Skip to main content
Top
Published in: Radiation Oncology 1/2017

Open Access 01-12-2017 | Research

Subventricular zones: new key targets for glioblastoma treatment

Authors: J. Khalifa, F. Tensaouti, A. Lusque, B. Plas, J.-A. Lotterie, A. Benouaich-Amiel, E. Uro-Coste, V. Lubrano, E. Cohen-Jonathan Moyal

Published in: Radiation Oncology | Issue 1/2017

Login to get access

Abstract

Background

We aimed to identify subventricular zone (SVZ)-related prognostic factors of survival and patterns of recurrence among patients with glioblastoma.

Methods

Forty-three patients with primary diagnosed glioblastoma treated in our Cancer Center between 2006 and 2010 were identified. All patients received surgical resection, followed by temozolomide-based chemoradiation. Ipsilateral (iSVZ), contralateral (cSVZ) and bilateral (bSVZ) SVZs were retrospectively segmented and radiation dose-volume histograms were generated. Multivariate analysis using the Cox proportional hazards model was assessed to examine the relationship between prognostic factors and time to progression (TTP) or overall survival (OS).

Results

Median age was 59 years (range: 25–85). Median follow-up, OS and TTP were 22.7 months (range 7.5–69.7 months), 22.7 months (95% CI 14.5–26.2 months) and 6.4 months (95% CI 4.4–9.3 months), respectively. On univariate analysis, initial contact to SVZ was a poor prognostic factor for OS (18.7 vs 41.7 months, p = 0.014) and TTP (4.6 vs 12.9 months, p = 0.002). Patients whose bSVZ volume receiving at least 20 Gy (V20Gy) was greater than 84% had a significantly improved TTP (17.7 months vs 5.2 months, p = 0.017). This radiation dose coverage was compatible with an hippocampal sparing. On multivariate analysis, initial contact to SVZ and V20 Gy to bSVZ lesser than 84% remained poor prognostic factors for TTP (HR = 3.07, p = 0.012 and HR = 2.67, p = 0.047, respectively).

