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Review Article

Cancer stem cells and radioresistance

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Pages 615-621 | Received 07 Oct 2013, Accepted 28 Jan 2014, Published online: 07 Mar 2014

References

  • Ahmed KM, Nantajit D, Fan M, Murley JS, Grdina DJ, Li JJ. 2009. Coactivation of ATM/ERK/NF-kappaB in the low-dose radiation-induced radioadaptive response in human skin keratinocytes. Free Radic Biol Med 46:1543–1550.
  • Bao S, Wu Q, Mclendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. 2006a. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760.
  • Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, Mclendon RE, Bigner DD, Rich JN. 2006b. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843–7848.
  • Baumann M, Krause M, Hill R. 2008. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 8:545–854.
  • Bhat KP, Balasubramaniyan V, Vaillant B, Ezhilarasan R, Hummelink K, Hollingsworth F, Wani K, Heathcock L, James JD, Goodman LD, Conroy S, Long L, Lelic N, Wang S, Gumin J, Raj D, Kodama Y, Raghunathan A, Olar A, Joshi K, Pelloski CE, Heimberger A, Kim SH, Cahill DP, Rao G, Den Dunnen WF, Boddeke HW, Phillips HS, Nakano I, Lang FF, Colman H, Sulman EP, Aldape K. 2013. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell 24:331–346.
  • Bonnet D, Dick JE. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3:730–737.
  • Cao N, Li S, Wang Z, Ahmed KM, Degnan ME, Fan M, Dynlacht JR, Li JJ. 2009. NF-kappaB-mediated HER2 overexpression in radiation-adaptive resistance. Radiat Res 171:9–21.
  • Chen J, Li Y, Yu TS, Mckay RM, Burns DK, Kernie SG, Parada LF. 2012. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488:522–526.
  • Cheng L, Wu Q, Huang Z, Guryanova OA, Huang Q, Shou W, Rich JN, Bao S. 2011. L1CAM regulates DNA damage checkpoint response of glioblastoma stem cells through NBS1. Embo J 30:800–813.
  • Clarke M, Collins R, Darby S, Davies C, Elphinstone P, Evans E, Godwin J, Gray R, Hicks C, James S, Mackinnon E, Mcgale P, Mchugh T, Peto R, Taylor C, Wang Y. 2005. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: An overview of the randomised trials. Lancet 366:2087–2106.
  • Danial NN, Korsmeyer SJ. 2004. Cell death: Critical control points. Cell 116:205–219.
  • Diehn M, Cho RW, Clarke MF. 2009a. Therapeutic implications of the cancer stem cell hypothesis. Semin Radiat Oncol 19:78–86.
  • Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, Clarke MF. 2009b. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458:780–783.
  • Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. 2012. Defining the mode of tumour growth by clonal analysis. Nature 488:527–530.
  • Duru N, Fan M, Candas D, Menaa C, Liu HC, Nantajit D, Wen Y, Xiao K, Eldridge A, Chromy BA, Li S, Spitz DR, Lam KS, Wicha MS, Li JJ. 2012. HER2-associated radioresistance of breast cancer stem cells isolated from HER2-negative breast cancer cells. Clin Cancer Res 18:6634–6647.
  • Eyler CE, Rich JN. 2008. Survival of the fittest: Cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 26:2839–2845.
  • Facchino S, Abdouh M, Chatoo W, Bernier G. 2010. BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J Neurosci 30:10096–10111.
  • Fassl A, Tagscherer KE, Richter J, Berriel Diaz M, Alcantara Llaguno SR, Campos B, Kopitz J, Herold-Mende C, Herzig S, Schmidt MH, Parada LF, Wiestler OD, Roth W. 2012. Notch1 signaling promotes survival of glioblastoma cells via EGFR-mediated induction of anti-apoptotic Mcl-1. Oncogene 31:4698–4708.
  • Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A. 2004. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64:7011–7021.
  • Gebski V, Lagleva M, Keech A, Simes J, Langlands AO. 2006. Survival effects of postmastectomy adjuvant radiation therapy using biologically equivalent doses: A clinical perspective. J Natl Cancer Inst 98:26–38.
  • Griner EM, Kazanietz MG. 2007. Protein kinase C and other diacylglycerol effectors in cancer. Nat Rev Cancer 7:281–294.
