Energy restriction mimetic agents to target cancer cells: Comparison between 2-deoxyglucose and thiazolidinediones

Biochemical Pharmacology

Volumn 92, Issue 1, 2014, Pages 102-111

  Kuntz, Sandra ^a,b   Mazerbourg, Sabine ^a,b   Boisbrun, Michel ^a,c   Cerella, Claudia ^d   Diederich, Marc ^d,e   Grillier Vuissoz, Isabelle ^a,b   Flament, Stephane ^a,b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b CENTRE DE RECHERCHE EN AUTOMATIQUE DE NANCY   (France)

^c NANCY UNIVERSITÉ   (France)

^d LABORATOIRE DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE DU CANCER   (Luxembourg)

^e Seoul National University   (South Korea)

Author keywords

2 deoxyglucose, Thiazolidinediones; Cancer; Glucose metabolism; Warburg effect

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTINEOPLASTIC AGENT; DEOXYGLUCOSE; ENERGY RESTRICTION MIMETIC AGENT; PROTEIN P53; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL; CELL METABOLISM; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; HELA CELL LINE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LNCAP CELL LINE; MCF 7 CELL LINE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN DEPLETION; TARGET CELL; TUMOR GROWTH; DRUG EFFECTS; ENERGY METABOLISM; NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; DEOXYGLUCOSE; ENERGY METABOLISM; HUMANS; NEOPLASMS; THIAZOLIDINEDIONES;

EID: 84908215040     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.07.021     Document Type: Review

References (114)

1. W.H. Koppenol, P.L. Bounds, and C.V. Dang Otto Warburg's contributions to current concepts of cancer metabolism Nat Rev Cancer 11 2011 325 337
2. S. Ben-Haim, and P. Ell 18F-FDG PET and PET/CT in the evaluation of cancer treatment response J Nucl Med 50 2009 88 99
3. R.A. Gatenby, and R.J. Gillies Why do cancers have high aerobic glycolysis Nat Rev Cancer 4 2004 891 899
4. R.J. DeBerardinis, J.J. Lum, G. Hatzivassiliou, and C.B. Thompson The biology of cancer: metabolic reprogramming fuels cell growth and proliferation Cell Metab 7 2008 11 20
5. M.G. Vander Heiden, L.C. Cantley, and C.B. Thompson Understanding the Warburg effect: the metabolic requirements of cell proliferation Science 324 2009 1029 1033
6. D.G. Hardie AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy Nat Rev Mol Cell Biol 8 2007 774 785
7. R.J. DeBerardinis, A. Mancuso, E. Daikhin, I. Nissim, M. Yudkoff, and S. Wehrli Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis Proc Natl Acad Sci USA 104 2007 19345 19350
8. W.G. Kaelin Jr.; and P.J. Ratcliffe Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway Mol Cell 30 2008 393 402
9. K.E. Wellen, and C.B. Thompson A two-way street: reciprocal regulation of metabolism and signalling Nat Rev Mol Cell Biol 13 2012 270 276
10. P.P. Hsu, and D.M. Sabatini Cancer cell metabolism: Warburg and beyond Cell 134 2008 703 707
11. C.V. Dang Links between metabolism and cancer Genes Dev 26 2012 877 890
12. C.V. Dang, and G.L. Semenza Oncogenic alterations of metabolism Trends Biochem Sci 24 1999 68 72
13. A. Ramanathan, C. Wang, and S.L. Schreiber Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements Proc Natl Acad Sci USA 102 2005 5992 5997
14. J.A. Engelman Targeting PI3K signalling in cancer: opportunities, challenges and limitations Nat Rev Cancer 9 2009 550 562
15. J.D. Gordan, C.B. Thompson, and M.C. Simon HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation Cancer Cell 12 2007 108 113
