Skip to main content
Top
Published in: Acta Neuropathologica 5/2007

Open Access 01-11-2007 | Review

Diffuse glioma growth: a guerilla war

Authors: An Claes, Albert J. Idema, Pieter Wesseling

Published in: Acta Neuropathologica | Issue 5/2007

Login to get access

Abstract

In contrast to almost all other brain tumors, diffuse gliomas infiltrate extensively in the neuropil. This growth pattern is a major factor in therapeutic failure. Diffuse infiltrative glioma cells show some similarities with guerilla warriors. Histopathologically, the tumor cells tend to invade individually or in small groups in between the dense network of neuronal and glial cell processes. Meanwhile, in large areas of diffuse gliomas the tumor cells abuse pre-existent “supply lines” for oxygen and nutrients rather than constructing their own. Radiological visualization of the invasive front of diffuse gliomas is difficult. Although the knowledge about migration of (tumor)cells is rapidly increasing, the exact molecular mechanisms underlying infiltration of glioma cells in the neuropil have not yet been elucidated. As the efficacy of conventional methods to fight diffuse infiltrative glioma cells is limited, a more targeted (“search & destroy”) tactic may be needed for these tumors. Hopefully, the study of original human glioma tissue and of genotypically and phenotypically relevant glioma models will soon provide information about the Achilles heel of diffuse infiltrative glioma cells that can be used for more effective therapeutic strategies.
Literature
1.
go back to reference Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, Breakefield XO, Snyder EY (2000) Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 97:12846–12851PubMed Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, Breakefield XO, Snyder EY (2000) Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 97:12846–12851PubMed
2.
go back to reference Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 34:45–60PubMed Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 34:45–60PubMed
3.
go back to reference Aronen HJ, Pardo FS, Kennedy DN, Belliveau JW, Packard SD, Hsu DW, Hochberg FH, Fischman AJ, Rosen BR (2000) High microvascular blood volume is associated with high glucose uptake and tumor angiogenesis in human gliomas. Clin Cancer Res 6:2189–2200PubMed Aronen HJ, Pardo FS, Kennedy DN, Belliveau JW, Packard SD, Hsu DW, Hochberg FH, Fischman AJ, Rosen BR (2000) High microvascular blood volume is associated with high glucose uptake and tumor angiogenesis in human gliomas. Clin Cancer Res 6:2189–2200PubMed
4.
go back to reference Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B (1990) CD44 is the principal cell surface receptor for hyaluronate. Cell 61:1303–1313PubMed Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B (1990) CD44 is the principal cell surface receptor for hyaluronate. Cell 61:1303–1313PubMed
5.
go back to reference Asano K, Duntsch CD, Zhou Q, Weimar JD, Bordelon D, Robertson JH, Pourmotabbed T (2004) Correlation of N-cadherin expression in high grade gliomas with tissue invasion. J Neurooncol 70:3–15PubMed Asano K, Duntsch CD, Zhou Q, Weimar JD, Bordelon D, Robertson JH, Pourmotabbed T (2004) Correlation of N-cadherin expression in high grade gliomas with tissue invasion. J Neurooncol 70:3–15PubMed
6.
go back to reference Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760PubMed Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760PubMed
7.
go back to reference Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843–7848PubMed Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843–7848PubMed
8.
go back to reference Barker FG, Chang SM, Huhn SL, Davis RL, Gutin PH, McDermott MW, Wilson CB, Prados MD (1997) Age and the risk of anaplasia in magnetic resonance-nonenhancing supratentorial cerebral tumors. Cancer 80:936–941PubMed Barker FG, Chang SM, Huhn SL, Davis RL, Gutin PH, McDermott MW, Wilson CB, Prados MD (1997) Age and the risk of anaplasia in magnetic resonance-nonenhancing supratentorial cerebral tumors. Cancer 80:936–941PubMed
9.
go back to reference Barker PB, Lin DD (2006) In vivo proton MR spectroscopy of the human brain. Prog Nucl Mag Res Sp 49:99–128 Barker PB, Lin DD (2006) In vivo proton MR spectroscopy of the human brain. Prog Nucl Mag Res Sp 49:99–128
10.
go back to reference Barnard RO, Geddes JF (1987) The incidence of multifocal cerebral gliomas. A histologic study of large hemisphere sections. Cancer 60:1519–1531PubMed Barnard RO, Geddes JF (1987) The incidence of multifocal cerebral gliomas. A histologic study of large hemisphere sections. Cancer 60:1519–1531PubMed
11.
go back to reference Batzdorf U, Malamud N (1963) The problem of multicentric gliomas. J Neurosurg 20:122–136PubMed Batzdorf U, Malamud N (1963) The problem of multicentric gliomas. J Neurosurg 20:122–136PubMed
12.
go back to reference Baumert BG, Rutten I, Dehing-Oberije C, Twijnstra A, Dirx MJ, Debougnoux-Huppertz RM, Lambin P, Kubat B (2006) A pathology-based substrate for target definition in radiosurgery of brain metastases. Int J Radiat Oncol Biol Phys 66:187–194PubMed Baumert BG, Rutten I, Dehing-Oberije C, Twijnstra A, Dirx MJ, Debougnoux-Huppertz RM, Lambin P, Kubat B (2006) A pathology-based substrate for target definition in radiosurgery of brain metastases. Int J Radiat Oncol Biol Phys 66:187–194PubMed
13.
go back to reference Bellail AC, Hunter SB, Brat DJ, Tan C, Van Meir EG (2004) Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int J Biochem Cell Biol 36:1046–1069PubMed Bellail AC, Hunter SB, Brat DJ, Tan C, Van Meir EG (2004) Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int J Biochem Cell Biol 36:1046–1069PubMed
14.
go back to reference Bello L, Lucini V, Carrabba G, Giussani C, Machluf M, Pluderi M, Nikas D, Zhang J, Tomei G, Villani RM, Carroll RS, Bikfalvi A, Black PM (2001) Simultaneous inhibition of glioma angiogenesis, cell proliferation, and invasion by a naturally occurring fragment of human metalloproteinase-2. Cancer Res 61:8730–8736PubMed Bello L, Lucini V, Carrabba G, Giussani C, Machluf M, Pluderi M, Nikas D, Zhang J, Tomei G, Villani RM, Carroll RS, Bikfalvi A, Black PM (2001) Simultaneous inhibition of glioma angiogenesis, cell proliferation, and invasion by a naturally occurring fragment of human metalloproteinase-2. Cancer Res 61:8730–8736PubMed
15.
go back to reference Bello L, Lucini V, Giussani C, Carrabba G, Pluderi M, Scaglione F, Tomei G, Villani R, Black PM, Bikfalvi A, Carroll RS (2003) IS20I, a specific alphavbeta3 integrin inhibitor, reduces glioma growth in vivo. Neurosurgery 52:177–185PubMed Bello L, Lucini V, Giussani C, Carrabba G, Pluderi M, Scaglione F, Tomei G, Villani R, Black PM, Bikfalvi A, Carroll RS (2003) IS20I, a specific alphavbeta3 integrin inhibitor, reduces glioma growth in vivo. Neurosurgery 52:177–185PubMed
16.
go back to reference Benard F, Romsa J, Hustinx R (2003) Imaging gliomas with positron emission tomography and single-photon emission computed tomography. Semin Nucl Med 33:148–162PubMed Benard F, Romsa J, Hustinx R (2003) Imaging gliomas with positron emission tomography and single-photon emission computed tomography. Semin Nucl Med 33:148–162PubMed
17.
go back to reference Berkman RA, Clark WC, Saxena A, Robertson JT, Oldfield EH, Ali IU (1992) Clonal composition of glioblastoma multiforme. J Neurosurg 77:432–437PubMed Berkman RA, Clark WC, Saxena A, Robertson JT, Oldfield EH, Ali IU (1992) Clonal composition of glioblastoma multiforme. J Neurosurg 77:432–437PubMed
18.
go back to reference Bernas LM, Foster PJ, Rutt BK (2007) Magnetic resonance imaging of in vitro glioma cell invasion. J Neurosurg 106:306–313PubMed Bernas LM, Foster PJ, Rutt BK (2007) Magnetic resonance imaging of in vitro glioma cell invasion. J Neurosurg 106:306–313PubMed
19.
go back to reference Bernsen H, van der Laak J, Kusters B, Van der Ven A, Wesseling P (2005) Gliomatosis cerebri: quantitative proof of vessel recruitment by cooptation instead of angiogenesis. J Neurosurg 103:702–706PubMedCrossRef Bernsen H, van der Laak J, Kusters B, Van der Ven A, Wesseling P (2005) Gliomatosis cerebri: quantitative proof of vessel recruitment by cooptation instead of angiogenesis. J Neurosurg 103:702–706PubMedCrossRef
20.
go back to reference Bettinger I, Thanos S, Paulus W (2002) Microglia promote glioma migration. Acta Neuropathol (Berl) 103:351–355 Bettinger I, Thanos S, Paulus W (2002) Microglia promote glioma migration. Acta Neuropathol (Berl) 103:351–355
21.
go back to reference Brack SS, Silacci M, Birchler M, Neri D (2006) Tumor-targeting properties of novel antibodies specific to the large isoform of tenascin-C. Clin Cancer Res 12:3200–3208PubMed Brack SS, Silacci M, Birchler M, Neri D (2006) Tumor-targeting properties of novel antibodies specific to the large isoform of tenascin-C. Clin Cancer Res 12:3200–3208PubMed
22.
go back to reference Brat DJ, Van Meir EG (2001) Glomeruloid microvascular proliferation orchestrated by VPF/VEGF: a new world of angiogenesis research. Am J Pathol 158:789–796PubMed Brat DJ, Van Meir EG (2001) Glomeruloid microvascular proliferation orchestrated by VPF/VEGF: a new world of angiogenesis research. Am J Pathol 158:789–796PubMed
23.
go back to reference Brat DJ, Castellano-Sanchez AA, Hunter SB, Pecot M, Cohen C, Hammond EH, Devi SN, Kaur B, Van Meir EG (2004) Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res 64:920–927PubMed Brat DJ, Castellano-Sanchez AA, Hunter SB, Pecot M, Cohen C, Hammond EH, Devi SN, Kaur B, Van Meir EG (2004) Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res 64:920–927PubMed
24.
go back to reference Brown MC, Cary LA, Jamieson JS, Cooper JA, Turner CE (2005) Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol Biol Cell 16:4316–4328PubMed Brown MC, Cary LA, Jamieson JS, Cooper JA, Turner CE (2005) Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol Biol Cell 16:4316–4328PubMed
25.
go back to reference Burger PC (1987) The anatomy of astrocytomas. Mayo Clin Proc 62:527–529PubMed Burger PC (1987) The anatomy of astrocytomas. Mayo Clin Proc 62:527–529PubMed
26.
go back to reference Burger PC, Kleihues P (1989) Cytologic composition of the untreated glioblastoma with implications for evaluation of needle biopsies. Cancer 63:2014–2023PubMed Burger PC, Kleihues P (1989) Cytologic composition of the untreated glioblastoma with implications for evaluation of needle biopsies. Cancer 63:2014–2023PubMed
27.
go back to reference Burger PC, Heinz ER, Shibata T, Kleihues P (1988) Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg 68:698–704PubMed Burger PC, Heinz ER, Shibata T, Kleihues P (1988) Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg 68:698–704PubMed
28.
