Intracellular ceramide synthesis and protein kinase Cζ activation play an essential role in palmitate-induced insulin resistance in rat L6 skeletal muscle cells

Biochemical Journal

Volumn 382, Issue 2, 2004, Pages 619-629

  Powell, Darren J ^a   Turban, Sophie ^a   Gray, Alexander ^a   Hajduch, Eric ^a,b   Hundal, Harinder S ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b INSERM   (France)

Author keywords

Adipocytes; Free fatty acids; Muscle; Protein kinase B (PKB) Akt; Serine palmitoyl transferase (SPT)

Indexed keywords

BIOLOGICAL MEMBRANES; FATTY ACIDS; GLUCOSE; INSULIN; MUSCULOSKELETAL SYSTEM;

INTRACELLUALAR CERAMIDE SYNTHESIS; NON-ESTERIFIED FATTY ACIDS (NEFA); PATHOGENESIS; SKELETAL MUSCLE INSULIN RESISTANCE;

PROTEINS;

CERAMIDE; FATTY ACID; GLUCOSE; INSULIN RECEPTOR SUBSTRATE 1; PALMITIC ACID; PHOSPHATE; PHOSPHATIDYL 3,4,5 TRIPHOSPHATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C ZETA; SERINE PALMITOYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GLUCOSE TRANSPORT; INSULIN RESISTANCE; LIPOGENESIS; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; SKELETAL MUSCLE;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CELL LINE; CERAMIDES; ENZYME ACTIVATION; INSULIN RESISTANCE; INTRACELLULAR SPACE; MICE; MUSCLE FIBERS; MUSCLE, SKELETAL; PALMITATES; PROTEIN KINASE C; RATS;

ANIMALIA;

EID: 4544242908     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040139     Document Type: Article

References (47)