16. C.V. Dang, A. Le, and P. Gao MYC-induced cancer cell energy metabolism and therapeutic opportunities Clin Cancer Res 15 2009 6479 6483
17. F. Schwartzenberg-Bar-Yoseph, M. Armoni, and E. Karnieli The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression Cancer Res 64 2004 2627 2633
18. I. Mor, E.C. Cheung, and K.H. Vousden Control of glycolysis through regulation of PFK1: old friends and recent additions Cold Spring Harb Symp Quant Biol 76 2011 211 216
19. P.E. Porporato, S. Dhup, R.K. Dadhich, T. Copetti, and P. Sonveaux Anticancer targets in the glycolytic metabolism of tumors: a comprehensive review Front Pharmacol 2 2011 49
20. N. Aykin-Burns, I.M. Ahmad, Y. Zhu, L.W. Oberley, and D.R. Spitz Increased levels of superoxide and H2O2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation Biochem J 418 2009 29 37
21. A.N. Wick, D.R. Drury, H.I. Nakada, and J.B. Wolfe Localization of the primary metabolic block produced by 2-deoxyglucose J Biol Chem 224 1957 963 969
22. W. Chen, and M. Gueron The inhibition of bovine heart hexokinase by 2-deoxy-D-glucose-6-phosphate: characterization by 31P NMR and metabolic implications Biochimie 74 1992 867 873
23. P.R. Wachsberger, E.L. Gressen, A. Bhala, S.B. Bobyock, C. Storck, and R.A. Coss Variability in glucose transporter-1 levels and hexokinase activity in human melanoma Melanoma Res 12 2002 35 43
24. S. Wei, S.K. Kulp, and C.S. Chen Energy restriction as an antitumor target of thiazolidinediones J Biol Chem 285 2010 9780 9791
25. O. Zagorodna, S.M. Martin, D.T. Rutkowski, T. Kuwana, D.R. Spitz, and C.M. Knudson 2-deoxyglucose-induced toxicity is regulated by Bcl-2 family members and is enhanced by antagonizing Bcl-2 in lymphoma cell lines Oncogene 31 2012 2738 2749
26. O. Kaplan, G. Navon, R.C. Lyon, P.J. Faustino, E.J. Straka, and J.S. Cohen Effects of 2-deoxyglucose on drug-sensitive and drug-resistant human breast cancer cells: toxicity and magnetic resonance spectroscopy studies of metabolism Cancer Res 50 1990 544 551
27. R.L. Aft, F.W. Zhang, and D. Gius Evaluation of 2-deoxy-D-glucose as a chemotherapeutic agent: mechanism of cell death Brit J Cancer 87 2002 805 812
28. S.L. Tagg, P.A. Foster, M.P. Leese, B.V. Potter, M.J. Reed, and A. Purohit 2-Methoxyoestradiol-3,17-O,O-bis-sulphamate and 2-deoxy-D-glucose in combination: a potential treatment for breast and prostate cancer Brit J Cancer 99 2008 1842 1848
29. M. Kurtoglu, N. Gao, J. Shang, J.C. Maher, M.A. Lehrman, and M. Wangpaichitr Under normoxia, 2-deoxy-D-glucose elicits cell death in select tumor types not by inhibition of glycolysis but by interfering with N-linked glycosylation Mol Cancer Ther 6 2007 3049 3058
30. G. Cheng, J. Zielonka, B.P. Dranka, D. McAllister, A.C. Mackinnon Jr.; and J. Joseph Mitochondria-targeted drugs synergize with 2-deoxyglucose to trigger breast cancer cell death Cancer Res 72 2012 2634 2644
31. B.K. Mohanti, G.K. Rath, N. Anantha, V. Kannan, B.S. Das, and B.A. Chandramouli Improving cancer radiotherapy with 2-deoxy-D-glucose: phase I/II clinical trials on human cerebral gliomas Int J Radiat Oncol Biol Phys 35 1996 103 111
32. D. Khaitan, S. Chandna, M.B. Arya, and B.S. Dwarakanath Differential mechanisms of radiosensitization by 2-deoxy-D-glucose in the monolayers and multicellular spheroids of a human glioma cell line Cancer Biol Ther 5 2006 1142 1151
33. R. Varshney, B. Dwarakanath, and V. Jain Radiosensitization by 6-aminonicotinamide and 2-deoxy-d-glucose in human cancer cells Int J Radiat Biol 81 2005 397 408