  • Gupta PB, Chaffer CL, Weinberg RA. 2009. Cancer stem cells: Mirage or reality?Nat Med 15:1010–1012.
  • Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K, Holland EC. 2008. PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 22:436–448.
  • Hardee ME, Marciscano AE, Medina-Ramirez CM, Zagzag D, Narayana A, Lonning SM, Barcellos-Hoff MH. 2012. Resistance of glioblastoma-initiating cells to radiation mediated by the tumor microenvironment can be abolished by inhibiting transforming growth factor-β. Cancer Res 72:4119–4129.
  • Hegi ME, Diserens AC, Gorlia T, Hamou MF, De Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R. 2005. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003.
  • Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI. 2003. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 100:15178–15183.
  • Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. 2003. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF- 2alpha in hypoxic gene regulation. Mol Cell Biol 23:9361–9374.
  • Huang PH, Cavenee WK, Furnari FB, White FM. 2007. Uncovering therapeutic targets for glioblastoma: A systems biology approach. Cell Cycle 6:2750–2754.
  • Jordan CT, Guzman ML, Noble M. 2006. Cancer stem cells. N Engl J Med, 355:1253–1261.
  • Kang MK, Hur BI, Ko MH, Kim CH, Cha SH, Kang SK. 2008. Potential identity of multi-potential cancer stem-like subpopulation after radiation of cultured brain glioma. BMC Neurosci 9:15.
  • Keith B, Simon MC. 2007. Hypoxia-inducible factors, stem cells, and cancer. Cell 129:465–472.
  • Kim JJ, Tannock IF. 2005. Repopulation of cancer cells during therapy: An important cause of treatment failure. Nat Rev Cancer 5:516–525.
  • Kim MJ, Kim RK, Yoon CH, An S, Hwang SG, Suh Y, Park MJ, Chung HY, Kim IG, Lee SJ. 2011. Importance of PKCdelta signaling in fractionated-radiation-induced expansion of glioma-initiating cells and resistance to cancer treatment. J Cell Sci 124:3084–3094.
  • Kirshner J, Jobling MF, Pajares MJ, Ravani SA, Glick AB, Lavin MJ, Koslov S, Shiloh Y, Barcellos-Hoff MH. 2006. Inhibition of transforming growth factor-beta1 signaling attenuates ataxia telangiectasia mutated activity in response to genotoxic stress. Cancer Res 66:10861–10869.
  • Lagadec C, Vlashi E, Della Donna L, Dekmezian C, Pajonk F. 2012. Radiation-induced reprogramming of breast cancer cells. Stem Cells 30:833–844.
  • Legler JM, Gloeckler Ries LA, Smith MA, Warren JL, Heineman EF, Kaplan RS, Linet MS. 1999. RESPONSE: Re: Brain and Other Central Nervous System Cancers: Recent trends in incidence and mortality. J Natl Cancer Inst 91:2050A–22051.
  • Li Z, Wang H, Eyler CE, Hjelmeland AB, Rich JN. 2009. Turning cancer stem cells inside out: an exploration of glioma stem cell signaling pathways. J Biol Chem 284:16705–16709.
  • Lim YC, Roberts TL, Day BW, Harding A, Kozlov S, Kijas AW, Ensbey KS, Walker DG, Lavin MF. 2012. A role for homologous recombination and abnormal cell-cycle progression in radioresistance of glioma-initiating cells. Mol Cancer Ther 11:1863–1872.
  • Lomonaco SL, Finniss S, Xiang C, Decarvalho A, Umansky F, Kalkanis SN, Mikkelsen T, Brodie C. 2009. The induction of autophagy by gamma-radiation contributes to the radioresistance of glioma stem cells. Int J Cancer 125:717–722.
  • Marie-Egyptienne DT, Lohse I, Hill RP. 2013. Cancer stem cells, the epithelial to mesenchymal transition (EMT) and radioresistance: Potential role of hypoxia. Cancer Lett 341:63–72.
  • Morgan WF. 2003. Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation?Oncogene 22:7094–7099.
  • Morgan WF, Murnane JP. 1995. A role for genomic instability in cellular radioresistance?Cancer Metastasis Rev 14:49–58.
  • Overgaard J. 2007. Hypoxic radiosensitization: Adored and ignored. J Clin Oncol 25:4066–4074.
  • Parekh DB, Ziegler W, Parker PJ. 2000. Multiple pathways control protein kinase C phosphorylation. Embo J 19:496–503.
