Glycogen synthase kinase-3 (GSK3) controls deoxyglucose-induced mitochondrial biogenesis in human neuroblastoma SH-SY5Y cells

Mitochondrion

Volumn 14, Issue 1, 2014, Pages 54-63

  Ngamsiri, Pronrumpa ^a,b   Watcharasit, Piyajit ^a,b,c   Satayavivad, Jutamaad ^a,b,c  

^a Chulabhorn Research Institute   (Thailand)

^b Research and Innovation   (Thailand)

^c Center of Excellence on Environmental Health and Toxicology (EHT) Office of the Higher Education Commission   (Thailand)

Author keywords

2 Deoxyglucose; Glycogen synthase kinase 3; Mitochondrial biogenesis

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; DEOXYGLUCOSE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; MITOCHONDRIAL PROTEIN; VOLTAGE DEPENDENT ANION CHANNEL;

ARTICLE; BIOGENESIS; BRAIN MITOCHONDRION; CANCER CELL CULTURE; COXII GENE; GLYCOLYSIS; HUMAN; HUMAN CELL; MITOCHONDRIAL GENE; NEUROBLASTOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; VDAC GENE; WILD TYPE;

2-DEOXYGLUCOSE; 2-DG; AMP-ACTIVATED PROTEIN KINASE; AMPK; GAPDH; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; GLYCOGEN SYNTHASE KINASE-3; GLYCOGEN SYNTHASE KINASE-3 (Α/Β); GLYCOGEN SYNTHASE KINASE-3Β-KINASE DEAD; GSK3; GSK3Β-KD; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL CYTOCHROME B; MITOCHONDRIAL CYTOCHROME C OXIDASE SUBUNIT II; MITOCHONDRIAL CYTOCHROME C OXIDASE SUBUNIT III; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MTCOXII; MTCOXIII; MTCYTB; NRF-1; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1Α; PGC-1Α; TFAM; THYMIDINE KINASE 2; TK2; VDAC; VOLTAGE-DEPENDENT ANION-SELECTIVE CHANNEL; WILD-TYPE-GLYCOGEN SYNTHASE KINASE-3Β; WT-GSK3Β;

CELL LINE, TUMOR; DEOXYGLUCOSE; ENZYME INHIBITORS; GENE EXPRESSION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INDOLES; MALEIMIDES; MITOCHONDRIAL TURNOVER; NEURONS;

EID: 84893016900     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2013.11.003     Document Type: Article

References (47)

