Targeting glucose metabolism in cancer: a new class of agents for loco-regional and systemic therapy of liver cancer and beyond?

References

• Forner A , LlovetJM, BruixJ. Hepatocellular carcinoma. Lancet379(9822), 1245–1255 (2012).
   PubMed Web of Science ®Google Scholar
• Yau T , TangVY, YaoTJ, FanST, LoCM, PoonRT. Development of Hong Kong Liver Cancer staging system with treatment stratification for patients with hepatocellular carcinoma. Gastroenterology146(7), 1691–1700; e1693 (2014).
   PubMed Web of Science ®Google Scholar
• Forner A , GilabertM, BruixJ, RaoulJL. Treatment of intermediate-stage hepatocellular carcinoma. Nat. Rev. Clin. Oncol.11(9), 525–535 (2014).
   PubMed Web of Science ®Google Scholar
• Chapiro J , TacherV, GeschwindJF. intra-arterial therapies for primary liver cancer: state of the art. Expert Rev. Anticancer Ther.13(10), 1157–1167 (2013).
   PubMed Web of Science ®Google Scholar
• Lewandowski RJ , GeschwindJF, LiapiE, SalemR. Transcatheter intra-arterial therapies: rationale and overview. Radiology259(3), 641–657 (2011).
   PubMed Web of Science ®Google Scholar
• Otto G , SchuchmannM, Hoppe-LotichiusMet al. How to decide about liver transplantation in patients with hepatocellular carcinoma: size and number of lesions or response to TACE? J. Hepatol. 59(2), 279–284 (2013).
   PubMed Web of Science ®Google Scholar
• Warburg O . On respiratory impairment in cancer cells. Science124(3215), 269–270 (1956).
   PubMed Web of Science ®Google Scholar
• Lunt SY , Vander HeidenMG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu. Rev. Cell. Dev. Biol.27, 441–464 (2011).
   PubMed Web of Science ®Google Scholar
• Hanahan D , WeinbergRA. Hallmarks of cancer: the next generation. Cell144(5), 646–674 (2011).
   PubMed Web of Science ®Google Scholar
• Amann T , MaegdefrauU, HartmannAet al. GLUT1 expression is increased in hepatocellular carcinoma and promotes tumorigenesis. Am. J. Pathol.174(4), 1544–1552 (2009).
   PubMed Web of Science ®Google Scholar
• Poon E , HarrisAL, AshcroftM. Targeting the hypoxia-inducible factor (HIF) pathway in cancer. Expert Rev. Mol. Med.11, e26 (2009).
   PubMed Web of Science ®Google Scholar
• Semenza GL . HIF-1: upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev.20(1), 51–56 (2010).
   PubMed Web of Science ®Google Scholar
• Luo W , SemenzaGL. Pyruvate kinase M2 regulates glucose metabolism by functioning as a coactivator for hypoxia-inducible factor 1 in cancer cells. Oncotarget2(7), 551–556 (2011).
   PubMedGoogle Scholar
• Végran F , BoidotR, MichielsC, SonveauxP, FeronO. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF- κ B/IL–8 pathway that drives tumor angiogenesis. Cancer Res.71(7), 2550–2560 (2011).
   PubMed Web of Science ®Google Scholar
• Gao HJ , ZhaoMC, ZhangYJet al. Monocarboxylate transporter 4 predicts poor prognosis in hepatocellular carcinoma and is associated with cell proliferation and migration. J. Cancer Res. Clin. Oncol.141(7), 1151–1162 (2015).
   PubMed Web of Science ®Google Scholar
• Ganapathy-Kanniappan S , GeschwindJF. Tumor glycolysis as a target for cancer therapy: progress and prospects. Mol. Cancer12, 152 (2013).
   PubMed Web of Science ®Google Scholar
• Jang M , KimSS, LeeJ. Cancer cell metabolism: implications for therapeutic targets. Exp. Mol. Med.45, e45 (2013).
   PubMed Web of Science ®Google Scholar
• Crane RK , SolsA. The non-competitive inhibition of brain hexokinase by glucose-6-phosphate and related compounds. J. Biol. Chem.210(2), 597–606 (1954).
