Repeated cisplatin treatment can lead to a multiresistant tumor cell population with stem cell features and sensitivity to 3-bromopyruvate

References

• Tinelli A, Vergara D, Martignago R, Leo G, Pisanò M, Malvasi A. An outlook on ovarian cancer and borderline ovarian tumors: focus on genomic and proteomic findings. Curr Genomics 2009; 10:240 - 9; http://dx.doi.org/10.2174/138920209788488553; PMID: 19949545
   PubMed Web of Science ®Google Scholar
• Landen CN Jr., Birrer MJ, Sood AK. Early events in the pathogenesis of epithelial ovarian cancer. J Clin Oncol 2008; 26:995 - 1005; http://dx.doi.org/10.1200/JCO.2006.07.9970; PMID: 18195328
   PubMed Web of Science ®Google Scholar
• Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 2005; 65:3025 - 9; PMID: 15833827
   PubMed Web of Science ®Google Scholar
• Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008; 68:4311 - 20; http://dx.doi.org/10.1158/0008-5472.CAN-08-0364; PMID: 18519691
   PubMed Web of Science ®Google Scholar
• Landen CN Jr., Goodman B, Katre AA, Steg AD, Nick AM, Stone RL, et al. Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer. Mol Cancer Ther 2010; 9:3186 - 99; http://dx.doi.org/10.1158/1535-7163.MCT-10-0563; PMID: 20889728
   PubMed Web of Science ®Google Scholar
• Steg AD, Bevis KS, Katre AA, Ziebarth A, Dobbin ZC, Alvarez RD, et al. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clin Cancer Res 2012; 18:869 - 81; http://dx.doi.org/10.1158/1078-0432.CCR-11-2188; PMID: 22142828
   PubMed Web of Science ®Google Scholar
• Alison MR, Lin WR, Lim SM, Nicholson LJ. Cancer stem cells: in the line of fire. Cancer Treat Rev 2012; 38:589 - 98; http://dx.doi.org/10.1016/j.ctrv.2012.03.003; PMID: 22469558
   PubMed Web of Science ®Google Scholar
• Luo L, Zeng J, Liang B, Zhao Z, Sun L, Cao D, et al. Ovarian cancer cells with the CD117 phenotype are highly tumorigenic and are related to chemotherapy outcome. Exp Mol Pathol 2011; 91:596 - 602; http://dx.doi.org/10.1016/j.yexmp.2011.06.005; PMID: 21787767
   PubMed Web of Science ®Google Scholar
• Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY, et al. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 2009; 27:2059 - 68; http://dx.doi.org/10.1002/stem.154; PMID: 19544473
   PubMed Web of Science ®Google Scholar
• Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008; 14:79 - 89; http://dx.doi.org/10.1016/j.ccr.2008.06.005; PMID: 18598946
   PubMed Web of Science ®Google Scholar
• Mandic A, Hansson J, Linder S, Shoshan MC. Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J Biol Chem 2003; 278:9100 - 6; http://dx.doi.org/10.1074/jbc.M210284200; PMID: 12509415
   PubMed Web of Science ®Google Scholar
• Kruidering M, Van de Water B, de Heer E, Mulder GJ, Nagelkerke JF. Cisplatin-induced nephrotoxicity in porcine proximal tubular cells: mitochondrial dysfunction by inhibition of complexes I to IV of the respiratory chain. J Pharmacol Exp Ther 1997; 280:638 - 49; PMID: 9023274
   PubMed Web of Science ®Google Scholar
• Berndtsson M, Hägg M, Panaretakis T, Havelka AM, Shoshan MC, Linder S. Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int J Cancer 2007; 120:175 - 80; http://dx.doi.org/10.1002/ijc.22132; PMID: 17044026
   PubMed Web of Science ®Google Scholar
• Dehne N, Lautermann J, Petrat F, Rauen U, de Groot H. Cisplatin ototoxicity: involvement of iron and enhanced formation of superoxide anion radicals. Toxicol Appl Pharmacol 2001; 174:27 - 34; http://dx.doi.org/10.1006/taap.2001.9171; PMID: 11437646
   PubMed Web of Science ®Google Scholar
• Olivero OA, Semino C, Kassim A, Lopez-Larraza DM, Poirier MC. Preferential binding of cisplatin to mitochondrial DNA of Chinese hamster ovary cells. Mutat Res 1995; 346:221 - 30; http://dx.doi.org/10.1016/0165-7992(95)90039-X; PMID: 7753115
   PubMed Web of Science ®Google Scholar
• Podratz JL, Knight AM, Ta LE, Staff NP, Gass JM, Genelin K, et al. Cisplatin induced mitochondrial DNA damage in dorsal root ganglion neurons. Neurobiol Dis 2011; 41:661 - 8; http://dx.doi.org/10.1016/j.nbd.2010.11.017; PMID: 21145397
   PubMed Web of Science ®Google Scholar
• Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 2008; 320:661 - 4; http://dx.doi.org/10.1126/science.1156906; PMID: 18388260