Conclusion

Our results suggest that contact to SVZ, as well as insufficient bSVZ radiation dose coverage (V20Gy <84%), might be independent poor prognostic factors for TTP. Therefore, targeting SVZ could be of crucial interest for optimizing glioblastoma treatment.
Literature
1.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96.CrossRefPubMed Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96.CrossRefPubMed
2.
go back to reference Marusyk A, Almendro V, Polyak K. Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer. 2012;12:323–34.CrossRefPubMed Marusyk A, Almendro V, Polyak K. Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer. 2012;12:323–34.CrossRefPubMed
3.
go back to reference Sottoriva A, Spiteri I, Piccirillo SGM, Touloumis A, Collins VP, Marioni JC, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A. 2013;110:4009–14.CrossRefPubMedPubMedCentral Sottoriva A, Spiteri I, Piccirillo SGM, Touloumis A, Collins VP, Marioni JC, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A. 2013;110:4009–14.CrossRefPubMedPubMedCentral
4.
go back to reference Parker NR, Khong P, Parkinson JF, Howell VM, Wheeler HR. Molecular heterogeneity in glioblastoma: potential clinical implications. Front Oncol. 2015;5:55.PubMedPubMedCentral Parker NR, Khong P, Parkinson JF, Howell VM, Wheeler HR. Molecular heterogeneity in glioblastoma: potential clinical implications. Front Oncol. 2015;5:55.PubMedPubMedCentral
7.
go back to reference Kroonen J, Nassen J, Boulanger Y-G, Provenzano F, Capraro V, Bours V, et al. Human glioblastoma-initiating cells invade specifically the subventricular zones and olfactory bulbs of mice after striatal injection. Int J Cancer. 2011;129:574–85.CrossRefPubMed Kroonen J, Nassen J, Boulanger Y-G, Provenzano F, Capraro V, Bours V, et al. Human glioblastoma-initiating cells invade specifically the subventricular zones and olfactory bulbs of mice after striatal injection. Int J Cancer. 2011;129:574–85.CrossRefPubMed
8.
go back to reference Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401.CrossRefPubMed Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401.CrossRefPubMed
9.
go back to reference Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64:7011–21.CrossRefPubMed Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64:7011–21.CrossRefPubMed
10.
go back to reference Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9:391–403.CrossRefPubMed Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9:391–403.CrossRefPubMed
11.
go back to reference Gupta T, Nair V, Jalali R. Stem cell niche irradiation in glioblastoma: providing a ray of hope? CNS Oncol. 2014;3:367–76.CrossRefPubMed Gupta T, Nair V, Jalali R. Stem cell niche irradiation in glioblastoma: providing a ray of hope? CNS Oncol. 2014;3:367–76.CrossRefPubMed
12.
go back to reference Purow BW, Haque RM, Noel MW, Su Q, Burdick MJ, Lee J, et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res. 2005;65:2353–63.CrossRefPubMed Purow BW, Haque RM, Noel MW, Su Q, Burdick MJ, Lee J, et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res. 2005;65:2353–63.CrossRefPubMed
13.
go back to reference Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, et al. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature. 2006;442:823–6.CrossRefPubMed Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, et al. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature. 2006;442:823–6.CrossRefPubMed
14.
go back to reference Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science. 2001;294:2186–9.CrossRefPubMed Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science. 2001;294:2186–9.CrossRefPubMed
15.
go back to reference Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A. 2003;100:15178–83.CrossRefPubMedPubMedCentral Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A. 2003;100:15178–83.CrossRefPubMedPubMedCentral
16.
17.
go back to reference Safa AR, Saadatzadeh MR, Cohen-Gadol AA, Pollok KE, Bijangi-Vishehsaraei K. Glioblastoma stem cells (GSCs) epigenetic plasticity and interconversion between differentiated non-GSCs and GSCs. Genes Dis. 2015;2:152–63.CrossRefPubMedPubMedCentral Safa AR, Saadatzadeh MR, Cohen-Gadol AA, Pollok KE, Bijangi-Vishehsaraei K. Glioblastoma stem cells (GSCs) epigenetic plasticity and interconversion between differentiated non-GSCs and GSCs. Genes Dis. 2015;2:152–63.CrossRefPubMedPubMedCentral
18.
go back to reference Dahan P, Martinez Gala J, Delmas C, Monferran S, Malric L, Zentkowski D, et al. Ionizing radiations sustain glioblastoma cell dedifferentiation to a stem-like phenotype through survivin: possible involvement in radioresistance. Cell Death Dis. 2014;5:e1543.CrossRefPubMedPubMedCentral Dahan P, Martinez Gala J, Delmas C, Monferran S, Malric L, Zentkowski D, et al. Ionizing radiations sustain glioblastoma cell dedifferentiation to a stem-like phenotype through survivin: possible involvement in radioresistance. Cell Death Dis. 2014;5:e1543.CrossRefPubMedPubMedCentral
