207
Views
12
CrossRef citations to date
0
Altmetric
Theme: Brain Cancer - Review

Enhancing radiation therapy for patients with glioblastoma

, &
Pages 569-581 | Published online: 10 Jan 2014

References

  • Walker MD, Alexander E Jr, Hunt WE et al. Evaluation of BCNU and/or radiotherapy in the treatment of anaplastic gliomas. A cooperative clinical trial. J. Neurosurg. 49(3), 333–343 (1978).
  • Stupp R, Mason WP, van den Bent MJ et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352(10), 987–996 (2005).
  • Hall EJ, Giaccia AJ. Radiobiology for the Radiologist. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, PA, USA (2012).
  • Walker MD, Strike TA, Sheline GE. An analysis of dose–effect relationship in the radiotherapy of malignant gliomas. Int. J. Radiat. Oncol. Biol. Phys. 5(10), 1725–1731 (1979).
  • Nelson DF, Diener-West M, Horton J, Chang CH, Schoenfeld D, Nelson JS. Combined modality approach to treatment of malignant gliomas – re-evaluation of RTOG 7401/ECOG 1374 with long-term follow-up: a joint study of the Radiation Therapy Oncology Group and the Eastern Cooperative Oncology Group. NCI Monogr. 6, 279–284 (1988).
  • Chan JL, Lee SW, Fraass BA et al. Survival and failure patterns of high-grade gliomas after three-dimensional conformal radiotherapy. J. Clin. Oncol. 20(6), 1635–1642 (2002).
  • Fitzek MM, Thornton AF, Rabinov JD et al. Accelerated fractionated proton/photon irradiation to 90 cobalt gray equivalent for glioblastoma multiforme: results of a Phase II prospective trial. J. Neurosurg. 91(2), 251–260 (1999).
  • Laperriere NJ, Leung PM, McKenzie S et al. Randomized study of brachytherapy in the initial management of patients with malignant astrocytoma. Int. J. Radiat. Oncol. Biol. Phys. 41(5), 1005–1011 (1998).
  • Selker RG, Shapiro WR, Burger P et al.; Brain Tumor Cooperative Group. The Brain Tumor Cooperative Group NIH Trial 87-01: a randomized comparison of surgery, external radiotherapy, and carmustine versus surgery, interstitial radiotherapy boost, external radiation therapy, and carmustine. Neurosurgery 51(2), 343–355; discussion 355 (2002).
  • Souhami L, Seiferheld W, Brachman D et al. Randomized comparison of stereotactic radiosurgery followed by conventional radiotherapy with carmustine to conventional radiotherapy with carmustine for patients with glioblastoma multiforme: report of Radiation Therapy Oncology Group 93-05 protocol. Int. J. Radiat. Oncol. Biol. Phys. 60(3), 853–860 (2004).
  • Hochberg FH, Pruitt A. Assumptions in the radiotherapy of glioblastoma. Neurology 30(9), 907–911 (1980).
  • Wallner KE, Galicich JH, Krol G, Arbit E, Malkin MG. Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma. Int. J. Radiat. Oncol. Biol. Phys. 16(6), 1405–1409 (1989).
  • Akudugu JM, Theron T, Serafin AM, Böhm L. Influence of DNA double-strand break rejoining on clonogenic survival and micronucleus yield in human cell lines. Int. J. Radiat. Biol. 80(2), 93–104 (2004).
  • Williams JR, Zhang Y, Russell J, Koch C, Little JB. Human tumor cells segregate into radiosensitivity groups that associate with ATM and TP53 status. Acta Oncol. 46(5), 628–638 (2007).
  • Williams JR, Zhang Y, Zhou H et al. A quantitative overview of radiosensitivity of human tumor cells across histological type and TP53 status. Int. J. Radiat. Biol. 84(4), 253–264 (2008).
  • Bao S, Wu Q, McLendon RE et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444(7120), 756–760 (2006).
  • McCord AM, Jamal M, Williams ES, Camphausen K, Tofilon PJ. CD133+ glioblastoma stem-like cells are radiosensitive with a defective DNA damage response compared with established cell lines. Clin. Cancer Res. 15(16), 5145–5153 (2009).
