Metabolic switching of human myotubes is improved by n-3 fatty acids

Journal of Lipid Research

Volumn 51, Issue 8, 2010, Pages 2090-2104

  Hessvik, N P ^a   Bakke, S S ^a   Fredriksson, K ^b   Boekschoten, M V ^c   Fjorkenstad A ^a   Koster, G ^a   Hesselink, M K ^b   Kersten, S ^c   Kase, E T ^a   Rustan, A C ^a   Thoresen, G H ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

Author keywords

Adaptability; Lipid metabolism; Metabolic flexibility; Substrate regulated flexibility; Suppressibility

Indexed keywords

GLUCOSE; ICOSAPENTAENOIC ACID; LINOLEIC ACID; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; OMEGA 3 FATTY ACID; PALMITIC ACID; FLUORINATED HYDROCARBON; INSULIN; LIVER X RECEPTOR; OLEIC ACID; ORPHAN NUCLEAR RECEPTOR; SULFONAMIDE; TO-901317;

ADULT; ARTICLE; CARBOHYDRATE METABOLISM; CELL SIZE; CONTROLLED STUDY; CULTURE MEDIUM; FATTY ACID ANALYSIS; FATTY ACID OXIDATION; FEMALE; GENETIC REGULATION; GLUCOSE UTILIZATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MALE; MICROARRAY ANALYSIS; MITOCHONDRION; MUSCLE METABOLISM; MYOTUBE; NORMAL HUMAN; PRIORITY JOURNAL; AGONISTS; CYTOLOGY; DRUG EFFECTS; ENERGY METABOLISM; GENE EXPRESSION PROFILING; METABOLISM; MIDDLE AGED; OXIDATION REDUCTION REACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; ENERGY METABOLISM; FATTY ACIDS, OMEGA-3; FEMALE; GENE EXPRESSION PROFILING; GLUCOSE; HUMANS; HYDROCARBONS, FLUORINATED; INSULIN; MALE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; OLEIC ACID; ORPHAN NUCLEAR RECEPTORS; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION; SULFONAMIDES;

EID: 77956846038     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M003319     Document Type: Article

References (74)