  • Pawlik TM, Keyomarsi K. 2004. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys 59:928–942.
  • Phillips TM, Mcbride WH, Pajonk F. 2006. The response of CD24(−/low)/CD44 + breast cancer-initiating cells to radiation. J Natl Cancer Inst 98:1777–1785.
  • Reya T, Morrison SJ, Clarke MF, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105–111.
  • Rosen JM, Jordan CT. 2009. The increasing complexity of the cancer stem cell paradigm. Science 324:1670–1673.
  • Schepers AG, Snippert HJ, Stange DE, Van Den Born M, Van Es JH, Van De Wetering M, Clevers H. 2012. Lineage tracing reveals Lgr5 + stem cell activity in mouse intestinal adenomas. Science 337:730–735.
  • Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828.
  • Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. 2004. Identification of human brain tumour initiating cells. Nature 432:396–401.
  • Spitz DR, Azzam EI, Li JJ, Gius D. 2004. Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: A unifying concept in stress response biology. Cancer Metastasis Rev 23:311–322.
  • Squatrito M, Brennan CW, Helmy K, Huse JT, Petrini JH, Holland EC. 2010. Loss of ATM/Chk2/p53 pathway components accelerates tumor development and contributes to radiation resistance in gliomas. Cancer Cell 18:619–629.
  • Steinberg SF. 2004. Distinctive activation mechanisms and functions for protein kinase Cdelta. Biochem J 384:449–459.
  • Tamura K, Aoyagi M, Ando N, Ogishima T, Wakimoto H, Yamamoto M, Ohno K. 2013. Expansion of CD133-positive glioma cells in recurrent de novo glioblastomas after radiotherapy and chemotherapy. J Neurosurg 119:1145–1155.
  • Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, Lin A. 2001. Inhibition of JNK activation through NF-kappaB target genes. Nature 414:313–317.
  • Thames HD Jr, Withers HR, Peters LJ, Fletcher GH. 1982. Changes in early and late radiation responses with altered dose fractionation: Implications for dose-survival relationships. Int J Radiat Oncol Biol Phys 8:219–226.
  • Tothova Z, Gilliland DG. 2009. A radical bailout strategy for cancer stem cells. Cell Stem Cell 4:196–197.
  • Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL. 2000. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97:14720–14725.
  • Vaupel P. 2004. Tumor microenvironmental physiology and its implications for radiation oncology. Semin Radiat Oncol 14:198–206.
  • Veronesi U, Boyle P, Goldhirsch A, Orecchia R, Viale G. 2005. Breast cancer. Lancet 365:1727–1741.
  • Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA. 2010. Notch promotes radioresistance of glioma stem cells. Stem Cells 28:17–28.
  • Wang Z, Li Y, Banerjee S, Sarkar FH. 2009. Emerging role of Notch in stem cells and cancer. Cancer Lett 279:8–12.
  • Wiegman EM, Blaese MA, Loeffler H, Coppes RP, Rodemann HP. 2007. TGFbeta-1 dependent fast stimulation of ATM and p53 phosphorylation following exposure to ionizing radiation does not involve TGFbeta-receptor I signalling. Radiother Oncol 83:289–295.
  • Yoon CH, Kim MJ, Kim RK, Lim EJ, Choi KS, An S, Hwang SG, Kang SG, Suh Y, Park MJ, Lee SJ. 2012. c-Jun N-terminal kinase has a pivotal role in the maintenance of self-renewal and tumorigenicity in glioma stem-like cells. Oncogene 31:4655–4666.
  • Zhang M, Atkinson RL, Rosen JM. 2010. Selective targeting of radiation-resistant tumor-initiating cells. Proc Natl Acad Sci USA 107:3522–3527.
  • Zhang M, Kleber S, Rohrich M, Timke C, Han N, Tuettenberg J, Martin-Villalba A, Debus J, Peschke P, Wirkner U, Lahn M, Huber PE. 2011. Blockade of TGF-beta signaling by the TGFbetaR-I kinase inhibitor LY2109761 enhances radiation response and prolongs survival in glioblastoma. Cancer Res 71:7155–7167.
  • Zhang XP, Zheng G, Zou L, Liu HL, Hou LH, Zhou P, Yin DD, Zheng QJ, Liang L, Zhang SZ, Feng L, Yao LB, Yang AG, Han H, Chen JY. 2008. Notch activation promotes cell proliferation and the formation of neural stem cell-like colonies in human glioma cells. Mol Cell Biochem 307:101–108.

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