AMPK: Positive and negative regulation, and its role in whole-body energy homeostasis

Current Opinion in Cell Biology

Volumn 33, Issue , 2015, Pages 1-7

  Hardie, D Grahame ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; HORMONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN KINASE LKB1; PROTEIN SERINE THREONINE KINASE;

ARTICLE; CELL ENERGY; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENERGY BALANCE; ENZYME ACTIVE SITE; HOMEOSTASIS; HYPOTHALAMUS; LYSOSOME; PHOSPHORYLATION AND DEPHOSPHORYLATION; PROTEIN EXPRESSION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENERGY METABOLISM; ENZYME ACTIVATION; HUMAN; METABOLISM;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ENERGY METABOLISM; ENZYME ACTIVATION; HOMEOSTASIS; HUMANS; HYPOTHALAMUS; LYSOSOMES; MODELS, MOLECULAR; PROTEIN-SERINE-THREONINE KINASES;

EID: 84907545906     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.09.004     Document Type: Review

References (50)

1. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 2007, 8:774-785.
2. Hardie D.G., Ross F.A., Hawley S.A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012, 13:251-262.
3. Gowans G.J., Hawley S.A., Ross F.A., Hardie D.G. AMP is a true physiological regulator of AMP-activated protein kinase by both allosteric activation and enhancing net phosphorylation. Cell Metab 2013, 18:556-566.
4. Oakhill J.S., Scott J.W., Kemp B.E. AMPK functions as an adenylate charge-regulated protein kinase. Trends Endocrinol Metab 2012, 23:125-132.
5. Cool B., Zinker B., Chiou W., Kifle L., Cao N., Perham M., Dickinson R., Adler A., Gagne G., Iyengar R., et al. Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab 2006, 3:403-416.
6. Xiao B., Sanders M.J., Carmena D., Bright N.J., Haire L.F., Underwood E., Patel B.R., Heath R.B., Walker P.A., Hallen S., et al. Structural basis of AMPK regulation by small molecule activators. Nat Commun 2013, 4:3017.
7. Zadra G., Photopoulos C., Tyekucheva S., Heidari P., Weng Q.P., Fedele G., Liu H., Scaglia N., Priolo C., Sicinska E., et al. A novel direct activator of AMPK inhibits prostate cancer growth by blocking lipogenesis. EMBO Mol Med 2014, 6:519-538.
8. Hawley S.A., Fullerton M.D., Ross F.A., Schertzer J.D., Chevtzoff C., Walker K.J., Peggie M.W., Zibrova D., Green K.A., Mustard K.J., et al. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012, 336:918-922.
9. Calabrese M.F., Rajamohan F., Harris M.S., Caspers N.L., Magyar R., Withka J.M., Wang H., Borzilleri K.A., Sahasrabudhe P.V., Hoth L.R., et al. Structural basis for AMPK activation: natural and synthetic ligands regulate kinase activity from opposite poles by different molecular mechanisms. Structure 2014, 22:1161-1172.
10. Gomez-Galeno J.E., Dang Q., Nguyen T.H., Boyer S.H., Grote M.P., Sun Z., Chen M., Craigo W.A., van Poelje P.D., MacKenna D.A., et al. A potent and selective AMPK activator that inhibits de novo lipogenesis. ACS Med Chem Lett 2010, 1:478-482.
11. Hunter R.W., Foretz M., Bultot L., Fullerton M.D., Deak M., Ross F.A., Hawley S.A., Shpiro N., Viollet B., Barron D., et al. Mechanism of action of Compound-13: an alpha1-selective small molecule activator of AMPK. Chem Biol 2014, 21:866-879.
12. Hawley S.A., Ross F.A., Chevtzoff C., Green K.A., Evans A., Fogarty S., Towler M.C., Brown L.J., Ogunbayo O.A., Evans A.M., et al. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab 2010, 11:554-565.
13. Auciello F.R., Ross F.A., Ikematsu N., Hardie D.G. Oxidative stress activates AMPK in cultured cells primarily by increasing cellular AMP and/or ADP. FEBS Lett 2014, 588:3361-3366.
14. Scott J.W., Ling N., Issa S.M., Dite T.A., O'Brien M.T., Chen Z.P., Galic S., Langendorf C.G., Steinberg G.R., Kemp B.E., et al. Small molecule drug A-769662 and AMP synergistically activate naive AMPK independent of upstream kinase signaling. Chem Biol 2014, 21:619-627.