  • Williams JR, Zhang Y, Zhou H et al. Genotype-dependent radiosensitivity: clonogenic survival, apoptosis and cell-cycle redistribution. Int. J. Radiat. Biol. 84(2), 151–164 (2008).
  • Eschrich S, Zhang H, Zhao H et al. Systems biology modeling of the radiation sensitivity network: a biomarker discovery platform. Int. J. Radiat. Oncol. Biol. Phys. 75(2), 497–505 (2009).
  • Britten RA, Liu D, Kuny S, Allalunis-Turner MJ. Differential level of DSB repair fidelity effected by nuclear protein extracts derived from radiosensitive and radioresistant human tumour cells. Br. J. Cancer 76(11), 1440–1447 (1997).
  • Cuddihy AR, Bristow RG. The p53 protein family and radiation sensitivity: yes or no? Cancer Metastasis Rev. 23(3–4), 237–257 (2004).
  • Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455(7216), 1061–1068 (2008).
  • Nakamura M, Watanabe T, Klangby U et al. p14ARF deletion and methylation in genetic pathways to glioblastomas. Brain Pathol. 11(2), 159–168 (2001).
  • Reifenberger G, Liu L, Ichimura K, Schmidt EE, Collins VP. Amplification and overexpression of the MDM2 gene in a subset of human malignant gliomas without p53 mutations. Cancer Res. 53(12), 2736–2739 (1993).
  • Mehta S, Huillard E, Kesari S et al. The central nervous system-restricted transcription factor Olig2 opposes p53 responses to genotoxic damage in neural progenitors and malignant glioma. Cancer Cell 19(3), 359–371 (2011).
  • Alexander BM, Pinnell N, Wen PY, D’Andrea A. Targeting DNA repair and the cell cycle in glioblastoma. J. Neurooncol. 107(3), 463–477 (2012).
  • Bobola MS, Kolstoe DD, Blank A, Silber JR. Minimally cytotoxic doses of temozolomide produce radiosensitization in human glioblastoma cells regardless of MGMT expression. Mol. Cancer Ther. 9(5), 1208–1218 (2010).
  • Chakravarti A, Erkkinen MG, Nestler U et al. Temozolomide-mediated radiation enhancement in glioblastoma: a report on underlying mechanisms. Clin. Cancer Res. 12(15), 4738–4746 (2006).
  • Kil WJ, Cerna D, Burgan WE et al. In vitro and in vivo radiosensitization induced by the DNA methylating agent temozolomide. Clin. Cancer Res. 14(3), 931–938 (2008).
  • Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 59(4), 928–942 (2004).
  • Fountzilas G, Karavelis A, Capizzello A et al. Radiation and concomitant weekly administration of paclitaxel in patients with glioblastoma multiforme. A Phase II study. J. Neurooncol. 45(2), 159–165 (1999).
  • Langer CJ, Ruffer J, Rhodes H et al. Phase II radiation therapy oncology group trial of weekly paclitaxel and conventional external beam radiation therapy for supratentorial glioblastoma multiforme. Int. J. Radiat. Oncol. Biol. Phys. 51(1), 113–119 (2001).
  • Prados MD, Seiferheld W, Sandler HM et al. Phase III randomized study of radiotherapy plus procarbazine, lomustine, and vincristine with or without BUdR for treatment of anaplastic astrocytoma: final report of RTOG 9404. Int. J. Radiat. Oncol. Biol. Phys. 58(4), 1147–1152 (2004).
  • Dungey FA, Löser DA, Chalmers AJ. Replication-dependent radiosensitization of human glioma cells by inhibition of poly(ADP-ribose) polymerase: mechanisms and therapeutic potential. Int. J. Radiat. Oncol. Biol. Phys. 72(4), 1188–1197 (2008).
  • Ziegler DS, Kung AL, Kieran MW. Anti-apoptosis mechanisms in malignant gliomas. J. Clin. Oncol. 26(3), 493–500 (2008).
  • Call JA, Eckhardt SG, Camidge DR. Targeted manipulation of apoptosis in cancer treatment. Lancet Oncol. 9(10), 1002–1011 (2008).