1. Kelley, D. E., J. P. Reilly, T. Veneman, and L. J. Mandarino. 1990. Effects of insulin on skeletal muscle glucose storage, oxidation, and glycolysis in humans. Am. J. Physiol. 258: E923-E929.
2. Andres, R., G. Cader, and K. L. Zierler. 1956. The quantitatively minor role of carbohydrate in oxidative metabolism by skeletal muscle in intact man in the basal state; measurements of oxygen and glucose uptake and carbon dioxide and lactate production in the forearm. J. Clin. Invest. 35: 671-682.
3. Kelley, D. E., and L. J. Mandarino. 2000. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes. 49: 677-683.
4. Corpeleijn, E., M. Mensink, M. E. Kooi, P. M. H. J. Roekaerts, W. H. M. Saris, and E. E. Blaak. 2008. Impaired skeletal muscle substrate oxidation in glucose-intolerant men improves after weight loss. Obesity (Silver Spring). 16: 1025-1032.
5. Kelley, D. E., B. Goodpaster, R. R. Wing, and J. A. Simoneau. 1999. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am. J. Physiol. 277: E1130-E1141.
6. Blaak, E. E., D. P. van Aggel-Leijssen, A. J. Wagenmakers, W. H. Saris, and M. A. van Baak. 2000. Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes. 49: 2102-2107.
7. Mensink, M., E. E. Blaak, M. A. van Baak, A. J. Wagenmakers, and W. H. Saris. 2001. Plasma free fatty acid uptake and oxidation are already diminished in subjects at high risk for developing type 2 diabetes. Diabetes. 50: 2548-2554.
8. Ukropcova, B., M. McNeil, O. Sereda, L. de Jonge, H. Xie, G. A. Bray, and S. R. Smith. 2005. Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor. [comment] J. Clin. Invest. 115: 1934-1941.
9. Goodpaster, B. H., A. Katsiaras, and D. E. Kelley. 2003. Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity. Diabetes. 52: 2191-2197.
10. Corpeleijn, E., W. H. M. Saris, and E. E. Blaak. 2009. Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle. Obes. Rev. 10: 178-193.
11. Sial, S., A. R. Coggan, R. C. Hickner, and S. Klein. 1998. Training-induced alterations in fat and carbohydrate metabolism during exercise in elderly subjects. Am. J. Physiol. 274: E785-E790.
12. Gan, S. K., A. D. Kriketos, B. A. Ellis, C. H. Thompson, E. W. Kraegen, and D. J. Chisholm. 2003. Changes in aerobic capacity and visceral fat but not myocyte lipid levels predict increased insulin action after exercise in overweight and obese men. Diabetes Care. 26: 1706-1713.
13. Lee, J. S., S. K. Pinnamaneni, S. J. Eo, I. H. Cho, J. H. Pyo, C. K. Kim, A. J. Sinclair, M. A. Febbraio, and M. J. Watt. 2006. Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites. J. Appl. Physiol. 100: 1467-1474.
14. Storlien, L. H., E. W. Kraegen, D. J. Chisholm, G. L. Ford, D. G. Bruce, and W. S. Pascoe. 1987. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science. 237: 885-888.
15. Ramel, A., A. Martinez, M. Kiely, G. Morais, N. M. Bandarra, and I. Thorsdottir. 2008. Beneficial effects of long-chain n-3 fatty acids included in an energy-restricted diet on insulin resistance in overweight and obese European young adults. Diabetologia. 51: 1261-1268.
16. Kabir, M., G. Skurnik, N. Naour, V. Pechtner, E. Meugnier, S. Rome, A. Quignard-Boulange, H. Vidal, G. Slama, K. Clement, et al. 2007. Treatment for 2 mo with n 3 polyunsaturated fatty acids reduces adiposity and some atherogenic factors but does not improve insulin sensitivity in women with type 2 diabetes: a randomized controlled study. Am. J. Clin. Nutr. 86: 1670-1679.
17. Browning, L. M., J. D. Krebs, C. S. Moore, G. D. Mishra, M. A. O'Connell, and S. A. Jebb. 2007. The impact of long chain n-3 polyunsaturated fatty acid supplementation on inflammation, insulin sensitivity and CVD risk in a group of overweight women with an inflammatory phenotype. Diabetes Obes. Metab. 9: 70-80.
18. Krebs, J. D., L. M. Browning, N. K. McLean, J. L. Rothwell, G. D. Mishra, C. S. Moore, and S. A. Jebb. 2006. Additive benefits of long-chain n-3 polyunsaturated fatty acids and weight-loss in the management of cardiovascular disease risk in overweight hyperinsulinaemic women. Int. J. Obes. 30: 1535-1544.
