Standard of care therapy for malignant glioma and its effect on tumor and stromal cells

Oncogene

Volumn 31, Issue 16, 2012, Pages 1995-2006

  Jones, T S ^a   Holland, E C ^b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

dexamethasone; glioblastoma; radiation; temozolomide; tumor stroma

Indexed keywords

ANGIOTENSIN II; ANTINEOPLASTIC AGENT; BEVACIZUMAB; BRAIN DERIVED NEUROTROPHIC FACTOR; BREAST CANCER RESISTANCE PROTEIN; CEDIRANIB; CHEMOKINE RECEPTOR CXCR4; CILEGENTIDE; DEXAMETHASONE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 6; ISOCITRATE DEHYDROGENASE; MATRIX METALLOPROTEINASE 14; MONOCYTE CHEMOTACTIC PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 1; PIGMENT EPITHELIUM DERIVED FACTOR; PLASMINOGEN; PLATELET DERIVED GROWTH FACTOR; TEMOZOLOMIDE; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; ASTROCYTE; BLOOD VESSEL; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER SURGERY; CANCER THERAPY; CELL INVASION; CELL PROLIFERATION; COPY NUMBER VARIATION; DRUG RESPONSE; DRUG TARGETING; ENDOTHELIUM CELL; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HUMAN; IN VITRO STUDY; MICROGLIA; MOLECULAR BIOLOGY; MULTIDRUG RESISTANCE; MULTIMODALITY CANCER THERAPY; NEUROFIBROMATOSIS; NONHUMAN; PATIENT CARE; PERICYTE; PERIVASCULAR NICHE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SOMATIC MUTATION; STEM CELL; STROMA CELL; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR RECURRENCE; TUMOR STEM LIKE CELL; VASCULAR SMOOTH MUSCLE;

BRAIN NEOPLASMS; GLIOMA; HUMANS; STANDARD OF CARE; STROMAL CELLS;

EID: 84859891989     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.398     Document Type: Review

References (122)