  • Dumont F, Altmeyer A, Bischoff P. Radiosensitising agents for the radiotherapy of cancer: novel molecularly targeted approaches. Expert Opin. Ther. Pat. 19(6), 775–799 (2009).
  • Streffer JR, Schuster M, Pohl U et al. Irradiation induced clonogenic cell death of human malignant glioma cells does not require CD95/CD95L interactions. Anticancer Res. 19(6B), 5265–5269 (1999).
  • Amundson SA, Do KT, Vinikoor LC et al. Integrating global gene expression and radiation survival parameters across the 60 cell lines of the National Cancer Institute Anticancer Drug Screen. Cancer Res. 68(2), 415–424 (2008).
  • Streffer JR, Rimner A, Rieger J, Naumann U, Rodemann HP, Weller M. BCL-2 family proteins modulate radiosensitivity in human malignant glioma cells. J. Neurooncol. 56(1), 43–49 (2002).
  • Weller M, Malipiero U, Aguzzi A, Reed JC, Fontana A. Protooncogene bcl-2 gene transfer abrogates Fas/APO-1 antibody-mediated apoptosis of human malignant glioma cells and confers resistance to chemotherapeutic drugs and therapeutic irradiation. J. Clin. Invest. 95(6), 2633–2643 (1995).
  • Strik H, Deininger M, Streffer J et al. BCL-2 family protein expression in initial and recurrent glioblastomas: modulation by radiochemotherapy. J. Neurol. Neurosurg. Psychiatr. 67(6), 763–768 (1999).
  • Fassl A, Tagscherer KE, Richter J et al. Notch1 signaling promotes survival of glioblastoma cells via EGFR-mediated induction of anti-apoptotic Mcl-1. Oncogene 31(44), 4698–4708 (2012).
  • Kouri FM, Jensen SA, Stegh AH. The role of Bcl-2 family proteins in therapy responses of malignant astrocytic gliomas: Bcl2L12 and beyond. ScientificWorldJournal 2012, 838916 (2012).
  • Tagscherer KE, Fassl A, Sinkovic T, Combs SE, Roth W. p53-dependent regulation of Mcl-1 contributes to synergistic cell death by ionizing radiation and the Bcl-2/Bcl-XL inhibitor ABT-737. Apoptosis 17(2), 187–199 (2012).
  • Wagenknecht B, Glaser T, Naumann U et al. Expression and biological activity of X-linked inhibitor of apoptosis (XIAP) in human malignant glioma. Cell Death Differ. 6(4), 370–376 (1999).
  • Ziegler DS, Keating J, Kesari S et al. A small-molecule IAP inhibitor overcomes resistance to cytotoxic therapies in malignant gliomas in vitro and in vivo. Neuro-oncology 13(8), 820–829 (2011).
  • Chakravarti A, Zhai GG, Zhang M et al. Survivin enhances radiation resistance in primary human glioblastoma cells via caspase-independent mechanisms. Oncogene 23(45), 7494–7506 (2004).
  • Reichert S, Rödel C, Mirsch J et al. Survivin inhibition and DNA double-strand break repair: a molecular mechanism to overcome radioresistance in glioblastoma. Radiother. Oncol. 101(1), 51–58 (2011).
  • Shirai K, Suzuki Y, Oka K et al. Nuclear survivin expression predicts poorer prognosis in glioblastoma. J. Neurooncol. 91(3), 353–358 (2009).
  • Saito T, Hama S, Izumi H et al. Centrosome amplification induced by survivin suppression enhances both chromosome instability and radiosensitivity in glioma cells. Br. J. Cancer 98(2), 345–355 (2008).
  • Reichert S, Reinboldt V, Hehlgans S, Efferth T, Rödel C, Rödel F. A radiosensitizing effect of artesunate in glioblastoma cells is associated with a diminished expression of the inhibitor of apoptosis protein survivin. Radiother. Oncol. 103(3), 394–401 (2012).
  • Chakravarti A, Noll E, Black PM et al. Quantitatively determined survivin expression levels are of prognostic value in human gliomas. J. Clin. Oncol. 20(4), 1063–1068 (2002).