go back to reference Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W (2006) Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: intergroup radiation therapy oncology group trial 9402. J Clin Oncol 24:2707–2714PubMed Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W (2006) Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: intergroup radiation therapy oncology group trial 9402. J Clin Oncol 24:2707–2714PubMed
29.
go back to reference Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296:1655–1657PubMed Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296:1655–1657PubMed
30.
go back to reference Cao Y, Sundgren PC, Tsien CI, Chenevert TT, Junck L (2006) Physiologic and metabolic magnetic resonance imaging in gliomas. J Clin Oncol 24:1228–1235PubMed Cao Y, Sundgren PC, Tsien CI, Chenevert TT, Junck L (2006) Physiologic and metabolic magnetic resonance imaging in gliomas. J Clin Oncol 24:1228–1235PubMed
31.
go back to reference CBTRUS (2006) CBTRUS statistical report. Primary brain tumors in the United States, 1998–2002. Central Brain Tumor Registry of the United States. http://www.cbtrus.org CBTRUS (2006) CBTRUS statistical report. Primary brain tumors in the United States, 1998–2002. Central Brain Tumor Registry of the United States. http://​www.​cbtrus.​org
32.
go back to reference Chan AY, Coniglio SJ, Chuang YY, Michaelson D, Knaus UG, Philips MR, Symons M (2005) Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 24:7821–7829PubMed Chan AY, Coniglio SJ, Chuang YY, Michaelson D, Knaus UG, Philips MR, Symons M (2005) Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 24:7821–7829PubMed
33.
go back to reference Chicoine MR, Silbergeld DL (1997) Mitogens as motogens. J Neurooncol 35:249–257PubMed Chicoine MR, Silbergeld DL (1997) Mitogens as motogens. J Neurooncol 35:249–257PubMed
34.
go back to reference Chuang YY, Tran NL, Rusk N, Nakada M, Berens ME, Symons M (2004) Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res 64:8271–8275PubMed Chuang YY, Tran NL, Rusk N, Nakada M, Berens ME, Symons M (2004) Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res 64:8271–8275PubMed
35.
go back to reference Croteau D, Scarpace L, Hearshen D, Gutierrez J, Fisher JL, Rock JP, Mikkelsen T (2001) Correlation between magnetic resonance spectroscopy imaging and image-guided biopsies: semiquantitative and qualitative histopathological analyses of patients with untreated glioma. Neurosurgery 49:823–829PubMed Croteau D, Scarpace L, Hearshen D, Gutierrez J, Fisher JL, Rock JP, Mikkelsen T (2001) Correlation between magnetic resonance spectroscopy imaging and image-guided biopsies: semiquantitative and qualitative histopathological analyses of patients with untreated glioma. Neurosurgery 49:823–829PubMed
36.
go back to reference Cummings TJ, Hulette CM, Longee DC, Bottom KS, McLendon RE, Chu CT (1999) Gliomatosis cerebri: cytologic and autopsy findings in a case involving the entire neuraxis. Clin Neuropathol 18:190–197PubMed Cummings TJ, Hulette CM, Longee DC, Bottom KS, McLendon RE, Chu CT (1999) Gliomatosis cerebri: cytologic and autopsy findings in a case involving the entire neuraxis. Clin Neuropathol 18:190–197PubMed
37.
go back to reference Dai B, Kang SH, Gong W, Liu M, Aldape KD, Sawaya R, Huang S (2007) Aberrant FoxM1B expression increases matrix metalloproteinase-2 transcription and enhances the invasion of glioma cells. Oncogene. doi:10.1038/sj.onc.1210443 Dai B, Kang SH, Gong W, Liu M, Aldape KD, Sawaya R, Huang S (2007) Aberrant FoxM1B expression increases matrix metalloproteinase-2 transcription and enhances the invasion of glioma cells. Oncogene. doi:​10.​1038/​sj.​onc.​1210443
38.
go back to reference Dandy WE (1928) Removal of the right hemisphere for certain tumors with hemiplegia: preliminary report. J Am Med Assoc 90:823–825 Dandy WE (1928) Removal of the right hemisphere for certain tumors with hemiplegia: preliminary report. J Am Med Assoc 90:823–825
39.
go back to reference De Vleeschouwer S, Rapp M, Sorg RV, Steiger HJ, Stummer W, van Gool S, Sabel M (2006) Dendritic cell vaccination in patients with malignant gliomas: current status and future directions. Neurosurgery 59:988–999PubMed De Vleeschouwer S, Rapp M, Sorg RV, Steiger HJ, Stummer W, van Gool S, Sabel M (2006) Dendritic cell vaccination in patients with malignant gliomas: current status and future directions. Neurosurgery 59:988–999PubMed
40.
go back to reference Demuth T, Berens ME (2004) Molecular mechanisms of glioma cell migration and invasion. J Neurooncol 70:217–228PubMed Demuth T, Berens ME (2004) Molecular mechanisms of glioma cell migration and invasion. J Neurooncol 70:217–228PubMed
41.
go back to reference Di Costanzo A, Scarabino T, Trojsi F, Giannatempo GM, Popolizio T, Catapano D, Bonavita S, Maggialetti N, Tosetti M, Salvolini U, d’Angelo VA, Tedeschi G (2006) Multiparametric 3T MR approach to the assessment of cerebral gliomas: tumor extent and malignancy. Neuroradiology 48:622–631PubMed Di Costanzo A, Scarabino T, Trojsi F, Giannatempo GM, Popolizio T, Catapano D, Bonavita S, Maggialetti N, Tosetti M, Salvolini U, d’Angelo VA, Tedeschi G (2006) Multiparametric 3T MR approach to the assessment of cerebral gliomas: tumor extent and malignancy. Neuroradiology 48:622–631PubMed
42.
go back to reference Duerr EM, Rollbrocker B, Hayashi Y, Peters N, Meyer-Puttlitz B, Louis DN, Schramm J, Wiestler OD, Parsons R, Eng C, von DA (1998) PTEN mutations in gliomas and glioneuronal tumors. Oncogene 16:2259–2264 Duerr EM, Rollbrocker B, Hayashi Y, Peters N, Meyer-Puttlitz B, Louis DN, Schramm J, Wiestler OD, Parsons R, Eng C, von DA (1998) PTEN mutations in gliomas and glioneuronal tumors. Oncogene 16:2259–2264
43.
go back to reference Earnest F, Kelly PJ, Scheithauer BW, Kall BA, Cascino TL, Ehman RL, Forbes GS, Axley PL (1988) Cerebral astrocytomas: histopathologic correlation of MR and CT contrast enhancement with stereotactic biopsy. Radiology 166:823–827PubMed Earnest F, Kelly PJ, Scheithauer BW, Kall BA, Cascino TL, Ehman RL, Forbes GS, Axley PL (1988) Cerebral astrocytomas: histopathologic correlation of MR and CT contrast enhancement with stereotactic biopsy. Radiology 166:823–827PubMed
44.
go back to reference Eckerich C, Zapf S, Fillbrandt R, Loges S, Westphal M, Lamszus K (2007) Hypoxia can induce c-Met expression in glioma cells and enhance SF/HGF-induced cell migration. Int J Cancer 121:276–283PubMed Eckerich C, Zapf S, Fillbrandt R, Loges S, Westphal M, Lamszus K (2007) Hypoxia can induce c-Met expression in glioma cells and enhance SF/HGF-induced cell migration. Int J Cancer 121:276–283PubMed
45.
go back to reference Ehtesham M, Winston JA, Kabos P, Thompson RC (2006) CXCR4 expression mediates glioma cell invasiveness. Oncogene 25:2801–2806PubMed Ehtesham M, Winston JA, Kabos P, Thompson RC (2006) CXCR4 expression mediates glioma cell invasiveness. Oncogene 25:2801–2806PubMed
46.
go back to reference El Andaloussi A, Lesniak MS (2006) An increase in CD4+CD25+FOXP3+ regulatory T cells in tumor-infiltrating lymphocytes of human glioblastoma multiforme. Neuro Oncol 8:234–243PubMed El Andaloussi A, Lesniak MS (2006) An increase in CD4+CD25+FOXP3+ regulatory T cells in tumor-infiltrating lymphocytes of human glioblastoma multiforme. Neuro Oncol 8:234–243PubMed
47.
go back to reference Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629–635PubMed Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629–635PubMed
48.
go back to reference Everson RG, Gromeier M, Sampson JH (2007) Viruses in the treatment of malignant glioma. Expert Rev Neurother 7:321–324PubMed Everson RG, Gromeier M, Sampson JH (2007) Viruses in the treatment of malignant glioma. Expert Rev Neurother 7:321–324PubMed
49.
go back to reference Fischer I, Gagner JP, Law M, Newcomb EW, Zagzag D (2005) Angiogenesis in gliomas: biology and molecular pathophysiology. Brain Pathol 15:297–310PubMedCrossRef Fischer I, Gagner JP, Law M, Newcomb EW, Zagzag D (2005) Angiogenesis in gliomas: biology and molecular pathophysiology. Brain Pathol 15:297–310PubMedCrossRef
50.
go back to reference Foehr ED, Lorente G, Kuo J, Ram R, Nikolich K, Urfer R (2006) Targeting of the receptor protein tyrosine phosphatase beta with a monoclonal antibody delays tumor growth in a glioblastoma model. Cancer Res 66:2271–2278PubMed Foehr ED, Lorente G, Kuo J, Ram R, Nikolich K, Urfer R (2006) Targeting of the receptor protein tyrosine phosphatase beta with a monoclonal antibody delays tumor growth in a glioblastoma model. Cancer Res 66:2271–2278PubMed
51.
go back to reference Folkman J (1972) Anti-angiogenesis: new concept for therapy of solid tumors. Ann Surg 175:409–416PubMed Folkman J (1972) Anti-angiogenesis: new concept for therapy of solid tumors. Ann Surg 175:409–416PubMed
52.
go back to reference Fukushima Y, Ohnishi T, Arita N, Hayakawa T, Sekiguchi K (1998) Integrin alpha3beta1-mediated interaction with laminin-5 stimulates adhesion, migration and invasion of malignant glioma cells. Int J Cancer 76:63–72PubMed Fukushima Y, Ohnishi T, Arita N, Hayakawa T, Sekiguchi K (1998) Integrin alpha3beta1-mediated interaction with laminin-5 stimulates adhesion, migration and invasion of malignant glioma cells. Int J Cancer 76:63–72PubMed
53.
go back to reference Furukawa K, Kumon Y, Harada H, Kohno S, Nagato S, Teraoka M, Fujiwara S, Nakagawa K, Hamada K, Ohnishi T (2006) PTEN gene transfer suppresses the invasive potential of human malignant gliomas by regulating cell invasion-related molecules. Int J Oncol 29:73–81PubMed Furukawa K, Kumon Y, Harada H, Kohno S, Nagato S, Teraoka M, Fujiwara S, Nakagawa K, Hamada K, Ohnishi T (2006) PTEN gene transfer suppresses the invasive potential of human malignant gliomas by regulating cell invasion-related molecules. Int J Oncol 29:73–81PubMed
54.
go back to reference Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De VS, 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 Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De VS, 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
55.
go back to reference Ganslandt O, Stadlbauer A, Fahlbusch R, Kamada K, Buslei R, Blumcke I, Moser E, Nimsky C (2005) Proton magnetic resonance spectroscopic imaging integrated into image-guided surgery: correlation to standard magnetic resonance imaging and tumor cell density. Neurosurgery 56:291–298PubMed Ganslandt O, Stadlbauer A, Fahlbusch R, Kamada K, Buslei R, Blumcke I, Moser E, Nimsky C (2005) Proton magnetic resonance spectroscopic imaging integrated into image-guided surgery: correlation to standard magnetic resonance imaging and tumor cell density. Neurosurgery 56:291–298PubMed
56.