   PubMed Web of Science ®Google Scholar
• Dwarakanath B , JainV. Targeting glucose metabolism with 2-deoxy-D-glucose for improving cancer therapy. Future Oncol.5(5), 581–585 (2009).
   PubMed Web of Science ®Google Scholar
• Maher JC , KrishanA, LampidisTJ. Greater cell cycle inhibition and cytotoxicity induced by 2-deoxy-D-glucose in tumor cells treated under hypoxic vs aerobic conditions. Cancer Chemother. Pharmacol.53(2), 116–122 (2004).
   PubMed Web of Science ®Google Scholar
• Zhang D , LiJ, WangF, HuJ, WangS, SunY. 2-Deoxy-D-glucose targeting of glucose metabolism in cancer cells as a potential therapy. Cancer Lett.355(2), 176–183 (2014).
   PubMed Web of Science ®Google Scholar
• Song HJ , ChengJY, HuSL, ZhangGY, FuY, ZhangYJ. Value of 18F-FDG PET/CT in detecting viable tumor and predicting prognosis of hepatocellular carcinoma after TACE. Clin. Radiol.70(2), 128–137 (2015).
   PubMed Web of Science ®Google Scholar
• Stokkel MP , DraismaA, PauwelsEK. Positron emission tomography with 2-[18F]-fluoro-2-deoxy-D-glucose in oncology. Part IIIb: Therapy response monitoring in colorectal and lung tumors, head and neck cancer, hepatocellular carcinoma and sarcoma. J. Cancer Res. Clin. Oncol.127(5), 278–285 (2001).
   PubMed Web of Science ®Google Scholar
• Laszlo J , HumphreysSR, GoldinA. Effects of glucose analogues (2-deoxy-D-glucose, 2-deoxy-D-galactose) on experimental tumors. J. Natl Cancer Inst.24, 267–281 (1960).
   PubMedGoogle Scholar
• Wang Z , ZhangL, ZhangD, SunR, WangQ, LiuX. Glycolysis inhibitor 2-deoxy-D-glucose suppresses carcinogen-induced rat hepatocarcinogenesis by restricting cancer cell metabolism. Mol. Med. Rep.11(3), 1917–1924 (2015).
   PubMed Web of Science ®Google Scholar
• Vijayaraghavan R , KumarD, DubeSNet al. Acute toxicity and cardio-respiratory effects of 2-deoxy-D-glucose: a promising radio sensitiser. Biomed. Environ. Sci.19(2), 96–103 (2006).
   PubMed Web of Science ®Google Scholar
• Landau BR , LaszloJ, StengleJ, BurkD. Certain metabolic and pharmacologic effects in cancer patients given infusions of 2-deoxy-D-glucose. J. Natl Cancer Inst.21(3), 485–494 (1958).
   PubMed Web of Science ®Google Scholar
• Stein M , LinH, JeyamohanCet al. Targeting tumor metabolism with 2-deoxyglucose in patients with castrate-resistant prostate cancer and advanced malignancies. Prostate70(13), 1388–1394 (2010).
   PubMed Web of Science ®Google Scholar
• Raez LE , PapadopoulosK, RicartADet al. A phase I dose-escalation trial of 2-deoxy-D-glucose alone or combined with docetaxel in patients with advanced solid tumors. Cancer Chemother. Pharmacol.71(2), 523–530 (2013).
   PubMed Web of Science ®Google Scholar
• Takemura A , CheXF, TabuchiT, MoriyaS, MiyazawaK, TomodaA. Enhancement of cytotoxic and pro-apoptotic effects of 2-aminophenoxazine-3-one on the rat hepatocellular carcinoma cell line dRLh-84, the human hepatocellular carcinoma cell line HepG2, and the rat normal hepatocellular cell line RLN-10 in combination with 2-deoxy-D-glucose. Oncol. Rep.27(2), 347–355 (2012).
   PubMed Web of Science ®Google Scholar
• Kalia VK , PrabhakaraS, NarayananV. Modulation of cellular radiation responses by 2-deoxy-D-glucose and other glycolytic inhibitors: implications for cancer therapy. J. Cancer Res. Ther.5(Suppl. 1), S57–S60 (2009).
