AMPK Phosphorylation of Raptor Mediates a Metabolic Checkpoint

Molecular Cell

Volumn 30, Issue 2, 2008, Pages 214-226

  Gwinn, Dana M ^a   Shackelford, David B ^a   Egan, Daniel F ^a   Mihaylova, Maria M ^a   Mery, Annabelle ^a   Vasquez, Debbie S ^a   Turk, Benjamin E ^b   Shaw, Reuben J ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

PROTEINS; SIGNALING

Indexed keywords

ADENYLATE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN SUBUNIT RAPTOR; PROTEIN 14 3 3; SERINE;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL GROWTH; CONTROLLED STUDY; EMBRYO; ENERGY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INHIBITION KINETICS; METABOLIC REGULATION; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION;

AMINO ACID MOTIFS; ANIMALS; APOPTOSIS; CELL CYCLE; CELL LINE; HUMANS; MALE; MICE; MICE, INBRED STRAINS; MULTIENZYME COMPLEXES; PEPTIDE LIBRARY; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; PROTEOMICS; SERINE; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS;

RAPTORES;

EID: 42949139481     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.03.003     Document Type: Article

References (52)

1. Apfeld J., O'Connor G., McDonagh T., DiStefano P.S., and Curtis R. The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev. 18 (2004) 3004-3009
2. Ashrafi K., Lin S.S., Manchester J.K., and Gordon J.I. Sip2p and its partner snf1p kinase affect aging in S. cerevisiae. Genes Dev. 14 (2000) 1872-1885
3. Baena-Gonzalez E., Rolland F., Thevelein J.M., and Sheen J. A central integrator of transcription networks in plant stress and energy signalling. Nature 448 (2007) 938-942
4. Baugh L.R., and Sternberg P.W. DAF-16/FOXO regulates transcription of cki-1/Cip/Kip and repression of lin-4 during C. elegans L1 arrest. Curr. Biol. 16 (2006) 780-785
5. Bokko P.B., Francione L., Bandala-Sanchez E., Ahmed A.U., Annesley S.J., Huang X., Khurana T., Kimmel A.R., and Fisher P.R. Diverse cytopathologies in mitochondrial disease are caused by AMP-activated protein kinase signaling. Mol. Biol. Cell 18 (2007) 1874-1886
6. Bridges D., and Moorhead G.B. 14-3-3 proteins: a number of functions for a numbered protein. Sci. STKE 2005 (2005) re10
7. Bullock A.N., Debreczeni J., Amos A.L., Knapp S., and Turk B.E. Structure and substrate specificity of the Pim-1 kinase. J. Biol. Chem. 280 (2005) 41675-41682
8. Bunkoczi G., Salah E., Filippakopoulos P., Federov O., Müller S., Sobott F., Parker S.A., Zhang H., Min W., Turk B.E., and Knapp S. Structural and functional characterization of the human protein kinase ASK1. Structure 15 (2007) 1215-1226
9. Buzzai M., Jones R.G., Amaravadi R.K., Lum J.J., DeBerardinis R.J., Zhao F., Viollet B., and Thompson C.B. Systemic treatment with the antidiabetic drug metformin selectively impairs p53-deficient tumor cell growth. Cancer Res. 67 (2007) 6745-6752
10. Carretero J., Medina P.P., Blanco R., Smit L., Tang M., Roncador G., Maestre L., Conde E., Lopez-Rios F., Clevers H.C., and Sanchez-Cespedes M. Dysfunctional AMPK activity, signalling through mTOR and survival in response to energetic stress in LKB1-deficient lung cancer. Oncogene 26 (2007) 1616-1625
11. Corradetti M.N., Inoki K., Bardeesy N., DePinho R., and Guan K.L. Regulation of the TSC pathway by LKB1: evidence of a molecular link between tuberous sclerosis complex and Peutz-Jeghers syndrome. Genes Dev. 18 (2004) 1533-1538