go back to reference Gardner WJ (1932) Removal of the right hemisphere for infiltrating glioma. Arch Neurol Psychiat Chic 28:470 Gardner WJ (1932) Removal of the right hemisphere for infiltrating glioma. Arch Neurol Psychiat Chic 28:470
57.
go back to reference Giese A, Westphal M (1996) Glioma invasion in the central nervous system. Neurosurgery 39:235–250PubMed Giese A, Westphal M (1996) Glioma invasion in the central nervous system. Neurosurgery 39:235–250PubMed
58.
go back to reference Giese A, Kluwe L, Laube B, Meissner H, Berens ME, Westphal M (1996) Migration of human glioma cells on myelin. Neurosurgery 38:755–764PubMed Giese A, Kluwe L, Laube B, Meissner H, Berens ME, Westphal M (1996) Migration of human glioma cells on myelin. Neurosurgery 38:755–764PubMed
59.
go back to reference Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624–1636PubMed Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624–1636PubMed
60.
go back to reference Gladson CL (1999) The extracellular matrix of gliomas: modulation of cell function. J Neuropathol Exp Neurol 58:1029–1040PubMed Gladson CL (1999) The extracellular matrix of gliomas: modulation of cell function. J Neuropathol Exp Neurol 58:1029–1040PubMed
61.
go back to reference Goetz CM, Rachinger W, Decker M, Gildehaus FJ, Stocker S, Jung G, Tatsch K, Tonn JC, Reulen HJ (2005) Distribution of labelled anti-tenascin antibodies and fragments after injection into intact or partly resected C6-gliomas in rats. Cancer Immunol Immunother 54:337–344PubMed Goetz CM, Rachinger W, Decker M, Gildehaus FJ, Stocker S, Jung G, Tatsch K, Tonn JC, Reulen HJ (2005) Distribution of labelled anti-tenascin antibodies and fragments after injection into intact or partly resected C6-gliomas in rats. Cancer Immunol Immunother 54:337–344PubMed
62.
go back to reference Goldberg L, Kloog Y (2006) A Ras inhibitor tilts the balance between Rac and Rho and blocks phosphatidylinositol 3-kinase-dependent glioblastoma cell migration. Cancer Res 66:11709–11717PubMed Goldberg L, Kloog Y (2006) A Ras inhibitor tilts the balance between Rac and Rho and blocks phosphatidylinositol 3-kinase-dependent glioblastoma cell migration. Cancer Res 66:11709–11717PubMed
63.
go back to reference Goldbrunner RH, Bernstein JJ, Tonn JC (1999) Cell-extracellular matrix interaction in glioma invasion. Acta Neurochir (Wien ) 141:295–305 Goldbrunner RH, Bernstein JJ, Tonn JC (1999) Cell-extracellular matrix interaction in glioma invasion. Acta Neurochir (Wien ) 141:295–305
64.
go back to reference Gondi CS, Lakka SS, Dinh DH, Olivero WC, Gujrati M, Rao JS (2004) Downregulation of uPA, uPAR and MMP-9 using small, interfering, hairpin RNA (siRNA) inhibits glioma cell invasion, angiogenesis and tumor growth. Neuron Glia Biol 1:165–176PubMed Gondi CS, Lakka SS, Dinh DH, Olivero WC, Gujrati M, Rao JS (2004) Downregulation of uPA, uPAR and MMP-9 using small, interfering, hairpin RNA (siRNA) inhibits glioma cell invasion, angiogenesis and tumor growth. Neuron Glia Biol 1:165–176PubMed
65.
go back to reference Grauer OM, Nierkens S, Bennink E, Toonen LW, Boon L, Wesseling P, Sutmuller RP, Adema GJ (2007) CD4+FoxP3+ regulatory T cells gradually accumulate in gliomas during tumor growth and efficiently suppress antiglioma immune responses in vivo. Int J Cancer 121:95–105PubMed Grauer OM, Nierkens S, Bennink E, Toonen LW, Boon L, Wesseling P, Sutmuller RP, Adema GJ (2007) CD4+FoxP3+ regulatory T cells gradually accumulate in gliomas during tumor growth and efficiently suppress antiglioma immune responses in vivo. Int J Cancer 121:95–105PubMed
66.
go back to reference Grotegut S, von SD, Christofori G, Lehembre F (2006) Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J 25:3534–3545 Grotegut S, von SD, Christofori G, Lehembre F (2006) Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J 25:3534–3545
67.
go back to reference Guha A, Mukherjee J (2004) Advances in the biology of astrocytomas. Curr Opin Neurol 17:655–662PubMed Guha A, Mukherjee J (2004) Advances in the biology of astrocytomas. Curr Opin Neurol 17:655–662PubMed
68.
go back to reference Guo P, Imanishi Y, Cackowski FC, Jarzynka MJ, Tao HQ, Nishikawa R, Hirose T, Hu B, Cheng SY (2005) Up-regulation of angiopoietin-2, matrix metalloprotease-2, membrane type 1 metalloprotease, and laminin 5 gamma 2 correlates with the invasiveness of human glioma. Am J Pathol 166:877–890PubMed Guo P, Imanishi Y, Cackowski FC, Jarzynka MJ, Tao HQ, Nishikawa R, Hirose T, Hu B, Cheng SY (2005) Up-regulation of angiopoietin-2, matrix metalloprotease-2, membrane type 1 metalloprotease, and laminin 5 gamma 2 correlates with the invasiveness of human glioma. Am J Pathol 166:877–890PubMed
69.
go back to reference Gupta M, Djalilvand A, Brat DJ (2005) Clarifying the diffuse gliomas: an update on the morphologic features and markers that discriminate oligodendroglioma from astrocytoma. Am J Clin Pathol 124:755–768PubMed Gupta M, Djalilvand A, Brat DJ (2005) Clarifying the diffuse gliomas: an update on the morphologic features and markers that discriminate oligodendroglioma from astrocytoma. Am J Clin Pathol 124:755–768PubMed
70.
go back to reference Harpold HL, Alvord EC Jr, Swanson KR (2007) The evolution of mathematical modeling of glioma proliferation and invasion. J Neuropathol Exp Neurol 66:1–9PubMed Harpold HL, Alvord EC Jr, Swanson KR (2007) The evolution of mathematical modeling of glioma proliferation and invasion. J Neuropathol Exp Neurol 66:1–9PubMed
71.
go back to reference Haubner R, Weber WA, Beer AJ, Vabuliene E, Reim D, Sarbia M, Becker KF, Goebel M, Hein R, Wester HJ, Kessler H, Schwaiger M (2005) Noninvasive visualization of the activated alphavbeta3 integrin in cancer patients by positron emission tomography and [18F]Galacto-RGD. PLoS Med 2:e70PubMed Haubner R, Weber WA, Beer AJ, Vabuliene E, Reim D, Sarbia M, Becker KF, Goebel M, Hein R, Wester HJ, Kessler H, Schwaiger M (2005) Noninvasive visualization of the activated alphavbeta3 integrin in cancer patients by positron emission tomography and [18F]Galacto-RGD. PLoS Med 2:e70PubMed
72.
go back to reference Henson JW, Gaviani P, Gonzalez RG (2005) MRI in treatment of adult gliomas. Lancet Oncol 6:167–175PubMed Henson JW, Gaviani P, Gonzalez RG (2005) MRI in treatment of adult gliomas. Lancet Oncol 6:167–175PubMed
73.
go back to reference Hentschel SJ, Lang FF (2003) Current surgical management of glioblastoma. Cancer J 9:113–125PubMed Hentschel SJ, Lang FF (2003) Current surgical management of glioblastoma. Cancer J 9:113–125PubMed
74.
go back to reference Higuchi M, Ohnishi T, Arita N, Hiraga S, Hayakawa T (1993) Expression of tenascin in human gliomas: its relation to histological malignancy, tumor dedifferentiation and angiogenesis. Acta Neuropathol (Berl) 85:481–487 Higuchi M, Ohnishi T, Arita N, Hiraga S, Hayakawa T (1993) Expression of tenascin in human gliomas: its relation to histological malignancy, tumor dedifferentiation and angiogenesis. Acta Neuropathol (Berl) 85:481–487
75.
go back to reference Hockaday DC, Shen S, Fiveash J, Raubitschek A, Colcher D, Liu A, Alvarez V, Mamelak AN (2005) Imaging glioma extent with 131I-TM-601. J Nucl Med 46:580–586PubMed Hockaday DC, Shen S, Fiveash J, Raubitschek A, Colcher D, Liu A, Alvarez V, Mamelak AN (2005) Imaging glioma extent with 131I-TM-601. J Nucl Med 46:580–586PubMed
76.
go back to reference Hu B, Guo P, Fang Q, Tao HQ, Wang D, Nagane M, Huang HJ, Gunji Y, Nishikawa R, Alitalo K, Cavenee WK, Cheng SY (2003) Angiopoietin-2 induces human glioma invasion through the activation of matrix metalloprotease-2. Proc Natl Acad Sci USA 100:8904–8909PubMed Hu B, Guo P, Fang Q, Tao HQ, Wang D, Nagane M, Huang HJ, Gunji Y, Nishikawa R, Alitalo K, Cavenee WK, Cheng SY (2003) Angiopoietin-2 induces human glioma invasion through the activation of matrix metalloprotease-2. Proc Natl Acad Sci USA 100:8904–8909PubMed
77.
go back to reference Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687PubMed Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687PubMed
78.
go back to reference Jackson A, Kassner A, Annesley-Williams D, Reid H, Zhu XP, Li KL (2002) Abnormalities in the recirculation phase of contrast agent bolus passage in cerebral gliomas: comparison with relative blood volume and tumor grade. AJNR Am J Neuroradiol 23:7–14PubMed Jackson A, Kassner A, Annesley-Williams D, Reid H, Zhu XP, Li KL (2002) Abnormalities in the recirculation phase of contrast agent bolus passage in cerebral gliomas: comparison with relative blood volume and tumor grade. AJNR Am J Neuroradiol 23:7–14PubMed
79.
go back to reference Juliano RL (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42:283–323PubMed Juliano RL (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42:283–323PubMed
80.
go back to reference Keime-Guibert F, Chinot O, Taillandier L, Cartalat-Carel S, Frenay M, Kantor G, Guillamo JS, Jadaud E, Colin P, Bondiau PY, Menei P, Loiseau H, Bernier V, Honnorat J, Barrie M, Mokhtari K, Mazeron JJ, Bissery A, Delattre JY (2007) Radiotherapy for glioblastoma in the elderly. N Engl J Med 356:1527–1535PubMed Keime-Guibert F, Chinot O, Taillandier L, Cartalat-Carel S, Frenay M, Kantor G, Guillamo JS, Jadaud E, Colin P, Bondiau PY, Menei P, Loiseau H, Bernier V, Honnorat J, Barrie M, Mokhtari K, Mazeron JJ, Bissery A, Delattre JY (2007) Radiotherapy for glioblastoma in the elderly. N Engl J Med 356:1527–1535PubMed
81.
