Glucose deprivation activates a metabolic and signaling amplification loop leading to cell death

Molecular Systems Biology

Volumn 8, Issue , 2012, Pages

  Graham, Nicholas A ^a,b   Tahmasian, Martik ^a,b   Kohli, Bitika ^a,b   Komisopoulou, Evangelia ^a,b   Zhu, Maggie ^a,b   Vivanco, Igor ^c   Teitell, Michael A ^a,b   Wu, Hong ^a,b   Ribas, Antoni ^a,b   Lo, Roger S ^a,b   Mellinghoff, Ingo K ^c,d   Mischel, Paul S ^b   Graeber, Thomas G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

cancer; metabolism; phosphatase; proteomics; reactive oxygen species

Indexed keywords

GLUCOSE; PHOSPHOTYROSINE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PTEN PROTEIN, MOUSE;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL DEATH; CELL METABOLISM; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; FEEDBACK SYSTEM; FOCAL ADHESION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MITOCHONDRION; MOLECULAR INTERACTION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

CELL DEATH; CELL LINE, TUMOR; FEEDBACK, PHYSIOLOGICAL; FOCAL ADHESIONS; GLUCOSE; HUMANS; MASS SPECTROMETRY; MITOCHONDRIA; MODELS, BIOLOGICAL; NADPH OXIDASE; NEOPLASMS; PHOSPHOTYROSINE; PROTEIN TYROSINE PHOSPHATASES; PROTEIN-TYROSINE KINASES; PTEN PHOSPHOHYDROLASE; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84863337299     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2012.20     Document Type: Article

References (63)

