Post-transcriptional gene silencing of ribosomal protein S6 kinase 1 restores insulin action in leucine-treated skeletal muscle

Cellular and Molecular Life Sciences

Volumn 66, Issue 8, 2009, Pages 1457-1466

  Deshmukh, A ^a   Salehzadeh, F ^a   Metayer Coustard, S ^a,c   Fahlman, R ^a   Nair, K S ^b   Al Khalili, L ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MAYO CLINIC COLLEGE OF MEDICINE   (United States)

^c CEMAGREF   (France)

Author keywords

Branched chain amino acids; Glucose uptake; Glycogen synthesis; Nutrient sensing; Signal transduction

Indexed keywords

GLYCOGEN; INSULIN; LEUCINE; PROTEIN KINASE B; S6 KINASE; S6 KINASE 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; GLYCOGEN SYNTHESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MYOTUBE; NEGATIVE FEEDBACK; POSTTRANSCRIPTIONAL GENE SILENCING; PROTEIN DEPLETION; REDUCTION; SKELETAL MUSCLE;

FEMALE; GLUCOSE; GLYCOGEN; HUMANS; INSULIN; LEUCINE; MALE; MIDDLE AGED; MUSCLE, SKELETAL; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RIBOSOMAL PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 67349240416     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-009-8818-y     Document Type: Article

References (49)