19. Fedor, D., and D. S. Kelley. 2009. Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr. Opin. Clin. Nutr. Metab. Care. 12: 138-146.
20. Haugaard, S. B., S. Madsbad, C-E. Hoy, and A. Vaag. 2006. Dietary intervention increases n-3 long-chain polyunsaturated fatty acids in skeletal muscle membrane phospholipids of obese subjects. Implications for insulin sensitivity. Clin. Endocrinol. (Oxf.). 64: 169-178.
21. Pickersgill, L., G. J. Litherland, A. S. Greenberg, M. Walker, and S. J. Yeaman. 2007. Key role for ceramides in mediating insulin resistance in human muscle cells. J. Biol. Chem. 282: 12583-12589.
22. Coll, T., E. Eyre, R. Rodriguez-Calvo, X. Palomer, R. M. Sanchez, M. Merlos, J. C. Laguna, and M. Vazquez-Carrera. 2008. Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J. Biol. Chem. 283: 11107-11116.
23. Aas, V., M. H. Rokling-Andersen, E. T. Kase, G. H. Thoresen, and A. C. Rustan. 2006. Eicosapentaenoic acid (20:5 n-3) increases fatty acid and glucose uptake in cultured human skeletal muscle cells. J. Lipid Res. 47: 366-374.
24. Wensaas, A. J., A. C. Rustan, M. Just, R. K. Berge, C. A. Drevon, and M. Gaster. 2009. Fatty acid incubation of myotubes from humans with type 2 diabetes leads to enhanced release of beta- oxidation products because of impaired fatty acid oxidation: effects of tetradecylthioacetic acid and eicosapentaenoic acid. Diabetes. 58: 527-535.
25. Ou, J., H. Tu, B. Shan, A. Luk, R. A. DeBose-Boyd, Y. Bashmakov, J. L. Goldstein, and M. S. Brown. 2001. Unsaturated fatty acids inhibit transcription of the sterol regulatory element-binding protein-1c (SREBP-1c) gene by antagonizing ligand-dependent activation of the LXR. Proc. Natl. Acad. Sci. USA. 98: 6027-6032.
26. Yoshikawa, T., H. Shimano, N. Yahagi, T. Ide, M. Amemiya-Kudo, T. Matsuzaka, M. Nakakuki, S. Tomita, H. Okazaki, Y. Tamura, et al. 2002. Polyunsaturated fatty acids suppress sterol regulatory element-binding protein 1c promoter activity by inhibition of liver X receptor (LXR) binding to LXR response elements. J. Biol. Chem. 277: 1705-1711.
27. Gottlicher, M., E. Widmark, Q. Li, and J. A. Gustafsson. 1992. Fatty acids activate a chimera of the clofibric acid-activated receptor and the glucocorticoid receptor. Proc. Natl. Acad. Sci. USA. 89: 4653-4657.
28. Gottlicher, M., A. Demoz, D. Svensson, P. Tollet, R. K. Berge, and J. A. Gustafsson. 1993. Structural and metabolic requirements for activators of the peroxisome proliferator-activated receptor. Biochem. Pharmacol. 46: 2177-2184.
29. Sampath, H., and J. M. Ntambi. 2005. Polyunsaturated fatty acid regulation of genes of lipid metabolism. Annu. Rev. Nutr. 25: 317-340.
30. Randle, P. J., P. B. Garland, C. N. Hales, and E. A. Newsholme. 1963. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet. 1: 785-789.
31. Sidossis, L. S., C. A. Stuart, G. I. Shulman, G. D. Lopaschuk, and R. R. Wolfe. 1996. Glucose plus insulin regulate fat oxidation by controlling the rate of fatty acid entry into the mitochondria. J. Clin. Invest. 98: 2244-2250.
32. Sidossis, L. S., and R. R. Wolfe. 1996. Glucose and insulin-induced inhibition of fatty acid oxidation: the glucose-fatty acid cycle reversed. Am. J. Physiol. 270: E733-E738.
33. Gaster, M., S. R. Kristensen, H. Beck-Nielsen, and H. D. Schroder. 2001. A cellular model system of differentiated human myotubes. APMIS. 109: 735-744.
34. Wensaas, A. J., A. C. Rustan, K. Lovstedt, B. Kull, S. Wikstrom, C. A. Drevon, and S. Hallen. 2007. Cell-based multiwell assays for the detection of substrate accumulation and oxidation. J. Lipid Res. 48: 961-967.
35. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
36. Skrede, S., J. Bremer, R. Berge, and A. Rustan. 1994. Stimulation of fatty acid oxidation by a 3-thia fatty acid reduces triacylglycerol secretion in cultured rat hepatocytes. J. Lipid Res. 35: 1395-1404.
37. Gaster, M., A. C. Rustan, V. Aas, and H. Beck-Nielsen. 2004. Reduced lipid oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin: evidence from cultured myotubes. Diabetes. 53: 542-548.
