siRNA-based gene silencing reveals specialized roles of IRS-1/Akt2 and IRS-2/Akt1 in glucose and lipid metabolism in human skeletal muscle

Cell Metabolism

Volumn 4, Issue 1, 2006, Pages 89-96

  Bouzakri, Karim ^a   Zachrisson, Anna ^a   Al Khalili, Lubna ^a   Zhang, Bei B ^b   Koistinen, Heikki A ^c   Krook, Anna ^d   Zierath, Juleen R ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b MERCK RESEARCH LABORATORIES   (United States)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

HUMDISEASE; SIGNALING

Indexed keywords

GLUCOSE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; LIPID; PROTEIN KINASE B BETA; SMALL INTERFERING RNA;

ADULT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; GENE SILENCING; GENETIC TRANSFECTION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPID METABOLISM; MALE; METABOLIC DISORDER; MYOBLAST; MYOTUBE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WESTERN BLOTTING;

CELLS, CULTURED; FEMALE; GENE SILENCING; GLUCOSE; HUMANS; INSULIN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPIDS; MALE; MIDDLE AGED; MUSCLE FIBERS; MUSCLE, SKELETAL; MYOBLASTS; OXIDATION-REDUCTION; PALMITATES; PHOSPHOPROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 33745668478     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2006.04.008     Document Type: Article

References (49)

