Hexokinase 2 confers resistance to cisplatin in ovarian cancer cells by enhancing cisplatin-induced autophagy

Angioli, 1997, Use of lonidamine to potentiate the effect of cisplatin and carboplatin on platinum resistant human ovarian cancer cells, Int. J. Oncol., 11, 777 Arzoine, 2009, Voltage-dependent anion channel 1-based peptides interact with hexokinase to prevent its anti-apoptotic activity, J. Biol. Chem., 284, 3946, 10.1074/jbc.M803614200 Azoulay-Zohar, 2004, In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death, Biochem. J., 377, 347, 10.1042/bj20031465 Bao, 2015, Induction of autophagy contributes to cisplatin resistance in human ovarian cancer cells, Mol. Med. Rep., 11, 91, 10.3892/mmr.2014.2671 Behrens, 1987, Characterization of a cis-diamminedichloroplatinum(II)-resistant human ovarian cancer cell line and its use in evaluation of platinum analogues, Cancer Res., 47, 414 Cagnol, 2010, ERK and cell death: mechanisms of ERK-induced cell death–apoptosis, autophagy and senescence, FEBS J., 277, 2, 10.1111/j.1742-4658.2009.07366.x Calvino, 2011, Increased apoptotic efficacy of lonidamine plus arsenic trioxide combination in human leukemia cells. Reactive oxygen species generation and defensive protein kinase (MEK/ERK Akt/mTOR) modulation, Biochem. Pharmacol., 82, 1619, 10.1016/j.bcp.2011.08.017 Chen, 2009, Role of mitochondria-associated hexokinase II in cancer cell death induced by 3-bromopyruvate, Biochim. Biophys. Acta, 1787, 553, 10.1016/j.bbabio.2009.03.003 Choi, 2004, Role of ERK activation in cisplatin-induced apoptosis in A172 human glioma cells, Neurotoxicology, 25, 915, 10.1016/j.neuro.2004.06.002 Chuang, 2013, 2-Deoxyglucose treatment complements the cisplatin- or BH3-only mimetic-induced suppression of neuroblastoma cell growth, Int. J. Biochem. Cell Biol., 45, 944, 10.1016/j.biocel.2013.01.019 Ciuffreda, 2010, The mTOR pathway: a new target in cancer therapy, Curr. Cancer Drug Targets, 10, 484, 10.2174/156800910791517172 Cui, 2000, Cisplatin-induced response of c-jun N-terminal kinase 1 and extracellular signal–regulated protein kinases 1 and 2 in a series of cisplatin-resistant ovarian carcinoma cell lines, Mol. Carcinog., 29, 219, 10.1002/1098-2744(200012)29:4<219::AID-MC1004>3.0.CO;2-D De Lena, 1997, Revertant and potentiating activity of lonidamine in patients with ovarian cancer previously treated with platinum, J. Clin. Oncol., 15, 3208, 10.1200/JCO.1997.15.10.3208 De Lena, 2001, Paclitaxel, cisplatin and lonidamine in advanced ovarian cancer. A phase II study, Eur. J. Cancer, 37, 364, 10.1016/S0959-8049(00)00400-7 Falck Miniotis, 2013, MEK1/2 inhibition decreases lactate in BRAF-driven human cancer cells, Cancer Res., 73, 4039, 10.1158/0008-5472.CAN-12-1969 Hayakawa, 1999, Inhibition of extracellular signal-regulated protein kinase or c-Jun N-terminal protein kinase cascade, differentially activated by cisplatin, sensitizes human ovarian cancer cell line, J. Biol. Chem., 274, 31648, 10.1074/jbc.274.44.31648 He, 2015, Downregulation of ATG14 by EGR1-MIR152 sensitizes ovarian cancer cells to cisplatin-induced apoptosis by inhibiting cyto-protective autophagy, Autophagy, 11, 373, 10.1080/15548627.2015.1009781 Hsu, 2008, Cancer cell metabolism: warburg and beyond, Cell, 134, 703, 10.1016/j.cell.2008.08.021 Huang, 2011, Frequent genetic abnormalities of the PI3K/AKT pathway in primary ovarian cancer predict patient outcome, Genes. Chromosomes Cancer, 50, 606, 10.1002/gcc.20883 Jin, 2014, Expression of hexokinase 2 in epithelial ovarian tumors and its clinical significance in serous ovarian cancer, Eur. J. Gynaecol. Oncol., 35, 519 Karam, 2017, Fifth Ovarian Cancer Consensus Conference of the Gynecologic Cancer InterGroup: first-line interventions, Ann. Oncol., 28, 711, 10.1093/annonc/mdx011 Kigawa, 1998, Gamma-glutamyl cysteine synthetase up-regulates glutathione and multidrug resistance-associated protein in patients with chemoresistant epithelial ovarian cancer, Clin. Cancer Res., 4, 1737 Kim, 2011, Combined RNA