38. Dai, M., P. Wang, A. D. Boyd, G. Kostov, B. Athey, E. G. Jones, W. E. Bunney, R. M. Myers, T. P. Speed, H. Akil, et al. 2005. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33: e175.
39. Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 19: 185-193.
40. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, and T. P. Speed. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31: e15.
41. Sartor, M. A., C. R. Tomlinson, S. C. Wesselkamper, S. Sivaganesan, G. D. Leikauf, and M. Medvedovic. 2006. Intensity-based hierarchical Bayes method improves testing for differentially expressed genes in microarray experiments. BMC Bioinformatics. 7: 538.
42. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA. 100: 9440-9445.
43. Subramanian, A., P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R. Golub, E. S. Lander, et al. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. [comment] Proc. Natl. Acad. Sci. USA. 102: 15545-15550.
44. Dahlquist, K. D., N. Salomonis, K. Vranizan, S. C. Lawlor, and B. R. Conklin. 2002. GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat. Genet. 31: 19-20.
45. Kanehisa, M., and S. Goto. 2000. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28: 27-30.
46. Murphy, S., S. Martin, and R. G. Parton. 2009. Lipid droplet-organelle interactions; sharing the fats. Biochim. Biophys. Acta. 1791: 441-447.
47. Staiger, H., C. Haas, J. Machann, R. Werner, M. Weisser, F. Schick, F. Machicao, N. Stefan, A. Fritsche, and H-U. Haring. 2009. Muscle-derived angiopoietin-like protein 4 is induced by fatty acids via peroxisome proliferator-activated receptor (PPAR)-delta and is of metabolic relevance in humans. Diabetes. 58: 579-589.
48. Al-Khalili, L., K. Bouzakri, S. Glund, F. Lonnqvist, H. A. Koistinen, and A. Krook. 2006. Signaling specificity of interleukin-6 action on glucose and lipid metabolism in skeletal muscle. Mol. Endocrinol. 20: 3364-3375.
49. Ruderman, N. B., C. Keller, A-M. Richard, A. K. Saha, Z. Luo, X. Xiang, M. Giralt, V. B. Ritov, E. V. Menshikova, D. E. Kelley, et al. 2006. Interleukin-6 regulation of AMP-activated protein kinase. Potential role in the systemic response to exercise and prevention of the metabolic syndrome. Diabetes. 55 ( Suppl. 2 ): S48-S54.
50. Alberti, S., G. Schuster, P. Parini, D. Feltkamp, U. Diczfalusy, M. Rudling, B. Angelin, I. Bjorkhem, S. Pettersson, and J. A. Gustafsson. 2001. Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXRbeta-deficient mice. J. Clin. Invest. 107: 565-573.
51. Peet, D. J., S. D. Turley, W. Ma, B. A. Janowski, J. M. Lobaccaro, R. E. Hammer, and D. J. Mangelsdorf. 1998. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell. 93: 693-704.
52. Cao, G., Y. Liang, C. L. Broderick, B. A. Oldham, T. P. Beyer, R. J. Schmidt, Y. Zhang, K. R. Stayrook, C. Suen, K. A. Otto, et al. 2003. Antidiabetic action of a liver x receptor agonist mediated by inhibition of hepatic gluconeogenesis. J. Biol. Chem. 278: 1131-1136.
53. Schultz, J. R., H. Tu, A. Luk, J. J. Repa, J. C. Medina, L. Li, S. Schwendner, S. Wang, M. Thoolen, D. J. Mangelsdorf, et al. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14: 2831-2838.
54. Laffitte, B. A., L. C. Chao, J. Li, R. Walczak, S. Hummasti, S. B. Joseph, A. Castrillo, D. C. Wilpitz, D. J. Mangelsdorf, J. L. Collins, et al. 2003. Activation of liver X receptor improves glucose tolerance through coordinate regulation of glucose metabolism in liver and adipose tissue. Proc. Natl. Acad. Sci. USA. 100: 5419-5424.
55. Stenson, B. M., M. Ryden, K. R. Steffensen, K. Wahlen, A. T. Pettersson, J. W. Jocken, P. Arner, and J. Laurencikiene. 2009. Activation of liver x receptor regulates substrate oxidation in white adipocytes. Endocrinology. 150: 4104-4113.
56. Kase, E. T., A. J. Wensaas, V. Aas, K. Hojlund, K. Levin, G. H. Thoresen, H. Beck-Nielsen, A. C. Rustan, and M. Gaster. 2005. Skeletal muscle lipid accumulation in type 2 diabetes may involve the liver X receptor pathway. Diabetes. 54: 1108-1115.
57. Kase, E. T., G. H. Thoresen, S. Westerlund, K. Hojlund, A. C. Rustan, and M. Gaster. 2007. Liver X receptor antagonist reduces lipid formation and increases glucose metabolism in myotubes from lean, obese and type 2 diabetic individuals. Diabetologia. 50: 2171-2180.