12. Gardino A.K., Smerdon S.J., and Yaffe M.B. Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the X-ray crystal structures of all human 14-3-3 isoforms. Semin. Cancer Biol. 16 (2006) 173-182
13. Hahn-Windgassen A., Nogueira V., Chen C.C., Skeen J.E., Sonenberg N., and Hay N. Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J. Biol. Chem. 280 (2005) 32081-32089
14. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 8 (2007) 774-785
15. Hemminki A., Markie D., Tomlinson I., Avizienyte E., Roth S., Loukola A., Bignell G., Warren W., Aminoff M., Hoglund P., et al. A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391 (1998) 184-187
16. Hong S.P., and Carlson M. Regulation of snf1 protein kinase in response to environmental stress. J. Biol. Chem. 282 (2007) 16838-16845
17. Hutti J.E., Jarrell E.T., Chang J.D., Abbott D.W., Storz P., Toker A., Cantley L.C., and Turk B.E. A rapid method for determining protein kinase phosphorylation specificity. Nat. Methods 1 (2004) 27-29
18. Hutti J.E., Turk B.E., Asara J.M., Ma A., Cantley L.C., and Abbott D.W. IKK{beta} phosphorylates the K63 deubiquitinase A20 to cause feedback inhibition of the NF{kappa}B pathway. Mol. Cell. Biol. 27 (2007) 7451-7461
19. Inoki K., Zhu T., and Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115 (2003) 577-590
20. Ji H., Ramsey M.R., Hayes D.N., Fan C., McNamara K., Kozlowski P., Torrice C., Wu M.C., Shimamura T., Perera S.A., et al. LKB1 modulates lung cancer differentiation and metastasis. Nature 448 (2007) 807-810
21. Jones R.G., Plas D.R., Kubek S., Buzzai M., Mu J., Xu Y., Birnbaum M.J., and Thompson C.B. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 18 (2005) 283-293
22. Lee C.H., Inoki K., Karbowniczek M., Petroulakis E., Sonenberg N., Henske E.P., and Guan K.L. Constitutive mTOR activation in TSC mutants sensitizes cells to energy starvation and genomic damage via p53. EMBO J. 26 (2007) 4812-4823
23. Lee J.H., Koh H., Kim M., Kim Y., Lee S.Y., Karess R.E., Lee S.H., Shong M., Kim J.M., Kim J., and Chung J. Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 447 (2007) 1017-1020
24. Liu L., Cash T.P., Jones R.G., Keith B., Thompson C.B., and Simon M.C. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 21 (2006) 521-531
25. Mandal S., Guptan P., Owusu-Ansah E., and Banerjee U. Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev. Cell 9 (2005) 843-854
26. Mirouse V., Swick L.L., Kazgan N., St Johnston D., and Brenman J.E. LKB1 and AMPK maintain epithelial cell polarity under energetic stress. J. Cell Biol. 177 (2007) 387-392
27. Moser K., and White F.M. Phosphoproteomic analysis of rat liver by high capacity IMAC and LC-MS/MS. J. Proteome Res. 5 (2006) 98-104
28. Narbonne P., and Roy R. Inhibition of germline proliferation during C. elegans dauer development requires PTEN, LKB1 and AMPK signalling. Development 133 (2006) 611-619
29. Nojima H., Tokunaga C., Eguchi S., Oshiro N., Hidayat S., Yoshino K., Hara K., Tanaka N., Avruch J., and Yonezawa K. The mammalian target of rapamycin (mTOR) partner, raptor, binds the mTOR substrates p70 S6 kinase and 4E-BP1 through their TOR signaling (TOS) motif. J. Biol. Chem. 278 (2003) 15461-15464
30. Rennefahrt U.E., Deacon S.W., Parker S.A., Devarajan K., Beeser A., Chernoff J., Knapp S., Turk B.E., and Peterson J.R. Specificity profiling of Pak kinases allows identification of novel phosphorylation sites. J. Biol. Chem. 282 (2007) 15667-15678
31. Rittinger K., Budman J., Xu J., Volinia S., Cantley L.C., Smerdon S.J., Gamblin S.J., and Yaffe M.B. Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol. Cell 4 (1999) 153-166