34. P.K. Sharma, B.S. Dwarakanath, and R. Varshney Radiosensitization by 2-deoxy-D-glucose and 6-aminonicotinamide involves activation of redox sensitive ASK1-JNK/p38MAPK signaling in head and neck cancer cells Free Radic Biol Med 53 2012 1500 1513
35. K.A. Kern, and J.A. Norton Inhibition of established rat fibrosarcoma growth by the glucose antagonist 2-deoxy-D-glucose Surgery 102 1987 380 385
36. O. Cay, M. Radnell, B. Jeppsson, B. Ahren, and S. Bengmark Inhibitory effect of 2-deoxy-d-glucose on liver tumor growth in rats Cancer Res 52 1992 5794 5796
37. M.C. Coleman, C.R. Asbury, D. Daniels, J. Du, N. Aykin-Burns, and B.J. Smith 2-deoxy-d-glucose causes cytotoxicity, oxidative stress, and radiosensitization in pancreatic cancer Free Radic Biol Med 44 2008 322 331
38. Y. Wang, Y. Liu, C. Wu, B. McNally, and P. Zheng Laforin confers cancer resistance to energy deprivation-induced apoptosis Cancer Res 68 2008 4039 4044
39. G. Maschek, N. Savaraj, W. Priebe, P. Braunschweiger, K. Hamilton, and G.F. Tidmarsh 2-deoxy-d-glucose increases the efficacy of adriamycin and paclitaxel in human osteosarcoma and non-small cell lung cancers in vivo Cancer Res 64 2004 31 34
40. S. Gupta, R. Mathur, and B.S. Dwarakanath The glycolytic inhibitor 2-deoxy-d-glucose enhances the efficacy of etoposide in ehrlich ascites tumor-bearing mice Cancer Biol Ther 4 2005 87 94
41. R.S. Wong Apoptosis in cancer: from pathogenesis to treatment J Exp Clin Cancer Res 30 2011 87
42. L. Ghibelli, and M. Diederich Multistep and multitask Bax activation Mitochondrion 10 2010 604 613
43. C. Munoz-Pinedo, C. Ruiz-Ruiz, C. Ruiz de Almodovar, C. Palacios, and A. Lopez-Rivas Inhibition of glucose metabolism sensitizes tumor cells to death receptor-triggered apoptosis through enhancement of death-inducing signaling complex formation and apical procaspase-8 processing J Biol Chem 278 2003 12759 12768
44. X.D. Zhang, E. Deslandes, M. Villedieu, L. Poulain, M. Duval, and P. Gauduchon Effect of 2-deoxy-d-glucose on various malignant cell lines in vitro Anticancer Res 26 2006 3561 3566
45. R.S. DiPaola, D. Dvorzhinski, A. Thalasila, V. Garikapaty, D. Doram, and M. May Therapeutic starvation and autophagy in prostate cancer: a new paradigm for targeting metabolism in cancer therapy Prostate 68 2008 1743 1752
46. P. Loar, H. Wahl, M. Kshirsagar, G. Gossner, K. Griffith, and J.R. Liu Inhibition of glycolysis enhances cisplatin-induced apoptosis in ovarian cancer cells Am J Obstet Gynecol 202 37 2010 e1 e8
47. F.M. Wensveen, N.L. Alves, I.A. Derks, K.A. Reedquist, and E. Eldering Apoptosis induced by overall metabolic stress converges on the Bcl-2 family proteins Noxa and Mcl-1 Apoptosis 16 2011 708 721
48. I. Ben Sahra, K. Laurent, S. Giuliano, F. Larbret, G. Ponzio, and P. Gounon Targeting cancer cell metabolism: the combination of metformin and 2-deoxyglucose induces p53-dependent apoptosis in prostate cancer cells Cancer Res 70 2010 2465 2475
49. E. Hernlund, L.S. Ihrlund, O. Khan, Y.O. Ates, S. Linder, and T. Panaretakis Potentiation of chemotherapeutic drugs by energy metabolism inhibitors 2-deoxyglucose and etomoxir Int J Cancer 123 2008 476 483
50. Y.Y. Huang, H. Liu, Y. Li, L.J. Pu, C.C. Jiang, and J.C. Xu Down-regulation of RIP1 by 2-deoxy-d-glucose sensitizes breast cancer cells to TRAIL-induced apoptosis Eur J Pharmacol 705 2013 26 34
51. S. Sridhar, Y. Botbol, F. Macian, and A.M. Cuervo Autophagy and disease: always two sides to a problem J Pathol 226 2012 255 273