  • Squatrito M, Brennan CW, Helmy K, Huse JT, Petrini JH, Holland EC. Loss of ATM/Chk2/p53 pathway components accelerates tumor development and contributes to radiation resistance in gliomas. Cancer Cell 18(6), 619–629 (2010).
  • Squatrito M, Holland EC. DNA damage response and growth factor signaling pathways in gliomagenesis and therapeutic resistance. Cancer Res. 71(18), 5945–5949 (2011).
  • Bartkova J, Hamerlik P, Stockhausen MT et al. Replication stress and oxidative damage contribute to aberrant constitutive activation of DNA damage signalling in human gliomas. Oncogene 29(36), 5095–5102 (2010).
  • Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 411(6835), 366–374 (2001).
  • Kennedy RD, D’Andrea AD. DNA repair pathways in clinical practice: lessons from pediatric cancer susceptibility syndromes. J. Clin. Oncol. 24(23), 3799–3808 (2006).
  • Hochegger H, Dejsuphong D, Fukushima T et al. Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J. 25(6), 1305–1314 (2006).
  • Wang M, Wu W, Wu W et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 34(21), 6170–6182 (2006).
  • Bryant HE, Schultz N, Thomas HD et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434(7035), 913–917 (2005).
  • Farmer H, McCabe N, Lord CJ et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434(7035), 917–921 (2005).
  • McCabe N, Turner NC, Lord CJ et al. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res. 66(16), 8109–8115 (2006).
  • Johnson N, Li YC, Walton ZE et al. Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat. Med. 17(7), 875–882 (2011).
  • McEllin B, Camacho CV, Mukherjee B et al. PTEN loss compromises homologous recombination repair in astrocytes: implications for glioblastoma therapy with temozolomide or poly(ADP-ribose) polymerase inhibitors. Cancer Res. 70(13), 5457–5464 (2010).
  • Mendes-Pereira AM, Martin SA, Brough R et al. Synthetic lethal targeting of PTEN mutant cells with PARP inhibitors. EMBO Mol. Med. 1(6–7), 315–322 (2009).
  • Hegan DC, Lu Y, Stachelek GC, Crosby ME, Bindra RS, Glazer PM. Inhibition of poly(ADP-ribose) polymerase down-regulates BRCA1 and RAD51 in a pathway mediated by E2F4 and p130. Proc. Natl Acad. Sci. USA 107(5), 2201–2206 (2010).
  • Thoms J, Bristow RG. DNA repair targeting and radiotherapy: a focus on the therapeutic ratio. Semin. Radiat. Oncol. 20(4), 217–222 (2010).
  • Russo AL, Kwon HC, Burgan WE et al. In vitro and in vivo radiosensitization of glioblastoma cells by the poly(ADP-ribose) polymerase inhibitor E7016. Clin. Cancer Res. 15(2), 607–612 (2009).
  • Yuan ZM, Huang Y, Ishiko T et al. Regulation of Rad51 function by c-Abl in response to DNA damage. J. Biol. Chem. 273(7), 3799–3802 (1998).
  • Russell JS, Brady K, Burgan WE et al. Gleevec-mediated inhibition of Rad51 expression and enhancement of tumor cell radiosensitivity. Cancer Res. 63(21), 7377–7383 (2003).
  • Holdhoff M, Kreuzer KA, Appelt C et al. Imatinib mesylate radiosensitizes human glioblastoma cells through inhibition of platelet-derived growth factor receptor. Blood Cells Mol. Dis. 34(2), 181–185 (2005).
  • Oertel S, Krempien R, Lindel K et al. Human glioblastoma and carcinoma xenograft tumors treated by combined radiation and imatinib (Gleevec). Strahlenther. Onkol. 182(7), 400–407 (2006).
  • Geng L, Shinohara ET, Kim D et al. STI571 (Gleevec) improves tumor growth delay and survival in irradiated mouse models of glioblastoma. Int. J. Radiat. Oncol. Biol. Phys. 64(1), 263–271 (2006).
  • Murakawa Y, Sonoda E, Barber LJ et al. Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res. 67(18), 8536–8543 (2007).
  • Shi W, Ma Z, Willers H et al. Disassembly of MDC1 foci is controlled by ubiquitin–proteasome-dependent degradation. J. Biol. Chem. 283(46), 31608–31616 (2008).