   PubMed Web of Science ®Google Scholar
• Brandon M, Baldi P, Wallace DC. Mitochondrial mutations in cancer. Oncogene 2006; 25:4647 - 62; http://dx.doi.org/10.1038/sj.onc.1209607; PMID: 16892079
   PubMed Web of Science ®Google Scholar
• Lu J, Sharma LK, Bai Y. Implications of mitochondrial DNA mutations and mitochondrial dysfunction in tumorigenesis. Cell Res 2009; 19:802 - 15; http://dx.doi.org/10.1038/cr.2009.69; PMID: 19532122
   PubMed Web of Science ®Google Scholar
• Varum S, Momcilović O, Castro C, Ben-Yehudah A, Ramalho-Santos J, Navara CS. Enhancement of human embryonic stem cell pluripotency through inhibition of the mitochondrial respiratory chain. Stem Cell Res 2009; 3:142 - 56; http://dx.doi.org/10.1016/j.scr.2009.07.002; PMID: 19716358
   PubMed Web of Science ®Google Scholar
• Amuthan G, Biswas G, Ananadatheerthavarada HK, Vijayasarathy C, Shephard HM, Avadhani NG. Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells. Oncogene 2002; 21:7839 - 49; http://dx.doi.org/10.1038/sj.onc.1205983; PMID: 12420221
   PubMed Web of Science ®Google Scholar
• Moro L, Arbini AA, Yao JL, di Sant’Agnese PA, Marra E, Greco M. Mitochondrial DNA depletion in prostate epithelial cells promotes anoikis resistance and invasion through activation of PI3K/Akt2. Cell Death Differ 2009; 16:571 - 83; http://dx.doi.org/10.1038/cdd.2008.178; PMID: 19079138
   PubMed Web of Science ®Google Scholar
• Naito A, Cook CC, Mizumachi T, Wang M, Xie CH, Evans TT, et al. Progressive tumor features accompany epithelial-mesenchymal transition induced in mitochondrial DNA-depleted cells. Cancer Sci 2008; 99:1584 - 8; http://dx.doi.org/10.1111/j.1349-7006.2008.00879.x; PMID: 18754870
   PubMed Web of Science ®Google Scholar
• Scatena R. Mitochondria and cancer: a growing role in apoptosis, cancer cell metabolism and dedifferentiation. Adv Exp Med Biol 2012; 942:287 - 308; http://dx.doi.org/10.1007/978-94-007-2869-1_13; PMID: 22399428
   PubMed Web of Science ®Google Scholar
• Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133:704 - 15; http://dx.doi.org/10.1016/j.cell.2008.03.027; PMID: 18485877
   PubMed Web of Science ®Google Scholar
• Morel AP, Lièvre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008; 3:e2888; http://dx.doi.org/10.1371/journal.pone.0002888; PMID: 18682804
   PubMed Web of Science ®Google Scholar
• Hernlund E, Hjerpe E, Avall-Lundqvist E, Shoshan M. Ovarian carcinoma cells with low levels of beta-F1-ATPase are sensitive to combined platinum and 2-deoxy-D-glucose treatment. Mol Cancer Ther 2009; 8:1916 - 23; http://dx.doi.org/10.1158/1535-7163.MCT-09-0179; PMID: 19567816
   PubMed Web of Science ®Google Scholar
• Björklund M, Roos J, Gogvadze V, Shoshan M. Resveratrol induces SIRT1- and energy-stress-independent inhibition of tumor cell regrowth after low-dose platinum treatment. Cancer Chemother Pharmacol 2011; 68:1459 - 67; http://dx.doi.org/10.1007/s00280-011-1640-x; PMID: 21479886
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V, Israelson A, Brdiczka D, Sheu SS. The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr Pharm Des 2006; 12:2249 - 70; http://dx.doi.org/10.2174/138161206777585111; PMID: 16787253
   PubMed Web of Science ®Google Scholar
• Pastorino JG, Shulga N, Hoek JB. Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J Biol Chem 2002; 277:7610 - 8; http://dx.doi.org/10.1074/jbc.M109950200; PMID: 11751859
   PubMed Web of Science ®Google Scholar
• Mathupala SP, Ko YH, Pedersen PL. Hexokinase II: cancer’s double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 2006; 25:4777 - 86; http://dx.doi.org/10.1038/sj.onc.1209603; PMID: 16892090
   PubMed Web of Science ®Google Scholar
• Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001; 344:1031 - 7; http://dx.doi.org/10.1056/NEJM200104053441401; PMID: 11287972
   PubMed Web of Science ®Google Scholar
• Tang SN, Fu J, Nall D, Rodova M, Shankar S, Srivastava RK. Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics. Int J Cancer 2011; 131:30 - 40; PMID: 21796625
   PubMed Web of Science ®Google Scholar
• Björklund M, Roos J, Gogvadze V, Shoshan M. Resveratrol induces SIRT1- and energy-stress-independent inhibition of tumor cell regrowth after low-dose platinum treatment. Cancer Chemother Pharmacol 2011; 68:1459 - 67; http://dx.doi.org/10.1007/s00280-011-1640-x; PMID: 21479886