1. Accili D., and Arden K.C. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117 (2004) 421-426
2. Al-Khalili L., Cartee G.D., and Krook A. RNA interference-mediated reduction in GLUT1 inhibits serum-induced glucose transport in primary human skeletal muscle cells. Biochem. Biophys. Res. Commun. 307 (2003) 127-132
3. Altomare D.A., Lyons G.E., Mitsuuchi Y., Cheng J.Q., and Testa J.R. Akt2 mRNA is highly expressed in embryonic brown at and the AKT2 kinase is activated by insulin. Oncogene 16 (1998) 2407-2411
4. Araki E., Lipes M.A., Patti M.E., Bruning J.C., Haag III B., Johnson R.S., and Kahn C.R. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature 372 (1994) 186-190
5. Biddinger S.B., and Kahn C.R. From mice to men: Insights into the insulin resistance syndromes. Annu. Rev. Physiol. 68 (2005) 123-158
6. Björnholm M., Kawano Y., Lehtihet M., and Zierath J.R. Insulin receptor substrate-1 phosphorylation and phosphatidylinositol 3-kinase activity in skeletal muscle from NIDDM subjects after in vivo insulin stimulation. Diabetes 46 (1997) 524-527
7. Björnholm M., He A.R., Attersand A., Lake S., Liu S.C., Lienhard G.E., Taylor S., Arner P., and Zierath J.R. Absence of functional insulin receptor substrate-3 (IRS-3) gene in humans. Diabetologia 45 (2002) 1697-1702
8. 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. 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 (2003) 1319-1325
9. Bouzakri K., Roques M., Debard C., Berbe V., Rieusset J., Laville M., and Vidal H. WY-14643 and 9- cis-retinoic acid induce IRS-2/PI 3-kinase signalling pathway and increase glucose transport in human skeletal muscle cells: differential effect in myotubes from healthy subjects and Type 2 diabetic patients. Diabetologia 47 (2004) 1314-1323
10. Brodbeck D., Cron P., and Hemmings B.A. A human protein kinase Bgamma with regulatory phosphorylation sites in the activation loop and in the C-terminal hydrophobic domain. J. Biol. Chem. 274 (1999) 9133-9136
11. Brozinick Jr. J.T., Roberts B.R., and Dohm G.L. Defective signaling through Akt-2 and -3 but not Akt-1 in insulin-resistant human skeletal muscle: potential role in insulin resistance. Diabetes 52 (2003) 935-941
12. Cho H., Mu J., Kim J.K., Thorvaldsen J.L., Chu Q., Crenshaw III E.B., Kaestner K.H., Bartolomei M.S., Shulman G.I., and Birnbaum M.J. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292 (2001) 1728-1731
13. Cho H., Thorvaldsen J.L., Chu Q., Feng F., and Birnbaum M.J. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276 (2001) 38349-38352
14. Easton R.M., Cho H., Roovers K., Shineman D.W., Mizrahi M., Forman M.S., Lee V.M., Szabolcs M., de Jong R., Oltersdorf T., et al. Role for Akt3/protein kinase Bgamma in attainment of normal brain size. Mol. Cell. Biol. 25 (2005) 1869-1878
15. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., and Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411 (2001) 494-498
16. Gaster M., Kristensen S.R., Beck-Nielsen H., and Schroder H.D. A cellular model system of differentiated human myotubes. APMIS 109 (2001) 735-744
17. Griffin M.E., Marcucci M.J., Cline G.W., Bell K., Barucci N., Lee D., Goodyear L.J., Kraegen E.W., White M.F., and Shulman G.I. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes 48 (1999) 1270-1274
18. Gosmanov A.R., Umpierrez G.E., Karabell A.H., Cuervo R., and Thomason D.B. Impaired expression and insulin-stimulated phosphorylation of Akt-2 in muscle of obese patients with atypical diabetes. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E8-E15
19. Higaki Y., Wojtaszewski J.F., Hirshman M.F., Withers D.J., Towery H., White M.F., and Goodyear L.J. Insulin receptor substrate-2 is not necessary for insulin- and exercise-stimulated glucose transport in skeletal muscle. J. Biol. Chem. 274 (1999) 20791-20795
20. Holgado-Madruga M., Emlet D.R., Moscatello D.K., Godwin A.K., and Wong A.J. A Grb2-associated docking protein in EGF- and insulin-receptor signalling. Nature 379 (1996) 560-564
21. Huang C., Thirone A.C., Huang X., and Klip A. Differential contribution of insulin receptor substrates 1 versus 2 to insulin signaling and glucose uptake in L6 myotubes. J. Biol. Chem. 280 (2005) 19426-19435
22. Ishiki M., and Klip A. Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146 (2005) 5071-5078
23. Jiang Z.Y., Zhou Q.L., Coleman K.A., Chouinard M., Boese Q., and Czech M.P. Insulin signaling through Akt/protein kinase B analyzed by small interfering RNA-mediated gene silencing. Proc. Natl. Acad. Sci. USA 100 (2003) 7569-7574
24. Kane S., Sano H., Liu S.C.H., Asara J.M., Lane W.S., Garner C.C., and Lienhard G.E. A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J. Biol. Chem. 277 (2002) 22115-22118
25. Krook A., Björnholm M., Galuska D., Jiang X.J., Fahlman R., Myers Jr. M.G., Wallberg-Henriksson H., and Zierath J.R. Characterization of signal transduction and glucose transport in skeletal muscle from type 2 diabetic patients. Diabetes 49 (2000) 284-292
