Targeting the facilitative glucose transporter GLUT1 inhibits the self-renewal and tumor-initiating capacity of cancer stem cells

Oncotarget

Volumn 6, Issue 2, 2015, Pages 651-661

  Shibuya, Keita ^a,b,c   Okada, Masashi ^a   Suzuki, Shuhei ^a   Seino, Manabu ^a   Seino, Shizuka ^a,b,c   Takeda, Hiroyuki ^a   Kitanaka, Chifumi ^a,b,c  

^a YAMAGATA UNIVERSITY   (Japan)

^b YAMAGATA UNIVERSITY   (Japan)

^c JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

Author keywords

Cancer initiating cell; Glioma; Tumorigenicity; Xenograft analysis

Indexed keywords

ANTINEOPLASTIC AGENT; GLUCOSE; GLUCOSE TRANSPORTER 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WZB 117; HYDROXYBENZOIC ACID DERIVATIVE; SLC2A1 PROTEIN, HUMAN; WZB117;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER STEM CELL; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; DRUG EFFECT; DRUG SELECTIVITY; DRUG TARGETING; DRUG TOLERABILITY; GENE SILENCING; GLIOBLASTOMA; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OVARY CANCER; PANCREAS CANCER; SYSTEMIC THERAPY; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; DRUG EFFECTS; DRUG SCREENING; FEMALE; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; PATHOLOGY; RANDOMIZATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; HYDROXYBENZOATES; MALE; MICE; MICE, INBRED BALB C; MOLECULAR TARGETED THERAPY; NEOPLASMS; NEOPLASTIC STEM CELLS; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84921816801     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2892     Document Type: Article

References (36)

