Inhibition of AMPK and krebs cycle gene expression drives metabolic remodeling of Pten-deficient preneoplastic thyroid cells

Cancer Research

Volumn 73, Issue 17, 2013, Pages 5459-5472

  Antico Arciuch, Valeria G ^a   Russo, Marika A ^a   Kang, Kristy S ^a   Di Cristofano, Antonio ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL RESPIRATION; CITRIC ACID CYCLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; FLOW CYTOMETRY; GENE EXPRESSION; GLYCOLYSIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRECANCER; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; THYMUS HYPERPLASIA; THYROID CELL; THYROID FOLLICULAR CARCINOMA; THYROID GLAND; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CELL RESPIRATION; CELLS, CULTURED; CITRIC ACID CYCLE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME INHIBITORS; FLOW CYTOMETRY; GLYCOLYSIS; IMMUNOPRECIPITATION; LACTATES; LUCIFERASES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHOSPHATIDYLINOSITOL 3-KINASES; PRECANCEROUS CONDITIONS; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; THYROID GLAND; THYROID NEOPLASMS;

EID: 84883486720     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1429     Document Type: Article

References (52)

1. Fritz V, Fajas L. Metabolism and proliferation share common regulatory pathways in cancer cells. Oncogene 2010;29:4369-77.
2. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
3. Ortega AD, Sanchez-Arago M, Giner-Sanchez D, Sanchez-Cenizo L, Willers I, Cuezva JM. Glucose avidity of carcinomas. Cancer Lett 2009;276:125-35.
4. Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, Plas DR, et al. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 2004;64:3892-9. (Pubitemid 38697301)
5. Levine AJ, Puzio-Kuter AM. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 2010;330:1340-4.
6. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell 2010;39:171-83.
7. Qing G, Skuli N, Mayes PA, Pawel B, Martinez D, Maris JM, et al. Combinatorial regulation of neuroblastoma tumor progression by NMyc and hypoxia inducible factor HIF-1alpha. Cancer Res 2010;70:10351-61.
8. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat Rev Cancer 2011;11:325-37.
9. Israel M, Schwartz L. The metabolic advantage of tumor cells. Mol Cancer 2011;10:70.
10. Raimundo N, Baysal BE, Shadel GS. Revisiting the TCA cycle: signaling to tumor formation. Trends Mol Med 2011;17:641-9.
11. Yeager N, Klein-Szanto A, Kimura S, Di Cristofano A. Pten loss in the mouse thyroid causes goiter and follicular adenomas: insights into thyroid function and Cowden disease pathogenesis. Cancer Res 2007;67:959-66.
12. Antico-Arciuch VG, Dima M, Liao XH, Refetoff S, Di Cristofano A. Cross-talk between PI3K and estrogen in the mouse thyroid predisposes to the development of follicular carcinomas with a higher incidence in females. Oncogene 2010;29:5678-86.
13. Miller KA, Yeager N, Baker K, Liao XH, Refetoff S, Di Cristofano A. Oncogenic Kras requires simultaneous PI3K signaling to induce ERK activation and transform thyroid epithelial cells in vivo. Cancer Res 2009;69:3689-94.
14. Antico Arciuch VG, Russo M, Dima M, Kang KS, Dasrath F, Liao XH, et al. Thyrocyte-specific inactivation of p53 and Pten results in anaplastic thyroid carcinomas faithfully recapitulating human tumors. Oncotarget 2011;2:1109-26.
15. Lawlor MA, Mora A, Ashby PR, Williams MR, Murray-Tait V, Malone L, et al. Essential role of PDK1 in regulating cell size and development in mice. EMBO J 2002;21:3728-38. (Pubitemid 34787046)
16. Patel BB, Li XM, Dixon MP, Blagoi EL, Seeholzer SH, Chen Y, et al. Searchable high-resolution 2D gel proteome of the human colon crypt. J Proteome Res 2007;6:2232-8. (Pubitemid 46985110)
17. Ke E, Patel BB, Liu T, Li XM, Haluszka O, Hoffman JP, et al. Proteomic analyses of pancreatic cyst fluids. Pancreas 2009;38:e33-42.
18. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 2008;118:789-800. (Pubitemid 351206566)
19. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev 2011;11:85-95.
20. Pearce LR, Komander D, Alessi DR. The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 2010;11:9-22.
21. Bayascas JR, Sakamoto K, Armit L, Arthur JS, Alessi DR. Evaluation of approaches to generation of tissue-specific knock-in mice. J Biol Chem 2006;281:28772-81. (Pubitemid 44507020)
22. Yeager N, Brewer C, Cai KQ, Xu XX, Di Cristofano A. Mammalian target of rapamycin is the key effector of phosphatidylinositol-3-OH-initiated proliferative signals in the thyroid follicular epithelium. Cancer Res 2008;68:444-9. (Pubitemid 351380070)
23. Sun Q, Chen X, Ma J, Peng H, Wang F, Zha X, et al. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proc Natl Acad Sci U S A 2011;108:4129-34.
