Aerobic glycolysis suppresses p53 activity to provide selective protection from apoptosis upon loss of growth signals or inhibition of BCR-Abl

Cancer Research

Volumn 70, Issue 20, 2010, Pages 8066-8076

  Mason, Emily F ^a   Zhao, Yuxing ^a   Goraksha Hicks, Pankuri ^a   Coloff, Jonathan L ^a   Gannon, Hugh ^b   Jones, Stephen N ^b   Rathmell, Jeffrey C ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; GLUCOSE; PROTEIN KINASE C DELTA; PROTEIN P53; PUMA PROTEIN;

AEROBIC METABOLISM; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL METABOLISM; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; METABOLIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AEROBIOSIS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; CELL CYCLE PROTEINS; CELL DIVISION; CELL SURVIVAL; DNA DAMAGE; FUSION PROTEINS, BCR-ABL; GLYCOLYSIS; HUMANS; LYMPHOCYTE ACTIVATION; NUCLEAR PROTEINS; PLASMIDS; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-MDM2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SRC HOMOLOGY DOMAINS; T-LYMPHOCYTES; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 78049295120     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0608     Document Type: Article

References (47)

1. Raff MC. Social controls on cell survival and cell death. Nature 1992;356:397-400.
2. Rathmell JC, Vander Heiden MG, Harris MH, Frauwirth KA, Thompson CB. In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability. Mol Cell 2000;6:683-92.
3. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
4. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
5. Vander Heiden MG, Plas DR, Rathmell JC, Fox CJ, Harris MH, Thompson CB. Growth factors can influence cell growth and survival through effects on glucose metabolism. Mol Cell Biol 2001;21:5899-912.
6. Ciofani M, Zuniga-Pflucker JC. Notch promotes survival of pre-T cells at the β-selection checkpoint by regulating cellular metabolism. Nat Immunol 2005;6:881-8. (Pubitemid 43090442)
7. Wieman HL, Wofford JA, Rathmell JC. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol Biol Cell 2007;18:1437-46.
8. Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB, Hay N. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 2001;15:1406-18. (Pubitemid 32524647)
9. Barnes K, McIntosh E, Whetton AD, Daley GQ, Bentley J, Baldwin SA. Chronic myeloid leukaemia: an investigation into the role of Bcr-Abl-induced abnormalities in glucose transport regulation. Oncogene 2005;24:3257-67. (Pubitemid 40695107)
10. Gottschalk S, Anderson N, Hainz C, Eckhardt SG, Serkova NJ. Imatinib (STI571)-mediated changes in glucose metabolism in human leukemia BCR-ABL-positive cells. Clin Cancer Res 2004;10:6661-8. (Pubitemid 39346563)
11. Cambier N, Chopra R, Strasser A, Metcalf D, Elefanty AG. BCR-ABL activates pathways mediating cytokine independence and protection against apoptosis in murine hematopoietic cells in a dose-dependent manner. Oncogene 1998;16:335-48. (Pubitemid 28052288)
12. Kruser TJ, Wheeler DL. Mechanisms of resistance to HER family targeting antibodies. Exp Cell Res 2010;316:1083-100.
13. Mauro MJ. Defining and managing imatinib resistance. Hematology Am Soc Hematol Educ Program 2006:219-25.
14. Wendel HG, de Stanchina E, Cepero E, et al. Loss of p53 impedes the antileukemic response to BCR-ABL inhibition. Proc Natl Acad Sci U S A 2006;103:7444-9. (Pubitemid 43727852)
15. Whiteside CI, Dlugosz JA. Mesangial cell protein kinase C isozyme activation in the diabetic milieu. Am J Physiol Renal Physiol 2002; 282:F975-80.
16. Zhao Y, Altman BJ, Coloff JL, et al. Glycogen synthase kinase 3α and 3β mediate a glucose-sensitive antiapoptotic signaling pathway to stabilize Mcl-1. Mol Cell Biol 2007;27:4328-39. (Pubitemid 46906557)
17. Zhao Y, Coloff JL, Ferguson EC, Jacobs SR, Cui K, Rathmell JC. Glucose metabolism attenuates p53 and Puma-dependent cell death upon growth factor deprivation. J Biol Chem 2008;283:36344-53.
18. Rathmell JC, Fox CJ, Plas DR, Hammerman PS, Cinalli RM, Thompson CB. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival. Mol Cell Biol 2003;23:7315-28.
19. Kajino T, Omori E, Ishii S, Matsumoto K, Ninomiya-Tsuji J. TAK1 MAPK kinase kinase mediates transforming growth factor-β signaling by targeting SnoN oncoprotein for degradation. J Biol Chem 2007;282:9475-81. (Pubitemid 47104619)
20. Erlacher M, Labi V, Manzl C, et al. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J Exp Med 2006;203:2939-51. (Pubitemid 46026171)