go back to reference Kim MS, Park MJ, Kim SJ, Lee CH, Yoo H, Shin SH, Song ES, Lee SH (2005) Emodin suppresses hyaluronic acid-induced MMP-9 secretion and invasion of glioma cells. Int J Oncol 27:839–846PubMed Kim MS, Park MJ, Kim SJ, Lee CH, Yoo H, Shin SH, Song ES, Lee SH (2005) Emodin suppresses hyaluronic acid-induced MMP-9 secretion and invasion of glioma cells. Int J Oncol 27:839–846PubMed
82.
go back to reference Kircher MF, Mahmood U, King RS, Weissleder R, Josephson L (2003) A multimodal nanoparticle for preoperative magnetic resonance imaging and intraoperative optical brain tumor delineation. Cancer Res 63:8122–8125PubMed Kircher MF, Mahmood U, King RS, Weissleder R, Josephson L (2003) A multimodal nanoparticle for preoperative magnetic resonance imaging and intraoperative optical brain tumor delineation. Cancer Res 63:8122–8125PubMed
83.
go back to reference Koga K, Todaka T, Morioka M, Hamada J, Kai Y, Yano S, Okamura A, Takakura N, Suda T, Ushio Y (2001) Expression of angiopoietin-2 in human glioma cells and its role for angiogenesis. Cancer Res 61:6248–6254PubMed Koga K, Todaka T, Morioka M, Hamada J, Kai Y, Yano S, Okamura A, Takakura N, Suda T, Ushio Y (2001) Expression of angiopoietin-2 in human glioma cells and its role for angiogenesis. Cancer Res 61:6248–6254PubMed
84.
go back to reference Koochekpour S, Merzak A, Pilkington GJ (1995) Growth factors and gangliosides stimulate laminin production by human glioma cells in vitro. Neurosci Lett 186:53–56PubMed Koochekpour S, Merzak A, Pilkington GJ (1995) Growth factors and gangliosides stimulate laminin production by human glioma cells in vitro. Neurosci Lett 186:53–56PubMed
85.
go back to reference Kunigal S, Gondi CS, Gujrati M, Lakka SS, Dinh DH, Olivero WC, Rao JS (2006) SPARC-induced migration of glioblastoma cell lines via uPA-uPAR signaling and activation of small GTPase RhoA. Int J Oncol 29:1349–1357PubMed Kunigal S, Gondi CS, Gujrati M, Lakka SS, Dinh DH, Olivero WC, Rao JS (2006) SPARC-induced migration of glioblastoma cell lines via uPA-uPAR signaling and activation of small GTPase RhoA. Int J Oncol 29:1349–1357PubMed
86.
go back to reference Kunkel P, Ulbricht U, Bohlen P, Brockmann MA, Fillbrandt R, Stavrou D, Westphal M, Lamszus K (2001) Inhibition of glioma angiogenesis and growth in vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Res 61:6624–6628PubMed Kunkel P, Ulbricht U, Bohlen P, Brockmann MA, Fillbrandt R, Stavrou D, Westphal M, Lamszus K (2001) Inhibition of glioma angiogenesis and growth in vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Res 61:6624–6628PubMed
87.
go back to reference Kunwar S, Prados MD, Chang SM, Berger MS, Lang FF, Piepmeier JM, Sampson JH, Ram Z, Gutin PH, Gibbons RD, Aldape KD, Croteau DJ, Sherman JW, Puri RK (2007) Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the Cintredekin Besudotox Intraparenchymal Study Group. J Clin Oncol 25:837–844PubMed Kunwar S, Prados MD, Chang SM, Berger MS, Lang FF, Piepmeier JM, Sampson JH, Ram Z, Gutin PH, Gibbons RD, Aldape KD, Croteau DJ, Sherman JW, Puri RK (2007) Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the Cintredekin Besudotox Intraparenchymal Study Group. J Clin Oncol 25:837–844PubMed
88.
go back to reference Kyritsis AP, Levin VA, Yung WK, Leeds NE (1993) Imaging patterns of multifocal gliomas. Eur J Radiol 16:163–170PubMed Kyritsis AP, Levin VA, Yung WK, Leeds NE (1993) Imaging patterns of multifocal gliomas. Eur J Radiol 16:163–170PubMed
89.
go back to reference Lafitte F, Morel-Precetti S, Martin-Duverneuil N, Guermazi A, Brunet E, Heran F, Chiras J (2001) Multiple glioblastomas: CT and MR features. Eur Radiol 11:131–136PubMed Lafitte F, Morel-Precetti S, Martin-Duverneuil N, Guermazi A, Brunet E, Heran F, Chiras J (2001) Multiple glioblastomas: CT and MR features. Eur Radiol 11:131–136PubMed
90.
go back to reference Lakka SS, Gondi CS, Yanamandra N, Olivero WC, Dinh DH, Gujrati M, Rao JS (2004) Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis. Oncogene 23:4681–4689PubMed Lakka SS, Gondi CS, Yanamandra N, Olivero WC, Dinh DH, Gujrati M, Rao JS (2004) Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis. Oncogene 23:4681–4689PubMed
91.
92.
go back to reference Lamszus K, Kunkel P, Westphal M (2003) Invasion as limitation to anti-angiogenic glioma therapy. Acta Neurochir Suppl 88:169–177PubMed Lamszus K, Kunkel P, Westphal M (2003) Invasion as limitation to anti-angiogenic glioma therapy. Acta Neurochir Suppl 88:169–177PubMed
93.
go back to reference Lang FF, Gilbert MR (2006) Diffusely infiltrative low-grade gliomas in adults. J Clin Oncol 24:1236–1245PubMed Lang FF, Gilbert MR (2006) Diffusely infiltrative low-grade gliomas in adults. J Clin Oncol 24:1236–1245PubMed
94.
go back to reference Lange R, Peng X, Wimmer E, Lipp M, Bernhardt G (2001) The poliovirus receptor CD155 mediates cell-to-matrix contacts by specifically binding to vitronectin. Virology 285:218–227PubMed Lange R, Peng X, Wimmer E, Lipp M, Bernhardt G (2001) The poliovirus receptor CD155 mediates cell-to-matrix contacts by specifically binding to vitronectin. Virology 285:218–227PubMed
95.
go back to reference Laperriere N, Zuraw L, Cairncross G (2002) Radiotherapy for newly diagnosed malignant glioma in adults: a systematic review. Radiother Oncol 64:259–273PubMed Laperriere N, Zuraw L, Cairncross G (2002) Radiotherapy for newly diagnosed malignant glioma in adults: a systematic review. Radiother Oncol 64:259–273PubMed
96.
go back to reference Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546PubMed Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13:534–546PubMed
97.
go back to reference Leavesley DI, Ferguson GD, Wayner EA, Cheresh DA (1992) Requirement of the integrin beta 3 subunit for carcinoma cell spreading or migration on vitronectin and fibrinogen. J Cell Biol 117:1101–1107PubMed Leavesley DI, Ferguson GD, Wayner EA, Cheresh DA (1992) Requirement of the integrin beta 3 subunit for carcinoma cell spreading or migration on vitronectin and fibrinogen. J Cell Biol 117:1101–1107PubMed
98.
go back to reference Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA (2006) 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 9:391–403PubMed Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA (2006) 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 9:391–403PubMed
99.
go back to reference Lefranc F, Brotchi J, Kiss R (2005) Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 23:2411–2422PubMed Lefranc F, Brotchi J, Kiss R (2005) Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 23:2411–2422PubMed
100.
go back to reference Li S, Gao Y, Tokuyama T, Yamamoto J, Yokota N, Yamamoto S, Terakawa S, Kitagawa M, Namba H (2007) Genetically engineered neural stem cells migrate and suppress glioma cell growth at distant intracranial sites. Cancer Lett 251:220–227PubMed Li S, Gao Y, Tokuyama T, Yamamoto J, Yokota N, Yamamoto S, Terakawa S, Kitagawa M, Namba H (2007) Genetically engineered neural stem cells migrate and suppress glioma cell growth at distant intracranial sites. Cancer Lett 251:220–227PubMed
101.
go back to reference Lipinski CA, Tran NL, Menashi E, Rohl C, Kloss J, Bay RC, Berens ME, Loftus JC (2005) The tyrosine kinase pyk2 promotes migration and invasion of glioma cells. Neoplasia 7:435–445PubMed Lipinski CA, Tran NL, Menashi E, Rohl C, Kloss J, Bay RC, Berens ME, Loftus JC (2005) The tyrosine kinase pyk2 promotes migration and invasion of glioma cells. Neoplasia 7:435–445PubMed
102.
go back to reference Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67PubMed Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67PubMed
103.
go back to reference Liu M, Dai B, Kang SH, Ban K, Huang FJ, Lang FF, Aldape KD, Xie TX, Pelloski CE, Xie K, Sawaya R, Huang S (2006) FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res 66:3593–3602PubMed Liu M, Dai B, Kang SH, Ban K, Huang FJ, Lang FF, Aldape KD, Xie TX, Pelloski CE, Xie K, Sawaya R, Huang S (2006) FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res 66:3593–3602PubMed
104.
go back to reference Lois C, Garcia-Verdugo JM, varez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981PubMed Lois C, Garcia-Verdugo JM, varez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981PubMed
105.
go back to reference Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) WHO classification of tumours of the central nervous system. IARC, Lyon Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) WHO classification of tumours of the central nervous system. IARC, Lyon
106.
go back to reference Macapinlac HA (2006) Positron emission tomography of the brain. Neuroimaging Clin N Am 16:591–603, viii Macapinlac HA (2006) Positron emission tomography of the brain. Neuroimaging Clin N Am 16:591–603, viii
107.
go back to reference Maglott A, Bartik P, Cosgun S, Klotz P, Ronde P, Fuhrmann G, Takeda K, Martin S, Dontenwill M (2006) The small alpha5beta1 integrin antagonist, SJ749, reduces proliferation and clonogenicity of human astrocytoma cells. Cancer Res 66:6002–6007PubMed Maglott A, Bartik P, Cosgun S, Klotz P, Ronde P, Fuhrmann G, Takeda K, Martin S, Dontenwill M (2006) The small alpha5beta1 integrin antagonist, SJ749, reduces proliferation and clonogenicity of human astrocytoma cells. Cancer Res 66:6002–6007PubMed
108.
go back to reference Mapara KY, Stevenson CB, Thompson RC, Ehtesham M (2007) Stem cells as vehicles for the treatment of brain cancer. Neurosurg Clin N Am 18:71–80, ix Mapara KY, Stevenson CB, Thompson RC, Ehtesham M (2007) Stem cells as vehicles for the treatment of brain cancer. Neurosurg Clin N Am 18:71–80, ix
109.
go back to reference Mariani L, McDonough WS, Hoelzinger DB, Beaudry C, Kaczmarek E, Coons SW, Giese A, Moghaddam M, Seiler RW, Berens ME (2001) Identification and validation of P311 as a glioblastoma invasion gene using laser capture microdissection. Cancer Res 61:4190–4196PubMed Mariani L, McDonough WS, Hoelzinger DB, Beaudry C, Kaczmarek E, Coons SW, Giese A, Moghaddam M, Seiler RW, Berens ME (2001) Identification and validation of P311 as a glioblastoma invasion gene using laser capture microdissection. Cancer Res 61:4190–4196PubMed
110.
go back to reference Martens T, Schmidt NO, Eckerich C, Fillbrandt R, Merchant M, Schwall R, Westphal M, Lamszus K (2006) A novel one-armed anti-c-Met antibody inhibits glioblastoma growth in vivo. Clin Cancer Res 12:6144–6152PubMed Martens T, Schmidt NO, Eckerich C, Fillbrandt R, Merchant M, Schwall R, Westphal M, Lamszus K (2006) A novel one-armed anti-c-Met antibody inhibits glioblastoma growth in vivo. Clin Cancer Res 12:6144–6152PubMed
111.
