Inhibition of AMPK catabolic action by GSK3

Molecular Cell

Volumn 50, Issue 3, 2013, Pages 407-419

  Suzuki, Tsukasa ^a   Bridges, Dave ^a   Nakada, Daisuke ^a,c   Skiniotis, Georgios ^a,b   Morrison, Sean J ^a,d   Lin, Jiandie D ^a,b   Saltiel, Alan R ^a,b   Inoki, Ken ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ARTICLE; CATABOLISM; CATALYSIS; CELL ENERGY; HUMAN; HUMAN CELL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SENSOR; CELL LINE; CELL STRAIN HEK293; DRUG ANTAGONISM; METABOLISM; PHOSPHORYLATION; PROTEIN SUBUNIT;

AMP-ACTIVATED PROTEIN KINASES; CELL LINE; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84887189624     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.03.022     Document Type: Article

References (42)

1. Banko M.R., Allen J.J., Schaffer B.E., Wilker E.W., Tsou P., White J.L., Villén J., Wang B., Kim S.R., Sakamoto K., et al. Chemical genetic screen for AMPKα2 substrates uncovers a network of proteins involved in mitosis. Mol. Cell 2011, 44:878-892.
2. Carling D., Clarke P.R., Zammit V.A., Hardie D.G. Purification and characterization of the AMP-activated protein kinase. Copurification of acetyl-CoA carboxylase kinase and 3-hydroxy-3-methylglutaryl-CoA reductase kinase activities. Eur. J. Biochem. 1989, 186:129-136.
3. Clarke P.R., Hardie D.G. Regulation of HMG-CoA reductase: identification of the site phosphorylated by the AMP-activated protein kinase in vitro and in intact rat liver. EMBO J. 1990, 9:2439-2446.
4. Cohen P., Frame S. The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2001, 2:769-776.
5. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378:785-789.
6. Dokken B.B., Sloniger J.A., Henriksen E.J. Acute selective glycogen synthase kinase-3 inhibition enhances insulin signaling in prediabetic insulin-resistant rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2005, 288:E1188-E1194.
7. Düvel K., Yecies J.L., Menon S., Raman P., Lipovsky A.I., Souza A.L., Triantafellow E., Ma Q., Gorski R., Cleaver S., et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol. Cell 2010, 39:171-183.
8. Egan D.F., Shackelford D.B., Mihaylova M.M., Gelino S., Kohnz R.A., Mair W., Vasquez D.S., Joshi A., Gwinn D.M., Taylor R., et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011, 331:456-461.
9. Fiol C.J., Mahrenholz A.M., Wang Y., Roeske R.W., Roach P.J. Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3. J. Biol. Chem. 1987, 262:14042-14048.
10. Frame S., Cohen P., Biondi R.M. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol. Cell 2001, 7:1321-1327.
11. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., Shaw R.J. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 2008, 30:214-226.
12. Hardie D.G., Ross F.A., Hawley S.A. AMP-activated protein kinase: a target for drugs both ancient and modern. Chem. Biol. 2012, 19:1222-1236.
13. Harrington L.S., Findlay G.M., Gray A., Tolkacheva T., Wigfield S., Rebholz H., Barnett J., Leslie N.R., Cheng S., Shepherd P.R., et al. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J. Cell Biol. 2004, 166:213-223.
14. Hawley S.A., Pan D.A., Mustard K.J., Ross L., Bain J., Edelman A.M., Frenguelli B.G., Hardie D.G. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2005, 2:9-19.
15. Horman S., Vertommen D., Heath R., Neumann D., Mouton V., Woods A., Schlattner U., Wallimann T., Carling D., Hue L., Rider M.H. Insulin antagonizes ischemia-induced Thr172 phosphorylation of AMP-activated protein kinase alpha-subunits in heart via hierarchical phosphorylation of Ser485/491. J. Biol. Chem. 2006, 281:5335-5340.
16. Hsu P.P., Kang S.A., Rameseder J., Zhang Y., Ottina K.A., Lim D., Peterson T.R., Choi Y., Gray N.S., Yaffe M.B., et al. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 2011, 332:1317-1322.
17. Hunter R.W., Treebak J.T., Wojtaszewski J.F., Sakamoto K. Molecular mechanism by which AMP-activated protein kinase activation promotes glycogen accumulation in muscle. Diabetes 2011, 60:766-774.
18. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
19. Inoki K., Ouyang H., Zhu T., Lindvall C., Wang Y., Zhang X., Yang Q., Bennett C., Harada Y., Stankunas K., et al. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 2006, 126:955-968.