52. H. Xi, M. Kurtoglu, H. Liu, M. Wangpaichitr, M. You, and X. Liu 2-Deoxy-D-glucose activates autophagy via endoplasmic reticulum stress rather than ATP depletion Cancer Chemother Pharmacol 67 2011 899 910
53. H. Xi, J.C. Barredo, J.R. Merchan, and T.J. Lampidis Endoplasmic reticulum stress induced by 2-deoxyglucose but not glucose starvation activates AMPK through CaMKKbeta leading to autophagy Biochem Pharmacol 85 2013 1463 1477
54. S. Ramirez-Peinado, C.L. Leon-Annicchiarico, J. Galindo-Moreno, R. Iurlaro, A. Caro-Maldonado, and J.H. Prehn Glucose-starved cells do not engage in prosurvival autophagy J Biol Chem 288 2013 30387 30398
55. J.H. Cheong, E.S. Park, J. Liang, J.B. Dennison, D. Tsavachidou, and C. Nguyen-Charles Dual inhibition of tumor energy pathway by 2-deoxyglucose and metformin is effective against a broad spectrum of preclinical cancer models Mol Cancer Ther 10 2011 2350 2362
56. D. Zhong, L. Guo, I. de Aguirre, X. Liu, N. Lamb, and S.Y. Sun LKB1 mutation in large cell carcinoma of the lung Lung Cancer 53 2006 285 294
57. D. Zhong, X. Liu, K. Schafer-Hales, A.I. Marcus, F.R. Khuri, and S.Y. Sun 2-Deoxyglucose induces Akt phosphorylation via a mechanism independent of LKB1/AMP-activated protein kinase signaling activation or glycolysis inhibition Mol Cancer Ther 7 2008 809 817
58. H. Wu, H. Zhu, D.X. Liu, T.K. Niu, X. Ren, and R. Patel Silencing of elongation factor-2 kinase potentiates the effect of 2-deoxy-D-glucose against human glioma cells through blunting of autophagy Cancer Res 69 2009 2453 2460
59. A. Priebe, L. Tan, H. Wahl, A. Kueck, G. He, and R. Kwok Glucose deprivation activates AMPK and induces cell death through modulation of Akt in ovarian cancer cells Gynecol Oncol 122 2011 389 395
60. Z. Zhu, W. Jiang, J.N. McGinley, and H.J. Thompson 2-Deoxyglucose as an energy restriction mimetic agent: effects on mammary carcinogenesis and on mammary tumor cell growth in vitro Cancer Res 65 2005 7023 7030
61. A. Murayama, K. Ohmori, A. Fujimura, H. Minami, K. Yasuzawa-Tanaka, and T. Kuroda Epigenetic control of rDNA loci in response to intracellular energy status Cell 133 2008 627 639
62. C.H. Chen, P.H. Huang, P.C. Chu, M.C. Chen, C.C. Chou, and D. Wang Energy restriction-mimetic agents induce apoptosis in prostate cancer cells in part through epigenetic activation of KLF6 tumor suppressor gene expression J Biol Chem 286 2011 9968 9976
63. H.Y. Lin, Y.C. Kuo, Y.I. Weng, I.L. Lai, T.H. Huang, and S.P. Lin Activation of silenced tumor suppressor genes in prostate cancer cells by a novel energy restriction-mimetic agent Prostate 72 2012 1767 1778
64. S. Wei, P.C. Chu, H.C. Chuang, W.C. Hung, S.K. Kulp, and C.S. Chen Targeting the oncogenic E3 ligase Skp2 in prostate and breast cancer cells with a novel energy restriction-mimetic agent PLoS One 7 2012 e47298
65. N. Naidoo ER and aging-Protein folding and the ER stress response Ageing Res Rev 8 2009 150 159
66. H. Liu, M. Kurtoglu, Y. Cao, H. Xi, R. Kumar, and J.M. Axten Conversion of 2-deoxyglucose-induced growth inhibition to cell death in normoxic tumor cells Cancer Chemother Pharmacol 72 2013 251 262
67. J. DeSalvo, J.N. Kuznetsov, J. Du, G.M. Leclerc, G.J. Leclerc, and T.J. Lampidis Inhibition of Akt potentiates 2-DG-induced apoptosis via downregulation of UPR in acute lymphoblastic leukemia Mol Cancer Res 10 2012 969 978