1. Ahmad IM, Aykin-Burns N, Sim JE,Walsh SA, Higashikubo R, Buettner GR, Venkataraman S, Mackey MA, Flanagan SW, Oberley LW, Spitz DR (2005) Mitochondrial O2*-and H2O2 mediate glucose deprivation-induced stress in human cancer cells. J Biol Chem 280: 4254-4263
2. Andringa KK, Coleman MC, Aykin-Burns N, Hitchler MJ, Walsh SA, Domann FE, Spitz DR (2006) Inhibition of glutamate cysteine ligase activity sensitizes human breast cancer cells to the toxicity of 2-deoxy-D-glucose. Cancer Res 66: 1605-1610 (Pubitemid 43259944)
3. Aykin-Burns N, Ahmad IM, Zhu Y, Oberley LW, Spitz DR (2009) Increased levels of superoxide and H2O2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem J 418: 29-37
4. Beausoleil SA, Villen J, Gerber SA, Rush J, Gygi SP (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 24: 1285-1292 (Pubitemid 44564776)
5. Beckman JS, Minor Jr. RL, White CW, Repine JE, Rosen GM, Freeman BA (1988) Superoxide dismutase and catalase conjugated to polyethylene glycol increases endothelial enzyme activity and oxidant resistance. J Biol Chem 263: 6884-6892
6. Blackburn RV, Spitz DR, Liu X, Galoforo SS, Sim JE, Ridnour LA, Chen JC, Davis BH, Corry PM, Lee YJ (1999) Metabolic oxidative stress activates signal transduction and gene expression during glucose deprivation in human tumor cells. Free Radic Biol Med 26: 419-430 (Pubitemid 29013474)
7. Boivin B, Zhang S, Arbiser JL, Zhang ZY, Tonks NK (2008) A modified cysteinyl-labeling assay reveals reversible oxidation of protein tyrosine phosphatases in angiomyolipoma cells. Proc Natl Acad Sci USA 105: 9959-9964
8. Buzzai M, Bauer DE, Jones RG, Deberardinis RJ, Hatzivassiliou G, Elstrom RL, Thompson CB (2005) The glucose dependence of Akttransformed cells can be reversed by pharmacologic activation of fatty acid beta-oxidation. Oncogene 24: 4165-4173 (Pubitemid 40961771)
9. Choo AY, Kim SG, Vander Heiden MG, Mahoney SJ, Vu H, Yoon SO, Cantley LC, Blenis J (2010) Glucose addiction of TSC null cells is caused by failed mTORC1-dependent balancing of metabolic demand with SUPPL.y. Mol Cell 38: 487-499
10. Chou TC, Talalay P (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55
11. Czernin J, Phelps ME (2002) Positron emission tomography scanning: current and future applications. Annu Rev Med 53: 89-112 (Pubitemid 34177873)
12. Deberardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB (2008) The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 7: 11-20
13. Diaz B, Shani G, Pass I, Anderson D, Quintavalle M, Courtneidge SA (2009) Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal 2: ra53
14. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868 (Pubitemid 29003722)
15. Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, Plas DR, Zhuang H, Cinalli RM, Alavi A, Rudin CM, Thompson CB (2004) Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 64: 3892-3899 (Pubitemid 38697301)
16. Fath MA, Diers AR, Aykin-Burns N, Simons AL, Hua L, Spitz DR (2009) Mitochondrial electron transport chain blockers enhance 2-deoxy-D-glucose induced oxidative stress and cell killing in human colon carcinoma cells. Cancer Biol Ther 8: 1228-1236
17. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91 (Pubitemid 26008141)
18. Guo D, Hildebrandt IJ, Prins RM, Soto H, Mazzotta MM, Dang J, Czernin J, Shyy JY,Watson AD, Phelps M, Radu CG, Cloughesy TF, Mischel PS (2009) The AMPK agonist AICAR inhibits the growth of EGFRvIII-expressing glioblastomas by inhibiting lipogenesis. Proc Natl Acad Sci USA 106: 12932-12937
19. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674
20. Hashiguchi K, Zhang-AkiyamaQM(2009) Establishment of human cell lines lacking mitochondrial DNA. Methods Mol Biol 554: 383-391
21. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K, Dong S, Lonial S, Wang X, Chen GZ, Xie J, Gu TL, Polakiewicz RD, Roesel JL, Boggon TJ, Khuri FR, Gilliland DG, Cantley LC, Kaufman J, Chen J (2009) Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2: ra73
22. Kalaany NY, Sabatini DM (2009) Tumours with PI3K activation are resistant to dietary restriction. Nature 458: 725-731
23. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M (2005) Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120: 649-661 (Pubitemid 40343077)
24. Kawahara T, Ritsick D, Cheng G, Lambeth JD (2005) Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1-and Nox2-dependent reactive oxygen generation. J Biol Chem 280: 31859-31869 (Pubitemid 41291936)
25. Kim JW, Gao P, Dang CV (2007) Effects of hypoxia on tumor metabolism. Cancer Metastasis Rev 26: 291-298 (Pubitemid 47103157)
26. Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, Rhee SG (2004) Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci USA 101: 16419-16424 (Pubitemid 39557728)
27. Kwon J, Shatynski KE, Chen H, Morand S, de Deken X, Miot F, Leto TL, Williams MS (2010) The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling. Sci Signal 3: ra59
28. Lee C, Raffaghello L, Brandhorst S, Safdie FM, Bianchi G, Martin-Montalvo A, Pistoia V,Wei M, Hwang S, Merlino A, Emionite L, de Cabo R, Longo VD (2012) Fasting cycles retard growth of tumors and sensitize a range of cancer cell types to chemotherapy. Sci Transl Med 4: 124ra127
29. Lee SR, Kwon KS, Kim SR, Rhee SG (1998a) Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem 273: 15366-15372 (Pubitemid 28298140)
30. Lee YJ, Galoforo SS, Berns CM, Chen JC, Davis BH, Sim JE, Corry PM, Spitz DR (1998b) Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J Biol Chem 273: 5294-5299 (Pubitemid 28108695)
31. Lee YJ, Galoforo SS, Sim JE, Ridnour LA, Choi J, Forman HJ, Corry PM, Spitz DR (2000) Dominant-negative Jun N-terminal protein kinase (JNK-1) inhibits metabolic oxidative stress during glucose deprivation in a human breast carcinoma cell line. Free Radic Biol Med 28: 575-584 (Pubitemid 30136039)
32. Liliental J, Moon SY, Lesche R, Mamillapalli R, Li D, Zheng Y, Sun H, Wu H (2000) Genetic deletion of the Pten tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases. Curr Biol 10: 401-404 (Pubitemid 30213387)
33. LouYW, Chen YY, Hsu SF, Chen RK, Lee CL, Khoo KH, Tonks NK, Meng TC (2008) Redox regulation of the protein tyrosine phosphatase PTP1B in cancer cells. FEBS J 275: 69-88 (Pubitemid 350294063)
34. Mahadev K, Zilbering A, Zhu L, Goldstein BJ (2001) Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J Biol Chem 276: 21938-21942
35. Mbaya E, Oules B, Caspersen C, Tacine R, Massinet H, Pennuto M, Chretien D, Munnich A, Rotig A, Rizzuto R, Rutter GA, Paterlini-Brechot P, Chami M (2010) Calcium signalling-dependent mitochondrial dysfunction and bioenergetics regulation in respiratory chain Complex II deficiency. Cell Death Differ 17: 1855-1866
36. Meng TC, Fukada T, Tonks NK (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 9: 387-399 (Pubitemid 34195563)
37. Myers MP, Stolarov JP, Eng C, Li J, Wang SI, Wigler MH, Parsons R, Tonks NK (1997) P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc Natl Acad Sci USA 94: 9052-9057
38. Nazarian R, Shi HB, Wang Q, Kong XJ, Koya RC, Lee H, Chen ZG, Lee MK, Attar N, Sazegar H, Chodon T, Nelson SF, McArthur G, Sosman JA, Ribas A, Lo RS (2010) Melanomas acquire resistance toBRAF( V600E) inhibition by RTK or N-RAS upregulation. Nature 468: 973-U377
39. Pani G, Colavitti R, Bedogni B, Anzevino R, Borrello S, Galeotti T (2000) A redox signaling mechanism for density-dependent inhibition of cell growth. J Biol Chem 275: 38891-38899 (Pubitemid 32010745)
40. Prakash A, Mallick P, Whiteaker J, Zhang HD, Paulovich A, Flory M, Lee H, Aebersold R, Schwikowski B (2006) Signal maps for mass spectrometry-based comparative proteomics. Mol Cell Proteomics 5: 423-432
41. Raj L, Ide T, Gurkar AU, FoleyM, Schenone M, Li X, Tolliday NJ, Golub TR, Carr SA, Shamji AF, Stern AM, Mandinova A, Schreiber SL, LeeSW (2011) Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475: 231-234
42. Rubbi L, Titz B, Brown L, Galvan E, Komisopoulou E, Chen SS, Low T, Tahmasian M, Skaggs B, Muschen M, Pellegrini M, Graeber TG (2011) Global phosphoproteomics reveals crosstalk between Bcr-Abl and negative feedback mechanisms controlling Src signaling. Sci Signal 4: ra18
43. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, Barford D (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423: 769-773 (Pubitemid 36735701)