  • Jacquemont C, Taniguchi T. Proteasome function is required for DNA damage response and Fanconi anemia pathway activation. Cancer Res. 67(15), 7395–7405 (2007).
  • Kubicek GJ, Werner-Wasik M, Machtay M et al. Phase I trial using proteasome inhibitor bortezomib and concurrent temozolomide and radiotherapy for central nervous system malignancies. Int. J. Radiat. Oncol. Biol. Phys. 74(2), 433–439 (2009).
  • Rowley R, Hudson J, Young PG. The wee1 protein kinase is required for radiation-induced mitotic delay. Nature 356(6367), 353–355 (1992).
  • Fernet M, Mégnin-Chanet F, Hall J, Favaudon V. Control of the G2/M checkpoints after exposure to low doses of ionising radiation: implications for hyper-radiosensitivity. DNA Repair (Amst.) 9(1), 48–57 (2010).
  • Mir SE, De Witt Hamer PC, Krawczyk PM et al. In silico analysis of kinase expression identifies WEE1 as a gatekeeper against mitotic catastrophe in glioblastoma. Cancer Cell 18(3), 244–257 (2010).
  • Sarcar B, Kahali S, Prabhu AH et al. Targeting radiation-induced G(2) checkpoint activation with the Wee-1 inhibitor MK-1775 in glioblastoma cell lines. Mol. Cancer Ther. 10(12), 2405–2414 (2011).
  • Golding SE, Rosenberg E, Valerie N et al. Improved ATM kinase inhibitor KU-60019 radiosensitizes glioma cells, compromises insulin, AKT and ERK prosurvival signaling, and inhibits migration and invasion. Mol. Cancer Ther. 8(10), 2894–2902 (2009).
  • Faigle R, Song H. Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim. Biophys. Acta 1830(2), 2435–2448 (2013).
  • Braun S, Oppermann H, Mueller A et al. Hedgehog signaling in glioblastoma multiforme. Cancer Biol. Ther. 13(7), 487–495 (2012).
  • Shih AH, Holland EC. Notch signaling enhances nestin expression in gliomas. Neoplasia 8(12), 1072–1082 (2006).
  • Fan X, Matsui W, Khaki L et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 66(15), 7445–7452 (2006).
  • Bar EE, Chaudhry A, Lin A et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 25(10), 2524–2533 (2007).
  • Jiang L, Wu J, Chen Q, Hu X, Li W, Hu G. Notch1 expression is upregulated in glioma and is associated with tumor progression. J. Clin. Neurosci. 18(3), 387–390 (2011).
  • Wang J, Wakeman TP, Lathia JD et al. Notch promotes radioresistance of glioma stem cells. Stem Cells 28(1), 17–28 (2010).
  • Krop I, Demuth T, Guthrie T et al. Phase I pharmacologic and pharmacodynamic study of the γ secretase (Notch) inhibitor MK-0752 in adult patients with advanced solid tumors. J. Clin. Oncol. 30(19), 2307–2313 (2012).
  • Ferruzzi P, Mennillo F, De Rosa A et al. In vitro and in vivo characterization of a novel Hedgehog signaling antagonist in human glioblastoma cell lines. Int. J. Cancer 131(2), E33–E44 (2012).
  • Rudin CM, Hann CL, Laterra J et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N. Engl. J. Med. 361(12), 1173–1178 (2009).
  • Von Hoff DD, LoRusso PM, Rudin CM et al. Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. N. Engl. J. Med. 361(12), 1164–1172 (2009).
  • Gray LH, Conger AD, Ebert M, Hornsey S, Scott OC. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br. J. Radiol. 26(312), 638–648 (1953).
  • Collingridge DR, Piepmeier JM, Rockwell S, Knisely JP. Polarographic measurements of oxygen tension in human glioma and surrounding peritumoural brain tissue. Radiother. Oncol. 53(2), 127–131 (1999).
  • Kayama T, Yoshimoto T, Fujimoto S, Sakurai Y. Intratumoral oxygen pressure in malignant brain tumor. J. Neurosurg. 74(1), 55–59 (1991).