1. Buse, M., G. and Reid, S. S. (1975) Leucine. A possible regulator of protein turnover in muscle. J. Clin. Invest. 56, 1250-1261
2. Li, J. B. and Jefferson, L. S. (1978) Influence of amino acid availability on protein turnover in perfused skeletal muscle. Biochim. Biophys. Acta 544, 351
3. Vary, T. C., Jefferson, L. S. and Kimball, S. R. (1999) Amino acid-induced stimulation of translation initiation in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 277, E1077-1086
4. Felig, P. (1975) Amino acid metabolism in man. Annu. Rev. Biochem. 44, 933-955
5. Felig, P., Marliss, E. and Cahill, G. F. Jr. (1969) Plasma amino acid levels and insulin secretion in obesity. N Engl. J. Med. 281, 811-816
6. Krebs, M. Krssak, M., Bemroider, E., Anderwald, C., Brehm, A., Meyerspeer, M., Nowotny, P., Roth, E., Waldhausl, W. and Roden, M. (2002) Mechanism of amino acid-induced skeletal muscle insulin resistance in humans. Diabetes 51, 599-605
7. Pisters, P. W., Restifo, H P., Cersosimo, E. and Brennan, M. F. (1991) The effects of euglycemic hyperinsulinemia and amino acid infusion on regional and whole body glucose disposal in man. Metabolism 40, 59-65
8. Anthony, J. C., Anthony, T. G., Kimball, S. R. and Jefferson, L. S. (2001 ) signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J. Nutr. 131, 856-860
9. Kimball, S. R., Shantz, L. M., Horetsky, R. L. and Jefferson, L. S. (1999) Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. J. Biol. Chem. 274, 11647-11652
10. Proud, C G. (2004) Role of mTOR signalling in the control of translation initiation and elongation by nutrients. Curr. Top. Microbiol. Immunol. 279, 215-244
11. Briaud, I., Dickson, L. M., Lingohr, M. K., McCuaig, J. F., Lawrence, J. C. and Rhodes, C J. (2005) Insulin receptor substrate-2 proteasomal degradation mediated by a mammalian target of rapamycin (mTOR)-induced negative feedback down-regulates protein kinase B-mediated signaling pathway in beta-Cells. J. Biol. Chem. 280, 2282-2293
12. Noda, S., Kishi, K., Yuasa, T., Hayashi, H., Ohnishi, T., Miyata, L1 Nishitani, H. and Ebina, Y (2000) Overexpression of wild-type Akt1 promoted insulin-stimulated p70S6 kinase (p70S6K) activity and affected GSK3 beta regulation, but did not promote insulin-stimulated GLUT4 translocation or glucose transport in L6 myotubes. J. Med. Invest. 47, 47-55
13. Hara, K., Yonezawa, K., Weng, Q-P., Kozlowski, M. T., Belham, C and Avruch, J. (1998) Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common, effector mechanism. J. Biol. Chem. 273, .14484-14494
14. Dann, S., Selvaraja, A. and Thomas, G. (2007) mTOR Complexl-S6K1 signaling: At the crossroads of obesity, diabetes and cancer. Trends Mol. Med. 13, 252-259
15. Krieg, J, Hofsteenge, J and Thomas, G. (1988) Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J. Biol. Chem. 263, 11473-11477
16. Ruvinsky, I. and Meyuhas, O. (2006) Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem. Sci. 6, 342-348
17. Patti, M-E. (1999) Nutrient modulation of cellular insulin action. Ann, NY Acad. Sci. 892, 187-203
18. Krebs, M. (2005) Amino acid-dependent modulation of glucose metabolism in humans. Eur. J. Clin. Invest. 35, 351 -354
19. Schwenk, W. F. and Haymond, M. W. (1987) Decreased uptake of glucose by human forearm during infusion of leucine, isoleucine, or threonine. Diabetes 36, 199-204
20. Um, S. H., D'Alessio, D. and Thomas, G. (2006) Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1, Cell Metab. 3, 393-402
21. Um, S. H., Frigerio, F., Watanabe, M., Picard, F., Joaquin, M., Sticker, M., Fumagalli, S., Allegrini, P. R., Kozma, S. C., Auwerx, J. and Thomas, G. (2004) Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431, 200-205
22. Rui, L. (2007) A link between protein translation and body weight. J. Clin. Invest. 117, 310-313
23. Tremblay, F., Gagnon, A., Veilleux, A., Sorisky, A. and Marette, A. (2005) Activation of the mammalian target of rapamycin pathway acutely inhibits insulin signaling to Akt and glucose transport in 3T3-L1 and human adipocytes. Endocrinology 146, 1328-1337
24. Baum, J. I., O'Connor, J. C., Seyler, J. E., Anthony, T. G., Freund, G. G. and Layman, D. K. (2005) Leucine reduces the duration, of insulin-induced PI 3-kinase activity in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 288, E86-91
25. Tremblay, F. and Marette, A. (2001) Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J. Biol. Chem. 276, 38052-38060
26. Zick, Y (2001) Insulin resistance: a phosphorylation-based uncoupling of insulin signaling. Trends Cell. Biol. 11, 437-441
27. Carlson, C J., White, M. R and Rondinone, C. M. (2004) Mammalian target of rapamycin regulates IRS-1 serine 307 phosphorylation. Biochem. Biophys. Res. Commun. 316, 533-539