32. Sabatini D.M. mTOR and cancer: insights into a complex relationship. Nat. Rev. Cancer 6 (2006) 729-734
33. Sakamoto K., McCarthy A., Smith D., Green K.A., Grahame Hardie D., Ashworth A., and Alessi D.R. Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO J. 24 (2005) 1810-1820
34. Sancak Y., Thoreen C.C., Peterson T.R., Lindquist R.A., Kang S.A., Spooner E., Carr S.A., and Sabatini D.M. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol. Cell 25 (2007) 903-915
35. Sanchez-Cespedes M., Parrella P., Esteller M., Nomoto S., Trink B., Engles J.M., Westra W.H., Herman J.G., and Sidransky D. Inactivation of LKB1/STK11 is a common event in adenocarcinomas of the lung. Cancer Res. 62 (2002) 3659-3662
36. Schalm S.S., Fingar D.C., Sabatini D.M., and Blenis J. TOS motif-mediated raptor binding regulates 4E-BP1 multisite phosphorylation and function. Curr. Biol. 13 (2003) 797-806
37. Schulz T.J., Zarse K., Voigt A., Urban N., Birringer M., and Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6 (2007) 280-293
38. Scott J.W., Norman D.G., Hawley S.A., Kontogiannis L., and Hardie D.G. Protein kinase substrate recognition studied using the recombinant catalytic domain of AMP-activated protein kinase and a model substrate. J. Mol. Biol. 317 (2002) 309-323
39. Shaw R.J., and Cantley L.C. Ras, PI(3)K, and mTOR signaling controls tumor cell growth. Nature 441 (2006) 424-430
40. Shaw R.J., Kosmatka M., Bardeesy N., Hurley R.L., Witters L.A., DePinho R.A., and Cantley L.C. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc. Natl. Acad. Sci. USA 101 (2004) 3329-3335
41. Shaw R.J., Bardeesy N., Manning B.D., Lopez L., Kosmatka M., DePinho R.A., and Cantley L.C. The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell 6 (2004) 91-99
42. Shaw R.J., Lamia K.A., Vasquez D., Koo S.H., Bardeesy N., Depinho R.A., Montminy M., and Cantley L.C. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 310 (2005) 1642-1646
43. Thelander M., Olsson T., and Ronne H. Snf1-related protein kinase 1 is needed for growth in a normal day-night light cycle. EMBO J. 23 (2004) 1900-1910
44. Towler M.C., and Hardie D.G. AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 100 (2007) 328-341
45. Turk B.E., Hutti J.E., and Cantley L.C. Determining protein kinase substrate specificity by parallel solution-phase assay of large numbers of peptide substrates. Nat. Protoc. 1 (2006) 375-379
46. Vander Haar E., Lee S.I., Bandhakavi S., Griffin T.J., and Kim D.H. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 9 (2007) 316-323
47. Villen J., Beausoleil S.A., Gerber S.A., and Gygi S.P. Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. USA 104 (2007) 1488-1493
48. Wilker E.W., Grant R.A., Artim S.C., and Yaffe M.B. A structural basis for 14-3-3sigma functional specificity. J. Biol. Chem. 280 (2005) 18891-18898
49. Wullschleger S., Loewith R., and Hall M.N. TOR signaling in growth and metabolism. Cell 124 (2006) 471-484
50. Yaffe M.B. How do 14-3-3 proteins work?-Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513 (2002) 53-57
51. Yaffe M.B., Rittinger K., Volinia S., Caron P.R., Aitken A., Leffers H., Gamblin S.J., Smerdon S.J., and Cantley L.C. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91 (1997) 961-971
52. Zhang H., Zha X., Tan Y., Hornbeck P.V., Mastrangelo A.J., Alessi D.R., Polakievicz R.D., and Comb M.J. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 277 (2002) 39379-39387