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. 1992 Sep 1;286(Pt 2):405–411. doi: 10.1042/bj2860405

Dietary omega 3 fatty acid alters prostaglandin synthesis, glucose transport and protein turnover in skeletal muscle of healthy and diabetic rats.

P S Sohal 1, V E Baracos 1, M T Clandinin 1
PMCID: PMC1132913  PMID: 1530573

Abstract

The present study was designed to determine if dietary-fat-induced alterations in the fatty acid composition of skeletal-muscle lipid alters insulin-dependent and basal muscle metabolism, including glucose and amino acid transport, prostaglandin (PG) synthesis and protein turnover. Rats were fed on high-fat semi-purified diets providing 19% or 1% omega 3 fatty acids in the form of fish oil, for 6 weeks. After 3 weeks, half of the rats were made diabetic by a single injection of streptozotocin (50 mg/kg body wt.). After a further 3 weeks, contralateral epitrochlearis and extensor digitorum longus (EDL) muscles from each rat were incubated in vitro. High levels of dietary omega 3 fatty acids decreased PGE2 and PGF2 alpha synthesis in EDL and epitrochlearis muscle (P less than 0.0001). Diabetes and insulin had no effect on PG synthesis. Diet did not alter basal glucose or amino acid transport in EDL muscle from healthy or diabetic rats. Insulin increased glucose and amino acid transport (P less than 0.0001); the increase in glucose transport by insulin was significantly greater in muscles of rats fed on high levels of omega 3 fatty acids (P less than 0.05). Epitrochlearis from rats fed on high levels of omega 3 fatty acids showed decreased net protein degradation in the presence and absence of insulin, owing to decreased rates of protein degradation and synthesis. The data suggest that high levels of dietary omega 3 fatty acids that alter muscle membrane composition also result in alterations in glucose transport and the metabolism of muscle protein.