26. Kornmann M., Maruyama H., Bergmann U., Tangvoranuntakul P., Beger H.G., White M.F., and Korc M. Enhanced expression of the insulin receptor substrate-2 docking protein in human pancreatic cancer. Cancer Res. 58 (1998) 4250-4254
27. Lavan B.E., Fantin V.R., Chang E.T., Lane W.S., Keller S.R., and Lienhard G.E. A novel 160-kDa phosphotyrosine protein in insulin-treated embryonic kidney cells is a new member of the insulin receptor substrate family. J. Biol. Chem. 272 (1997) 21403-21407
28. Lavan B.E., Lane W.S., and Lienhard G.E. The 60-kDa phosphotyrosine protein in insulin-treated adipocytes is a new member of the insulin receptor substrate family. J. Biol. Chem. 272 (1997) 11439-11443
29. Lefai E., Roques M., Vega N., Laville M., and Vidal H. Expression of the splice variants of the p85alpha regulatory subunit of phosphoinositide 3-kinase in muscle and adipose tissue of healthy subjects and type 2 diabetic patients. Biochem. J. 360 (2001) 117-126
30. Petersen E.W., Carey A.L., Sacchetti M., Steinberg G.R., Macaulay S.L., Febbraio M.A., and Pedersen B.K. Acute IL-6 treatment increases fatty acid turnover in elderly humans in vivo and in tissue culture in vitro. Am. J. Physiol. Endocrinol. Metab. 288 (2005) E155-E162
31. Randle P.J., Garland P.B., Hales C.N., and Newsholme E.A. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1 (1963) 785-789
32. Sandri M., Sandri C., Gilbert A., Skurk C., Calabria E., Picard A., Walsh K., Schiaffino S., Lecker S.H., and Goldberg A.L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117 (2004) 399-412
33. Sano H., Kane S., Sano E., Miinea C.P., Asara J.M., Lane W.S., Garner C.W., and Lienhard G.E. Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem. 278 (2003) 14599-14602
34. Schuppin G.T., Pons S., Hügl S., Aiello L.P., King G.L., White M., and Rhodes C.J. A specific increased expression of insulin receptor substrate 2 in pancreatic beta-cell lines is involved in mediating serum-stimulated beta-cell growth. Diabetes 47 (1998) 1074-1085
35. Shepherd P.R. Mechanisms regulating phosphoinositide 3-kinase signalling in insulin-sensitive tissues. Acta Physiol. Scand. 18 (2005) 3-12
36. Shepherd P.R., Nave B.T., Rincon J., Nolte L.A., Bevan A.P., Siddle K., Zierath J.R., and Wallberg-Henriksson H. Differential regulation of phosphoinositide 3-kinase adapter subunit variants by insulin in human skeletal muscle. J. Biol. Chem. 272 (1997) 19000-19007
37. Stitt T.N., Drujan D., Clarke B.A., Panaro F., Timofeyva Y., Kline W.O., Gonzalez M., Yancopoulos G.D., and Glass D.J. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14 (2004) 395-403
38. Sun X.J., Rothenberg P., Kahn C.R., Backer J.M., Araki E., Wilden P.A., Cahill D.A., Goldstein B.J., and White M.F. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352 (1991) 73-77
39. Sun X.J., Wang L.M., Zhang Y., Yenush L., Myers Jr. M.G., Glasheen E., Lane W.S., Pierce J.H., and White M.F. Role of IRS-2 in insulin and cytokine signalling. Nature 377 (1995) 173-177
40. Taniguchi C.M., Ueki K., and Kahn R. Complementary roles of IRS-1 and IRS-2 in the hepatic regulation of metabolism. J. Clin. Invest. 115 (2005) 718-727
41. Taniguchi C.M., Emanuelli B., and Kahn C.R. Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 103 (2006) 4481-4486
42. Tseng Y.H., Butte A.J., Kokkotou E., Yechoor V.K., Taniguchi C.M., Kriauciunas K.M., Cypess A.M., Niinobe M., Yoshikawa K., Patti M.E., and Kahn C.R. Prediction of preadipocyte differentiation by gene expression reveals role of insulin receptor substrates and necdin. Nat. Cell Biol. 7 (2005) 601-611
43. Tsuchida H., Björnholm M., Fernstrom M., Galuska D., Johansson P., Wallberg-Henriksson H., Zierath J.R., Lake S., and Krook A. Gene expression of the p85alpha regulatory subunit of phosphatidylinositol 3-kinase in skeletal muscle from type 2 diabetic subjects. Pflugers Arch. 445 (2002) 25-31
44. Turcotte L.P., Raney M.A., and Todd M.K. ERK1/2 inhibition prevents contraction-induced increase in plasma membrane FAT/CD36 content and FA uptake in rodent muscle. Acta Physiol. Scand. 184 (2005) 131-139
45. Whiteman E.L., Cho H., and Birnbaum M.J. Role of Akt/protein kinase B in metabolism. Trends Endocrinol. Metab. 13 (2002) 444-451
46. Withers D.J., Gutierrez J.S., Towery H., Burks D.J., Ren J.M., Previs S., Zhang Y., Bernal D., Pons S., Shulman G.I., et al. Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391 (1998) 900-904
47. Yamanashi Y., Fukuda T., Nishizumi H., Inazu T., Higashi K., Kitamura D., Ishida T., Yamamura H., Watanabe T., and Yamamoto T. Role of tyrosine phosphorylation of HS1 in B cell antigen receptor-mediated apoptosis. J. Exp. Med. 185 (1997) 1387-1392
48. Zeigerer A., McBrayer M.K., and McGraw T.E. Insulin stimulation of GLUT4 exocytosis, but not its inhibition of endocytosis, is dependent on RabGAP AS160. Mol. Biol. Cell 15 (2004) 4406-4415
49. Zierath J.R., Krook A., and Wallberg-Henriksson H. Insulin action and insulin resistance in human skeletal muscle. Diabetologia 43 (2000) 821-835