1. Reya T, Morrison SJ, Clarke MF and Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001; 414(6859):105-111.
2. Dick JE. Stem cell concepts renew cancer research. Blood. 2008; 112(13):4793-4807.
3. Yu Z, Pestell TG, Lisanti MP and Pestell RG. Cancer stem cells. Int J Biochem Cell Biol. 2012; 44(12):2144-2151.
4. Yu Y, Ramena G and Elble RC. The role of cancer stem cells in relapse of solid tumors. Front Biosci (Elite Ed). 2012; 4:1528-1541.
5. Malik B and Nie D. Cancer stem cells and resistance to chemo and radio therapy. Front Biosci (Elite Ed). 2012; 4:2142-2149.
6. Bao B, Ahmad A, Azmi AS, Ali S and Sarkar FH. Overview of cancer stem cells (CSCs) and mechanisms of their regulation: implications for cancer therapy. Curr Protoc Pharmacol. 2013; Chapter 14:Unit 14.25.
7. Garg M. Gain of antitumor functions and induction of differentiation in cancer stem cells contribute to complete cure and no relapse. Crit Rev Oncog. 2009; 15(1-2):65-90.
8. Alison MR, Lin WR, Lim SM and Nicholson LJ. Cancer stem cells: in the line of fire. Cancer Treat Rev. 2012; 38(6):589-598.
9. Miles KA. PET-CT in oncology: making the most of CT. Cancer Imaging. 2008; 8 Spec No A:S87-93.
10. Hanahan D and Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144(5):646-674.
11. Bensinger SJ and Christofk HR. New aspects of the Warburg effect in cancer cell biology. Semin Cell Dev Biol. 2012; 23(4):352-361.
12. Hirschhaeuser F, Sattler UG and Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res. 2011; 71(22):6921-6925.
13. Munoz-Pinedo C, El Mjiyad N and Ricci JE. Cancer metabolism: current perspectives and future directions. Cell Death Dis. 2012; 3:e248.
14. Butler EB, Zhao Y, Munoz-Pinedo C, Lu J and Tan M. Stalling the engine of resistance: targeting cancer metabolism to overcome therapeutic resistance. Cancer Res. 2013; 73(9):2709-2717.
15. Jang M, Kim SS and Lee J. Cancer cell metabolism: implications for therapeutic targets. Exp Mol Med. 2013; 45:e45.
16. Zhao Y, Butler EB and Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis. 2013; 4:e532.
17. Sato A, Sunayama J, Okada M, Watanabe E, Seino S, Shibuya K, Suzuki K, Narita Y, Shibui S, Kayama T and Kitanaka C. Glioma-initiating cell elimination by metformin activation of FOXO3 via AMPK. Stem Cells Transl Med. 2012; 1(11):811-824.
18. Szablewski L. Expression of glucose transporters in cancers. Biochim Biophys Acta. 2013; 1835(2):164-169.
19. Furuta E, Okuda H, Kobayashi A and Watabe K. Metabolic genes in cancer: their roles in tumor progression and clinical implications. Biochim Biophys Acta. 2010; 1805(2):141-152.
20. Ganapathy V, Thangaraju M and Prasad PD. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther. 2009; 121(1):29-40.
21. Macheda ML, Rogers S and Best JD. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol. 2005; 202(3):654-662.
22. Liu Y, Cao Y, Zhang W, Bergmeier S, Qian Y, Akbar H, Colvin R, Ding J, Tong L, Wu S, Hines J and Chen X. A small-molecule inhibitor of glucose transporter 1 downregulates glycolysis, induces cell-cycle arrest, and inhibits cancer cell growth in vitro and in vivo. Mol Cancer Ther. 2012; 11(8):1672-1682.
23. Liu PP, Liao J, Tang ZJ, Wu WJ, Yang J, Zeng ZL, Hu Y, Wang P, Ju HQ, Xu RH and Huang P. Metabolic regulation of cancer cell side population by glucose through activation of the Akt pathway. Cell Death Differ. 2014; 21(1):124-135.
24. Nakano A, Tsuji D, Miki H, Cui Q, El Sayed SM, Ikegame A, Oda A, Amou H, Nakamura S, Harada T, Fujii S, Kagawa K, Takeuchi K, Sakai A, Ozaki S, Okano K, et al. Glycolysis inhibition inactivates ABC transporters to restore drug sensitivity in malignant cells. PLoS One. 2011; 6(11):e27222.
25. Yuan S, Wang F, Chen G, Zhang H, Feng L, Wang L, Colman H, Keating MJ, Li X, Xu RH, Wang J and Huang P. Effective elimination of cancer stem cells by a novel drug combination strategy. Stem Cells. 2013; 31(1):23-34.
26. Zhou Y, Zhou Y, Shingu T, Feng L, Chen Z, Ogasawara M, Keating MJ, Kondo S and Huang P. Metabolic alterations in highly tumorigenic glioblastoma cells: preference for hypoxia and high dependency on glycolysis. J Biol Chem. 2011; 286(37):32843-32853.
27. Flavahan WA, Wu Q, Hitomi M, Rahim N, Kim Y, Sloan AE, Weil RJ, Nakano I, Sarkaria JN, Stringer BW, Day BW, Li M, Lathia JD, Rich JN and Hjelmeland AB. Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake. Nat Neurosci. 2013; 16(10):1373-1382.
28. Isayev O, Rausch V, Bauer N, Liu L, Fan P, Zhang Y, Gladkich J, Nwaeburu CC, Mattern J, Mollenhauer M, Ruckert F, Zach S, Haberkorn U, Gross W, Schonsiegel F, Bazhin AV, et al. Inhibition of glucose turnover by 3-bromopyruvate counteracts pancreatic cancer stem cell features and sensitizes cells to gemcitabine. Oncotarget. 2014; 5(13):5177-5189.
29. DeBerardinis RJ, Lum JJ, Hatzivassiliou G and Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008; 7(1):11-20.
30. Perales-Clemente E, Folmes CD and Terzic A. METABOLIC REGULATION OF REDOX STATUS IN STEM CELLS. Antioxid Redox Signal. 2014.
31. Sato A, Okada M, Shibuya K, Watanabe E, Seino S, Narita Y, Shibui S, Kayama T and Kitanaka C. Pivotal role for ROS activation of p38 MAPK in the control of differentiation and tumor-initiating capacity of glioma-initiating cells. Stem Cell Res. 2014; 12(1):119-131.
32. Patra KC, Wang Q, Bhaskar PT, Miller L, Wang Z, Wheaton W, Chandel N, Laakso M, Muller WJ, Allen EL, Jha AK, Smolen GA, Clasquin MF, Robey RB and Hay N. Hexokinase 2 is required for tumor initiation and maintenance and its systemic deletion is therapeutic in mouse models of cancer. Cancer Cell. 2013; 24(2):213-228.
33. Pereira da Silva AP, El-Bacha T, Kyaw N, dos Santos RS, da-Silva WS, Almeida FC, Da Poian AT and Galina A. Inhibition of energy-producing pathways of HepG2 cells by 3-bromopyruvate. Biochem J. 2009; 417(3):717-726.
34. Okada M, Shibuya K, Sato A, Seino S, Suzuki S, Seino M and Kitanaka C. Targeting the K-Ras-JNK axis eliminates cancer stem-like cells and prevents pancreatic tumor formation. Oncotarget. 2014; 5(13):5100-5112.
35. Seino M, Okada M, Shibuya K, Seino S, Suzuki S, Ohta T, Kurachi H and Kitanaka C. Requirement of JNK Signaling for Self-renewal and Tumor-initiating Capacity of Ovarian Cancer Stem Cells. ANTICANCER RESEARCH. 2014; in press.
36. Wang X, Wang L, Zhu L, Pan Y, Xiao F, Liu W, Wang Z, Guo F, Liu Y, Thomas WG and Chen Y. PAQR3 modulates insulin signaling by shunting phosphoinositide 3-kinase p110alpha to the Golgi apparatus. Diabetes. 2013; 62(2):444-456.