  • Bischoff P, Altmeyer A, Dumont F. Radiosensitising agents for the radiotherapy of cancer: advances in traditional and hypoxia targeted radiosensitisers. Expert Opin. Ther. Pat. 19(5), 643–662 (2009).
  • [No authors listed]. A study of the effect of misonidazole in conjunction with radiotherapy for the treatment of grades 3 and 4 astrocytomas. A report from the MRC Working Party on misonidazole in gliomas. Br. J. Radiol. 56(669), 673–682 (1983).
  • Stadler B, Kärcher KH, Kogelnik HD, Szepesi T. Misonidazole and irradiation in the treatment of high-grade astrocytomas: further report of the Vienna Study Group. Int. J. Radiat. Oncol. Biol. Phys. 10(9), 1713–1717 (1984).
  • Urtasun R, Feldstein ML, Partington J et al. Radiation and nitroimidazoles in supratentorial high grade gliomas: a second clinical trial. Br. J. Cancer 46(1), 101–108 (1982).
  • Deutsch M, Green SB, Strike TA et al. Results of a randomized trial comparing BCNU plus radiotherapy, streptozotocin plus radiotherapy, BCNU plus hyperfractionated radiotherapy, and BCNU following misonidazole plus radiotherapy in the postoperative treatment of malignant glioma. Int. J. Radiat. Oncol. Biol. Phys. 16(6), 1389–1396 (1989).
  • Goel S, Duda DG, Xu L et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev. 91(3), 1071–1121 (2011).
  • Chinot O, Wick W, Mason W et al. Phase III trial of bevacizumab added to standard radiotherapy and temozolomide for newly-diagnosed glioblastoma: mature progression-free survival and preliminary overall survival results in AVAglio. Neuro Oncol. 14, vi101–vi105, Abstract OT-3 (2012).
  • Kleinberg L, Grossman SA, Carson K et al. Survival of patients with newly diagnosed glioblastoma multiforme treated with RSR13 and radiotherapy: results of a Phase II New Approaches to Brain Tumor Therapy CNS Consortium safety and efficacy study. J. Clin. Oncol. 20(14), 3149–3155 (2002).
  • Sheehan J, Sherman J, Cifarelli C et al. Effect of trans sodium crocetinate on brain tumor oxygenation. Laboratory investigation. J. Neurosurg. 111(2), 226–229 (2009).
  • Sheehan J, Cifarelli CP, Dassoulas K, Olson C, Rainey J, Han S. Trans-sodium crocetinate enhancing survival and glioma response on magnetic resonance imaging to radiation and temozolomide. J. Neurosurg. 113(2), 234–239 (2010).
  • Sheehan J, Ionescu A, Pouratian N et al. Use of trans sodium crocetinate for sensitizing glioblastoma multiforme to radiation: laboratory investigation. J. Neurosurg. 108(5), 972–978 (2008).
  • Beppu T, Kamada K, Yoshida Y, Arai H, Ogasawara K, Ogawa A. Change of oxygen pressure in glioblastoma tissue under various conditions. J. Neurooncol. 58(1), 47–52 (2002).
  • Ogawa K, Yoshii Y, Inoue O et al. Phase II trial of radiotherapy after hyperbaric oxygenation with chemotherapy for high-grade gliomas. Br. J. Cancer 95(7), 862–868 (2006).
  • Cardinale RM, Dillehay LE, Williams JA, Tabassi K, Brem H, Lee DJ. Effect of interstitial and/or systemic delivery of tirapazamine on the radiosensitivity of human glioblastoma multiforme in nude mice. Radiat. Oncol. Investig. 6(2), 63–70 (1998).
  • Del Rowe J, Scott C, Werner-Wasik M et al. Single-arm, open-label Phase II study of intravenously administered tirapazamine and radiation therapy for glioblastoma multiforme. J. Clin. Oncol. 18(6), 1254–1259 (2000).
  • Griffin TW, Davis R, Laramore G et al. Fast neutron radiation therapy for glioblastoma multiforme. Results of an RTOG study. Am. J. Clin. Oncol. 6(6), 661–667 (1983).