19.
go back to reference Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004;116:769–78.CrossRefPubMed Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004;116:769–78.CrossRefPubMed
20.
go back to reference Wodarz A, Gonzalez C. Connecting cancer to the asymmetric division of stem cells. Cell. 2006;124:1121–3.CrossRefPubMed Wodarz A, Gonzalez C. Connecting cancer to the asymmetric division of stem cells. Cell. 2006;124:1121–3.CrossRefPubMed
22.
go back to reference Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69–82.CrossRefPubMed Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69–82.CrossRefPubMed
23.
go back to reference Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97:703–16.CrossRefPubMed Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97:703–16.CrossRefPubMed
24.
go back to reference Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci. 2002;22:629–34.PubMed Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci. 2002;22:629–34.PubMed
26.
go back to reference Chen L, Chaichana KL, Kleinberg L, Ye X, Quinones-Hinojosa A, Redmond K. Glioblastoma recurrence patterns near neural stem cell regions. Radiother Oncol. 2015;116:294.CrossRefPubMedPubMedCentral Chen L, Chaichana KL, Kleinberg L, Ye X, Quinones-Hinojosa A, Redmond K. Glioblastoma recurrence patterns near neural stem cell regions. Radiother Oncol. 2015;116:294.CrossRefPubMedPubMedCentral
27.
go back to reference Adeberg S, König L, Bostel T, Harrabi S, Welzel T, Debus J, et al. Glioblastoma recurrence patterns after radiation therapy with regard to the subventricular zone. Int J Radiat Oncol Biol Phys. 2014;90:886–93.CrossRefPubMed Adeberg S, König L, Bostel T, Harrabi S, Welzel T, Debus J, et al. Glioblastoma recurrence patterns after radiation therapy with regard to the subventricular zone. Int J Radiat Oncol Biol Phys. 2014;90:886–93.CrossRefPubMed
28.
go back to reference Lim DA, Cha S, Mayo MC, Chen M-H, Keles E, VandenBerg S, et al. Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neuro Oncol. 2007;9:424–9.CrossRefPubMedPubMedCentral Lim DA, Cha S, Mayo MC, Chen M-H, Keles E, VandenBerg S, et al. Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neuro Oncol. 2007;9:424–9.CrossRefPubMedPubMedCentral
29.
go back to reference Jafri NF, Clarke JL, Weinberg V, Barani IJ, Cha S. Relationship of glioblastoma multiforme to the subventricular zone is associated with survival. Neuro Oncol. 2013;15:91–6.CrossRefPubMed Jafri NF, Clarke JL, Weinberg V, Barani IJ, Cha S. Relationship of glioblastoma multiforme to the subventricular zone is associated with survival. Neuro Oncol. 2013;15:91–6.CrossRefPubMed
30.
go back to reference Adeberg S, Bostel T, König L, Welzel T, Debus J, Combs SE. A comparison of long-term survivors and short-term survivors with glioblastoma, subventricular zone involvement: a predictive factor for survival? Radiat Oncol. 2014;9:95.CrossRefPubMedPubMedCentral Adeberg S, Bostel T, König L, Welzel T, Debus J, Combs SE. A comparison of long-term survivors and short-term survivors with glioblastoma, subventricular zone involvement: a predictive factor for survival? Radiat Oncol. 2014;9:95.CrossRefPubMedPubMedCentral
31.
go back to reference Chaichana KL, McGirt MJ, Frazier J, Attenello F, Guerrero-Cazares H, Quinones-Hinojosa A. Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J Neurooncol. 2008;89:219–24.CrossRefPubMed Chaichana KL, McGirt MJ, Frazier J, Attenello F, Guerrero-Cazares H, Quinones-Hinojosa A. Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J Neurooncol. 2008;89:219–24.CrossRefPubMed
32.
go back to reference Gong X, Schwartz PH, Linskey ME, Bota DA. Neural stem/progenitors and glioma stem-like cells have differential sensitivity to chemotherapy. Neurology. 2011;76:1126–34.CrossRefPubMedPubMedCentral Gong X, Schwartz PH, Linskey ME, Bota DA. Neural stem/progenitors and glioma stem-like cells have differential sensitivity to chemotherapy. Neurology. 2011;76:1126–34.CrossRefPubMedPubMedCentral
33.
go back to reference Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.CrossRefPubMed Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.CrossRefPubMed
34.
go back to reference Evers P, Lee PP, DeMarco J, Agazaryan N, Sayre JW, Selch M, et al. Irradiation of the potential cancer stem cell niches in the adult brain improves progression-free survival of patients with malignant glioma. BMC Cancer. 2010;10:384.CrossRefPubMedPubMedCentral Evers P, Lee PP, DeMarco J, Agazaryan N, Sayre JW, Selch M, et al. Irradiation of the potential cancer stem cell niches in the adult brain improves progression-free survival of patients with malignant glioma. BMC Cancer. 2010;10:384.CrossRefPubMedPubMedCentral
