteins, and heparin releasable lipolytic enzymes during moderate physical training in man: a longitudinal study. Metabolism. 1981 May;30(5):518–526. doi: 10.1016/0026-0495(81)90190-6. [DOI] [PubMed] [Google Scholar]
- Previato L., Parrott C. L., Santamarina-Fojo S., Brewer H. B., Jr Transcriptional regulation of the human lipoprotein lipase gene in 3T3-L1 adipocytes. J Biol Chem. 1991 Oct 5;266(28):18958–18963. [PubMed] [Google Scholar]
- Querfeld U., Ong J. M., Prehn J., Carty J., Saffari B., Jordan S. C., Kern P. A. Effects of cytokines on the production of lipoprotein lipase in cultured human macrophages. J Lipid Res. 1990 Aug;31(8):1379–1386. [PubMed] [Google Scholar]
- Saffari B., Ong J. M., Kern P. A. Regulation of adipose tissue lipoprotein lipase gene expression by thyroid hormone in rats. J Lipid Res. 1992 Feb;33(2):241–249. [PubMed] [Google Scholar]
- Schwartz R. S., Brunzell J. D. Increase of adipose tissue lipoprotein lipase activity with weight loss. J Clin Invest. 1981 May;67(5):1425–1430. doi: 10.1172/JCI110171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Segal K. R., Gutin B., Presta E., Wang J., Van Itallie T. B. Estimation of human body composition by electrical impedance methods: a comparative study. J Appl Physiol (1985) 1985 May;58(5):1565–1571. doi: 10.1152/jappl.1985.58.5.1565. [DOI] [PubMed] [Google Scholar]
- Shrago E., Spennetta T., Gordon E. Fatty acid synthesis in human adipose tissue. J Biol Chem. 1969 May 25;244(10):2761–2766. [PubMed] [Google Scholar]
- Simsolo R. B., Ong J. M., Saffari B., Kern P. A. Effect of improved diabetes control on the expression of lipoprotein lipase in human adipose tissue. J Lipid Res. 1992 Jan;33(1):89–95. [PubMed] [Google Scholar]
- Svedenhag J., Lithell H., Juhlin-Dannfelt A., Henriksson J. Increase in skeletal muscle lipoprotein lipase following endurance training in man. Atherosclerosis. 1983 Nov;49(2):203–207. doi: 10.1016/0021-9150(83)90198-3. [DOI] [PubMed] [Google Scholar]
- Taskinen M. R., Nikkilä E. A. Effect of acute vigorous exercise on lipoprotein lipase activity of adipose tissue and skeletal muscle in physically active men. Artery. 1980;6(6):471–483. [PubMed] [Google Scholar]
- Walberg J. L., Greenwood M. R., Stern J. S. Lipoprotein lipase activity and lipolysis after swim training in obese Zucker rats. Am J Physiol. 1983 Nov;245(5 Pt 1):R706–R712. doi: 10.1152/ajpregu.1983.245.5.R706. [DOI] [PubMed] [Google Scholar]
- Walden W. E., Patino M. M., Gaffield L. Purification of a specific repressor of ferritin mRNA translation from rabbit liver. J Biol Chem. 1989 Aug 15;264(23):13765–13769. [PubMed] [Google Scholar]
- Weintraub M. S., Rosen Y., Otto R., Eisenberg S., Breslow J. L. Physical exercise conditioning in the absence of weight loss reduces fasting and postprandial triglyceride-rich lipoprotein levels. Circulation. 1989 May;79(5):1007–1014. doi: 10.1161/01.cir.79.5.1007. [DOI] [PubMed] [Google Scholar]
- Wion K. L., Kirchgessner T. G., Lusis A. J., Schotz M. C., Lawn R. M. Human lipoprotein lipase complementary DNA sequence. Science. 1987 Mar 27;235(4796):1638–1641. doi: 10.1126/science.3823907. [DOI] [PubMed] [Google Scholar]