  • Catterall M, Bloom HJ, Ash DV et al. Fast neutrons compared with megavoltage x-rays in the treatment of patients with supratentorial glioblastoma: a controlled pilot study. Int. J. Radiat. Oncol. Biol. Phys. 6(3), 261–266 (1980).
  • Duncan W, McLelland J, Jack WJ et al. The results of a randomised trial of mixed-schedule (neutron/photon) irradiation in the treatment of supratentorial grade III and grade IV astrocytoma. Br. J. Radiol. 59(700), 379–383 (1986).
  • Duncan W, McLelland J, Jack WJ et al. Report of a randomised pilot study of the treatment of patients with supratentorial gliomas using neutron irradiation. Br. J. Radiol. 59(700), 373–377 (1986).
  • Laramore GE, Diener-West M, Griffin TW et al. Randomized neutron dose searching study for malignant gliomas of the brain: results of an RTOG study. Radiation Therapy Oncology Group. Int. J. Radiat. Oncol. Biol. Phys. 14(6), 1093–1102 (1988).
  • Pickles T, Goodman GB, Rheaume DE et al. Pion radiation for high grade astrocytoma: results of a randomized study. Int. J. Radiat. Oncol. Biol. Phys. 37(3), 491–497 (1997).
  • Castro JR, Phillips TL, Prados M et al. Neon heavy charged particle radiotherapy of glioblastoma of the brain. Int. J. Radiat. Oncol. Biol. Phys. 38(2), 257–261 (1997).
  • Mizoe JE, Tsujii H, Hasegawa A et al.; Organizing Committee of the Central Nervous System Tumor Working Group. Phase I/II clinical trial of carbon ion radiotherapy for malignant gliomas: combined x-ray radiotherapy, chemotherapy, and carbon ion radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 69(2), 390–396 (2007).
  • Combs SE, Kieser M, Rieken S et al. Randomized Phase II study evaluating a carbon ion boost applied after combined radiochemotherapy with temozolomide versus a proton boost after radiochemotherapy with temozolomide in patients with primary glioblastoma: the CLEOPATRA trial. BMC Cancer 10, 478 (2010).
  • Chakravarti A, Zhai G, Suzuki Y et al. The prognostic significance of phosphatidylinositol 3-kinase pathway activation in human gliomas. J. Clin. Oncol. 22(10), 1926–1933 (2004).
  • Kao GD, Jiang Z, Fernandes AM, Gupta AK, Maity A. Inhibition of phosphatidylinositol-3-OH kinase/Akt signaling impairs DNA repair in glioblastoma cells following ionizing radiation. J. Biol. Chem. 282(29), 21206–21212 (2007).
  • Toulany M, Rodemann HP. Membrane receptor signaling and control of DNA repair after exposure to ionizing radiation. Nuklearmedizin 49(Suppl. 1), S26–S30 (2010).
  • Mukherjee B, McEllin B, Camacho CV et al. EGFRvIII and DNA double-strand break repair: a molecular mechanism for radioresistance in glioblastoma. Cancer Res. 69(10), 4252–4259 (2009).
  • Golding SE, Morgan RN, Adams BR, Hawkins AJ, Povirk LF, Valerie K. Pro-survival AKT and ERK signaling from EGFR and mutant EGFRvIII enhances DNA double-strand break repair in human glioma cells. Cancer Biol. Ther. 8(8), 730–738 (2009).
  • O’Rourke DM, Kao GD, Singh N et al. Conversion of a radioresistant phenotype to a more sensitive one by disabling erbB receptor signaling in human cancer cells. Proc. Natl Acad. Sci. USA 95(18), 10842–10847 (1998).
  • Matsuoka S, Ballif BA, Smogorzewska A et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316(5828), 1160–1166 (2007).
  • Stommel JM, Kimmelman AC, Ying H et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318(5848), 287–290 (2007).
  • Brown PD, Krishnan S, Sarkaria JN et al.; North Central Cancer Treatment Group Study N0177. Phase I/II trial of erlotinib and temozolomide with radiation therapy in the treatment of newly diagnosed glioblastoma multiforme: North Central Cancer Treatment Group Study N0177. J. Clin. Oncol. 26(34), 5603–5609 (2008).