1. Anderson R.M., Barger J.L., Edwards M.G., Braun K.H., O'Connor C.E., Prolla T.A., Weindruch R. Dynamic regulation of PGC-1alpha localization and turnover implicates mitochondrial adaptation in calorie restriction and the stress response. Aging Cell 2008, 7:101-111.
2. Bergeron R., Ren J.M., Cadman K.S., Moore I.K., Perret P., Pypaert M., Young L.H., Semenkovich C.F., Shulman G.I. Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am. J. Physiol. Endocrinol. Metab. 2001, 281:E1340-E1346.
3. Bullock B.P., Habener J.F. Phosphorylation of the cAMP response element binding protein CREB by cAMP-dependent protein kinase A and glycogen synthase kinase-3 alters DNA-binding affinity, conformation, and increases net charge. Biochemistry 1998, 37:3795-3809.
4. Campbell C.T., Kolesar J.E., Kaufman B.A. Mitochondrial transcription factor A regulates mitochondrial transcription initiation, DNA packaging, and genome copy number. Biochim. Biophys. Acta 2012, 1819:921-929.
5. Chiara F., Rasola A. GSK-3 and mitochondria in cancer cells. Front. Oncol. 2013, 3:16.
6. Coghlan M.P., Culbert A.A., Cross D.A., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Murphy G.J., Carter P.S., Roxbee Cox L., Mills D., Brown M.J., Haigh D., Ward R.W., Smith D.G., Murray K.J., Reith A.D., Holder J.C. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol. 2000, 7:793-803.
7. Cole A.R. GSK3 as a sensor determining cell fate in the Brain. Front. Mol. Neurosci. 2012, 5:4.
8. de Lange P., Moreno M., Silvestri E., Lombardi A., Goglia F., Lanni A. Fuel economy in food-deprived skeletal muscle: signaling pathways and regulatory mechanisms. FASEB J. 2007, 21:3431-3441.
9. Dhar S.S., Ongwijitwat S., Wong-Riley M.T. Nuclear respiratory factor 1 regulates all ten nuclear-encoded subunits of cytochrome c oxidase in neurons. J. Biol. Chem. 2008, 283:3120-3129.
10. Dreyfus M., Regnier P. The poly(A) tail of mRNAs: bodyguard in eukaryotes, scavenger in bacteria. Cell 2002, 111:611-613.
11. Embi N., Rylatt D.B., Cohen P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 1980, 107:519-527.
12. Evans M.J., Scarpulla R.C. Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. Characterization of upstream NRF-1, ATF, and intron Sp1 recognition sequences. J. Biol. Chem. 1989, 264:14361-14368.
13. Fujimura R.K., Reiner T., Ma F., Phillips V., de las Pozas A., Dickson D.W., Roos B.A., Howard G.A., Perez-Stable C. Changes in the expression of genes associated with intraneuronal amyloid-beta and tau in Alzheimer's disease. J Alzheimers Dis 2010, 19:97-109.
14. Gegg M.E., Cooper J.M., Schapira A.H., Taanman J.W. Silencing of PINK1 expression affects mitochondrial DNA and oxidative phosphorylation in dopaminergic cells. PLoS One 2009, 4:e4756.
15. Granot Z., Kobiler O., Melamed-Book N., Eimerl S., Bahat A., Lu B., Braun S., Maurizi M.R., Suzuki C.K., Oppenheim A.B., Orly J. Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors. Mol. Endocrinol. 2007, 21:2164-2177.
16. Grimes C.A., Jope R.S. CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium. J. Neurochem. 2001, 78:1219-1232.
17. Hoshi M., Takashima A., Noguchi K., Murayama M., Sato M., Kondo S., Saitoh Y., Ishiguro K., Hoshino T., Imahori K. Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:2719-2723.
18. Hughes K., Ramakrishna S., Benjamin W.B., Woodgett J.R. Identification of multifunctional ATP-citrate lyase kinase as the alpha-isoform of glycogen synthase kinase-3. Biochem. J. 1992, 288(Pt 1):309-314.
19. Jope R.S., Johnson G.V. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 2004, 29:95-102.
20. Joseph A.M., Joanisse D.R., Baillot R.G., Hood D.A. Mitochondrial dysregulation in the pathogenesis of diabetes: potential for mitochondrial biogenesis-mediated interventions. Exp. Diabetes Res. 2012, 2012:642038.
21. Juhaszova M., Zorov D.B., Kim S.H., Pepe S., Fu Q., Fishbein K.W., Ziman B.D., Wang S., Ytrehus K., Antos C.L., Olson E.N., Sollott S.J. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest. 2004, 113:1535-1549.
22. Karamanlidis G., Nascimben L., Couper G.S., Shekar P.S., del Monte F., Tian R. Defective DNA replication impairs mitochondrial biogenesis in human failing hearts. Circ Res 2010, 106:1541-1548.
23. Karczmar G.S., Arbeit J.M., Toy B.J., Speder A., Weiner M.W. Selective depletion of tumor ATP by 2-deoxyglucose and insulin, detected by 31P magnetic resonance spectroscopy. Cancer Res. 1992, 52:71-76.