interference of hexokinase II and (131)I-sodium iodide symporter gene therapy for anaplastic thyroid carcinoma, J. Nucl. Med., 52, 1756, 10.2967/jnumed.111.090266 Krasnov, 2013, Targeting VDAC-bound hexokinase II: a promising approach for concomitant anti-cancer therapy, Expert Opin. Ther. Targets, 17, 1221, 10.1517/14728222.2013.833607 Liang, 2016, Inhibition of autophagy sensitizes MDR-phenotype ovarian cancer SKVCR cells to chemotherapy, Biomed. Pharmacother., 82, 98, 10.1016/j.biopha.2016.04.054 Lu, 2007, The mode of cisplatin-induced cell death in CYP2E1-overexpressing HepG2 cells: modulation by ERK, ROS, glutathione, and thioredoxin, Free Radic. Biol. Med., 43, 1061, 10.1016/j.freeradbiomed.2007.06.021 Luvero, 2014, Treatment options in recurrent ovarian cancer: latest evidence and clinical potential, Ther. Adv. Med. Oncol., 6, 229, 10.1177/1758834014544121 Maschek, 2004, 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, 31, 10.1158/0008-5472.CAN-03-3294 Mathupala, 1997, Aberrant glycolytic metabolism of cancer cells: a remarkable coordination of genetic, transcriptional, post-translational, and mutational events that lead to a critical role for type II hexokinase, J. Bioenerg. Biomembr., 29, 339, 10.1023/A:1022494613613 Mizushima, 2011, Autophagy: renovation of cells and tissues, Cell, 147, 728, 10.1016/j.cell.2011.10.026 Ogier-Denis, 2000, Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells, J. Biol. Chem., 275, 39090, 10.1074/jbc.M006198200 Ozols, 2003, Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a Gynecologic Oncology Group study, J. Clin. Oncol., 21, 3194, 10.1200/JCO.2003.02.153 Pedersen, 2008, Voltage dependent anion channels (VDACs): a brief introduction with a focus on the outer mitochondrial compartment’s roles together with hexokinase-2 in the Warburg effect in cancer, J. Bioenergy Biomembr., 40, 123, 10.1007/s10863-008-9165-7 Persons, 1999, Cisplatin-induced activation of mitogen-activated protein kinases in ovarian carcinoma cells: inhibition of extracellular signal-regulated kinase activity increases sensitivity to cisplatin, Clin. Cancer Res., 5, 1007 Reles, 2001, Correlation of p53 mutations with resistance to platinum-based chemotherapy and shortened survival in ovarian cancer, Clin. Cancer Res., 7, 2984 Roberts, 2014, Hexokinase-II positively regulates glucose starvation-induced autophagy through TORC1 inhibition, Mol. Cell, 53, 521, 10.1016/j.molcel.2013.12.019 Siegel, 2016, Cancer statistics, 2016, CA Cancer J. Clin., 66, 7, 10.3322/caac.21332 Sivaprasad, 2008, Inhibition of ERK attenuates autophagy and potentiates tumour necrosis factor-alpha-induced cell death in MCF-7 cells, J. Cell. Mol. Med., 12, 1265, 10.1111/j.1582-4934.2008.00282.x Spowart, 2012, The autophagy protein LC3A correlates with hypoxia and is a prognostic marker of patient survival in clear cell ovarian cancer, J. Pathol., 228, 437, 10.1002/path.4090 Suh, 2014, Association of overexpression of hexokinase II with chemoresistance in epithelial ovarian cancer, Clin. Exp. Med., 14, 345, 10.1007/s10238-013-0250-9 Sui, 2013, Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment, Cell. Death. Dis., 4, e838, 10.1038/cddis.2013.350 Vartanian, 2016, Targeting hexokinase 2 enhances response to radio-chemotherapy in glioblastoma, Oncotarget, 7, 69518, 10.18632/oncotarget.11680 Wang, 2014, Role of autophagy in cisplatin resistance in ovarian cancer cells, J. Biol. Chem., 289, 17163, 10.1074/jbc.M114.558288 Wang, 2000, Requirement for ERK activation in cisplatin-induced apoptosis, J. Biol. Chem., 275, 39435, 10.1074/jbc.M004583200 Wilson, 2003, Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function, J. Exp. Biol., 206, 2049, 10.1242/jeb.00241 Zhang, 2009, Alterations in the expression of the apurinic/apyrimidinic endonuclease-1/redox factor-1 (APE1/Ref-1) in human ovarian cancer and indentification of the therapeutic potential of APE1/Ref-1 inhibitor, Int. J. Oncol., 35, 1069 Zhi, 2015, Autophagy in cancer, F1000Prime Rep., 7, 18, 10.12703/P7-18