AMPK-Dependent Phosphorylation of GAPDH Triggers Sirt1 Activation and Is Necessary for Autophagy upon Glucose Starvation

Molecular Cell

Volumn 60, Issue 6, 2015, Pages 930-940

  Chang, Chunmei ^a   Su, Hua ^a   Zhang, Danhong ^a   Wang, Yusha ^a   Shen, Qiuhong ^a   Liu, Bo ^a   Huang, Rui ^a   Zhou, Tianhua ^a   Peng, Chao ^b   Wong, Catherine C L ^b   Shen, Han Ming ^c   Lippincott Schwartz, Jennifer ^d   Liu, Wei ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENYLATE KINASE; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; SIRTUIN 1; DBC1 PROTEIN, HUMAN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; SERINE; SIRT1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; AUTOPHAGY; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; MICROSCOPY; PROTEIN LOCALIZATION; TANDEM MASS SPECTROMETRY; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CHEMISTRY; CYTOLOGY; DEFICIENCY; EMBRYONIC STEM CELL; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; PHOSPHORYLATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; CELL NUCLEUS; EMBRYONIC STEM CELLS; GLUCOSE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEK293 CELLS; HUMANS; MICE; PHOSPHORYLATION; SERINE; SIRTUIN 1; TUMOR SUPPRESSOR PROTEINS;

EID: 84953638824     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.10.037     Document Type: Article

References (54)