68. L.X. Fan, C.M. Liu, A.H. Gao, Y.B. Zhou, and J. Li Berberine combined with 2-deoxy-d-glucose synergistically enhances cancer cell proliferation inhibition via energy depletion and unfolded protein response disruption Biochim Biophys Acta 1830 2013 5175 5183
69. G. Derosa, and P. Maffioli Peroxisome proliferator-activated receptor-gamma (PPAR-gamma) agonists on glycemic control, lipid profile and cardiovascular risk Curr Mol Pharmacol 5 2012 272 281
70. E. Mueller, M. Smith, P. Sarraf, T. Kroll, A. Aiyer, and D.S. Kaufman Effects of ligand activation of peroxisome proliferator-activated receptor gamma in human prostate cancer Proc Natl Acad Sci USA 97 2000 10990 10995
71. P.D. Home, S.J. Pocock, H. Beck-Nielsen, P.S. Curtis, R. Gomis, and M. Hanefeld Rosiglitazone evaluated for cardiovascular outcomes in oral agent combination therapy for type 2 diabetes (RECORD): a multicentre, randomised, open-label trial Lancet 373 2009 2125 2135
72. M. Monami, C. Lamanna, N. Marchionni, and E. Mannucci Rosiglitazone and risk of cancer: a meta-analysis of randomized clinical trials Diabetes Care 31 2008 1455 1460
73. I.N. Colmers, S.L. Bowker, and J.A. Johnson Thiazolidinedione use and cancer incidence in type 2 diabetes: a systematic review and meta-analysis Diabetes Metab 38 2012 475 484
74. H.C. Lin, Y.T. Hsu, B.H. Kachingwe, C.Y. Hsu, Y.S. Uang, and L.H. Wang Dose effect of thiazolidinedione on cancer risk in type 2 diabetes mellitus patients: a six-year population-based cohort study J Clin Pharm Ther 2014
75. Grillier-Vuissoz I, Mazerbourg S, Boisbrun M, Kuntz S, Chapleur Y, Flament S. PPARg-independent Activity Of Thiazolidinediones: A Promising Mechanism Of Action For New Anticancer Drugs? J Carcinog mutag 2014; Accepted In press.
76. E. Kebebew, M. Peng, E. Reiff, P. Treseler, K.A. Woeber, and O.H. Clark A phase II trial of rosiglitazone in patients with thyroglobulin-positive and radioiodine-negative differentiated thyroid cancer Surgery 140 2006 960 966 discussion 6-7
77. W.L. Read, M.Q. Baggstrom, P.M. Fracasso, and R. Govindan A phase I study of bexarotene and rosiglitazone in patients with refractory cancers Chemotherapy 54 2008 236 241
78. J. Lecomte, S. Flament, S. Salamone, M. Boisbrun, S. Mazerbourg, and Y. Chapleur Disruption of ERalpha signalling pathway by PPARgamma agonists: evidences of PPARgamma-independent events in two hormone-dependent breast cancer cell lines Breast Cancer Res Treat 112 2008 437 451
79. C. Colin, S. Salamone, I. Grillier-Vuissoz, M. Boisbrun, S. Kuntz, and J. Lecomte New troglitazone derivatives devoid of PPARgamma agonist activity display an increased antiproliferative effect in both hormone-dependent and hormone-independent breast cancer cell lines Breast Cancer Res Treat 124 2010 101 110
80. S. Salamone, C. Colin, I. Grillier-Vuissoz, S. Kuntz, S. Mazerbourg, and S. Flament Synthesis of new troglitazone derivatives: anti-proliferative activity in breast cancer cell lines and preliminary toxicological study Eur J Med Chem 51 2012 206 215
81. C.W. Shiau, C.C. Yang, S.K. Kulp, K.F. Chen, C.S. Chen, and J.W. Huang Thiazolidenediones mediate apoptosis in prostate cancer cells in part through inhibition of Bcl-xL/Bcl-2 functions independently of PPARgamma Cancer Res 65 2005 1561 1569
82. J. Yang, S. Wei, D.S. Wang, Y.C. Wang, S.K. Kulp, and C.S. Chen Pharmacological exploitation of the peroxisome proliferator-activated receptor gamma agonist ciglitazone to develop a novel class of androgen receptor-ablative agents J Med Chem 51 2008 2100 2107