24. King T.D., Song L., Jope R.S. AMP-activated protein kinase (AMPK) activating agents cause dephosphorylation of Akt and glycogen synthase kinase-3. Biochem. Pharmacol. 2006, 71:1637-1647.
25. King T.D., Clodfelder-Miller B., Barksdale K.A., Bijur G.N. Unregulated mitochondrial GSK3beta activity results in NADH: ubiquinone oxidoreductase deficiency. Neurotox. Res. 2008, 14:367-382.
26. Laderoute K.R., Amin K., Calaoagan J.M., Knapp M., Le T., Orduna J., Foretz M., Viollet B. 5'-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol. Cell. Biol. 2006, 26:5336-5347.
27. Lee D.Y., Clayton D.A. Initiation of mitochondrial DNA replication by transcription and R-loop processing. J. Biol. Chem. 1998, 273:30614-30621.
28. Lopez-Lluch G., Irusta P.M., Navas P., de Cabo R. Mitochondrial biogenesis and healthy aging. Exp. Gerontol. 2008, 43:813-819.
29. McComb R.B., Yushok W.D. Metabolism of ascites tumor cells. III. Effect of 2-deoxyglucose phosphorylation on phosphorus metabolism. Cancer Res. 1964, 24:193-197.
30. Nagaike T., Suzuki T., Katoh T., Ueda T. Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochondria-specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem. 2005, 280:19721-19727.
31. Nikoletopoulou V., Tavernarakis N. Mitochondrial biogenesis and dynamics in neurodegeneration: a causative relationship. Neurochem. Res. 2013, 10.1007/s11064-013-0997-0.
32. Olson B.L., Hock M.B., Ekholm-Reed S., Wohlschlegel J.A., Dev K.K., Kralli A., Reed S.I. SCFCdc4 acts antagonistically to the PGC-1alpha transcriptional coactivator by targeting it for ubiquitin-mediated proteolysis. Genes Dev. 2008, 22:252-264.
33. Patti M.E., Corvera S. The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr. Rev. 2010, 31:364-395.
34. Piantadosi C.A., Carraway M.S., Babiker A., Suliman H.B. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ. Res. 2008, 103:1232-1240.
35. Premkumar A., Simantov R. Mitochondrial voltage-dependent anion channel is involved in dopamine-induced apoptosis. J Neurochem 2002, 82:345-352.
36. Salt I.P., Johnson G., Ashcroft S.J., Hardie D.G. AMP-activated protein kinase is activated by low glucose in cell lines derived from pancreatic beta cells, and may regulate insulin release. Biochem. J. 1998, 335(Pt 3):533-539.
37. Scarpulla R.C. Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann. N. Y. Acad. Sci. 2008, 1147:321-334.
38. Slomovic S., Portnoy V., Yehudai-Resheff S., Bronshtein E., Schuster G. Polynucleotide phosphorylase and the archaeal exosome as poly(A)-polymerases. Biochim. Biophys. Acta 2008, 1779:247-255.
39. Struewing I.T., Barnett C.D., Tang T., Mao C.D. Lithium increases PGC-1alpha expression and mitochondrial biogenesis in primary bovine aortic endothelial cells. FEBS J. 2007, 274:2749-2765.
40. 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.
41. Vadrot N., Ghanem S., Braut F., Gavrilescu L., Pilard N., Mansouri A., Moreau R., Reyl-Desmars F. Mitochondrial DNA maintenance is regulated in human hepatoma cells by glycogen synthase kinase 3beta and p53 in response to tumor necrosis factor alpha. PLoS One 2012, 7:e40879.
42. Valerio A., Bertolotti P., Delbarba A., Perego C., Dossena M., Ragni M., Spano P., Carruba M.O., De Simoni M.G., Nisoli E. Glycogen synthase kinase-3 inhibition reduces ischemic cerebral damage, restores impaired mitochondrial biogenesis and prevents ROS production. J. Neurochem. 2011, 116:1148-1159.
43. Watcharasit P., Visitnonthachai D., Suntararuks S., Thiantanawat A., Satayavivad J. Low arsenite concentrations induce cell proliferation via activation of VEGF signaling in human neuroblastoma SH-SY5Y cells. Environ Toxicol Pharmacol 2012, 33:53-59.
44. Weber K., Ridderskamp D., Alfert M., Hoyer S., Wiesner R.J. Cultivation in glucose-deprived medium stimulates mitochondrial biogenesis and oxidative metabolism in HepG2 hepatoma cells. Biol. Chem. 2002, 383:283-290.
45. Zhu Z., Jiang W., McGinley J.N., Thompson H.J. 2-Deoxyglucose as an energy restriction mimetic agent: effects on mammary carcinogenesis and on mammary tumor cell growth in vitro. Cancer Res. 2005, 65:7023-7030.
46. Zhu L., Wang Q., Zhang L., Fang Z., Zhao F., Lv Z., Gu Z., Zhang J., Wang J., Zen K., Xiang Y., Wang D., Zhang C.Y. Hypoxia induces PGC-1alpha expression and mitochondrial biogenesis in the myocardium of TOF patients. Cell Res. 2010, 20:676-687.
47. Zong H., Ren J.M., Young L.H., Pypaert M., Mu J., Birnbaum M.J., Shulman G.I. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15983-15987.