35.
go back to reference Slotman BJ, Eppinga WSC, de Haan PF, Lagerwaard FJ. Is irradiation of potential cancer stem cell niches in the subventricular zones indicated in GBM? Int J Radiat Oncol. 2011;81:S184.CrossRef Slotman BJ, Eppinga WSC, de Haan PF, Lagerwaard FJ. Is irradiation of potential cancer stem cell niches in the subventricular zones indicated in GBM? Int J Radiat Oncol. 2011;81:S184.CrossRef
36.
go back to reference Lee P, Eppinga W, Lagerwaard F, Cloughesy T, Slotman B, Nghiemphu PL, et al. Evaluation of high ipsilateral subventricular zone radiation therapy dose in glioblastoma: a pooled analysis. Int J Radiat Oncol Biol Phys. 2013;86:609–15.CrossRefPubMed Lee P, Eppinga W, Lagerwaard F, Cloughesy T, Slotman B, Nghiemphu PL, et al. Evaluation of high ipsilateral subventricular zone radiation therapy dose in glioblastoma: a pooled analysis. Int J Radiat Oncol Biol Phys. 2013;86:609–15.CrossRefPubMed
37.
go back to reference Gupta T, Nair V, Paul SN, Kannan S, Moiyadi A, Epari S, et al. Can irradiation of potential cancer stem-cell niche in the subventricular zone influence survival in patients with newly diagnosed glioblastoma? J Neurooncol. 2012;109:195–203.CrossRefPubMed Gupta T, Nair V, Paul SN, Kannan S, Moiyadi A, Epari S, et al. Can irradiation of potential cancer stem-cell niche in the subventricular zone influence survival in patients with newly diagnosed glioblastoma? J Neurooncol. 2012;109:195–203.CrossRefPubMed
38.
go back to reference Chen L, Guerrero-Cazares H, Ye X, Ford E, McNutt T, Kleinberg L, et al. Increased subventricular zone radiation dose correlates with survival in glioblastoma patients after gross total resection. Int J Radiat Oncol Biol Phys. 2013;86:616–22.CrossRefPubMedPubMedCentral Chen L, Guerrero-Cazares H, Ye X, Ford E, McNutt T, Kleinberg L, et al. Increased subventricular zone radiation dose correlates with survival in glioblastoma patients after gross total resection. Int J Radiat Oncol Biol Phys. 2013;86:616–22.CrossRefPubMedPubMedCentral
39.
go back to reference Elicin O, Inac E, Uzel EK, Karacam S, Uzel OE. Relationship between survival and increased radiation dose to subventricular zone in glioblastoma is controversial. J Neurooncol. 2014;118:413–9.CrossRefPubMed Elicin O, Inac E, Uzel EK, Karacam S, Uzel OE. Relationship between survival and increased radiation dose to subventricular zone in glioblastoma is controversial. J Neurooncol. 2014;118:413–9.CrossRefPubMed
40.
go back to reference Adeberg S, Ben HS, Bougatf N, Bernhardt D, Mohr A, Rieber J, et al. Do increased doses to stem-cell niches during radiation therapy improve glioblastoma survival? Stem Cells Int. 2016;2016:1–10.CrossRef Adeberg S, Ben HS, Bougatf N, Bernhardt D, Mohr A, Rieber J, et al. Do increased doses to stem-cell niches during radiation therapy improve glioblastoma survival? Stem Cells Int. 2016;2016:1–10.CrossRef
41.
go back to reference Smith AW, Mehta MP, Wernicke AG. Neural stem cells, the subventricular zone and radiotherapy: implications for treating glioblastoma. J Neurooncol. 2016;128:207.CrossRefPubMed Smith AW, Mehta MP, Wernicke AG. Neural stem cells, the subventricular zone and radiotherapy: implications for treating glioblastoma. J Neurooncol. 2016;128:207.CrossRefPubMed
42.
go back to reference Monje ML, Mizumatsu S, Fike JR, Palmer TD. Irradiation induces neural precursor-cell dysfunction. Nat Med. 2002;8:955–62.CrossRefPubMed Monje ML, Mizumatsu S, Fike JR, Palmer TD. Irradiation induces neural precursor-cell dysfunction. Nat Med. 2002;8:955–62.CrossRefPubMed
43.
go back to reference Gondi V, Pugh SL, Tome WA, Caine C, Corn B, Kanner A, et al. Preservation of memory with conformal avoidance of the hippocampal neural stem-cell compartment during whole-brain radiotherapy for brain metastases (RTOG 0933): a phase II multi-institutional trial. J Clin Oncol. 2014;32:3810–6.CrossRefPubMedPubMedCentral Gondi V, Pugh SL, Tome WA, Caine C, Corn B, Kanner A, et al. Preservation of memory with conformal avoidance of the hippocampal neural stem-cell compartment during whole-brain radiotherapy for brain metastases (RTOG 0933): a phase II multi-institutional trial. J Clin Oncol. 2014;32:3810–6.CrossRefPubMedPubMedCentral
44.
go back to reference McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg. 2009;110:156–62.CrossRefPubMed McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg. 2009;110:156–62.CrossRefPubMed
45.