83. L.D. Berman-Booty, P.C. Chu, J.M. Thomas-Ahner, B. Bolon, D. Wang, and T. Yang Suppression of prostate epithelial proliferation and intraprostatic progrowth signaling in transgenic mice by a new energy restriction-mimetic agent Cancer Prev Res (Phila) 6 2013 232 241
84. D. Wang, P.C. Chu, C.N. Yang, R. Yan, Y.C. Chuang, and S.K. Kulp Development of a novel class of glucose transporter inhibitors J Med Chem 55 2012 3827 3836
85. J.H. Guh, W.L. Chang, J. Yang, S.L. Lee, S. Wei, and D. Wang Development of novel adenosine monophosphate-activated protein kinase activators J Med Chem 53 2010 2552 2561
86. K.H. Lee, E.C. Hsu, J.H. Guh, H.C. Yang, D. Wang, and S.K. Kulp Targeting energy metabolic and oncogenic signaling pathways in triple-negative breast cancer by a novel adenosine monophosphate-activated protein kinase (AMPK) activator J Biol Chem 286 2011 39247 39258
87. H. Liu, C. Zang, M.H. Fenner, D. Liu, K. Possinger, and H.P. Koeffler Growth inhibition and apoptosis in human Philadelphia chromosome-positive lymphoblastic leukemia cell lines by treatment with the dual PPARalpha/gamma ligand TZD18 Blood 107 2006 3683 3692
88. M.L. Plissonnier, S. Fauconnet, H. Bittard, and I. Lascombe Insights on distinct pathways of thiazolidinediones (PPARgamma ligand)-promoted apoptosis in TRAIL-sensitive or -resistant malignant urothelial cells Int J Cancer 127 2010 1769 1784
89. M.L. Plissonnier, S. Fauconnet, H. Bittard, and I. Lascombe The antidiabetic drug ciglitazone induces high grade bladder cancer cells apoptosis through the up-regulation of TRAIL PLoS One 6 2011 e28354
90. C. Colin-Cassin, X. Yao, C. Cerella, S. Chbicheb, S. Kuntz, and S. Mazerbourg PPARgamma-inactive Delta2-troglitazone independently triggers ER stress and apoptosis in breast cancer cells Mol Carcinog 2013
91. C. Zang, H. Liu, J. Bertz, K. Possinger, H.P. Koeffler, and E. Elstner Induction of endoplasmic reticulum stress response by TZD18, a novel dual ligand for peroxisome proliferator-activated receptor alpha/gamma, in human breast cancer cells Mol Cancer Ther 8 2009 2296 2307
92. M. Fujita, T. Yagami, M. Fujio, C. Tohji, K. Takase, and Y. Yamamoto Cytotoxicity of troglitazone through PPARgamma-independent pathway and p38 MAPK pathway in renal cell carcinoma Cancer Lett 312 2011 219 227
93. A. Mieczkowska, M.F. Basle, D. Chappard, and G. Mabilleau Thiazolidinediones induce osteocyte apoptosis by a G protein-coupled receptor 40-dependent mechanism J Biol Chem 287 2012 23517 23526
94. M. Lu, T. Kwan, C. Yu, F. Chen, B. Freedman, and J.M. Schafer Peroxisome proliferator-activated receptor gamma agonists promote TRAIL-induced apoptosis by reducing survivin levels via cyclin D3 repression and cell cycle arrest J Biol Chem 280 2005 6742 6751
95. K. Schultze, B. Bock, A. Eckert, L. Oevermann, D. Ramacher, and O. Wiestler Troglitazone sensitizes tumor cells to TRAIL-induced apoptosis via down-regulation of FLIP and Survivin Apoptosis 11 2006 1503 1512
96. W. Zou, X. Liu, P. Yue, F.R. Khuri, and S.Y. Sun PPARgamma ligands enhance TRAIL-induced apoptosis through DR5 upregulation and c-FLIP downregulation in human lung cancer cells Cancer Biol Ther 6 2007 99 106
97. Y.H. Kim, E.M. Jung, T.J. Lee, S.H. Kim, Y.H. Choi, and J.W. Park Rosiglitazone promotes tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by reactive oxygen species-mediated up-regulation of death receptor 5 and down-regulation of c-FLIP Free Radic Biol Med 44 2008 1055 1068