  • Peereboom DM, Shepard DR, Ahluwalia MS et al. Phase II trial of erlotinib with temozolomide and radiation in patients with newly diagnosed glioblastoma multiforme. J. Neurooncol. 98(1), 93–99 (2010).
  • Prados MD, Chang SM, Butowski N et al. Phase II study of erlotinib plus temozolomide during and after radiation therapy in patients with newly diagnosed glioblastoma multiforme or gliosarcoma. J. Clin. Oncol. 27(4), 579–584 (2009).
  • Camphausen K, Tofilon PJ. Inhibition of histone deacetylation: a strategy for tumor radiosensitization. J. Clin. Oncol. 25(26), 4051–4056 (2007).
  • Camphausen K, Burgan W, Cerra M et al. Enhanced radiation-induced cell killing and prolongation of γH2AX foci expression by the histone deacetylase inhibitor MS-275. Cancer Res. 64(1), 316–321 (2004).
  • Camphausen K, Cerna D, Scott T et al. Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int. J. Cancer 114(3), 380–386 (2005).
  • Chinnaiyan P, Cerna D, Burgan WE et al. Postradiation sensitization of the histone deacetylase inhibitor valproic acid. Clin. Cancer Res. 14(17), 5410–5415 (2008).
  • Chinnaiyan P, Vallabhaneni G, Armstrong E, Huang SM, Harari PM. Modulation of radiation response by histone deacetylase inhibition. Int. J. Radiat. Oncol. Biol. Phys. 62(1), 223–229 (2005).
  • Kim JH, Shin JH, Kim IH. Susceptibility and radiosensitization of human glioblastoma cells to trichostatin A, a histone deacetylase inhibitor. Int. J. Radiat. Oncol. Biol. Phys. 59(4), 1174–1180 (2004).
  • Camphausen K, Tofilon PJ. Inhibition of Hsp90: a multitarget approach to radiosensitization. Clin. Cancer Res. 13(15 Pt 1), 4326–4330 (2007).
  • Bull EE, Dote H, Brady KJ et al. Enhanced tumor cell radiosensitivity and abrogation of G2 and S phase arrest by the Hsp90 inhibitor 17-(dimethylaminoethylamino)-17-demethoxygeldanamycin. Clin. Cancer Res. 10(23), 8077–8084 (2004).
  • Russell JS, Burgan W, Oswald KA, Camphausen K, Tofilon PJ. Enhanced cell killing induced by the combination of radiation and the heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin: a multitarget approach to radiosensitization. Clin. Cancer Res. 9(10 Pt 1), 3749–3755 (2003).
  • Niewidok N, Wack LJ, Schiessl S et al. Hsp90 Inhibitors NVP-AUY922 and NVP-BEP800 may exert a significant radiosensitization on tumor cells along with a cell type-specific cytotoxicity. Transl. Oncol. 5(5), 356–369 (2012).
  • Sauvageot CM, Weatherbee JL, Kesari S et al. Efficacy of the HSP90 inhibitor 17-AAG in human glioma cell lines and tumorigenic glioma stem cells. Neuro-oncology 11(2), 109–121 (2009).
  • Stingl L, Stühmer T, Chatterjee M, Jensen MR, Flentje M, Djuzenova CS. Novel HSP90 inhibitors, NVP-AUY922 and NVP-BEP800, radiosensitise tumour cells through cell-cycle impairment, increased DNA damage and repair protraction. Br. J. Cancer 102(11), 1578–1591 (2010).
  • Djuzenova CS, Blassl C, Roloff K et al. Hsp90 inhibitor NVP-AUY922 enhances radiation sensitivity of tumor cell lines under hypoxia. Cancer Biol. Ther. 13(6), 425–434 (2012).
  • Dote H, Burgan WE, Camphausen K, Tofilon PJ. Inhibition of hsp90 compromises the DNA damage response to radiation. Cancer Res. 66(18), 9211–9220 (2006).
  • Noguchi M, Yu D, Hirayama R et al. Inhibition of homologous recombination repair in irradiated tumor cells pretreated with Hsp90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Biochem. Biophys. Res. Commun. 351(3), 658–663 (2006).

Website

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.