go back to reference Mawrin C (2005) Molecular genetic alterations in gliomatosis cerebri: what can we learn about the origin and course of the disease? Acta Neuropathol (Berl) 110:527–536 Mawrin C (2005) Molecular genetic alterations in gliomatosis cerebri: what can we learn about the origin and course of the disease? Acta Neuropathol (Berl) 110:527–536
112.
go back to reference McComb RD, Bigner DD (1985) Immunolocalization of laminin in neoplasms of the central and peripheral nervous systems. J Neuropathol Exp Neurol 44:242–253PubMedCrossRef McComb RD, Bigner DD (1985) Immunolocalization of laminin in neoplasms of the central and peripheral nervous systems. J Neuropathol Exp Neurol 44:242–253PubMedCrossRef
113.
go back to reference McDonough WS, Tran NL, Berens ME (2005) Regulation of glioma cell migration by serine-phosphorylated P311. Neoplasia 7:862–872PubMed McDonough WS, Tran NL, Berens ME (2005) Regulation of glioma cell migration by serine-phosphorylated P311. Neoplasia 7:862–872PubMed
114.
go back to reference McKnight TR, von dem Bussche MH, Vigneron DB, Lu Y, Berger MS, McDermott MW, Dillon WP, Graves EE, Pirzkall A, Nelson SJ (2002) Histopathological validation of a three-dimensional magnetic resonance spectroscopy index as a predictor of tumor presence. J Neurosurg 97:794–802PubMed McKnight TR, von dem Bussche MH, Vigneron DB, Lu Y, Berger MS, McDermott MW, Dillon WP, Graves EE, Pirzkall A, Nelson SJ (2002) Histopathological validation of a three-dimensional magnetic resonance spectroscopy index as a predictor of tumor presence. J Neurosurg 97:794–802PubMed
115.
go back to reference Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, Lu KV, Yoshimoto K, Huang JH, Chute DJ, Riggs BL, Horvath S, Liau LM, Cavenee WK, Rao PN, Beroukhim R, Peck TC, Lee JC, Sellers WR, Stokoe D, Prados M, Cloughesy TF, Sawyers CL, Mischel PS (2005) Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 353:2012–2024PubMed Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, Lu KV, Yoshimoto K, Huang JH, Chute DJ, Riggs BL, Horvath S, Liau LM, Cavenee WK, Rao PN, Beroukhim R, Peck TC, Lee JC, Sellers WR, Stokoe D, Prados M, Cloughesy TF, Sawyers CL, Mischel PS (2005) Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 353:2012–2024PubMed
116.
go back to reference Mijatovic S, Maksimovic-Ivanic D, Radovic J, Miljkovic D, Harhaji L, Vuckovic O, Stosic-Grujicic S, Mostarica SM, Trajkovic V (2005) Anti-glioma action of aloe emodin: the role of ERK inhibition. Cell Mol Life Sci 62:589–598PubMed Mijatovic S, Maksimovic-Ivanic D, Radovic J, Miljkovic D, Harhaji L, Vuckovic O, Stosic-Grujicic S, Mostarica SM, Trajkovic V (2005) Anti-glioma action of aloe emodin: the role of ERK inhibition. Cell Mol Life Sci 62:589–598PubMed
117.
go back to reference Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6:56–68PubMed Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6:56–68PubMed
118.
go back to reference Murad GJ, Walbridge S, Morrison PF, Garmestani K, Degen JW, Brechbiel MW, Oldfield EH, Lonser RR (2006) Real-time, image-guided, convection-enhanced delivery of interleukin 13 bound to pseudomonas exotoxin. Clin Cancer Res 12:3145–3151PubMed Murad GJ, Walbridge S, Morrison PF, Garmestani K, Degen JW, Brechbiel MW, Oldfield EH, Lonser RR (2006) Real-time, image-guided, convection-enhanced delivery of interleukin 13 bound to pseudomonas exotoxin. Clin Cancer Res 12:3145–3151PubMed
119.
go back to reference Murad GJ, Walbridge S, Morrison PF, Szerlip N, Butman JA, Oldfield EH, Lonser RR (2007) Image-guided convection-enhanced delivery of gemcitabine to the brainstem. J Neurosurg 106:351–356PubMed Murad GJ, Walbridge S, Morrison PF, Szerlip N, Butman JA, Oldfield EH, Lonser RR (2007) Image-guided convection-enhanced delivery of gemcitabine to the brainstem. J Neurosurg 106:351–356PubMed
120.
go back to reference Murai T, Miyazaki Y, Nishinakamura H, Sugahara KN, Miyauchi T, Sako Y, Yanagida T, Miyasaka M (2004) Engagement of CD44 promotes Rac activation and CD44 cleavage during tumor cell migration. J Biol Chem 279:4541–4550PubMed Murai T, Miyazaki Y, Nishinakamura H, Sugahara KN, Miyauchi T, Sako Y, Yanagida T, Miyasaka M (2004) Engagement of CD44 promotes Rac activation and CD44 cleavage during tumor cell migration. J Biol Chem 279:4541–4550PubMed
121.
go back to reference Nakada M, Niska JA, Miyamori H, McDonough WS, Wu J, Sato H, Berens ME (2004) The phosphorylation of EphB2 receptor regulates migration and invasion of human glioma cells. Cancer Res 64:3179–3185PubMed Nakada M, Niska JA, Miyamori H, McDonough WS, Wu J, Sato H, Berens ME (2004) The phosphorylation of EphB2 receptor regulates migration and invasion of human glioma cells. Cancer Res 64:3179–3185PubMed
122.
go back to reference Nakada M, Drake KL, Nakada S, Niska JA, Berens ME (2006) Ephrin-B3 ligand promotes glioma invasion through activation of Rac1. Cancer Res 66:8492–8500PubMed Nakada M, Drake KL, Nakada S, Niska JA, Berens ME (2006) Ephrin-B3 ligand promotes glioma invasion through activation of Rac1. Cancer Res 66:8492–8500PubMed
123.
go back to reference Nakamura JL (2007) The epidermal growth factor receptor in malignant gliomas: pathogenesis and therapeutic implications. Expert Opin Ther Targets 11:463–472PubMed Nakamura JL (2007) The epidermal growth factor receptor in malignant gliomas: pathogenesis and therapeutic implications. Expert Opin Ther Targets 11:463–472PubMed
124.
go back to reference Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235–1244PubMed Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235–1244PubMed
125.
go back to reference Owens GC, Orr EA, DeMasters BK, Muschel RJ, Berens ME, Kruse CA (1998) Overexpression of a transmembrane isoform of neural cell adhesion molecule alters the invasiveness of rat CNS-1 glioma. Cancer Res 58:2020–2028PubMed Owens GC, Orr EA, DeMasters BK, Muschel RJ, Berens ME, Kruse CA (1998) Overexpression of a transmembrane isoform of neural cell adhesion molecule alters the invasiveness of rat CNS-1 glioma. Cancer Res 58:2020–2028PubMed
126.
go back to reference Patel SJ, Shapiro WR, Laske DW, Jensen RL, Asher AL, Wessels BW, Carpenter SP, Shan JS (2005) Safety and feasibility of convection-enhanced delivery of Cotara for the treatment of malignant glioma: initial experience in 51 patients. Neurosurgery 56:1243–1252PubMed Patel SJ, Shapiro WR, Laske DW, Jensen RL, Asher AL, Wessels BW, Carpenter SP, Shan JS (2005) Safety and feasibility of convection-enhanced delivery of Cotara for the treatment of malignant glioma: initial experience in 51 patients. Neurosurgery 56:1243–1252PubMed
127.
go back to reference Paulus W, Huettner C, Tonn JC (1994) Collagens, integrins and the mesenchymal drift in glioblastomas: a comparison of biopsy specimens, spheroid and early monolayer cultures. Int J Cancer 58:841–846PubMed Paulus W, Huettner C, Tonn JC (1994) Collagens, integrins and the mesenchymal drift in glioblastomas: a comparison of biopsy specimens, spheroid and early monolayer cultures. Int J Cancer 58:841–846PubMed
128.
go back to reference Pedersen PH, Marienhagen K, Mork S, Bjerkvig R (1993) Migratory pattern of fetal rat brain cells and human glioma cells in the adult rat brain. Cancer Res 53:5158–5165PubMed Pedersen PH, Marienhagen K, Mork S, Bjerkvig R (1993) Migratory pattern of fetal rat brain cells and human glioma cells in the adult rat brain. Cancer Res 53:5158–5165PubMed
129.
go back to reference Peiffer J, Kleihues P (1999) Hans-Joachim Scherer (1906–1945), pioneer in glioma research. Brain Pathol 9:241–245PubMedCrossRef Peiffer J, Kleihues P (1999) Hans-Joachim Scherer (1906–1945), pioneer in glioma research. Brain Pathol 9:241–245PubMedCrossRef
130.
go back to reference Pilkington CJ (1996) The role of the extracellular matrix in neoplastic glial invasion of the nervous system. Braz J Med Biol Res 29:1159–1172PubMed Pilkington CJ (1996) The role of the extracellular matrix in neoplastic glial invasion of the nervous system. Braz J Med Biol Res 29:1159–1172PubMed
131.
go back to reference Pirotte B, Goldman S, Dewitte O, Massager N, Wikler D, Lefranc F, Ben Taib NO, Rorive S, David P, Brotchi J, Levivier M (2006) Integrated positron emission tomography and magnetic resonance imaging-guided resection of brain tumors: a report of 103 consecutive procedures. J Neurosurg 104:238–253PubMed Pirotte B, Goldman S, Dewitte O, Massager N, Wikler D, Lefranc F, Ben Taib NO, Rorive S, David P, Brotchi J, Levivier M (2006) Integrated positron emission tomography and magnetic resonance imaging-guided resection of brain tumors: a report of 103 consecutive procedures. J Neurosurg 104:238–253PubMed
132.
go back to reference Pirzkall A, McKnight TR, Graves EE, Carol MP, Sneed PK, Wara WW, Nelson SJ, Verhey LJ, Larson DA (2001) MR-spectroscopy guided target delineation for high-grade gliomas. Int J Radiat Oncol Biol Phys 50:915–928PubMed Pirzkall A, McKnight TR, Graves EE, Carol MP, Sneed PK, Wara WW, Nelson SJ, Verhey LJ, Larson DA (2001) MR-spectroscopy guided target delineation for high-grade gliomas. Int J Radiat Oncol Biol Phys 50:915–928PubMed
133.
go back to reference Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465PubMed Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465PubMed
134.
go back to reference Popperl G, Kreth FW, Herms J, Koch W, Mehrkens JH, Gildehaus FJ, Kretzschmar HA, Tonn JC, Tatsch K (2006) Analysis of 18F–FET PET for grading of recurrent gliomas: is evaluation of uptake kinetics superior to standard methods? J Nucl Med 47:393–403PubMed Popperl G, Kreth FW, Herms J, Koch W, Mehrkens JH, Gildehaus FJ, Kretzschmar HA, Tonn JC, Tatsch K (2006) Analysis of 18F–FET PET for grading of recurrent gliomas: is evaluation of uptake kinetics superior to standard methods? J Nucl Med 47:393–403PubMed
135.
go back to reference Provenzale JM, Mukundan S, Barboriak DP (2006) Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology 239:632–649PubMed Provenzale JM, Mukundan S, Barboriak DP (2006) Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology 239:632–649PubMed
136.