   PubMedGoogle Scholar
• Dwarakanath BS , SinghD, BanerjiAKet al. Clinical studies for improving radiotherapy with 2-deoxy-D-glucose: present status and future prospects. J. Cancer Res. Ther.5(Suppl. 1), S21–S26 (2009).
   PubMed Web of Science ®Google Scholar
• Dwarakanath BS , SinghS, JainV. Optimization of tumor radiotherapy: part V-radiosensitization by 2-deoxy-D-glucose and DNA ligand Hoechst–33342 in a murine tumor. Indian J. Exp. Biol.37(9), 865–870 (1999).
   PubMedGoogle Scholar
• Aghaee F , Pirayesh IslamianJ, BaradaranB. Enhanced radiosensitivity and chemosensitivity of breast cancer cells by 2-deoxy-D-glucose in combination therapy. J. Breast Cancer15(2), 141–147 (2012).
   PubMed Web of Science ®Google Scholar
• Mohanti BK , RathGK, AnanthaNet al. Improving cancer radiotherapy with 2-deoxy-D-glucose: Phase I/II clinical trials on human cerebral gliomas. Int. J. Radiat. Oncol. Biol. Phys.35(1), 103–111 (1996).
   PubMed Web of Science ®Google Scholar
• Singh D , BanerjiAK, DwarakanathBSet al. Optimizing cancer radiotherapy with 2-deoxy-D-glucose dose escalation studies in patients with glioblastoma multiforme. Strahlenther. Onkol.181(8), 507–514 (2005).
   PubMed Web of Science ®Google Scholar
• Prasanna VK , VenkataramanaNK, DwarakanathBS, SanthoshV. Differential responses of tumors and normal brain to the combined treatment of 2-DG and radiation in glioablastoma. J. Cancer Res. Ther.5(Suppl. 1), S44–S47 (2009).
   PubMed Web of Science ®Google Scholar
• Venkataramanaa NK , VenkateshPK, DwarakanathBS, VaniS. Protective effect on normal brain tissue during a combinational therapy of 2-deoxy-D-glucose and hypofractionated irradiation in malignant gliomas. Asian. J. Neurosurg.8(1), 9–14 (2013).
   PubMedGoogle Scholar
• Coude FX , SaudubrayJM, DemaugreF, MarsacC, LerouxJP, CharpentierC. Dichloroacetate as treatment for congenital lactic acidosis. N. Engl. J. Med.299(24), 1365–1366 (1978).
   PubMed Web of Science ®Google Scholar
• Kankotia S , StacpoolePW. Dichloroacetate and cancer: new home for an orphan drug?Biochim. Biophys. Acta1846(2), 617–629 (2014).
   PubMed Web of Science ®Google Scholar
• Bonnet S , ArcherSL, Allalunis-TurnerJet al. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell11(1), 37–51 (2007).
   PubMed Web of Science ®Google Scholar
• Vella S , ContiM, TassoR, CanceddaR, PaganoA. Dichloroacetate inhibits neuroblastoma growth by specifically acting against malignant undifferentiated cells. Int. J. Cancer130(7), 1484–1493 (2012).
   PubMed Web of Science ®Google Scholar
• Feuerecker B , SeidlC, PirsigS, BrucheltG, Senekowitsch-SchmidtkeR. DCA promotes progression of neuroblastoma tumors in nude mice. Am. J. Cancer Res.5(2), 812–820 (2015).
   PubMed Web of Science ®Google Scholar
• Dunbar EM , CoatsBS, ShroadsALet al. Phase 1 trial of dichloroacetate (DCA) in adults with recurrent malignant brain tumors. Invest. New Drugs32(3), 452–464 (2014).
   PubMed Web of Science ®Google Scholar
• Chu QS , SanghaR, SpratlinJet al. A phase I open-labeled, single-arm, dose-escalation, study of dichloroacetate (DCA) in patients with advanced solid tumors. Invest. New Drugs33(3), 603–610 (2015).
   PubMed Web of Science ®Google Scholar
• Shen YC , OuDL, HsuCet al. Activating oxidative phosphorylation by a pyruvate dehydrogenase kinase inhibitor overcomes sorafenib resistance of hepatocellular carcinoma. Br. J. Cancer108(1), 72–81 (2013).