15. Sakamoto K., Goransson O., Hardie D.G., Alessi D.R. Activity of LKB1 and AMPK-related kinases in skeletal muscle: effects of contraction, phenformin, and AICAR. Am J Physiol Endocrinol Metab 2004, 287:E310-E317.
16. 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, 332:1433-1440.
17. Oakhill J.S., Chen Z.P., Scott J.W., Steel R., Castelli L.A., Ling N., Macaulay S.L., Kemp B.E. beta-Subunit myristoylation is the gatekeeper for initiating metabolic stress sensing by AMP-activated protein kinase (AMPK). Proc Natl Acad Sci U S A 2010, 107:19237-19241.
18. 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.
19. Goransson O., McBride A., Hawley S.A., Ross F.A., Shpiro N., Foretz M., Viollet B., Hardie D.G., Sakamoto K. Mechanism of action of A-769662, a valuable tool for activation of AMP-activated protein kinase. J Biol Chem 2007, 282:32549-32560.
20. Sanders M.J., Ali Z.S., Hegarty B.D., Heath R., Snowden M.A., Carling D. Defining the mechanism of activation of AMP-activated protein kinase by the small molecule A-769662, a member of the thienopyridone family. J Biol Chem 2007, 282:32539-32548.
21. Zhang C.S., Jiang B., Li M., Zhu M., Peng Y., Zhang Y.L., Wu Y.Q., Li T.Y., Liang Y., Lu Z., et al. The lysosomal v-ATPase-ragulator complex is a common activator for AMPK and mTORC1, acting as a switch between catabolism and anabolism. Cell Metab 2014, 20:526-540.
22. Zhang Y.L., Guo H., Zhang C.S., Lin S.Y., Yin Z., Peng Y., Luo H., Shi Y., Lian G., Zhang C., et al. AMP as a low-energy charge signal autonomously initiates assembly of AXIN-AMPK-LKB1 complex for AMPK activation. Cell Metab 2013, 18:546-555.
23. Bar-Peled L., Sabatini D.M. Regulation of mTORC1 by amino acids. Trends Cell Biol 2014, 24:400-406.
24. Petit C.S., Roczniak-Ferguson A., Ferguson S.M. Recruitment of folliculin to lysosomes supports the amino acid-dependent activation of Rag GTPases. J Cell Biol 2013, 202:1107-1110.
25. Baba M., Hong S.B., Sharma N., Warren M.B., Nickerson M.L., Iwamatsu A., Esposito D., Gillette W.K., Hopkins R.F., Hartley J.L., et al. Folliculin encoded by the BHD gene interacts with a binding protein. FNIP1, and AMPK, and is involved in AMPK and mTOR signaling. Proc Natl Acad Sci U S A 2006, 103:15552-15557.
26. Wang L., Kobayashi T., Piao X., Shiono M., Takagi Y., Mineki R., Taka H., Zhang D., Abe M., Sun G., et al. Serine 62 is a phosphorylation site in folliculin, the Birt-Hogg-Dube gene product. FEBS Lett 2010, 584:39-43.
27. Yan M., Gingras M.C., Dunlop E.A., Nouet Y., Dupuy F., Jalali Z., Possik E., Coull B.J., Kharitidi D., Dydensborg A.B., et al. The tumor suppressor folliculin regulates AMPK-dependent metabolic transformation. J Clin Invest 2014, 124:2640-2650.
28. Houde V.P., Ritorto M.S., Gourlay R., Varghese J., Davies P., Shpiro N., Sakamoto K., Alessi D.R. Investigation of LKB1 Ser431 phosphorylation and Cys433 farnesylation using mouse knockin analysis reveals an unexpected role of prenylation in regulating AMPK activity. Biochem J 2014, 458:41-56.
29. Andersson U., Filipsson K., Abbott C.R., Woods A., Smith K., Bloom S.R., Carling D., Small C.J. AMP-activated protein kinase plays a role in the control of food intake. J Biol Chem 2004, 279:12005-12008.
30. Kubota N., Yano W., Kubota T., Yamauchi T., Itoh S., Kumagai H., Kozono H., Takamoto I., Okamoto S., Shiuchi T., et al. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab 2007, 6:55-68.
31. Hardie D.G., Ashford M.L. AMPK: regulating energy balance at the cellular and whole body levels. Physiology 2014, 29:99-107.
32. Lopez M., Varela L., Vazquez M.J., Rodriguez-Cuenca S., Gonzalez C.R., Velagapudi V.R., Morgan D.A., Schoenmakers E., Agassandian K., Lage R., et al. Hypothalamic AMPK and fatty acid metabolism mediate thyroid regulation of energy balance. Nat Med 2010, 16:1001-1008.