go back to reference Raghavan R, Brady ML, Rodriguez-Ponce MI, Hartlep A, Pedain C, Sampson JH (2006) Convection-enhanced delivery of therapeutics for brain disease, and its optimization. Neurosurg Focus 20:E12PubMed Raghavan R, Brady ML, Rodriguez-Ponce MI, Hartlep A, Pedain C, Sampson JH (2006) Convection-enhanced delivery of therapeutics for brain disease, and its optimization. Neurosurg Focus 20:E12PubMed
137.
go back to reference Rao JS (2003) Molecular mechanisms of glioma invasiveness: the role of proteases. Nat Rev Cancer 3:489–501PubMed Rao JS (2003) Molecular mechanisms of glioma invasiveness: the role of proteases. Nat Rev Cancer 3:489–501PubMed
138.
go back to reference Raza SM, Lang FF, Aggarwal BB, Fuller GN, Wildrick DM, Sawaya R (2002) Necrosis and glioblastoma: a friend or a foe? A review and a hypothesis. Neurosurgery 51:2–12PubMed Raza SM, Lang FF, Aggarwal BB, Fuller GN, Wildrick DM, Sawaya R (2002) Necrosis and glioblastoma: a friend or a foe? A review and a hypothesis. Neurosurgery 51:2–12PubMed
139.
go back to reference Reardon DA, Akabani G, Coleman RE, Friedman AH, Friedman HS, Herndon JE, McLendon RE, Pegram CN, Provenzale JM, Quinn JA, Rich JN, Vredenburgh JJ, Desjardins A, Gururangan S, Badruddoja M, Dowell JM, Wong TZ, Zhao XG, Zalutsky MR, Bigner DD (2006) Salvage radioimmunotherapy with murine iodine-131-labeled antitenascin monoclonal antibody 81C6 for patients with recurrent primary and metastatic malignant brain tumors: phase II study results. J Clin Oncol 24:115–122PubMed Reardon DA, Akabani G, Coleman RE, Friedman AH, Friedman HS, Herndon JE, McLendon RE, Pegram CN, Provenzale JM, Quinn JA, Rich JN, Vredenburgh JJ, Desjardins A, Gururangan S, Badruddoja M, Dowell JM, Wong TZ, Zhao XG, Zalutsky MR, Bigner DD (2006) Salvage radioimmunotherapy with murine iodine-131-labeled antitenascin monoclonal antibody 81C6 for patients with recurrent primary and metastatic malignant brain tumors: phase II study results. J Clin Oncol 24:115–122PubMed
140.
go back to reference Reardon DA, Rich JN, Friedman HS, Bigner DD (2006) Recent advances in the treatment of malignant astrocytoma. J Clin Oncol 24:1253–1265PubMed Reardon DA, Rich JN, Friedman HS, Bigner DD (2006) Recent advances in the treatment of malignant astrocytoma. J Clin Oncol 24:1253–1265PubMed
141.
go back to reference Rees J (2003) Advances in magnetic resonance imaging of brain tumours. Curr Opin Neurol 16:643–650PubMed Rees J (2003) Advances in magnetic resonance imaging of brain tumours. Curr Opin Neurol 16:643–650PubMed
142.
go back to reference Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302:1704–1709PubMed Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302:1704–1709PubMed
143.
go back to reference Roggendorf W, Strupp S, Paulus W (1996) Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol (Berl) 92:288–293 Roggendorf W, Strupp S, Paulus W (1996) Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol (Berl) 92:288–293
144.
go back to reference Rollins KE, Kleinschmidt-DeMasters BK, Corboy JR, Damek DM, Filley CM (2005) Lymphomatosis cerebri as a cause of white matter dementia. Hum Pathol 36:282–290PubMed Rollins KE, Kleinschmidt-DeMasters BK, Corboy JR, Damek DM, Filley CM (2005) Lymphomatosis cerebri as a cause of white matter dementia. Hum Pathol 36:282–290PubMed
145.
go back to reference Rubin JB, Kung AL, Klein RS, Chan JA, Sun Y, Schmidt K, Kieran MW, Luster AD, Segal RA (2003) A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci USA 100:13513–13518PubMed Rubin JB, Kung AL, Klein RS, Chan JA, Sun Y, Schmidt K, Kieran MW, Luster AD, Segal RA (2003) A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci USA 100:13513–13518PubMed
146.
go back to reference Sahai E (2005) Mechanisms of cancer cell invasion. Curr Opin Genet Dev 15:87–96PubMed Sahai E (2005) Mechanisms of cancer cell invasion. Curr Opin Genet Dev 15:87–96PubMed
147.
go back to reference Sakariassen PO, Prestegarden L, Wang J, Skaftnesmo KO, Mahesparan R, Molthoff C, Sminia P, Sundlisaeter E, Misra A, Tysnes BB, Chekenya M, Peters H, Lende G, Kalland KH, Oyan AM, Petersen K, Jonassen I, van der KA, Feuerstein BG, Terzis AJ, Bjerkvig R, Enger PO (2006) Angiogenesis-independent tumor growth mediated by stem-like cancer cells. Proc Natl Acad Sci USA 103:16466–16471 Sakariassen PO, Prestegarden L, Wang J, Skaftnesmo KO, Mahesparan R, Molthoff C, Sminia P, Sundlisaeter E, Misra A, Tysnes BB, Chekenya M, Peters H, Lende G, Kalland KH, Oyan AM, Petersen K, Jonassen I, van der KA, Feuerstein BG, Terzis AJ, Bjerkvig R, Enger PO (2006) Angiogenesis-independent tumor growth mediated by stem-like cancer cells. Proc Natl Acad Sci USA 103:16466–16471
148.
go back to reference Salhia B, Tran NL, Symons M, Winkles JA, Rutka JT, Berens ME (2006) Molecular pathways triggering glioma cell invasion. Expert Rev Mol Diagn 6:613–626PubMed Salhia B, Tran NL, Symons M, Winkles JA, Rutka JT, Berens ME (2006) Molecular pathways triggering glioma cell invasion. Expert Rev Mol Diagn 6:613–626PubMed
149.
go back to reference Salvati M, Caroli E, Orlando ER, Frati A, Artizzu S, Ferrante L (2003) Multicentric glioma: our experience in 25 patients and critical review of the literature. Neurosurg Rev 26:275–279PubMed Salvati M, Caroli E, Orlando ER, Frati A, Artizzu S, Ferrante L (2003) Multicentric glioma: our experience in 25 patients and critical review of the literature. Neurosurg Rev 26:275–279PubMed
150.
go back to reference Sampson JH, Akabani G, Archer GE, Bigner DD, Berger MS, Friedman AH, Friedman HS, Herndon JE, Kunwar S, Marcus S, McLendon RE, Paolino A, Penne K, Provenzale J, Quinn J, Reardon DA, Rich J, Stenzel T, Tourt-Uhlig S, Wikstrand C, Wong T, Williams R, Yuan F, Zalutsky MR, Pastan I (2003) Progress report of a Phase I study of the intracerebral microinfusion of a recombinant chimeric protein composed of transforming growth factor (TGF)-alpha and a mutated form of the Pseudomonas exotoxin termed PE-38 (TP-38) for the treatment of malignant brain tumors. J Neurooncol 65:27–35PubMed Sampson JH, Akabani G, Archer GE, Bigner DD, Berger MS, Friedman AH, Friedman HS, Herndon JE, Kunwar S, Marcus S, McLendon RE, Paolino A, Penne K, Provenzale J, Quinn J, Reardon DA, Rich J, Stenzel T, Tourt-Uhlig S, Wikstrand C, Wong T, Williams R, Yuan F, Zalutsky MR, Pastan I (2003) Progress report of a Phase I study of the intracerebral microinfusion of a recombinant chimeric protein composed of transforming growth factor (TGF)-alpha and a mutated form of the Pseudomonas exotoxin termed PE-38 (TP-38) for the treatment of malignant brain tumors. J Neurooncol 65:27–35PubMed
151.
go back to reference Sampson JH, Brady ML, Petry NA, Croteau D, Friedman AH, Friedman HS, Wong T, Bigner DD, Pastan I, Puri RK, Pedain C (2007) Intracerebral infusate distribution by convection-enhanced delivery in humans with malignant gliomas: descriptive effects of target anatomy and catheter positioning. Neurosurgery 60:ONS89–ONS98PubMed Sampson JH, Brady ML, Petry NA, Croteau D, Friedman AH, Friedman HS, Wong T, Bigner DD, Pastan I, Puri RK, Pedain C (2007) Intracerebral infusate distribution by convection-enhanced delivery in humans with malignant gliomas: descriptive effects of target anatomy and catheter positioning. Neurosurgery 60:ONS89–ONS98PubMed
152.
go back to reference Sanai N, varez-Buylla A, Berger MS (2005) Neural stem cells and the origin of gliomas. N Engl J Med 353:811–822PubMed Sanai N, varez-Buylla A, Berger MS (2005) Neural stem cells and the origin of gliomas. N Engl J Med 353:811–822PubMed
153.
go back to reference Sarkar S, Nuttall RK, Liu S, Edwards DR, Yong VW (2006) Tenascin-C stimulates glioma cell invasion through matrix metalloproteinase-12. Cancer Res 66:11771–11780PubMed Sarkar S, Nuttall RK, Liu S, Edwards DR, Yong VW (2006) Tenascin-C stimulates glioma cell invasion through matrix metalloproteinase-12. Cancer Res 66:11771–11780PubMed
154.
go back to reference Sarkaria JN, Carlson BL, Schroeder MA, Grogan P, Brown PD, Giannini C, Ballman KV, Kitange GJ, Guha A, Pandita A, James CD (2006) Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res 12:2264–2271PubMed Sarkaria JN, Carlson BL, Schroeder MA, Grogan P, Brown PD, Giannini C, Ballman KV, Kitange GJ, Guha A, Pandita A, James CD (2006) Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res 12:2264–2271PubMed
155.
go back to reference Sasaki H, Yoshida K, Ikeda E, Asou H, Inaba M, Otani M, Kawase T (1998) Expression of the neural cell adhesion molecule in astrocytic tumors: an inverse correlation with malignancy. Cancer 82:1921–1931PubMed Sasaki H, Yoshida K, Ikeda E, Asou H, Inaba M, Otani M, Kawase T (1998) Expression of the neural cell adhesion molecule in astrocytic tumors: an inverse correlation with malignancy. Cancer 82:1921–1931PubMed
156.
go back to reference Sawaya RE, Yamamoto M, Gokaslan ZL, Wang SW, Mohanam S, Fuller GN, McCutcheon IE, Stetler-Stevenson WG, Nicolson GL, Rao JS (1996) Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin Exp Metastasis 14:35–42PubMed Sawaya RE, Yamamoto M, Gokaslan ZL, Wang SW, Mohanam S, Fuller GN, McCutcheon IE, Stetler-Stevenson WG, Nicolson GL, Rao JS (1996) Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin Exp Metastasis 14:35–42PubMed
157.
go back to reference Scherer HJ (1938) Structural development in gliomas. Am J Cancer 34:333–351 Scherer HJ (1938) Structural development in gliomas. Am J Cancer 34:333–351
158.