   PubMed Web of Science ®Google Scholar
• Dai Y , XiongX, HuangGet al. Dichloroacetate enhances adriamycin-induced hepatoma cell toxicity in vitro and in vivo by increasing reactive oxygen species levels. PLoS ONE9(4), e92962 (2014).
   PubMed Web of Science ®Google Scholar
• Barnard JP , ReynafarjeB, PedersenPL. Glucose catabolism in African trypanosomes. Evidence that the terminal step is catalyzed by a pyruvate transporter capable of facilitating uptake of toxic analogs. J. Biol. Chem.268(5), 3654–3661 (1993).
   PubMed Web of Science ®Google Scholar
• Ganapathy-Kanniappan S , GeschwindJF, KunjithapathamRet al. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is pyruvylated during 3-bromopyruvate mediated cancer cell death. Anticancer Res.29(12), 4909–4918 (2009).
   PubMed Web of Science ®Google Scholar
• Ganapathy-Kanniappan S , KunjithapathamR, GeschwindJF. Glyceraldehyde-3-phosphate dehydrogenase: a promising target for molecular therapy in hepatocellular carcinoma. Oncotarget3(9), 940–953 (2012).
   PubMedGoogle Scholar
• Zhou Y , YiX, StofferJBet al. The multifunctional protein glyceraldehyde–3–phosphate dehydrogenase is both regulated and controls colony-stimulating factor-1 messenger RNA stability in ovarian cancer. Mol. Cancer Res.6(8), 1375–1384 (2008).
   PubMed Web of Science ®Google Scholar
• Wintzell M , LöfstedtL, JohanssonJ, PedersenAB, FuxeJ, ShoshanM. Repeated cisplatin treatment can lead to a multiresistant tumor cell population with stem cell features and sensitivity to 3-Bromopyruvate. Cancer Biol. Ther.13(14), 1454–1462 (2012).
   PubMed Web of Science ®Google Scholar
• Nakano A , TsujiD, MikiHet al. Glycolysis inhibition inactivates ABC transporters to restore drug sensitivity in malignant cells. PLoS ONE6(11), e27222 (2011).
   PubMed Web of Science ®Google Scholar
• Ihrlund LS , HernlundE, KhanO, ShoshanMC. 3-Bromopyruvate as inhibitor of tumor cell energy metabolism and chemopotentiator of platinum drugs. Mol. Oncol.2(1), 94–101 (2008).
   PubMed Web of Science ®Google Scholar
• Cao X , JiaG, ZhangTet al. Non-invasive MRI tumor imaging and synergistic anticancer effect of HSP90 inhibitor and glycolysis inhibitor in RIP1-Tag2 transgenic pancreatic tumor model. Cancer Chemother. Pharmacol.62(6), 985–994 (2008).
   PubMed Web of Science ®Google Scholar
• Pereira Da Silva AP , El-BachaT, KyawNet al. Inhibition of energy-producing pathways of HepG2 cells by 3-bromopyruvate. Biochem. J.417(3), 717–726 (2009).
   PubMedGoogle Scholar
• Ganapathy-Kanniappan S , GeschwindJ-FH. 3-Bromopyruvate induces endoplasmic reticulum stress, overcomes autophagy and causes apoptosis in human HCC cell lines. Anticancer Res.30, 923–936 (2010).
   PubMed Web of Science ®Google Scholar
• Kim JS , AhnKJ, KimJAet al. Role of reactive oxygen species-mediated mitochondrial dysregulation in 3-bromopyruvate induced cell death in hepatoma cells : ROS-mediated cell death by 3-BrPA. J. Bioenerg. Biomembr.40(6), 607–618 (2008).
   PubMed Web of Science ®Google Scholar
• Ganapathy-Kanniappan S , KunjithapathamR, GeschwindJF. Anticancer efficacy of the metabolic blocker 3-bromopyruvate: specific molecular targeting. Anticancer Res.33(1), 13–20 (2013).
   PubMed Web of Science ®Google Scholar
• Birsoy K , WangT, PossematoRet al. MCT1-mediated transport of a toxic molecule is an effective strategy for targeting glycolytic tumors. Nat. Genet.45(1), 104–108 (2013).