go back to reference Vogelbaum MA, Jost S, Aghi MK, Heimberger AB, Sampson JH, Wen PY, et al. Application of novel response/progression measures for surgically delivered therapies for gliomas: Response Assessment in Neuro-Oncology (RANO) Working Group. Neurosurgery. 2012;70:234–43. discussion 243–4.CrossRefPubMed Vogelbaum MA, Jost S, Aghi MK, Heimberger AB, Sampson JH, Wen PY, et al. Application of novel response/progression measures for surgically delivered therapies for gliomas: Response Assessment in Neuro-Oncology (RANO) Working Group. Neurosurgery. 2012;70:234–43. discussion 243–4.CrossRefPubMed
46.
go back to reference Liang TH-K, Kuo S-H, Wang C-W, Chen W-Y, Hsu C-Y, Lai S-F, et al. Adverse prognosis and distinct progression patterns after concurrent chemoradiotherapy for glioblastoma with synchronous subventricular zone and corpus callosum invasion. Radiother Oncol. 2016;118:16–23. Liang TH-K, Kuo S-H, Wang C-W, Chen W-Y, Hsu C-Y, Lai S-F, et al. Adverse prognosis and distinct progression patterns after concurrent chemoradiotherapy for glioblastoma with synchronous subventricular zone and corpus callosum invasion. Radiother Oncol. 2016;118:16–23.
47.
go back to reference Barani IJ, Cuttino LW, Benedict SH, Todor D, Bump EA, Wu Y, et al. Neural stem cell-preserving external-beam radiotherapy of central nervous system malignancies. Int J Radiat Oncol Biol Phys. 2007;68:978–85.CrossRefPubMed Barani IJ, Cuttino LW, Benedict SH, Todor D, Bump EA, Wu Y, et al. Neural stem cell-preserving external-beam radiotherapy of central nervous system malignancies. Int J Radiat Oncol Biol Phys. 2007;68:978–85.CrossRefPubMed
48.
go back to reference Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28:1963–72.CrossRefPubMed Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28:1963–72.CrossRefPubMed
49.
go back to reference Aguirre A, Gallo V. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci. 2004;24:10530–41.CrossRefPubMed Aguirre A, Gallo V. Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci. 2004;24:10530–41.CrossRefPubMed
50.
go back to reference Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen H-J. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006;7:392–401.CrossRefPubMed Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen H-J. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006;7:392–401.CrossRefPubMed
51.
go back to reference Hegi ME, Diserens A-C, Gorlia T, Hamou M-F, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997–1003.CrossRefPubMed Hegi ME, Diserens A-C, Gorlia T, Hamou M-F, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997–1003.CrossRefPubMed
52.
go back to reference Gondi V, Hermann BP, Mehta MP, Tomé WA. Hippocampal dosimetry predicts neurocognitive function impairment after fractionated stereotactic radiotherapy for benign or low-grade adult brain tumors. Int J Radiat Oncol Biol Phys. 2013;85:348–54.CrossRefPubMed Gondi V, Hermann BP, Mehta MP, Tomé WA. Hippocampal dosimetry predicts neurocognitive function impairment after fractionated stereotactic radiotherapy for benign or low-grade adult brain tumors. Int J Radiat Oncol Biol Phys. 2013;85:348–54.CrossRefPubMed
53.
54.
go back to reference Chang EL, Akyurek S, Avalos T, Rebueno N, Spicer C, Garcia J, et al. Evaluation of peritumoral edema in the delineation of radiotherapy clinical target volumes for glioblastoma. Int J Radiat Oncol Biol Phys. 2007;68:144–50.CrossRefPubMed Chang EL, Akyurek S, Avalos T, Rebueno N, Spicer C, Garcia J, et al. Evaluation of peritumoral edema in the delineation of radiotherapy clinical target volumes for glioblastoma. Int J Radiat Oncol Biol Phys. 2007;68:144–50.CrossRefPubMed
55.
go back to reference Minniti G, Amelio D, Amichetti M, Salvati M, Muni R, Bozzao A, et al. Patterns of failure and comparison of different target volume delineations in patients with glioblastoma treated with conformal radiotherapy plus concomitant and adjuvant temozolomide. Radiother Oncol. 2010;97:377–81.CrossRefPubMed Minniti G, Amelio D, Amichetti M, Salvati M, Muni R, Bozzao A, et al. Patterns of failure and comparison of different target volume delineations in patients with glioblastoma treated with conformal radiotherapy plus concomitant and adjuvant temozolomide. Radiother Oncol. 2010;97:377–81.CrossRefPubMed
56.
go back to reference Wild-Bode C, Weller M, Rimner A, Dichgans J, Wick W. Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma. Cancer Res. 2001;61:2744–50.PubMed Wild-Bode C, Weller M, Rimner A, Dichgans J, Wick W. Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma. Cancer Res. 2001;61:2744–50.PubMed
Metadata
Title
Subventricular zones: new key targets for glioblastoma treatment
Authors
J. Khalifa
F. Tensaouti
A. Lusque
B. Plas
J.-A. Lotterie
A. Benouaich-Amiel
E. Uro-Coste
V. Lubrano
E. Cohen-Jonathan Moyal
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Radiation Oncology / Issue 1/2017
Electronic ISSN: 1748-717X
DOI
https://doi.org/10.1186/s13014-017-0791-2

Other articles of this Issue 1/2017

Radiation Oncology 1/2017 Go to the issue