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Selected References

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  1. Baracos V. E., Goldberg A. L. Maintenance of normal length improves protein balance and energy status in isolated rat skeletal muscles. Am J Physiol. 1986 Oct;251(4 Pt 1):C588–C596. doi: 10.1152/ajpcell.1986.251.4.C588. [DOI] [PubMed] [Google Scholar]
  2. Baracos V. E., Langman M., Mak A. An in vitro preparation of the extensor digitorum communis muscle from the chick (Gallus domesticus) for studies of protein turnover. Comp Biochem Physiol A Comp Physiol. 1989;92(4):555–563. doi: 10.1016/0300-9629(89)90365-4. [DOI] [PubMed] [Google Scholar]
  3. Berdanier C. D. Role of membrane lipids in metabolic regulation. Nutr Rev. 1988 Apr;46(4):145–149. doi: 10.1111/j.1753-4887.1988.tb05408.x. [DOI] [PubMed] [Google Scholar]
  4. Bollag G. E., Roth R. A., Beaudoin J., Mochly-Rosen D., Koshland D. E., Jr Protein kinase C directly phosphorylates the insulin receptor in vitro and reduces its protein-tyrosine kinase activity. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5822–5824. doi: 10.1073/pnas.83.16.5822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buse M. G., Weigand D. A., Peeler D., Hedden M. P. The effect of diabetes and the redox potential on amino acid content and release by isolated rat hemidiaphragms. Metabolism. 1980 Jul;29(7):605–616. doi: 10.1016/0026-0495(80)90104-3. [DOI] [PubMed] [Google Scholar]
  6. Clandinin M. T., Field C. J., Hargreaves K., Morson L., Zsigmond E. Role of diet fat in subcellular structure and function. Can J Physiol Pharmacol. 1985 May;63(5):546–556. doi: 10.1139/y85-094. [DOI] [PubMed] [Google Scholar]
  7. Dice J. F., Walker C. D., Byrne B., Cardiel A. General characteristics of protein degradation in diabetes and starvation. Proc Natl Acad Sci U S A. 1978 May;75(5):2093–2097. doi: 10.1073/pnas.75.5.2093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. FOLCH J., LEES M., SLOANE STANLEY G. H. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957 May;226(1):497–509. [PubMed] [Google Scholar]
  9. Fagan J. M., Satarug S., Cook P., Tischler M. E. Rat muscle protein turnover and redox state in progressive diabetes. Life Sci. 1987 Feb 23;40(8):783–790. doi: 10.1016/0024-3205(87)90306-7. [DOI] [PubMed] [Google Scholar]
  10. Field C. J., Ryan E. A., Thomson A. B., Clandinin M. T. Diet fat composition alters membrane phospholipid composition, insulin binding, and glucose metabolism in adipocytes from control and diabetic animals. J Biol Chem. 1990 Jul 5;265(19):11143–11150. [PubMed] [Google Scholar]
  11. Field C. J., Ryan E. A., Thomson A. B., Clandinin M. T. Dietary fat and the diabetic state alter insulin binding and the fatty acyl composition of the adipocyte plasma membrane. Biochem J. 1988 Jul 15;253(2):417–424. doi: 10.1042/bj2530417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fisher B. D., Baracos V. E., Reid D. C. Effect of systemic inhibition of prostaglandin synthesis on muscle protein balance after trauma in the rat. Can J Physiol Pharmacol. 1991 Jun;69(6):831–836. doi: 10.1139/y91-125. [DOI] [PubMed] [Google Scholar]
  13. Fulks R. M., Li J. B., Goldberg A. L. Effects of insulin, glucose, and amino acids on protein turnover in rat diaphragm. J Biol Chem. 1975 Jan 10;250(1):290–298. [PubMed] [Google Scholar]
  14. Garg M. L., Sebokova E., Thomson A. B., Clandinin M. T. Delta 6-desaturase activity in liver microsomes of rats fed diets enriched with cholesterol and/or omega 3 fatty acids. Biochem J. 1988 Jan 15;249(2):351–356. doi: 10.1042/bj2490351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Goldberg A. L., Tischler M., DeMartino G., Griffin G. Hormonal regulation of protein degradation and synthesis in skeletal muscle. Fed Proc. 1980 Jan;39(1):31–36. [PubMed] [Google Scholar]
  16. Grataroli R., Léonardi J., Charbonnier M., Lafont R., Lafont H., Nalbone G. Effects of dietary corn oil and salmon oil on lipids and prostaglandin E2 in rat gastric mucosa. Lipids. 1988 Jul;23(7):666–670. doi: 10.1007/BF02535665. [DOI] [PubMed] [Google Scholar]