33. Beiroa D., Imbernon M., Gallego R., Senra A., Herranz D., Villaroya F., Serrano M., Ferno J., Salvador J., Escalada J., et al. GLP-1 agonism stimulates brown adipose tissue thermogenesis and browning through hypothalamic AMPK. Diabetes 2014, (in press). 10.2337/db14-0302.
34. Yang Y., Atasoy D., Su H.H., Sternson S.M. Hunger states switch a flip-flop memory circuit via a synaptic AMPK-dependent positive feedback loop. Cell 2011, 146:992-1000.
35. Polakiewicz R.D., Schieferl S.M., Gingras A.C., Sonenberg N., Comb M.J. mu-Opioid receptor activates signaling pathways implicated in cell survival and translational control. J Biol Chem 1998, 273:23534-23541.
36. Dagon Y., Hur E., Zheng B., Wellenstein K., Cantley L.C., Kahn B.B. p70S6 Kinase phosphorylates AMPK on serine 491 to mediate leptin's effect on food intake. Cell Metab 2012, 16:104-112.
37. Krasner N.M., Ido Y., Ruderman N.B., Cacicedo J.M. Glucagon-like peptide-1 (GLP-1) analog liraglutide inhibits endothelial cell inflammation through a calcium and AMPK dependent mechanism. PLOS ONE 2014, 9:e97554.
38. Riek U., Scholz R., Konarev P., Rufer A., Suter M., Nazabal A., Ringler P., Chami M., Muller S.A., Neumann D., et al. Structural properties of AMP-activated protein kinase. Dimerization, molecular shape, and changes upon ligand binding. J Biol Chem 2008, 283:18331-18343.
39. Hudson E.R., Pan D.A., James J., Lucocq J.M., Hawley S.A., Green K.A., Baba O., Terashima T., Hardie D.G. A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr Biol 2003, 13:861-866.
40. Polekhina G., Gupta A., Michell B.J., van Denderen B., Murthy S., Feil S.C., Jennings I.G., Campbell D.J., Witters L.A., Parker M.W., et al. AMPK b-Subunit targets metabolic stress-sensing to glycogen. Curr Biol 2003, 13:867-871.
41. Polekhina G., Gupta A., van Denderen B.J., Feil S.C., Kemp B.E., Stapleton D., Parker M.W. Structural basis for glycogen recognition by AMP-activated protein kinase. Structure (Camb) 2005, 13:1453-1460.
42. Pang T., Xiong B., Li J.Y., Qiu B.Y., Jin G.Z., Shen J.K., Li J. Conserved alpha-helix acts as autoinhibitory sequence in AMP-activated protein kinase alpha subunits. J Biol Chem 2007, 282:495-506.
43. Chen L., Jiao Z.H., Zheng L.S., Zhang Y.Y., Xie S.T., Wang Z.X., Wu J.W. Structural insight into the autoinhibition mechanism of AMP-activated protein kinase. Nature 2009, 459:1146-1150.
44. Chen L., Xin F.J., Wang J., Hu J., Zhang Y.Y., Wan S., Cao L.S., Lu C., Li P., Yan S.F., et al. Conserved regulatory elements in AMPK. Nature 2013, 498:E8-E10.
45. Xin F.J., Wang J., Zhao R.Q., Wang Z.X., Wu J.W. Coordinated regulation of AMPK activity by multiple elements in the alpha-subunit. Cell Res 2013, 23:1237-1240.
46. Hawley S.A., Ross F.A., Gowans G.J., Tibarewal P., Leslie N.R., Hardie D.G. Phosphorylation by Akt within the ST loop of AMPK-α1 down-regulates its activation in tumour cells. Biochem J 2014, 459:275-287.
47. Horman S., Vertommen D., Heath R., Neumann D., Mouton V., Woods A., Schlattner U., Wallimann T., Carling D., Hue L., et al. 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.
48. Hurley R.L., Barre L.K., Wood S.D., Anderson K.A., Kemp B.E., Means A.R., Witters L.A. Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J Biol Chem 2006, 281:36662-36672.
49. Suzuki T., Bridges D., Nakada D., Skiniotis G., Morrison S.J., Lin J.D., Saltiel A.R., Inoki K. Inhibition of AMPK catabolic action by GSK3. Mol Cell 2013, 50:407-419.
50. Djouder N., Tuerk R.D., Suter M., Salvioni P., Thali R.F., Scholz R., Vaahtomeri K., Auchli Y., Rechsteiner H., Brunisholz R.A., et al. PKA phosphorylates and inactivates AMPKalpha to promote efficient lipolysis. EMBO J 2010, 29:469-481.