98. X. Jin, D. Yuan, X. Chen, and X. Jiang [AMP-activated protein kinase-alpha is involved in the autophagy and apoptosis caused by troglitazone] Wei Sheng Wu Xue Bao 52 2012 840 849
99. J. Yan, H. Yang, G. Wang, L. Sun, Y. Zhou, and Y. Guo Autophagy augmented by troglitazone is independent of EGFR transactivation and correlated with AMP-activated protein kinase signaling Autophagy 6 2010 67 73
100. J. Zhou, W. Zhang, B. Liang, M.C. Casimiro, D. Whitaker-Menezes, and M. Wang PPARgamma activation induces autophagy in breast cancer cells Int J Biochem Cell Biol 41 2009 2334 2342
101. L. Cerquetti, C. Sampaoli, D. Amendola, B. Bucci, L. Masuelli, and R. Marchese Rosiglitazone induces autophagy in H295R and cell cycle deregulation in SW13 adrenocortical cancer cells Exp Cell Res 317 2011 1397 1410
102. Y.S. Sohn, S. Tamir, L. Song, D. Michaeli, I. Matouk, and A.R. Conlan NAF-1 and mitoNEET are central to human breast cancer proliferation by maintaining mitochondrial homeostasis and promoting tumor growth Proc Natl Acad Sci USA 110 2013 14676 14681
103. S. Tamir, J.A. Zuris, L. Agranat, C.H. Lipper, A.R. Conlan, and D. Michaeli Nutrient-deprivation autophagy factor-1 (NAF-1): biochemical properties of a novel cellular target for anti-diabetic drugs PLoS One 8 2013 e61202
104. W.J. Geldenhuys, M.O. Funk, P.S. Awale, L. Lin, and R.T. Carroll A novel binding assay identifies high affinity ligands to the rosiglitazone binding site of mitoNEET Bioorg Med Chem Lett 21 2011 5498 5501
105. S.E. Wiley, A.N. Murphy, S.A. Ross, P. van der Geer, and J.E. Dixon MitoNEET is an iron-containing outer mitochondrial membrane protein that regulates oxidative capacity Proc Natl Acad Sci USA 104 2007 5318 5323
106. S. Wei, H.C. Yang, H.C. Chuang, J. Yang, S.K. Kulp, and P.J. Lu A novel mechanism by which thiazolidinediones facilitate the proteasomal degradation of cyclin D1 in cancer cells J Biol Chem 283 2008 26759 26770
107. S. Wei, L.F. Lin, C.C. Yang, Y.C. Wang, G.D. Chang, and H. Chen Thiazolidinediones modulate the expression of beta-catenin and other cell-cycle regulatory proteins by targeting the F-box proteins of Skp1-Cul1-F-box protein E3 ubiquitin ligase independently of peroxisome proliferator-activated receptor gamma Mol Pharmacol 72 2007 725 733
108. S.A. Arafa el, A.H. Abdelazeem, H.H. Arab, and H.A. Omar OSU-CG5, a novel energy restriction mimetic agent, targets human colorectal cancer cells in vitro Acta Pharmacol Sin 35 2014 394 400
109. J.W. Huang, C.W. Shiau, Y.T. Yang, S.K. Kulp, K.F. Chen, and R.W. Brueggemeier Peroxisome proliferator-activated receptor gamma-independent ablation of cyclin D1 by thiazolidinediones and their derivatives in breast cancer cells Mol Pharmacol 67 2005 1342 1348
110. A. Bordessa, C. Colin-Cassin, I. Grillier-Vuissoz, S. Kuntz, S. Mazerbourg, and G. Husson Optimization of troglitazone derivatives as potent anti-proliferative agents: Towards more active and less toxic compounds Eur J Med Chem 83 2014 129 140
111. H.A. Omar, L. Berman-Booty, S.K. Kulp, and C.S. Chen Energy restriction as an antitumor target Future Oncol 6 2010 1675 1679
112. R.A. Cairns, I. Harris, S. McCracken, and T.W. Mak Cancer cell metabolism Cold Spring Harb Symp Quant Biol 76 2011 299 311
113. J.W. Locasale Metabolic rewiring drives resistance to targeted cancer therapy Mol Syst Biol 8 2012 597
114. B.S. Dwarakanath Cytotoxicity, radiosensitization, and chemosensitization of tumor cells by 2-deoxy-d-glucose in vitro J Cancer Res Ther 5 Suppl 1 2009 S27 S31