1. Wang, L., Folsom, A. R., Zheng, Z. J., Pankow, J. S. and Eckfeldt, J. H. (2003) Plasma fatty acid composition and incidence of diabetes in middle-aged adults: the Atherosclerosis Risk in Communities (ARIC) study. Am. J. Clin. Nutr. 78, 91-98
2. Mcgarty, J. D. (2002) Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of Type 2 diabetes. Diabetes 51, 7-18
3. Randle, P. J. (1998) Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab. Rev. 14, 263-283
4. Roden, M., Price, T. B., Perseghin, G., Petersen, K. F., Rothman, D. L., Cline, G. W. and Shulman, G. I. (1996) Mechanism of free fatty acid-induced insulin resistance in humans. J. Clin. Invest 97, 2859-2865
5. Storz, P., Doppler, H., Wernig, A., Pfizenmaier, K. and Muller, G. (1999) Cross-talk mechanisms in the development of insulin resistance of skeletal muscle cells palmitate rather than tumour necrosis factor inhibits insulin-dependent protein kinase B (PKB)/Akt stimulation and glucose uptake. Eur. J. Biochem. 266, 17-25
6. Reynoso, R., Salgado, L. M. and Calderon, V. (2003) High levels of palmitic acid lead to insulin resistance due to changes in the level of phosphorylation of the insulin receptor and insulin receptor substrate-1. Mol. Cell Biochem. 246, 155-162
7. Yu, C., Chen, Y., Cline, G. W., Zhang, D., Zong, H., Wang, Y., Bergeron, R., Kim, J. K., Cushman, S. W., Cooney, G. J. et al. (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277, 50230-50236
8. Schmitz-Peiffer, C., Craig, D. L. and Biden, T. J. (1999) Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J. Biol. Chem 274, 24202-24210
9. 12 myotubes. Arch. Biochem. Biophys. 419, 101-109
10. Dobrzyn, A. and Gorski, J. (2002) Ceramides and sphingomyelins in skeletal muscles of the rat: content and composition. Effect of prolonged exercise. Am. J. Physiol. Endocrinol. Metab. 282, E277-E285
11. Whiteman, E. L., Cho, H. and Birnbaum, M. J. (2002) Role of Akt/protein kinase B in metabolism. Trends Endocrinol. Metab. 13, 444-451
12. Hajduch, E., Litherland, G. J. and Hundal, H. S. (2001) Protein kinase B: a key regulator of glucose transport? FEBS Lett. 492, 199-203
13. Vanhaesebroeck, B. and Alessi, D. R. (2000) The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346, 561-576
14. Milburn, C. C., Deak, M., Kelly, S. M., Price, N. C., Alessi, D. R. and van Aalten, D. M. (2003) Binding of phosphatidylinositol 3,4,5-trisphosphate to the pleckstrin homology domain of protein kinase B induces a conformational change. Biochem. J. 375, 531-538
15. Salinas, M., Lopez-Valdaliso, R., Martin, D., Alvarez, A. and Cuadrado, A. (2000) Inhibition of PKB/Akt1 by C2-ceramide involves activation of ceramide-activated protein phosphatase in PC12 cells. Mol. Cell. Neurosci. 15, 156-169
16. Hajduch, E., Balendran, A., Batty, I. H., Litherland, G. J., Blair, A. S., Downes, C. P. and Hundal, H. S. (2001) Ceramide impairs the insulin-dependent membrane recruitment of protein kinase B leading to a loss in downstream signalling in L6 skeletal muscle cells. Diabetologia 44, 173-183
17. Cazzolli, R., Carpenter, L., Biden, T. J. and Schmitz-Peiffer, C. (2001) A role for protein phosphatase 2A-like activity, but not atypical protein kinase Czeta, in the inhibition of protein kinase B/Akt and glycogen synthesis by palmitate. Diabetes 50, 2210-2218
18. Bourbon, N. A., Sandirasegarane, L. and Kester, M. (2002) Ceramide-induced inhibition of Akt is mediated through protein kinase Czeta: implications for growth arrest. J. Biol. Chem. 277, 3286-3292
19. Powell, D. J., Hajduch, E., Kular, G. and Hundal, H. S. (2003) Ceramide disables 3-phosphoinositide binding to the Pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCzeta-dependent mechanism. Mol. Cell. Biol. 23, 7794-7808
20. Tsakiridis, T., McDowell, H. E., Walker, T., Downes, C. P., Hundal, H. S., Vranic, M. and Klip, A. (1995) Multiple roles of phosphatidylinositol 3-kinase in regulation of glucose-transport, amino-acid-transport, and glucose transporters in L6 skeletal-muscle cells. Endocrinology 136, 4315-4322
21. Mitsumoto, Y. and Klip, A. (1992) Developmental regulation of subcellular distribution and glycosylation of GLUT1 and GLUT4 glucose transporters during myogenesis of L6 muscle cells. J. Biol. Chem. 267, 4947-4962
22. Hajduch, E., Alessi, D. R., Hemmings, B. A. and Hundal, H. S. (1998) Constitutive activation of protein kinase Bα (PKBα) by membrane targeting promotes glucose and system A amino acid transport, protein synthesis and GSK3 inactivation in L6 muscle cells. Diabetes 47, 1006-1013
23. Frost, S. C. and Lane, M. D. (1985) Evidence for the involvement of vicinal sulfhydryl groups in insulin- activated hexose transport by 3T3-L1 adipocytes. J. Biol. Chem. 260, 2646-2652