go back to reference Senner V, Schmidtpeter S, Braune S, Puttmann S, Thanos S, Bartsch U, Schachner M, Paulus W (2003) AMOG/beta2 and glioma invasion: does loss of AMOG make tumour cells run amok? Neuropathol Appl Neurobiol 29:370–377PubMed Senner V, Schmidtpeter S, Braune S, Puttmann S, Thanos S, Bartsch U, Schachner M, Paulus W (2003) AMOG/beta2 and glioma invasion: does loss of AMOG make tumour cells run amok? Neuropathol Appl Neurobiol 29:370–377PubMed
159.
go back to reference Shah AC, Benos D, Gillespie GY, Markert JM (2003) Oncolytic viruses: clinical applications as vectors for the treatment of malignant gliomas. J Neurooncol 65:203–226PubMed Shah AC, Benos D, Gillespie GY, Markert JM (2003) Oncolytic viruses: clinical applications as vectors for the treatment of malignant gliomas. J Neurooncol 65:203–226PubMed
160.
go back to reference Shi Q, Bao S, Song L, Wu Q, Bigner DD, Hjelmeland AB, Rich JN (2007) Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 26:4084–4094PubMed Shi Q, Bao S, Song L, Wu Q, Bigner DD, Hjelmeland AB, Rich JN (2007) Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 26:4084–4094PubMed
161.
go back to reference Shi Q, Hjelmeland AB, Keir ST, Song L, Wickman S, Jackson D, Ohmori O, Bigner DD, Friedman HS, Rich JN (2007) A novel low-molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol Carcinog 46(6):488–496PubMed Shi Q, Hjelmeland AB, Keir ST, Song L, Wickman S, Jackson D, Ohmori O, Bigner DD, Friedman HS, Rich JN (2007) A novel low-molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol Carcinog 46(6):488–496PubMed
162.
go back to reference 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 63:5821–5828PubMed 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 63:5821–5828PubMed
163.
go back to reference 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 432:396–401PubMed 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 432:396–401PubMed
164.
go back to reference Sloan KE, Eustace BK, Stewart JK, Zehetmeier C, Torella C, Simeone M, Roy JE, Unger C, Louis DN, Ilag LL, Jay DG (2004) CD155/PVR plays a key role in cell motility during tumor cell invasion and migration. BMC Cancer 4:73 Sloan KE, Eustace BK, Stewart JK, Zehetmeier C, Torella C, Simeone M, Roy JE, Unger C, Louis DN, Ilag LL, Jay DG (2004) CD155/PVR plays a key role in cell motility during tumor cell invasion and migration. BMC Cancer 4:73
165.
go back to reference Sloan KE, Stewart JK, Treloar AF, Matthews RT, Jay DG (2005) CD155/PVR enhances glioma cell dispersal by regulating adhesion signaling and focal adhesion dynamics. Cancer Res 65:10930–10937PubMed Sloan KE, Stewart JK, Treloar AF, Matthews RT, Jay DG (2005) CD155/PVR enhances glioma cell dispersal by regulating adhesion signaling and focal adhesion dynamics. Cancer Res 65:10930–10937PubMed
166.
go back to reference Smith JS, Cha S, Mayo MC, McDermott MW, Parsa AT, Chang SM, Dillon WP, Berger MS (2005) Serial diffusion-weighted magnetic resonance imaging in cases of glioma: distinguishing tumor recurrence from postresection injury. J Neurosurg 103:428–438PubMed Smith JS, Cha S, Mayo MC, McDermott MW, Parsa AT, Chang SM, Dillon WP, Berger MS (2005) Serial diffusion-weighted magnetic resonance imaging in cases of glioma: distinguishing tumor recurrence from postresection injury. J Neurosurg 103:428–438PubMed
167.
go back to reference Sonabend AM, Ulasov IV, Han Y, Lesniak MS (2006) Oncolytic adenoviral therapy for glioblastoma multiforme. Neurosurg Focus 20:E19PubMed Sonabend AM, Ulasov IV, Han Y, Lesniak MS (2006) Oncolytic adenoviral therapy for glioblastoma multiforme. Neurosurg Focus 20:E19PubMed
168.
go back to reference Song SW, Fuller GN, Khan A, Kong S, Shen W, Taylor E, Ramdas L, Lang FF, Zhang W (2003) IIp45, an insulin–like growth factor binding protein 2 (IGFBP-2) binding protein, antagonizes IGFBP-2 stimulation of glioma cell invasion. Proc Natl Acad Sci USA 100:13970–13975PubMed Song SW, Fuller GN, Khan A, Kong S, Shen W, Taylor E, Ramdas L, Lang FF, Zhang W (2003) IIp45, an insulin–like growth factor binding protein 2 (IGFBP-2) binding protein, antagonizes IGFBP-2 stimulation of glioma cell invasion. Proc Natl Acad Sci USA 100:13970–13975PubMed
169.
go back to reference Song SW, Fuller GN, Zheng H, Zhang W (2005) Inactivation of the invasion inhibitory gene IIp45 by alternative splicing in gliomas. Cancer Res 65:3562–3567PubMed Song SW, Fuller GN, Zheng H, Zhang W (2005) Inactivation of the invasion inhibitory gene IIp45 by alternative splicing in gliomas. Cancer Res 65:3562–3567PubMed
170.
go back to reference Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401PubMed Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401PubMed
171.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMed Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMed
172.
go back to reference Subramanian A, Harris A, Piggott K, Shieff C, Bradford R (2002) Metastasis to and from the central nervous system–the ‘relatively protected site’. Lancet Oncol 3:498–507PubMed Subramanian A, Harris A, Piggott K, Shieff C, Bradford R (2002) Metastasis to and from the central nervous system–the ‘relatively protected site’. Lancet Oncol 3:498–507PubMed
173.
go back to reference Sugahara T, Korogi Y, Kochi M, Ikushima I, Hirai T, Okuda T, Shigematsu Y, Liang L, Ge Y, Ushio Y, Takahashi M (1998) Correlation of MR imaging-determined cerebral blood volume maps with histologic and angiographic determination of vascularity of gliomas. AJR Am J Roentgenol 171:1479–1486PubMed Sugahara T, Korogi Y, Kochi M, Ikushima I, Hirai T, Okuda T, Shigematsu Y, Liang L, Ge Y, Ushio Y, Takahashi M (1998) Correlation of MR imaging-determined cerebral blood volume maps with histologic and angiographic determination of vascularity of gliomas. AJR Am J Roentgenol 171:1479–1486PubMed
174.
go back to reference Suzuki M, Suzuki M, Nakayama J, Suzuki A, Angata K, Chen S, Sakai K, Hagihara K, Yamaguchi Y, Fukuda M (2005) Polysialic acid facilitates tumor invasion by glioma cells. Glycobiology 15:887–894PubMed Suzuki M, Suzuki M, Nakayama J, Suzuki A, Angata K, Chen S, Sakai K, Hagihara K, Yamaguchi Y, Fukuda M (2005) Polysialic acid facilitates tumor invasion by glioma cells. Glycobiology 15:887–894PubMed
175.
go back to reference Taga T, Suzuki A, Gonzalez-Gomez I, Gilles FH, Stins M, Shimada H, Barsky L, Weinberg KI, Laug WE (2002) alpha v-Integrin antagonist EMD 121974 induces apoptosis in brain tumor cells growing on vitronectin and tenascin. Int J Cancer 98:690–697PubMed Taga T, Suzuki A, Gonzalez-Gomez I, Gilles FH, Stins M, Shimada H, Barsky L, Weinberg KI, Laug WE (2002) alpha v-Integrin antagonist EMD 121974 induces apoptosis in brain tumor cells growing on vitronectin and tenascin. Int J Cancer 98:690–697PubMed
176.
go back to reference Tate AR, Underwood J, Acosta DM, Julia-Sape M, Majos C, Moreno-Torres A, Howe FA, van der Graaf M, Lefournier V, Murphy MM, Loosemore A, Ladroue C, Wesseling P, Luc Bosson J, Cabanas ME, Simonetti AW, Gajewicz W, Calvar J, Capdevila A, Wilkins PR, Bell BA, Remy C, Heerschap A, Watson D, Griffiths JR, Arus C (2006) Development of a decision support system for diagnosis and grading of brain tumours using in vivo magnetic resonance single voxel spectra. NMR Biomed 19:411–434PubMed Tate AR, Underwood J, Acosta DM, Julia-Sape M, Majos C, Moreno-Torres A, Howe FA, van der Graaf M, Lefournier V, Murphy MM, Loosemore A, Ladroue C, Wesseling P, Luc Bosson J, Cabanas ME, Simonetti AW, Gajewicz W, Calvar J, Capdevila A, Wilkins PR, Bell BA, Remy C, Heerschap A, Watson D, Griffiths JR, Arus C (2006) Development of a decision support system for diagnosis and grading of brain tumours using in vivo magnetic resonance single voxel spectra. NMR Biomed 19:411–434PubMed
177.
go back to reference Tonn JC, Kerkau S, Hanke A, Bouterfa H, Mueller JG, Wagner S, Vince GH, Roosen K (1999) Effect of synthetic matrix-metalloproteinase inhibitors on invasive capacity and proliferation of human malignant gliomas in vitro. Int J Cancer 80:764–772PubMed Tonn JC, Kerkau S, Hanke A, Bouterfa H, Mueller JG, Wagner S, Vince GH, Roosen K (1999) Effect of synthetic matrix-metalloproteinase inhibitors on invasive capacity and proliferation of human malignant gliomas in vitro. Int J Cancer 80:764–772PubMed
178.
go back to reference Tran NL, McDonough WS, Savitch BA, Fortin SP, Winkles JA, Symons M, Nakada M, Cunliffe HE, Hostetter G, Hoelzinger DB, Rennert JL, Michaelson JS, Burkly LC, Lipinski CA, Loftus JC, Mariani L, Berens ME (2006) Increased fibroblast growth factor-inducible 14 expression levels promote glioma cell invasion via Rac1 and nuclear factor-{kappa}B and correlate with poor patient outcome. Cancer Res 66:9535–9542PubMed Tran NL, McDonough WS, Savitch BA, Fortin SP, Winkles JA, Symons M, Nakada M, Cunliffe HE, Hostetter G, Hoelzinger DB, Rennert JL, Michaelson JS, Burkly LC, Lipinski CA, Loftus JC, Mariani L, Berens ME (2006) Increased fibroblast growth factor-inducible 14 expression levels promote glioma cell invasion via Rac1 and nuclear factor-{kappa}B and correlate with poor patient outcome. Cancer Res 66:9535–9542PubMed
179.
go back to reference Tysnes BB, Mahesparan R (2001) Biological mechanisms of glioma invasion and potential therapeutic targets. J Neurooncol 53:129–147PubMed Tysnes BB, Mahesparan R (2001) Biological mechanisms of glioma invasion and potential therapeutic targets. J Neurooncol 53:129–147PubMed
180.
go back to reference Uhm JH, Dooley NP, Kyritsis AP, Rao JS, Gladson CL (1999) Vitronectin, a glioma-derived extracellular matrix protein, protects tumor cells from apoptotic death. Clin Cancer Res 5:1587–1594PubMed Uhm JH, Dooley NP, Kyritsis AP, Rao JS, Gladson CL (1999) Vitronectin, a glioma-derived extracellular matrix protein, protects tumor cells from apoptotic death. Clin Cancer Res 5:1587–1594PubMed
181.
go back to reference Ulmer S, Braga TA, Barker FG, Lev MH, Gonzalez RG, Henson JW (2006) Clinical and radiographic features of peritumoral infarction following resection of glioblastoma. Neurology 67:1668–1670PubMed Ulmer S, Braga TA, Barker FG, Lev MH, Gonzalez RG, Henson JW (2006) Clinical and radiographic features of peritumoral infarction following resection of glioblastoma. Neurology 67:1668–1670PubMed
182.