  17. Gumà A., Camps M., Palacín M., Testar X., Zorzano A. Protein kinase C activators selectively inhibit insulin-stimulated system A transport activity in skeletal muscle at a post-receptor level. Biochem J. 1990 Jun 15;268(3):633–639. doi: 10.1042/bj2680633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gumà A., Testar X., Palacín M., Zorzano A. Insulin-stimulated alpha-(methyl)aminoisobutyric acid uptake in skeletal muscle. Evidence for a short-term activation of uptake independent of Na+ electrochemical gradient and protein synthesis. Biochem J. 1988 Aug 1;253(3):625–629. doi: 10.1042/bj2530625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hausman R. E., Berggrun D. A. Prostaglandin binding does not require direct cell-cell contact during chick myogenesis in vitro. Exp Cell Res. 1987 Feb;168(2):457–462. doi: 10.1016/0014-4827(87)90018-8. [DOI] [PubMed] [Google Scholar]
  20. Hill M. A., Davis M. J., Meininger G. A. Cyclooxygenase inhibition potentiates myogenic activity in skeletal muscle arterioles. Am J Physiol. 1990 Jan;258(1 Pt 2):H127–H133. doi: 10.1152/ajpheart.1990.258.1.H127. [DOI] [PubMed] [Google Scholar]
  21. Jackson M. J., Roberts J., Edwards R. H. Effects of dietary-fish-oil feeding on muscle growth and damage in the rat. Br J Nutr. 1988 Sep;60(2):217–224. doi: 10.1079/bjn19880093. [DOI] [PubMed] [Google Scholar]
  22. Jefferson L. S., Rannels D. E., Munger B. L., Morgan H. E. Insulin in the regulation of protein turnover in heart and skeletal muscle. Fed Proc. 1974 Apr;33(4):1098–1104. [PubMed] [Google Scholar]
  23. Kadowaki M., Harada N., Takahashi S., Noguchi T., Naito H. Differential regulation of the degradation of myofibrillar and total proteins in skeletal muscle of rats: effects of streptozotocin-induced diabetes, dietary protein and starvation. J Nutr. 1989 Mar;119(3):471–477. doi: 10.1093/jn/119.3.471. [DOI] [PubMed] [Google Scholar]
  24. Kettelhut I. C., Wing S. S., Goldberg A. L. Endocrine regulation of protein breakdown in skeletal muscle. Diabetes Metab Rev. 1988 Dec;4(8):751–772. doi: 10.1002/dmr.5610040805. [DOI] [PubMed] [Google Scholar]
  25. Klip A., Pâquet M. R. Glucose transport and glucose transporters in muscle and their metabolic regulation. Diabetes Care. 1990 Mar;13(3):228–243. doi: 10.2337/diacare.13.3.228. [DOI] [PubMed] [Google Scholar]
  26. Knapp H. R., Miller A. J., Lawson J. A. Urinary excretion of diols derived from eicosapentaenoic acid during n-3 fatty acid ingestion by man. Prostaglandins. 1991 Jul;42(1):47–54. doi: 10.1016/0090-6980(91)90093-u. [DOI] [PubMed] [Google Scholar]
  27. Maroni B. J., Karapanos G., Mitch W. E. System A amino acid transport in incubated muscle: effects of insulin and acute uremia. Am J Physiol. 1986 Jul;251(1 Pt 2):F74–F80. doi: 10.1152/ajprenal.1986.251.1.F74. [DOI] [PubMed] [Google Scholar]
  28. Maroni B. J., Karapanos G., Mitch W. E. System ASC and sodium-independent neutral amino acid transport in muscle of uremic rats. Am J Physiol. 1986 Jul;251(1 Pt 2):F81–F86. doi: 10.1152/ajprenal.1986.251.1.F81. [DOI] [PubMed] [Google Scholar]
  29. Millward D. J., Garlick P. J., Stewart R. J., Nnanyelugo D. O., Waterlow J. C. Skeletal-muscle growth and protein turnover. Biochem J. 1975 Aug;150(2):235–243. doi: 10.1042/bj1500235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Murphy M. G. Dietary fatty acids and membrane protein function. J Nutr Biochem. 1990 Feb;1(2):68–79. doi: 10.1016/0955-2863(90)90052-m. [DOI] [PubMed] [Google Scholar]
  31. Newsholme E. A., Leighton B., Challiss R. A., Lozeman F. J. Assessment of biochemical viability of isolated incubated muscle preparations. Biochem J. 1986 Sep 1;238(2):621–622. doi: 10.1042/bj2380621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pain V. M., Albertse E. C., Garlick P. J. Protein metabolism in skeletal muscle, diaphragm, and heart of diabetic rats. Am J Physiol. 1983 Dec;245(6):E604–E610. doi: 10.1152/ajpendo.1983.245.6.E604. [DOI] [PubMed] [Google Scholar]
  33. Palmer R. M. Prostaglandins and the control of muscle protein synthesis and degradation. Prostaglandins Leukot Essent Fatty Acids. 1990 Feb;39(2):95–104. doi: 10.1016/0952-3278(90)90017-f. [DOI] [PubMed] [Google Scholar]