21. Simonian PL, Grillot DA, Nunez G. Bcl-2 and Bcl-XL can differentially block chemotherapy-induced cell death. Blood 1997;90:1208-16. (Pubitemid 27314158)
22. Karnauskas R, Niu Q, Talapatra S, et al. Bcl-x(L) and Akt cooperate to promote leukemogenesis in vivo. Oncogene 2003;22:688-98. (Pubitemid 36269282)
23. Vousden KH. Outcomes of p53 activation-spoilt for choice. J Cell Sci 2006;119:5015-20.
24. Sluss HK, Armata H, Gallant J, Jones SN. Phosphorylation of serine 18 regulates distinct p53 functions in mice. Mol Cell Biol 2004;24:976-84. (Pubitemid 38112163)
25. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell 2008;133:612-26.
26. Ito A, Lai CH, Zhao X, et al. p300/CBP-mediated p53 acetylation is commonly induced by p53-activating agents and inhibited by MDM2. EMBO J 2001;20:1331-40. (Pubitemid 32233973)
27. Jones RG, Plas DR, Kubek S, et al. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 2005;18:283-93. (Pubitemid 41350534)
28. Romero Rosales K, Peralta ER, Guenther GG, Wong SY, Edinger AL. Rab7 activation by growth factor withdrawal contributes to the induction of apoptosis. Mol Biol Cell 2009;20:2831-40.
29. Lee SJ, Kim DC, Choi BH, Ha H, Kim KT. Regulation of p53 by activated protein kinase C-δ during nitric oxide-induced dopaminergic cell death. J Biol Chem 2006;281:2215-24. (Pubitemid 43845812)
30. 46 phosphorylation of p53 tumor suppressor in the apoptotic response to DNA damage. J Biol Chem 2006;281:5734-40.
31. Calabretta B, Perrotti D. The biology of CML blast crisis. Blood 2004;103:4010-22.
32. Yamamoto K, Yakushijin K, Nishikawa S, et al. Imatinib resistance in a novel translocation der(17)t(1;17)(q25;p13) with loss of TP53 but without BCR/ABL kinase domain mutation in chronic myelogenous leukemia. Cancer Genet Cytogenet 2008;183:77-81.
33. Minowada J, Tsubota T, Greaves MF, Walters TR. A non-T, non-B human leukemia cell line (NALM-1): establishment of the cell line and presence of leukemia-associated antigens. J Natl Cancer Inst 1977;59:83-7. (Pubitemid 8144839)
34. Law JC, Ritke MK, Yalowich JC, Leder GH, Ferrell RE. Mutational inactivation of the p53 gene in the human erythroid leukemic K562 cell line. Leuk Res 1993;17:1045-50.
35. Takeuchi K, Ito F. EGF receptor in relation to tumor development: molecular basis of responsiveness of cancer cells to EGFR-targeting tyrosine kinase inhibitors. FEBS J 2010;277:316-26.
36. + leukemic cells, and resistance due to their loss is overcome by a BH3 mimetic. Proc Natl Acad Sci U S A 2006;103:14907-12.
37. Kruse JP, Gu W. Modes of p53 regulation. Cell 2009;137:609-22.
38. Wu D, Peng F, Zhang B, et al. PKC-β1 mediates glucose-induced Akt activation and TGF-β1 upregulation in mesangial cells. J Am Soc Nephrol 2009;20:554-66.
39. Cosentino F, Eto M, De Paolis P, et al. High glucose causes upregulation of cyclooxygenase-2 and alters prostanoid profile in human endothelial cells: role of protein kinase C and reactive oxygen species. Circulation 2003;107:1017-23. (Pubitemid 36258726)
40. Altman BJ, Wofford JA, Zhao Y, et al. Autophagy provides nutrients but can lead to Chop-dependent induction of Bim to sensitize growth factor-deprived cells to apoptosis. Mol Biol Cell 2009;20:1180-91.
41. You H, Pellegrini M, Tsuchihara K, et al. FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J Exp Med 2006;203:1657-63. (Pubitemid 44036270)
42. de Lavallade H, Apperley JF, Khorashad JS, et al. Imatinib for newly diagnosed patients with chronic myeloid leukemia: incidence of sustained responses in an intention-to-treat analysis. J Clin Oncol 2008;26:3358-63.
43. Druker BJ, Guilhot F, O'Brien SG, et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 2006;355:2408-17. (Pubitemid 44903745)
44. Gorre ME, Mohammed M, Ellwood K, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001;293:876-80. (Pubitemid 32743979)
45. de Lavallade H, Finetti P, Carbuccia N, et al. A gene expression signature of primary resistance to imatinib in chronic myeloid leukemia. Leuk Res 2009;34:254-7.
46. Soverini S, Colarossi S, Gnani A, et al. Contribution of ABL kinase domain mutations to imatinib resistance in different subsets of Philadelphia-positive patients: by the GIMEMA Working Party on Chronic Myeloid Leukemia. Clin Cancer Res 2006;12:7374-9. (Pubitemid 46095411)
47. Kominsky DJ, Klawitter J, Brown JL, et al. Abnormalities in glucose uptake and metabolism in imatinib-resistant human BCR-ABL-positive cells. Clin Cancer Res 2009;15:3442-50.