1. Azam S., Jouvet N., Jilani A., Vongsamphanh R., Yang X., Yang S., Ramotar D. Human glyceraldehyde-3-phosphate dehydrogenase plays a direct role in reactivating oxidized forms of the DNA repair enzyme APE1. J. Biol. Chem. 2008, 283:30632-30641.
2. Baba T., Kobayashi H., Kawasaki H., Mineki R., Naito H., Ohmori D. Glyceraldehyde-3-phosphate dehydrogenase interacts with phosphorylated Akt resulting from increased blood glucose in rat cardiac muscle. FEBS Lett. 2010, 584:2796-2800.
3. 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.
4. Cantó C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., Elliott P.J., Puigserver P., Auwerx J. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
5. Chuang D.M., Ishitani R. A role for GAPDH in apoptosis and neurodegeneration. Nat. Med. 1996, 2:609-610.
6. Colell A., Ricci J.E., Tait S., Milasta S., Maurer U., Bouchier-Hayes L., Fitzgerald P., Guio-Carrion A., Waterhouse N.J., Li C.W., et al. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell 2007, 129:983-997.
7. Dastoor Z., Dreyer J.L. Potential role of nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase in apoptosis and oxidative stress. J. Cell Sci. 2001, 114:1643-1653.
8. Finkel T., Deng C.X., Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 2009, 460:587-591.
9. Fulco M., Cen Y., Zhao P., Hoffman E.P., McBurney M.W., Sauve A.A., Sartorelli V. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev. Cell 2008, 14:661-673.
10. Geng J., Klionsky D.J. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep. 2008, 9:859-864.
11. Gerhart-Hines Z., Dominy J.E., Blättler S.M., Jedrychowski M.P., Banks A.S., Lim J.H., Chim H., Gygi S.P., Puigserver P. The cAMP/PKA pathway rapidly activates SIRT1 to promote fatty acid oxidation independently of changes in NAD(+). Mol. Cell 2011, 44:851-863.
12. Guo Y., Chang C., Huang R., Liu B., Bao L., Liu W. AP1 is essential for generation of autophagosomes from the trans-Golgi network. J. Cell Sci. 2012, 125:1706-1715.
13. 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.
14. Hara M.R., Snyder S.H. Nitric oxide-GAPDH-Siah: a novel cell death cascade. Cell. Mol. Neurobiol. 2006, 26:527-538.
15. Hara M.R., Agrawal N., Kim S.F., Cascio M.B., Fujimuro M., Ozeki Y., Takahashi M., Cheah J.H., Tankou S.K., Hester L.D., et al. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 2005, 7:665-674.
16. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 2007, 8:774-785.
17. Hariharan N., Maejima Y., Nakae J., Paik J., Depinho R.A., Sadoshima J. Deacetylation of FoxO by Sirt1 plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ. Res. 2010, 107:1470-1482.
18. Hariharan N., Zhai P., Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid. Redox Signal. 2011, 14:2179-2190.
19. Hasmann M., Schemainda I. FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyltransferase, represents a novel mechanism for induction of tumor cell apoptosis. Cancer Res. 2003, 63:7436-7442.
20. Huang R., Xu Y., Wan W., Shou X., Qian J., You Z., Liu B., Chang C., Zhou T., Lippincott-Schwartz J., Liu W. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol. Cell 2015, 57:456-466.
21. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
22. Jeong J.K., Moon M.H., Lee Y.J., Seol J.W., Park S.Y. Autophagy induced by the class III histone deacetylase Sirt1 prevents prion peptide neurotoxicity. Neurobiol. Aging 2013, 34:146-156.
23. Kim E.J., Kho J.H., Kang M.R., Um S.J. Active regulator of SIRT1 cooperates with SIRT1 and facilitates suppression of p53 activity. Mol. Cell 2007, 28:277-290.
24. Kim J.E., Chen J., Lou Z. DBC1 is a negative regulator of SIRT1. Nature 2008, 451:583-586.
25. Kim J., Kim Y.C., Fang C., Russell R.C., Kim J.H., Fan W., Liu R., Zhong Q., Guan K.L. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 2013, 152:290-303.
26. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
27. Kornberg M.D., Sen N., Hara M.R., Juluri K.R., Nguyen J.V., Snowman A.M., Law L., Hester L.D., Snyder S.H. GAPDH mediates nitrosylation of nuclear proteins. Nat. Cell Biol. 2010, 12:1094-1100.
28. Kume S., Uzu T., Horiike K., Chin-Kanasaki M., Isshiki K., Araki S., Sugimoto T., Haneda M., Kashiwagi A., Koya D. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 2010, 120:1043-1055.
29. Kusner L.L., Sarthy V.P., Mohr S. Nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase: a role in high glucose-induced apoptosis in retinal Müller cells. Invest. Ophthalmol. Vis. Sci. 2004, 45:1553-1561.
30. Kwon H.J., Rhim J.H., Jang I.S., Kim G.E., Park S.C., Yeo E.J. Activation of AMP-activated protein kinase stimulates the nuclear localization of glyceraldehyde 3-phosphate dehydrogenase in human diploid fibroblasts. Exp. Mol. Med. 2010, 42:254-269.