44. Schafer ZT, Grassian AR, Song L, Jiang Z, Gerhart-Hines Z, Irie HY, Gao S, Puigserver P, Brugge JS (2009) Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 461: 109-113
45. Shaw AT, Winslow MM, Magendantz M, Ouyang C, Dowdle J, Subramanian A, Lewis TA, Maglathin RL, Tolliday N, Jacks T (2011) Selective killing of K-ras mutant cancer cells by small molecule inducers of oxidative stress. Proc Natl Acad Sci USA 108: 8773-8778
46. Simons AL, Mattson DM, Dornfeld K, Spitz DR (2009) Glucose deprivation-induced metabolic oxidative stress and cancer therapy. J Cancer Res Ther 5(SUPPL. 1): S2-S6
47. Skaggs BJ, Gorre ME, Ryvkin A, Burgess MR, Xie Y, Han Y, Komisopoulou E, Brown LM, Loo JA, Landaw EM, Sawyers CL, Graeber TG (2006) Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCR-ABL mutants. Proc Natl Acad Sci USA 103: 19466-19471 (Pubitemid 46026054)
48. Sondergaard JN, Nazarian R,Wang Q, Guo D, Hsueh T, Mok S, Sazegar H, MacConaill LE, Barretina JG, Kehoe SM, Attar N, von Euw E, Zuckerman JE, Chmielowski B, Comin-Anduix B, Koya RC, Mischel PS, Lo RS, Ribas A (2010) Differential sensitivity of melanoma cell lines with BRAFV600E mutation to the specific Raf inhibitor PLX4032. J Transl Med 8: 39
49. Spitz DR, Sim JE, Ridnour LA, Galoforo SS, Lee YJ (2000) Glucose deprivation-induced oxidative stress in human tumor cells. A fundamental defect in metabolism?. Ann NYAcad Sci 899: 349-362 (Pubitemid 30352799)
50. Szatrowski TP, Nathan CF (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798
51. Toyokuni S, Okamoto K, Yodoi J, Hiai H (1995) Persistent oxidative stress in cancer. FEBS Lett 358: 1-3
52. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu J, Huang P (2006) Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10: 241-252 (Pubitemid 44311067)
53. Ushio-Fukai M (2006) Localizing NADPH oxidase-derived ROS. Sci STKE 2006: re8
54. Vivanco I, Palaskas N, Tran C, Finn SP, Getz G, Kennedy NJ, Jiao J, Rose J, Xie W, Loda M, Golub T, Mellinghoff IK, Davis RJ, Wu H, Sawyers CL (2007) Identification of the JNK signaling pathway as a functional target of the tumor suppressor PTEN. Cancer Cell 11: 555-569 (Pubitemid 46856910)
55. Wang MY, Lu KV, Zhu S, Dia EQ, Vivanco I, Shackleford GM, Cavenee WK, Mellinghoff IK, Cloughesy TF, Sawyers CL, Mischel PS (2006) Mammalian target of rapamycin inhibition promotes response to epidermal growth factor receptor kinase inhibitors in PTENdeficient and PTEN-intact glioblastoma cells. Cancer Res 66: 7864-7869 (Pubitemid 44299148)
56. Warburg O (1956) On respiratory impairment in cancer cells. Science 124: 269-270
57. Wellen KE, Lu C, Mancuso A, Lemons JM, Ryczko M, Dennis JW, Rabinowitz JD, Coller HA, Thompson CB (2010) The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism. Genes Dev 24: 2784-2799
58. Wu RF, Xu YC, Ma Z, Nwariaku FE, Sarosi Jr. GA, Terada LS (2005) Subcellular targeting of oxidants during endothelial cell migration. J Cell Biol 171: 893-904 (Pubitemid 41746590)
59. Yang C, Sudderth J, Dang T, Bachoo RG, McDonald JG, DeBerardinis RJ (2009) Glioblastoma cells require glutamate dehydrogenase to survive impairments of glucose metabolism or Akt signaling. Cancer Res 69: 7986-7993
60. Yun J, Rago C, Cheong I, Pagliarini R, Angenendt P, Rajagopalan H, Schmidt K, Wilson JK, Markowitz S, Zhou S, Diaz Jr. LA, Velculescu V, Lengauer C, Kinzler KW, Vogelstein B, Papadopoulos N (2009) Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science 325: 1555-1559
61. Yuneva M (2008) Finding an 'Achilles' heel' of cancer: the role of glucose and glutamine metabolism in the survival of transformed cells. Cell Cycle 7: 2083-2089 (Pubitemid 352031507)
62. Yuneva M, Zamboni N, Oefner P, SachidanandamR, Lazebnik Y (2007) Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J Cell Biol 178: 93-105 (Pubitemid 47026405)
63. Zimman A, Chen SS, Komisopoulou E, Titz B, Martinez-Pinna R, Kafi A, Berliner JA, Graeber TG (2010) Activation of aortic endothelial cells by oxidized phospholipids: a phosphoproteomic analysis. J Proteome Res 9: 2812-2824