20. Inoki K., Mori H., Wang J., Suzuki T., Hong S., Yoshida S., Blattner S.M., Ikenoue T., Ruegg M.A., Hall M.N., et al. mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J. Clin. Invest. 2011, 121:2181-2196.
21. Jørgensen S.B., Nielsen J.N., Birk J.B., Olsen G.S., Viollet B., Andreelli F., Schjerling P., Vaulont S., Hardie D.G., Hansen B.F., et al. The alpha2-5'AMP-activated protein kinase is a site 2 glycogen synthase kinase in skeletal muscle and is responsive to glucose loading. Diabetes 2004, 53:3074-3081.
22. Kahn B.B., Alquier T., Carling D., Hardie D.G. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 2005, 1:15-25.
23. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
24. Koo S.H., Flechner L., Qi L., Zhang X., Screaton R.A., Jeffries S., Hedrick S., Xu W., Boussouar F., Brindle P., et al. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 2005, 437:1109-1111.
25. Kovacic S., Soltys C.L., Barr A.J., Shiojima I., Walsh K., Dyck J.R. Akt activity negatively regulates phosphorylation of AMP-activated protein kinase in the heart. J. Biol. Chem. 2003, 278:39422-39427.
26. Liu C., Li Y., Semenov M., Han C., Baeg G.H., Tan Y., Zhang Z., Lin X., He X. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002, 108:837-847.
27. Lochhead P.A., Salt I.P., Walker K.S., Hardie D.G., Sutherland C. 5-aminoimidazole-4-carboxamide riboside mimics the effects of insulin on the expression of the 2 key gluconeogenic genes PEPCK and glucose-6-phosphatase. Diabetes 2000, 49:896-903.
28. Lochhead P.A., Coghlan M., Rice S.Q., Sutherland C. Inhibition of GSK-3 selectively reduces glucose-6-phosphatase and phosphatase and phosphoenolypyruvate carboxykinase gene expression. Diabetes 2001, 50:937-946.
29. Manning B.D., Tee A.R., Logsdon M.N., Blenis J., Cantley L.C. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell 2002, 10:151-162.
30. Merrill G.F., Kurth E.J., Hardie D.G., Winder W.W. AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am. J. Physiol. 1997, 273:E1107-E1112.
31. Oakhill J.S., Steel R., Chen Z.P., Scott J.W., Ling N., Tam S., Kemp B.E. AMPK is a direct adenylate charge-regulated protein kinase. Science 2011, 332:1433-1435.
32. Peterson T.R., Sengupta S.S., Harris T.E., Carmack A.E., Kang S.A., Balderas E., Guertin D.A., Madden K.L., Carpenter A.E., Finck B.N., Sabatini D.M. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 2011, 146:408-420.
33. Ring D.B., Johnson K.W., Henriksen E.J., Nuss J.M., Goff D., Kinnick T.R., Ma S.T., Reeder J.W., Samuels I., Slabiak T., et al. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 2003, 52:588-595.
34. Samuel V.T., Shulman G.I. Mechanisms for insulin resistance: common threads and missing links. Cell 2012, 148:852-871.
35. Sengupta S., Peterson T.R., Sabatini D.M. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 2010, 40:310-322.
36. Skurat A.V., Wang Y., Roach P.J. Rabbit skeletal muscle glycogen synthase expressed in COS cells. Identification of regulatory phosphorylation sites. J. Biol. Chem. 1994, 269:25534-25542.
37. Steinberg G.R., Kemp B.E. AMPK in health and disease. Physiol. Rev. 2009, 89:1025-1078.
38. Stoothoff W.H., Cho J.H., McDonald R.P., Johnson G.V. FRAT-2 preferentially increases glycogen synthase kinase 3 beta-mediated phosphorylation of primed sites, which results in enhanced tau phosphorylation. J. Biol. Chem. 2005, 280:270-276.
39. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 1990, 9:2431-2438.
40. Woods A., Johnstone S.R., Dickerson K., Leiper F.C., Fryer L.G., Neumann D., Schlattner U., Wallimann T., Carlson M., Carling D. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr. Biol. 2003, 13:2004-2008.
41. Xiao B., Sanders M.J., Underwood E., Heath R., Mayer F.V., Carmena D., Jing C., Walker P.A., Eccleston J.F., Haire L.F., et al. Structure of mammalian AMPK and its regulation by ADP. Nature 2011, 472:230-233.
42. Yu Y., Yoon S.O., Poulogiannis G., Yang Q., Ma X.M., Villén J., Kubica N., Hoffman G.R., Cantley L.C., Gygi S.P., Blenis J. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 2011, 332:1322-1326.