   PubMed Web of Science ®Google Scholar
• Ko YH , PedersenPL, GeschwindJF. Glucose catabolism in the rabbit VX2 tumor model for liver cancer: characterization and targeting hexokinase. Cancer Lett.173(1), 83–91 (2001).
   PubMed Web of Science ®Google Scholar
• Liapi E , GeschwindJF. Interventional oncology: new options for interstitial treatments and intravascular approaches: targeting tumor metabolism via a loco-regional approach: a new therapy against liver cancer. J. Hepatobiliary Pancreat. Sci.17(4), 405–406 (2010).
   PubMed Web of Science ®Google Scholar
• Ota S , GeschwindJF, BuijsM, WijlemansJW, KwakBK, Ganapathy-KanniappanS. Ultrasound-guided direct delivery of 3-Bromopyruvate blocks tumor progression in an orthotopic mouse model of human pancreatic cancer. Target. Oncol.8(2), 145–151 (2013).
   PubMed Web of Science ®Google Scholar
• Buijs M , WijlemansJW, KwakBK, OtaS, GeschwindJF. Antiglycolytic Therapy combined with an image-guided minimally invasive delivery strategy for the treatment of breast cancer. J. Vasc. Interv. Radiol.24(5), 737–743 (2013).
   PubMed Web of Science ®Google Scholar
• Geschwind JF , KoYH, TorbensonMS, MageeC, PedersenPL. Novel therapy for liver cancer: direct intra-arterial injection of a potent inhibitor of ATP production. Cancer Res.62(14), 3909–3913 (2002).
   PubMed Web of Science ®Google Scholar
• Vali M , LiapiE, KowalskiJet al. intra-arterial therapy with a new potent inhibitor of tumor metabolism (3-bromopyruvate): identification of therapeutic dose and method of injection in an animal model of liver cancer. J. Vasc. Interv. Radiol.18(1 Pt 1), 95–101 (2007).
   PubMed Web of Science ®Google Scholar
• Vali M , VossenJA, BuijsMet al. Targeting of VX2 rabbit liver tumor by selective delivery of 3-bromopyruvate: a biodistribution and survival study. J. Pharmacol. Exp. Ther.327(1), 32–37 (2008).
   PubMed Web of Science ®Google Scholar
• Ko YH , SmithBL, WangYet al. Advanced cancers: eradication in all cases using 3-bromopyruvate therapy to deplete ATP. Biochem. Biophys. Res. Commun.324(1), 269–275 (2004).
   PubMed Web of Science ®Google Scholar
• Ganapathy-Kanniappan S , KunjithapathamR, TorbensonMSet al. Human hepatocellular carcinoma in a mouse model: assessment of tumor response to percutaneous ablation by using glyceraldehyde-3-phosphate dehydrogenase antagonists. Radiology262(3), 834–845 (2012).
   PubMed Web of Science ®Google Scholar
• Vossen JA , BuijsM, SyedLet al. Development of a new orthotopic animal model of metastatic liver cancer in the rabbit VX2 model: effect on metastases after partial hepatectomy, intra-arterial treatment with 3-bromopyruvate and chemoembolization. Clin. Exp. Metastasis25(7), 811–817 (2008).
   PubMed Web of Science ®Google Scholar
• Liapi E , GeschwindJF, ValiMet al. Assessment of tumoricidal efficacy and response to treatment with 18F-FDG PET/CT after intra-arterial infusion with the antiglycolytic agent 3-bromopyruvate in the VX2 model of liver tumor. J. Nucl. Med.52(2), 225–230 (2011).
   PubMed Web of Science ®Google Scholar
• Prescience Labs L . PreScience Labs announced that the FDA accepts IND application for novel oncology drug (2013). http://presciencelabs.com/prescience-labs-investors/press.php.
   Google Scholar
• Chapiro J , SurS, SavicLJet al. Systemic delivery of microencapsulated 3-bromopyruvate for the therapy of pancreatic cancer. Clin. Cancer Res.20(24), 6406–6417 (2014).
   PubMed Web of Science ®Google Scholar