28. Pende, M., Kozma, S. C., Jaquet, M., Oorschot, V., Burcelin, R., Le Marchand-Brustel, Y., Klumperman, J., Thorens, B. and Thomas, G. (2000) Hypoinsulinaemia, glucose intolerance and diminished beta-cell size in S6K1-deficient mice. Nature 408, 994-997
29. Krook, A., Roth, R. A., Jiang, X. J., Zierath, J. R. and Wallberg-Henriksson, H. (1998) Insulin-stimulated Akt kinase activity is reduced in skeletal muscle from non-insulin-dependent diabetic subjects. Diabetes 47, 1281-1286
30. Bouzakri, K. Roques, M., Gual, P., Espinosa, S., Guebre-Egziabher, F., Riou, J. P., Laville, M., Le Marchand-Brustel, Y., Tanti, J. F. and Vidal, H. (2003) Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 52, 1319-1325
31. Al-Khalili, L., Chibalin, A. V., Kannisto, K., Zhang, B. B., Permert, J., Holman, G. D., Ehrenborg, E., Ding, V. D., Zierath, J. R. and Krook, A. (2003) Insulin action in cultured human skeletal muscle cells during differentiation : Assessment of cell surface GLUT4 and GLUT1 content. Cell. Mol. Life Sci. 60, 991-998
32. Al-Khalili, L., Kramer, D., Wretenberg, P. and Krook, A. (2004) Human skeletal muscle cell differentiation is associated with changes in myogenic markers and enhanced insulin-mediated MAPK and PKB phosphorylation. Acta Physiol. Scand. 180, 395-403
33. Al-Khalili, L., Cartee, G. D. and Krook, A. (2003) RNA interference-mediated reduction in GLUT1 inhibits serum-induced glucose transport in primary human skeletal muscle cells. Biochem. Biophys. Res. Commun. 307, 127-132
34. Al-Khalili, L., Bouzakri, K., Glund, S., Lonnqvist, F., Koistinen, H. A. and Krook, A. (2006) Signaling specificity of interleukin-6 action on glucose and lipid metabolism in skeletal muscle. Mol. Endocrinol. 20, 3364-3375
35. Groop, L., Bonadonna, R. C., DelPrato, S., Ratheiser, K., Zyck, K., Ferannini, E. and DeFronzo, R. A. (1989) Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus: Evidence for multiple sites of insulin resistance. J. Clin. Invest. 84, 205-213
36. Zierath, J. R., Krook, A. and Wallberg-Henriksson, H. (2000) Insulin action, and insulin resistance in human skeletal muscle. Diabetologia 43, 82.1-835
37. Boden, G. (1997) Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes 46, 3-10
38. Hegarty, B. D., Furier, S. M., Ye, J., Cooney, G. J. and Kraegen, E. W. (2003) The role of intramuscular lipid in insulin resistance. Acta Physiol. Scand. 178, 373-383
39. Linn, T., Geyer, R., Prassek, S. and Laube, H. (1996) Effect of dietary protein intake on insulin secretion and glucose metabolism in insulin-dependent diabetes mellitus. J. Clin. Endocrinol. Metab. 81, 3938-3943
40. Song, Y., Manson, J. E., Buring, J. E. and Liu, S. (2004) A prospective study of red meat consumption and type 2 diabetes in middle-aged and elderly women : The women's health study. Diabetes Care 27, 2108-2115
41. Flakoll, P. J., Wentzel, L. S., Rice, D. E., Hill, J. O. and Abumrad, H H (1992) Short-term regulation of insulin-mediated glucose utilization in four-day fasted human volunteers: Role of amino acid availability. Diabetologia 35, 357-366
42. Fried, S. K. and Watford, M. (2007) Leucing weight with a futile cycle. Cell Metab. 6, 155-156
43. She, P., Van Horn, C., Reid, T., Hutson, S. M., Cooney, R. H and Lynch, C J. (2007) Obesity-related elevations in plasma leucine are associated with alterations in enzymes involved in branched-chain amino acid metabolism. Am. J. Physiol. Endocrinol. Metab. 293, E1552-1563
44. Doi, M., Yamaoka, I., Fukunaga, T. and Nakayama, M. (2003) Isoleucine, a potent plasma glucose-lowering amino acid, stimulates glucose uptake in C2C12 myotubes. Biochem. Biophys. Res. Commun. 312, 1111-1117
45. Armstrong, J. L., Bonavaud, S. M., Toole, B. J. and Yeaman, S. J. (2001) Regulation of glycogen synthesis by amino acids in cultured human muscle cells. J. Biol. Chem. 276, 952-956
46. Tremblay F., Brûlé S., Hee Um S., Li Y, Masuda K., Roden M., Sun X. J., Krebs M., Polakiewicz R. D., Thomas G. and Marette A. (2007) Identification of IRS-1 Ser-11.0.1 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. Proc. Natl. Acad. Sci. USA 104, 14056-14061
47. Pende, M. (2006) mTOR, Akt, S6 kinases and the control of skeletal muscle growth. Bull. Cancer 93, E39-43
48. Manning, B. D. (2004) Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J. Cell Biol. 167, 399-403
49. Li. Y., Soos T. J., Li X., Wu J., Degennaro M., Sun X., Littman D. R., Birnbaum M. J. and Polakiewicz R. D. (2004) Protein kinase C theta inhibits insulin signaling by phosphorylating IRS1 at Ser1101. J. Biol. Chem. 279, 45304-45307