24. Green, H. and Kehinde, O. (1975) An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell (Washington, D.C.) 5, 19-27
25. 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
26. Gray, A., Olsson, H., Batty, I. H., Priganica, L. and Peter, D. C. (2003) Nonradioactive methods for the assay of phosphoinositide 3-kinases and phosphoinositide phosphatases and selective detection of signaling lipids in cell and tissue extracts. Anal. Biochem. 313, 234-245
27. Montell, E., Turini, M., Marotta, M., Roberts, M., Noe, V., Ciudad, C. J., Mace, K. and Gomez-Foix, A. M. (2001) DAG accumulation from saturated fatty acids desensitizes insulin stimulation of glucose uptake in muscle cells. Am. J. Physiol. Endocrinol. Metab. 280, E229-E237
28. Summers, S. A., Garza, L. A., Zhou, H. and Birnbaum, M. J. (1998) Regulation of insulin-stimulated glucose transporter GLUT4 translocation and Akt kinase activity by ceramide. Mol. Cell. Biol. 18, 5457-5464
29. Standaert, M. L., Galloway, L., Karnam, P., Bandyopadhyay, G., Moscat, J. and Farese, R. V. (1997) Protein kinase Cζ as a downstream effector of phosphatidylinositol 3-kinase during insulin stimulation in rat adipocytes-potential role in glucose transport. J. Biol. Chem. 272, 30075-30082
30. Alessi, D. R. (1997) The protein kinase c inhibitors R0318220 and GF109203X are equally potent inhibitors of MAPKAP kinase-1 beta (Rsk-2) and p70 s6 kinase. FEBS Lett. 402, 121-123
31. Cousin, S. P., Hugl, S. R., Wrede, C. E., Kajio, H., Myers, Jr. M. G. and Rhodes, C. J. (2001) Free fatty acid-induced inhibition of glucose and insulin-like growth factor I-induced deoxyribonucleic acid synthesis in the pancreatic beta-cell line INS-1. Endocrinology 142, 229-240
32. Yaney, G. C., Korchak, H. M. and Corkey, B. E. (2000) Long-chain acyl CoA regulation of protein kinase C and fatty acid potentiation of glucose-stimulated insulin secretion in clonal β-cells. Endocrinology 141, 1989-1998
33. Bourbon, N. A., Yun, J. and Kester, M. (2000) Ceramide directly activates protein kinase C zeta to regulate a stress-activated protein kinase signaling complex. J. Biol. Chem. 275, 35617-35623
34. Hundal, H. S., Marette, A., Mitsumoto, Y., Ramial, T., Blostein, R. and Klip, A. (1992) Insulin induces translocation of the α2 and β1 subunits of the Na/K-ATPase from intracellular compartments to the plasma membrane in mammalian skeletal muscle. J. Biol. Chem. 267, 5040-5043
35. Randle, P. J., Newsholme, E. A. and Garland, P. B. (1964) Effects of fatty acids, ketone bodies and pyruvate and of alloxan diabetes and starvation on the uptake and metabolic fate of glucose in rat heart and diaphragm muscles. Biochem. J. 93, 652-665
36. Chavez, J. A., Knotts, T. A., Wang, L. P., Li, G., Dobrowsky, R. T., Florant, G. L. and Summers, S. A. (2003) A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids. J. Biol. Chem. 278, 10297-10303
37. Hanada, K. (2003) Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim. Biophys. Acta 1632, 16-30
38. Merrill, Jr, A. H. (2002) De novo sphingolipid biosynthesis: a necessary, but dangerous, pathway. J. Biol. Chem. 277, 25843-25846
39. Mathias, S., Pena, L. A. and Kolesnick, R. N. (1998) Signal transduction of stress via ceramide. Biochem. J. 335, 465-480
40. Turinsky, J., O'Sullivan, D. M. and Bayly, B. P. (1990) 1,2-Diacylglycerol and ceramide levels in insulin-resistant tissues of the rat in vivo. J. Biol. Chem. 265, 16880-16885
41. Zhou, H., Summers, S. A., Birnbaum, M. J. and Pittman, R. N. (1998) Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J. Biol. Chem. 273, 16568-16575
42. Doornbos, R. P., Theelen, M., van der Hoeven, P. C., van Blitterswijk, W. J., Verkleij, A. J. and van Bergen en Henegouwen, P. M. (1999) Protein kinase Cζ is a negative regulator of protein kinase B activity. J. Biol. Chem. 274, 8589-8596
43. Konishi, H., Kuroda, S. and Kikkawa, U. (1994) The pleckstrin homology domain of RAC protein kinase associates with the regulatory domain of protein kinase Cζ. Biochem. Biophys. Res. Commun. 205, 1770-1775
44. Mao, M., Fang, X., Lu, Y., Lapushin, R., Bast, J. R. and Mills, G. B. (2000) Inhibition of growth-factor-induced phosphorylation and activation of protein kinase B/Akt by atypical protein kinase C in breast cancer cells. Biochem. J. 352, 475-482
45. Cussac, D., Newman-Tancredi, A., Pasteau, V. and Millan, M. J. (1999) Human dopamine D(3) receptors mediate mitogen-activated protein kinase activation via a phosphatidylinositol 3-kinase and an atypical protein kinase C-dependent mechanism. Mol. Pharmacol. 56, 1025-1030
46. Idris, I., Gray, S. and Donnelly, R. (2001) Protein kinase C activation: isozyme-specific effects on metabolism and cardiovascular complications in diabetes. Diabetologia 44, 659-673
47. White, M. F. (2002) IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 283, E413-E422