go back to reference van den Bent MJ, Chinot O, Boogerd W, Bravo MJ, Taphoorn MJ, Kros JM, van der Rijt CC, Vecht CJ, De BN, Baron B (2003) Second-line chemotherapy with temozolomide in recurrent oligodendroglioma after PCV (procarbazine, lomustine and vincristine) chemotherapy: EORTC Brain Tumor Group phase II study 26972. Ann Oncol 14:599–602 van den Bent MJ, Chinot O, Boogerd W, Bravo MJ, Taphoorn MJ, Kros JM, van der Rijt CC, Vecht CJ, De BN, Baron B (2003) Second-line chemotherapy with temozolomide in recurrent oligodendroglioma after PCV (procarbazine, lomustine and vincristine) chemotherapy: EORTC Brain Tumor Group phase II study 26972. Ann Oncol 14:599–602
183.
go back to reference Vandergrift WA, Patel SJ, Nicholas JS, Varma AK (2006) Convection-enhanced delivery of immunotoxins and radioisotopes for treatment of malignant gliomas. Neurosurg Focus 20:E13PubMed Vandergrift WA, Patel SJ, Nicholas JS, Varma AK (2006) Convection-enhanced delivery of immunotoxins and radioisotopes for treatment of malignant gliomas. Neurosurg Focus 20:E13PubMed
184.
go back to reference Veiseh O, Sun C, Gunn J, Kohler N, Gabikian P, Lee D, Bhattarai N, Ellenbogen R, Sze R, Hallahan A, Olson J, Zhang M (2005) Optical and MRI multifunctional nanoprobe for targeting gliomas. Nano Lett 5:1003–1008PubMed Veiseh O, Sun C, Gunn J, Kohler N, Gabikian P, Lee D, Bhattarai N, Ellenbogen R, Sze R, Hallahan A, Olson J, Zhang M (2005) Optical and MRI multifunctional nanoprobe for targeting gliomas. Nano Lett 5:1003–1008PubMed
185.
go back to reference Vescovi AL, Galli R, Reynolds BA (2006) Brain tumour stem cells. Nat Rev Cancer 6:425–436PubMed Vescovi AL, Galli R, Reynolds BA (2006) Brain tumour stem cells. Nat Rev Cancer 6:425–436PubMed
186.
go back to reference Wang H, Wang H, Shen W, Huang H, Hu L, Ramdas L, Zhou YH, Liao WS, Fuller GN, Zhang W (2003) Insulin-like growth factor binding protein 2 enhances glioblastoma invasion by activating invasion-enhancing genes. Cancer Res 63:4315–4321PubMed Wang H, Wang H, Shen W, Huang H, Hu L, Ramdas L, Zhou YH, Liao WS, Fuller GN, Zhang W (2003) Insulin-like growth factor binding protein 2 enhances glioblastoma invasion by activating invasion-enhancing genes. Cancer Res 63:4315–4321PubMed
187.
go back to reference Wang L, Zhang ZG, Zhang RL, Gregg SR, Hozeska-Solgot A, LeTourneau Y, Wang Y, Chopp M (2006) Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci 26:5996–6003PubMed Wang L, Zhang ZG, Zhang RL, Gregg SR, Hozeska-Solgot A, LeTourneau Y, Wang Y, Chopp M (2006) Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci 26:5996–6003PubMed
188.
go back to reference Watters JJ, Schartner JM, Badie B (2005) Microglia function in brain tumors. J Neurosci Res 81:447–455PubMed Watters JJ, Schartner JM, Badie B (2005) Microglia function in brain tumors. J Neurosci Res 81:447–455PubMed
189.
go back to reference Weaver JD, Vinters HV, Koretz B, Xiong Z, Mischel P, Kado D (2007) Lymphomatosis cerebri presenting as rapidly progressive dementia. Neurologist 13:150–153PubMed Weaver JD, Vinters HV, Koretz B, Xiong Z, Mischel P, Kado D (2007) Lymphomatosis cerebri presenting as rapidly progressive dementia. Neurologist 13:150–153PubMed
190.
go back to reference Weaver M, Laske DW (2003) Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) for therapy of malignant gliomas. J Neurooncol 65:3–13PubMed Weaver M, Laske DW (2003) Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) for therapy of malignant gliomas. J Neurooncol 65:3–13PubMed
191.
go back to reference Wesseling P, van der Laak JA, de Leeuw H, Ruiter DJ, Burger PC (1994) Quantitative immunohistological analysis of the microvasculature in untreated human glioblastoma multiforme. Computer-assisted image analysis of whole-tumor sections. J Neurosurg 81:902–909 Wesseling P, van der Laak JA, de Leeuw H, Ruiter DJ, Burger PC (1994) Quantitative immunohistological analysis of the microvasculature in untreated human glioblastoma multiforme. Computer-assisted image analysis of whole-tumor sections. J Neurosurg 81:902–909
192.
go back to reference Wesseling P, van der Laak JA, Link M, Teepen HL, Ruiter DJ (1998) Quantitative analysis of microvascular changes in diffuse astrocytic neoplasms with increasing grade of malignancy. Hum Pathol 29:352–358PubMed Wesseling P, van der Laak JA, Link M, Teepen HL, Ruiter DJ (1998) Quantitative analysis of microvascular changes in diffuse astrocytic neoplasms with increasing grade of malignancy. Hum Pathol 29:352–358PubMed
193.
go back to reference Wick W, Platten M, Weller M (2001) Glioma cell invasion: regulation of metalloproteinase activity by TGF-beta. J Neurooncol 53:177–185PubMed Wick W, Platten M, Weller M (2001) Glioma cell invasion: regulation of metalloproteinase activity by TGF-beta. J Neurooncol 53:177–185PubMed
194.
go back to reference Widera D, Mikenberg I, Kaltschmidt B, Kaltschmidt C (2006) Potential role of NF-kappaB in adult neural stem cells: the underrated steersman? Int J Dev Neurosci 24:91–102PubMed Widera D, Mikenberg I, Kaltschmidt B, Kaltschmidt C (2006) Potential role of NF-kappaB in adult neural stem cells: the underrated steersman? Int J Dev Neurosci 24:91–102PubMed
195.
go back to reference Wu M, Chen Q, Li D, Li X, Li X, Huang C, Tang Y, Zhou Y, Wang D, Tang K, Cao L, Shen S, Li G (2007) LRRC4 inhibits human glioblastoma cells proliferation, invasion, and proMMP-2 activation by reducing SDF-1alpha/CXCR4-mediated ERK1/2 and Akt signaling pathways. J Cell Biochem. doi:10.1002/jcp.21163 Wu M, Chen Q, Li D, Li X, Li X, Huang C, Tang Y, Zhou Y, Wang D, Tang K, Cao L, Shen S, Li G (2007) LRRC4 inhibits human glioblastoma cells proliferation, invasion, and proMMP-2 activation by reducing SDF-1alpha/CXCR4-mediated ERK1/2 and Akt signaling pathways. J Cell Biochem. doi:​10.​1002/​jcp.​21163
196.
go back to reference Yamada S, Bu XY, Khankaldyyan V, Gonzales-Gomez I, McComb JG, Laug WE (2006) Effect of the angiogenesis inhibitor Cilengitide (EMD 121974) on glioblastoma growth in nude mice. Neurosurgery 59:1304–1312PubMed Yamada S, Bu XY, Khankaldyyan V, Gonzales-Gomez I, McComb JG, Laug WE (2006) Effect of the angiogenesis inhibitor Cilengitide (EMD 121974) on glioblastoma growth in nude mice. Neurosurgery 59:1304–1312PubMed
197.
go back to reference Yip S, Sabetrasekh R, Sidman RL, Snyder EY (2006) Neural stem cells as novel cancer therapeutic vehicles. Eur J Cancer 42:1298–1308PubMed Yip S, Sabetrasekh R, Sidman RL, Snyder EY (2006) Neural stem cells as novel cancer therapeutic vehicles. Eur J Cancer 42:1298–1308PubMed
198.
go back to reference Yong VW, Power C, Forsyth P, Edwards DR (2001) Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2:502–511PubMed Yong VW, Power C, Forsyth P, Edwards DR (2001) Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2:502–511PubMed
199.
go back to reference Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS (2004) Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23:9392–9400PubMed Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS (2004) Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23:9392–9400PubMed
200.
go back to reference Yuh WT, Nguyen HD, Tali ET, Mayr NA, Fisher DJ, Atlas SW, Carvlin MC, Drayer BP, Pollei SR, Runge VM (1994) Delineation of gliomas with various doses of MR contrast material. AJNR Am J Neuroradiol 15:983–989PubMed Yuh WT, Nguyen HD, Tali ET, Mayr NA, Fisher DJ, Atlas SW, Carvlin MC, Drayer BP, Pollei SR, Runge VM (1994) Delineation of gliomas with various doses of MR contrast material. AJNR Am J Neuroradiol 15:983–989PubMed
201.
go back to reference Zagzag D, Friedlander DR, Margolis B, Grumet M, Semenza GL, Zhong H, Simons JW, Holash J, Wiegand SJ, Yancopoulos GD (2000) Molecular events implicated in brain tumor angiogenesis and invasion. Pediatr Neurosurg 33:49–55PubMed Zagzag D, Friedlander DR, Margolis B, Grumet M, Semenza GL, Zhong H, Simons JW, Holash J, Wiegand SJ, Yancopoulos GD (2000) Molecular events implicated in brain tumor angiogenesis and invasion. Pediatr Neurosurg 33:49–55PubMed
202.
go back to reference Zagzag D, Shiff B, Jallo GI, Greco MA, Blanco C, Cohen H, Hukin J, Allen JC, Friedlander DR (2002) Tenascin-C promotes microvascular cell migration and phosphorylation of focal adhesion kinase. Cancer Res 62:2660–2668PubMed Zagzag D, Shiff B, Jallo GI, Greco MA, Blanco C, Cohen H, Hukin J, Allen JC, Friedlander DR (2002) Tenascin-C promotes microvascular cell migration and phosphorylation of focal adhesion kinase. Cancer Res 62:2660–2668PubMed
203.
go back to reference Zagzag D, Salnikow K, Chiriboga L, Yee H, Lan L, Ali MA, Garcia R, Demaria S, Newcomb EW (2005) Downregulation of major histocompatibility complex antigens in invading glioma cells: stealth invasion of the brain. Lab Invest 85:328–341PubMed Zagzag D, Salnikow K, Chiriboga L, Yee H, Lan L, Ali MA, Garcia R, Demaria S, Newcomb EW (2005) Downregulation of major histocompatibility complex antigens in invading glioma cells: stealth invasion of the brain. Lab Invest 85:328–341PubMed
204.
go back to reference Zamecnik J (2005) The extracellular space and matrix of gliomas. Acta Neuropathol (Berl) 110:435–442 Zamecnik J (2005) The extracellular space and matrix of gliomas. Acta Neuropathol (Berl) 110:435–442
Metadata
Title
Diffuse glioma growth: a guerilla war
Authors
An Claes
Albert J. Idema
Pieter Wesseling
Publication date
01-11-2007
Publisher
Springer-Verlag
Published in
Acta Neuropathologica / Issue 5/2007
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-007-0293-7

Other articles of this Issue 5/2007

Acta Neuropathologica 5/2007 Go to the issue