  34. Powell W. S. Rapid extraction of arachidonic acid metabolites from biological samples using octadecylsilyl silica. Methods Enzymol. 1982;86:467–477. doi: 10.1016/0076-6879(82)86218-6. [DOI] [PubMed] [Google Scholar]
  35. Reeds P. J., Hay S. M., Glennie R. T., Mackie W. S., Garlick P. J. The effect of indomethacin on the stimulation of protein synthesis by insulin in young post-absorptive rats. Biochem J. 1985 Apr 1;227(1):255–261. doi: 10.1042/bj2270255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Reeds P. J., Palmer R. M. The possible involvement of prostaglandin F2 alpha in the stimulation of muscle protein synthesis by insulin. Biochem Biophys Res Commun. 1983 Nov 15;116(3):1084–1090. doi: 10.1016/s0006-291x(83)80253-8. [DOI] [PubMed] [Google Scholar]
  37. Rodemann H. P., Goldberg A. L. Arachidonic acid, prostaglandin E2 and F2 alpha influence rates of protein turnover in skeletal and cardiac muscle. J Biol Chem. 1982 Feb 25;257(4):1632–1638. [PubMed] [Google Scholar]
  38. Shargill N. S., Ohshima K., Bray G. A., Chan T. M. Muscle protein turnover in the perfused hindquarters of lean and genetically obese-diabetic (db/db) mice. Diabetes. 1984 Dec;33(12):1160–1164. doi: 10.2337/diab.33.12.1160. [DOI] [PubMed] [Google Scholar]
  39. Smith O. L., Wong C. Y., Gelfand R. A. Skeletal muscle proteolysis in rats with acute streptozocin-induced diabetes. Diabetes. 1989 Sep;38(9):1117–1122. doi: 10.2337/diab.38.9.1117. [DOI] [PubMed] [Google Scholar]
  40. Sowell M. O., Boggs K. P., Robinson K. A., Dutton S. L., Buse M. G. Effects of insulin and phospholipase C in control and denervated rat skeletal muscle. Am J Physiol. 1991 Feb;260(2 Pt 1):E247–E256. doi: 10.1152/ajpendo.1991.260.2.E247. [DOI] [PubMed] [Google Scholar]
  41. Storlien L. H., Jenkins A. B., Chisholm D. J., Pascoe W. S., Khouri S., Kraegen E. W. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes. 1991 Feb;40(2):280–289. doi: 10.2337/diab.40.2.280. [DOI] [PubMed] [Google Scholar]
  42. Storlien L. H., Kraegen E. W., Chisholm D. J., Ford G. L., Bruce D. G., Pascoe W. S. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science. 1987 Aug 21;237(4817):885–888. doi: 10.1126/science.3303333. [DOI] [PubMed] [Google Scholar]
  43. Strelkov A. B., Fields A. L., Baracos V. E. Effects of systemic inhibition of prostaglandin production on protein metabolism in tumor-bearing rats. Am J Physiol. 1989 Aug;257(2 Pt 1):C261–C269. doi: 10.1152/ajpcell.1989.257.2.C261. [DOI] [PubMed] [Google Scholar]
  44. Sugden P. H., Fuller S. J. Regulation of protein turnover in skeletal and cardiac muscle. Biochem J. 1991 Jan 1;273(Pt 1):21–37. doi: 10.1042/bj2730021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tischler M. E., Desautels M., Goldberg A. L. Does leucine, leucyl-tRNA, or some metabolite of leucine regulate protein synthesis and degradation in skeletal and cardiac muscle? J Biol Chem. 1982 Feb 25;257(4):1613–1621. [PubMed] [Google Scholar]
  46. Turinsky J. Phospholipids, prostaglandin E2, and proteolysis in denervated muscle. Am J Physiol. 1986 Jul;251(1 Pt 2):R165–R173. doi: 10.1152/ajpregu.1986.251.1.R165. [DOI] [PubMed] [Google Scholar]
  47. WAALKES T. P., UDENFRIEND S. A fluorometric method for the estimation of tyrosine in plasma and tissues. J Lab Clin Med. 1957 Nov;50(5):733–736. [PubMed] [Google Scholar]
  48. Yeagle P. L. Lipid regulation of cell membrane structure and function. FASEB J. 1989 May;3(7):1833–1842. [PubMed] [Google Scholar]
  49. Zorzano A., Balon T. W., Garetto L. P., Goodman M. N., Ruderman N. B. Muscle alpha-aminoisobutyric acid transport after exercise: enhanced stimulation by insulin. Am J Physiol. 1985 May;248(5 Pt 1):E546–E552. doi: 10.1152/ajpendo.1985.248.5.E546. [DOI] [PubMed] [Google Scholar]
  50. Zorzano A., Balon T. W., Jakubowski J. A., Goodman M. N., Deykin D., Ruderman N. B. Effects of insulin and prior exercise on prostaglandin release from perfused rat muscle. Evidence that prostaglandins do not mediate changes in glucose uptake. Biochem J. 1986 Dec 1;240(2):437–443. doi: 10.1042/bj2400437. [DOI] [PMC free article] [PubMed] [Google Scholar]

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