31. Lee I.H., Finkel T. Regulation of autophagy by the p300 acetyltransferase. J. Biol. Chem. 2009, 284:6322-6328.
32. Lee I.H., Cao L., Mostoslavsky R., Lombard D.B., Liu J., Bruns N.E., Tsokos M., Alt F.W., Finkel T. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl. Acad. Sci. USA 2008, 105:3374-3379.
33. Lee M.N., Ha S.H., Kim J., Koh A., Lee C.S., Kim J.H., Jeon H., Kim D.H., Suh P.G., Ryu S.H. Glycolytic flux signals to mTOR through glyceraldehyde-3-phosphate dehydrogenase-mediated regulation of Rheb. Mol. Cell. Biol. 2009, 29:3991-4001.
34. Li C., Feng J.J., Wu Y.P., Zhang G.Y. Cerebral ischemia-reperfusion induces GAPDH S-nitrosylation and nuclear translocation. Biochemistry (Mosc.) 2012, 77:671-678.
35. Lin S.Y., Li T.Y., Liu Q., Zhang C., Li X., Chen Y., Zhang S.M., Lian G., Liu Q., Ruan K., et al. GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy. Science 2012, 336:477-481.
36. Marsin A.S., Bertrand L., Rider M.H., Deprez J., Beauloye C., Vincent M.F., Van den Berghe G., Carling D., Hue L. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 2000, 10:1247-1255.
37. Mizushima N., Klionsky D.J. Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 2007, 27:19-40.
38. Mizushima N., Yoshimori T., Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2011, 27:107-132.
39. Nagy E., Henics T., Eckert M., Miseta A., Lightowlers R.N., Kellermayer M. Identification of the NAD(+)-binding fold of glyceraldehyde-3-phosphate dehydrogenase as a novel RNA-binding domain. Biochem. Biophys. Res. Commun. 2000, 275:253-260.
40. Nasrin N., Kaushik V.K., Fortier E., Wall D., Pearson K.J., de Cabo R., Bordone L. JNK1 phosphorylates SIRT1 and promotes its enzymatic activity. PLoS ONE 2009, 4:e8414.
41. Nin V., Escande C., Chini C.C., Giri S., Camacho-Pereira J., Matalonga J., Lou Z., Chini E.N. Role of deleted in breast cancer 1 (DBC1) protein in SIRT1 deacetylase activation induced by protein kinase A and AMP-activated protein kinase. J. Biol. Chem. 2012, 287:23489-23501.
42. Ortiz-Ortiz M.A., Morán J.M., Ruiz-Mesa L.M., Bravo-San Pedro J.M., Fuentes J.M. Paraquat exposure induces nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and the activation of the nitric oxide-GAPDH-Siah cell death cascade. Toxicol. Sci. 2010, 116:614-622.
43. Powell M.J., Casimiro M.C., Cordon-Cardo C., He X., Yeow W.S., Wang C., McCue P.A., McBurney M.W., Pestell R.G. Disruption of a Sirt1-dependent autophagy checkpoint in the prostate results in prostatic intraepithelial neoplasia lesion formation. Cancer Res. 2011, 71:964-975.
44. Revollo J.R., Grimm A.A., Imai S. The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J. Biol. Chem. 2004, 279:50754-50763.
45. Sawa A., Khan A.A., Hester L.D., Snyder S.H. Glyceraldehyde-3-phosphate dehydrogenase: nuclear translocation participates in neuronal and nonneuronal cell death. Proc. Natl. Acad. Sci. USA 1997, 94:11669-11674.
46. Schmitz H.D. Reversible nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase upon serum depletion. Eur. J. Cell Biol. 2001, 80:419-427.
47. Sen N., Hara M.R., Kornberg M.D., Cascio M.B., Bae B.I., Shahani N., Thomas B., Dawson T.M., Dawson V.L., Snyder S.H., Sawa A. Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol. 2008, 10:866-873.
48. Sun Q., Gao W., Loughran P., Shapiro R., Fan J., Billiar T.R., Scott M.J. Caspase 1 activation is protective against hepatocyte cell death by up-regulating beclin 1 protein and mitochondrial autophagy in the setting of redox stress. J. Biol. Chem. 2013, 288:15947-15958.
49. Tristan C., Shahani N., Sedlak T.W., Sawa A. The diverse functions of GAPDH: views from different subcellular compartments. Cell. Signal. 2011, 23:317-323.
50. Yang Y., Fu W., Chen J., Olashaw N., Zhang X., Nicosia S.V., Bhalla K., Bai W. SIRT1 sumoylation regulates its deacetylase activity and cellular response to genotoxic stress. Nat. Cell Biol. 2007, 9:1253-1262.
51. Yi C., Ma M., Ran L., Zheng J., Tong J., Zhu J., Ma C., Sun Y., Zhang S., Feng W., et al. Function and molecular mechanism of acetylation in autophagy regulation. Science 2012, 336:474-477.
52. Ylä-Anttila P., Vihinen H., Jokitalo E., Eskelinen E.L. Monitoring autophagy by electron microscopy in Mammalian cells. Methods Enzymol. 2009, 452:143-164.
53. Zhao W., Kruse J.P., Tang Y., Jung S.Y., Qin J., Gu W. Negative regulation of the deacetylase SIRT1 by DBC1. Nature 2008, 451:587-590.
54. Zheng L., Roeder R.G., Luo Y. S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 2003, 114:255-266.