58. Ide, T., H. Shimano, T. Yoshikawa, N. Yahagi, M. Amemiya-Kudo, T. Matsuzaka, M. Nakakuki, S. Yatoh, Y. Iizuka, S. Tomita, et al. 2003. Cross-talk between peroxisome proliferator-activated receptor (PPAR) alpha and liver X receptor (LXR) in nutritional regulation of fatty acid metabolism. II. LXRs suppress lipid degradation gene promoters through inhibition of PPAR signaling. [comment] Mol. Endocrinol. 17: 1255-1267.
59. Yoshikawa, T., T. Ide, H. Shimano, N. Yahagi, M. Amemiya-Kudo, T. Matsuzaka, S. Yatoh, T. Kitamine, H. Okazaki, Y. Tamura, et al. 2003. Cross-talk between peroxisome proliferator-activated receptor (PPAR) alpha and liver X receptor (LXR) in nutritional regulation of fatty acid metabolism. I. PPARs suppress sterol regulatory element binding protein-1c promoter through inhibition of LXR signaling. [comment] Mol. Endocrinol. 17: 1240-1254.
60. Tobin, K. A., H. H. Steineger, S. Alberti, O. Spydevold, J. Auwerx, J. A. Gustafsson, and H. I. Nebb. 2000. Cross-talk between fatty acid and cholesterol metabolism mediated by liver X receptor-alpha. Mol. Endocrinol. 14: 741-752.
61. Colin, S., E. Bourguignon, A-B. Boullay, J-J. Tousaint, S. Huet, F. Caira, B. Staels, S. Lestavel, J-M. A. Lobaccaro, and P. Delerive. 2008. Intestine-specific regulation of PPARalpha gene transcription by liver X receptors. Endocrinology. 149: 5128-5135.
62. Chinetti, G., S. Lestavel, V. Bocher, A. T. Remaley, B. Neve, I. P. Torra, E. Teissier, A. Minnich, M. Jaye, N. Duverger, et al. 2001. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. [comment] Nat. Med. 7: 53-58.
63. Chapkin, R. S., D. N. McMurray, L. A. Davidson, B. S. Patil, Y-Y. Fan, and J. R. Lupton. 2008. Bioactive dietary long-chain fatty acids: emerging mechanisms of action. Br. J. Nutr. 100: 1152-1157.
64. Ma, D. W. L., J. Seo, K. C. Switzer, Y-Y. Fan, D. N. McMurray, J. R. Lupton, and R. S. Chapkin. 2004. n-3 PUFA and membrane micro-domains: a new frontier in bioactive lipid research. J. Nutr. Biochem. 15: 700-706.
65. Hulbert, A. J., N. Turner, L. H. Storlien, and P. L. Else. 2005. Dietary fats and membrane function: implications for metabolism and disease. Biol. Rev. Camb. Philos. Soc. 80: 155-169.
66. Hulbert, A. J., and P. L. Else. 1999. Membranes as possible pacemakers of metabolism. J. Theor. Biol. 199: 257-274.
67. Hulbert, A. J., and P. L. Else. 2000. Mechanisms underlying the cost of living in animals. Annu. Rev. Physiol. 62: 207-235
68. Hulbert, A. J. 2003. Life, death and membrane bilayers. J. Exp. Biol. 206: 2303-2311.
69. Cozzone, D., C. Debard, N. Dif, N. Ricard, E. Disse, J. Vouillarmet, R. Rabasa-Lhoret, M. Laville, D. Pruneau, J. Rieusset, et al. 2006. Activation of liver X receptors promotes lipid accumulation but does not alter insulin action in human skeletal muscle cells. Diabetologia. 49: 990-999.
70. Kim, H. J., M. Takahashi, and O. Ezaki. 1999. Fish oil feeding decreases mature sterol regulatory element-binding protein 1 (SREBP-1) by down-regulation of SREBP-1c mRNA in mouse liver. A possible mechanism for down-regulation of lipogenic enzyme mRNAs. J. Biol. Chem. 274: 25892-25898.
71. Howell, G. I., X. Deng, C. Yellaturu, E. A. Park, H. G. Wilcox, R. Raghow, and M. B. Elam. 2009. N-3 polyunsaturated fatty acids suppress insulin-induced SREBP-1c transcription via reduced trans-activating capacity of LXRα. Biochim. Biophys. Acta. 1791: 1190-1196.
72. Kopecky, J., M. Rossmeisl, P. Flachs, O. Kuda, P. Brauner, Z. Jilkova, B. Stankova, E. Tvrzicka, and M. Bryhn. 2009. Symposium on "Frontiers in adipose tisssue biology" n-3 PUFA: bioavailability and modulation of adipose tissue function. Proc. Nutr. Soc. .
73. Liu, L., Y. Zhang, N. Chen, X. Shi, B. Tsang, and Y-H. Yu. 2007. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J. Clin. Invest. 117: 1679-1689.
74. Listenberger, L. L., X. Han, S. E. Lewis, S. Cases, R. V. Farese, Jr., D. S. Ory, and J. E. Schaffer. 2003. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. USA. 100: 3077-3082.