24. Narkar VA, Fan W, Downes M, Yu RT, Jonker JW, Alaynick WA, et al. Exercise and PGC-1alpha-independent synchronization of type I muscle metabolism and vasculature by ERRgamma. Cell Metab 2011;13:283-93.
25. Jager S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 2007;104:12017-22. (Pubitemid 47185622)
26. Giguere V. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev 2008;29:677-96.
27. Mankouri J, Tedbury PR, Gretton S, Hughes ME, Griffin SD, Dallas ML, et al. Enhanced hepatitis C virus genome replication and lipid accumulation mediated by inhibition of AMP-activated protein kinase. Proc Natl Acad Sci U S A 2010;107:11549-54.
28. Horman S, Vertommen D, Heath R, Neumann D, Mouton V, Woods A, 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;281:5335-40. (Pubitemid 43847626)
29. Hurley RL, Barre LK, Wood SD, Anderson KA, Kemp BE, Means AR, et al. Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J Biol Chem 2006;281:36662-72. (Pubitemid 46042133)
30. Djouder N, Tuerk RD, Suter M, Salvioni P, Thali RF, Scholz R, et al. PKA phosphorylates and inactivates AMPKalpha to promote efficient lipolysis. EMBO J 2010;29:469-81.
31. Robey RB, Hay N. Is Akt the "Warburg kinase"?-Akt-energy metabolism interactions and oncogenesis. Semin Cancer Biol 2009;19:25-31.
32. Kim JW, Gao P, Liu YC, Semenza GL, Dang CV. Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol Cell Biol 2007;27:7381-93. (Pubitemid 350033646)
33. Deprez J, Vertommen D, Alessi DR, Hue L, Rider MH. Phosphorylation and activation of heart 6-phosphofructo-2-kinase by protein kinase B and other protein kinases of the insulin signaling cascades. J Biol Chem 1997;272:17269-75. (Pubitemid 27311150)
34. Barthel A, Okino ST, Liao J, Nakatani K, Li J, Whitlock JP Jr, et al. Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1. J Biol Chem 1999;274:20281-6.
35. Zha X, Wang F, Wang Y, He S, Jing Y, Wu X, et al. Lactate dehydrogenase B is critical for hyperactive mTOR-mediated tumorigenesis. Cancer Res 2011;71:13-8.
36. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, et al.Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 1996;271:32529-37.
37. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 2011;27:441-64.
38. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 2011;35:871-82.
39. Morani F, Pagano L, Prodam F, Aimaretti G, Isidoro C. Loss of expression of the oncosuppressor PTEN in thyroid incidentalomas associates with GLUT1 plasmamembrane expression. Panminerva Med 2012;54:59-63.
40. Garcia-Cao I, Song MS, Hobbs RM, Laurent G, Giorgi C, de Boer VC, et al. Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell 2012;149:49-62.
41. Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 2011;13:1016-23.
42. Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012;13:251-62.
43. Ning J, Xi G, Clemmons DR. Suppression of AMPK activation via S485 phosphorylation by IGF-I during hyperglycemia is mediated by AKT activation in vascular smooth muscle cells. Endocrinology 2011;152:3143-54.
44. Dagon Y, Hur E, Zheng B, Wellenstein K, Cantley LC, Kahn BB. p70S6 kinase phosphorylates AMPK on serine 491 to mediate leptin's effect on food intake. Cell Metab 2012;16:104-12.
45. Faubert B, Boily G, Izreig S, Griss T, Samborska B, Dong Z, et al. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell Metab 2013;17:113-24.
46. Alaynick WA, Kondo RP, Xie W, He W, Dufour CR, Downes M, et al. ERRgamma directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab 2007;6:13-24. (Pubitemid 46995781)
47. Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta 2011;1813:1269-78.
48. Eichner LJ, Perry MC, Dufour CR, Bertos N, Park M, St-Pierre J, et al. miR-378(*) mediates metabolic shift in breast cancer cells via the PGC-1beta/ERRgamma transcriptional pathway. Cell Metab 2010;12: 352-61.
49. Hobert JA, Mester JL, Moline J, Eng C. Elevated plasma succinate in PTEN, SDHB, and SDHD mutation-positive individuals. Genet Med 2012;14:616-9.
50. Mutter GL, Lin MC, Fitzgerald JT, Kum JB, Baak JP, Lees JA, et al. Altered PTEN expression as a diagnostic marker for the earliest endometrial precancers. J Natl Cancer Inst 2000;92:924-30.
51. Hong Y, Downey T, Eu KW, Koh PK, Cheah PY. A 'metastasis-prone' signature for early-stage mismatch-repair proficient sporadic colorectal cancer patients and its implications for possible therapeutics. Clin Exp Metastasis 2010;27:83-90.
52. Cai Z, Zhao JS, Li JJ, Peng DN, Wang XY, Chen TL, et al. A combined proteomics and metabolomics profiling of gastric cardia cancer reveals characteristic dysregulations in glucose metabolism. Mol Cell Proteomics 2010;9:2617-28.