   PubMed Web of Science ®Google Scholar
• Chen Z, Zhang H, Lu W, Huang P. Role of mitochondria-associated hexokinase II in cancer cell death induced by 3-bromopyruvate. Biochim Biophys Acta 2009; 1787:553 - 60; http://dx.doi.org/10.1016/j.bbabio.2009.03.003; PMID: 19285479
   PubMed Web of Science ®Google Scholar
• Shoshan MC. 3-Bromopyruvate: targets and outcomes. J Bioenerg Biomembr 2012; 44:7 - 15; http://dx.doi.org/10.1007/s10863-012-9419-2; PMID: 22298255
   PubMed Web of Science ®Google Scholar
• Latifi A, Abubaker K, Castrechini N, Ward AC, Liongue C, Dobill F, et al. Cisplatin treatment of primary and metastatic epithelial ovarian carcinomas generates residual cells with mesenchymal stem cell-like profile. J Cell Biochem 2011; 112:2850 - 64; http://dx.doi.org/10.1002/jcb.23199; PMID: 21618587
   PubMed Web of Science ®Google Scholar
• Kryczek I, Liu S, Roh M, Vatan L, Szeliga W, Wei S, et al. Expression of aldehyde dehydrogenase and CD133 defines ovarian cancer stem cells. Int J Cancer 2012; 130:29 - 39; http://dx.doi.org/10.1002/ijc.25967; PMID: 21480217
   PubMed Web of Science ®Google Scholar
• Wang YC, Yo YT, Lee HY, Liao YP, Chao TK, Su PH, et al. ALDH1-bright epithelial ovarian cancer cells are associated with CD44 expression, drug resistance, and poor clinical outcome. Am J Pathol 2012; 180:1159 - 69; http://dx.doi.org/10.1016/j.ajpath.2011.11.015; PMID: 22222226
   PubMed Web of Science ®Google Scholar
• Ye XQ, Li Q, Wang GH, Sun FF, Huang GJ, Bian XW, et al. Mitochondrial and energy metabolism-related properties as novel indicators of lung cancer stem cells. Int J Cancer 2011; 129:820 - 31; http://dx.doi.org/10.1002/ijc.25944; PMID: 21520032
   PubMed Web of Science ®Google Scholar
• Rehman J. Empowering self-renewal and differentiation: the role of mitochondria in stem cells. J Mol Med (Berl) 2010; 88:981 - 6; http://dx.doi.org/10.1007/s00109-010-0678-2; PMID: 20809088
   PubMed Web of Science ®Google Scholar
• Gao XN, Lin J, Gao L, Li YH, Wang LL, Yu L. MicroRNA-193b regulates c-Kit proto-oncogene and represses cell proliferation in acute myeloid leukemia. Leuk Res 2011; 35:1226 - 32; http://dx.doi.org/10.1016/j.leukres.2011.06.010; PMID: 21724256
   PubMed Web of Science ®Google Scholar
• Smiraglia DJ, Kulawiec M, Bistulfi GL, Gupta SG, Singh KK. A novel role for mitochondria in regulating epigenetic modification in the nucleus. Cancer Biol Ther 2008; 7:1182 - 90; http://dx.doi.org/10.4161/cbt.7.8.6215; PMID: 18458531
   PubMed Web of Science ®Google Scholar
• Brozovic A, Osmak M. Activation of mitogen-activated protein kinases by cisplatin and their role in cisplatin-resistance. Cancer Lett 2007; 251:1 - 16; http://dx.doi.org/10.1016/j.canlet.2006.10.007; PMID: 17125914
   PubMed Web of Science ®Google Scholar
• Mathupala SP, Ko YH, Pedersen PL. Hexokinase-2 bound to mitochondria: cancer’s stygian link to the “Warburg Effect” and a pivotal target for effective therapy. Semin Cancer Biol 2009; 19:17 - 24; http://dx.doi.org/10.1016/j.semcancer.2008.11.006; PMID: 19101634
   PubMed Web of Science ®Google Scholar
• Ihrlund LS, Hernlund E, Khan O, Shoshan MC. 3-Bromopyruvate as inhibitor of tumour cell energy metabolism and chemopotentiator of platinum drugs. Mol Oncol 2008; 2:94 - 101; http://dx.doi.org/10.1016/j.molonc.2008.01.003; PMID: 19383331
   PubMed Web of Science ®Google Scholar
• Shulga N, Wilson-Smith R, Pastorino JG. Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria. J Cell Sci 2010; 123:894 - 902; http://dx.doi.org/10.1242/jcs.061846; PMID: 20159966
   PubMed Web of Science ®Google Scholar
• Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CA 4th, Ramalho-Santos J, et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 2011; 6:e20914; http://dx.doi.org/10.1371/journal.pone.0020914; PMID: 21698063
   PubMed Web of Science ®Google Scholar
• Gong L, Cui Z, Yu X, Wei Y, Peng J, Leng X. Hexokinase II in CD133+ and CD133- hepatoma BEL-7402 Cells. Pathol Oncol Res 2012; 18:377 - 81; http://dx.doi.org/10.1007/s12253-011-9455-y; PMID: 21909686
   PubMed Web of Science ®Google Scholar