1. Alterman RL, Stanley ER. (1994). Colony stimulating factor-1 expression in human glioma. Mol Chem Neuropathol 21: 177-188. (Pubitemid 24174521)
2. Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA et al. (2010). TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell 18: 655-668.
3. Arko L, Katsyv I, Park GE, Luan WP, Park JK. (2010). Experimental approaches for the treatment of malignant gliomas. Pharmacol Ther 128: 1-36.
4. Bajetto A, Bonavia R, Barbero S, Florio T, Costa A, Schettini G. (1999a). Expression of chemokine receptors in the rat brain. Ann N Y Acad Sci 876: 201-209. (Pubitemid 29352127)
5. Bajetto A, Bonavia R, Barbero S, Piccioli P, Costa A, Florio T et al. (1999b). Glial and neuronal cells express functional chemokine receptor CXCR4 and its natural ligand stromal cell-derived factor 1. J Neurochem 73: 2348-2357.
6. Banissi C, Ghiringhelli F, Chen L, Carpentier AF. (2009). Treg depletion with a low-dose metronomic temozolomide regimen in a rat glioma model. Cancer Immunol Immunother 58: 1627-1634.
7. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al. (2006a). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760. (Pubitemid 44949604)
8. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB et al. (2006b). Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66: 7843-7848. (Pubitemid 44299144)
9. Barbero S, Bajetto A, Bonavia R, Porcile C, Piccioli P, Pirani P et al. (2002). Expression of the chemokine receptor CXCR4 and its ligand stromal cell-derived factor 1 in human brain tumors and their involvement in glial proliferation in vitro. Ann N Y Acad Sci 973: 60-69. (Pubitemid 36124978)
10. Baron M. (2003). An overview of the Notch signalling pathway. Semin Cell Dev Biol 14: 113-119.
11. Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D. (2003). Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest 111: 1287-1295. (Pubitemid 36554699)
12. Betsholtz C. (2004). Insight into the physiological functions of PDGF through genetic studies in mice. Cytokine Growth Factor Rev 15: 215-228.
13. Bettinger I, Thanos S, Paulus W. (2002). Microglia promote glioma migration. Acta Neuropathologica 103: 351-355. (Pubitemid 36097029)
14. Bhattacharya S, Das A, Mallya K, Ahmad I. (2007). Maintenance of retinal stem cells by Abcg2 is regulated by notch signaling. J Cell Sci 120: 2652-2662. (Pubitemid 47323873)
15. Bjarnegard M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A et al. (2004). Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131: 1847-1857. (Pubitemid 38559851)
16. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW et al. (2009). PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4: 226-235.
17. Brennan C, Momota H, Hambardzumyan D, Ozawa T, Tandon A, Pedraza A et al. (2009). Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS One 4: e7752.
18. Cairncross JG, Macdonald DR, Pexman JH, Ives FJ. (1988). Steroid-induced CT changes in patients with recurrent malignant glioma. Neurology 38: 724-726.
19. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B et al. (2007). A perivascular niche for brain tumor stem cells. Cancer Cell 11: 69-82. (Pubitemid 46054518)
20. Cavaliere R, Lopes MB, Schiff D. (2005). Low-grade gliomas: an update on pathology and therapy. Lancet Neurol 4: 760-770. (Pubitemid 41457292)
21. Central Brain Tumor Registry of the United States. (2011). CBTRUS Statistical Report: Primary Brain and Central Nervous System Tumors Diagnosed in the United States in 2004-2007.
22. Chang JY, Liu LZ. (2000). Inhibition of microglial nitric oxide production by hydrocortisone and glucocorticoid precursors. Neurochem Res 25: 903-908. (Pubitemid 30636988)
23. Charles N, Holland EC. (2009). Brain tumor treatment increases the number of cancer stem-like cells. Expert Rev Neurother 9: 1447-1449.
24. Charles N, Ozawa T, Squatrito M, Bleau AM, Brennan CW, Hambardzumyan D et al. (2010). Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 6: 141-152.
25. Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H. (2011). The brain tumor microenvironment. Glia 59: 1169-1180.
26. Chiang CS, McBride WH. (1991). Radiation enhances tumor necrosis factor alpha production by murine brain cells. Brain Res 566: 265-269.
27. Cleaver O, Melton DA. (2003). Endothelial signaling during development. Nat Med 9: 661-668. (Pubitemid 36749214)
28. Daginakatte GC, Gutmann DH. (2007). Neurofibromatosis-1 (Nf1) heterozygous brain microglia elaborate paracrine factors that promote Nf1-deficient astrocyte and glioma growth. Hum Mol Genet 16: 1098-1112. (Pubitemid 47062730)
29. Diaz-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E et al. (2009). Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24: 909-969.
30. Dix AR, Brooks WH, Roszman TL, Morford LA. (1999). Immune defects observed in patients with primary malignant brain tumors. J Neuroimmunol 100: 216-232. (Pubitemid 30038255)
31. Ehrenkranz JRL, Posner JB (eds). (1980). Adrenocorticosteroid Hormones. C.K. Hall & Co.: Boston, MA.
32. Eisenberg HM, Barlow CF, Lorenzo AV. (1970). Effect of dexamethasone on altered brain vascular permeability. Arch Neurol 23: 18-22.
33. El Andaloussi A, Han Y, Lesniak MS. (2006). Prolongation of survival following depletion of CD4+CD25+ regulatory T cells in mice with experimental brain tumors. J Neurosurg 105: 430-437. (Pubitemid 44358755)
34. Enge M, Bjarnegard M, Gerhardt H, Gustafsson E, Kalen M, Asker N et al. (2002). Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21: 4307-4316.
35. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM et al. (2006). Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 66: 7445-7452. (Pubitemid 44289197)
36. Folkes AJ, Ahmadi K, Alderton WK, Alix S, Baker SJ, Box G et al. (2008). The identification of 2-(1H-indazol-4-yl)-6-(4-methanesulfonyl-piperazin-1- ylmethyl)-4-morpholin -4-yl-thieno[3,2-d]pyrimidine (GDC-0941) as a potent, selective, orally bioavailable inhibitor of class I PI3 kinase for the treatment of cancer. J Med Chem 51: 5522-5532.
37. Frederick L, Wang XY, Eley G, James CD. (2000). Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas. Cancer Res 60: 1383-1387. (Pubitemid 30152011)
38. Furnari FB, Fenton T, Bachoo RM,Mukasa A, Stommel JM, Stegh A et al. (2007). Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 21: 2683-2710. (Pubitemid 350070717)
39. Galicich JH, French LA. (1961). Use of dexamethasone in the treatment of cerebral edema resulting from brain tumors and brain surgery. Am Pract Dig Treat 12: 169-174.
40. Gallagher PG, Bao Y, Prorock A, Zigrino P, Nischt R, Politi V et al. (2005). Gene expression profiling reveals cross-talk between melanoma and fibroblasts: implications for host-tumor interactions in metastasis. Cancer Res 65: 4134-4146. (Pubitemid 40775651)
41. Ganter S, Northoff H, Mannel D, Gebicke-Harter PJ. (1992). Growth control of cultured microglia. J Neurosci Res 33: 218-230.
42. Gerhardt H, Betsholtz C. (2003). Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res 314: 15-23. (Pubitemid 37409909)
43. Goldstein LJ, Chen H, Bauer RJ, Bauer SM, Velazquez OC. (2005). Normal human fibroblasts enable melanoma cells to induce angiogenesis in type I collagen. Surgery 138: 439-449. (Pubitemid 41415570)
44. Gong X, Schwartz PH, Linskey ME, Bota DA. (2011). Neural stem/progenitors and glioma stem-like cells have differential sensitivity to chemotherapy. Neurology 76: 1126-1134.
45. Graeber MB, Scheithauer BW, Kreutzberg GW. (2002). Microglia in brain tumors. Glia 40: 252-259. (Pubitemid 35337382)
46. Grauer OM, Nierkens S, Bennink E, Toonen LW, Boon L, Wesseling P et al. (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: 95-105. (Pubitemid 46753856)
47. Green SB, Byar DP, Walker MD, Pistenmaa DA, Alexander Jr E, Batzdorf U et al. (1983). Comparisons of carmustine, procarbazine, and high-dose methylprednisolone as additions to surgery and radiotherapy for the treatment of malignant glioma. Cancer Treat Rep 67: 121-132. (Pubitemid 13110644)
48. Gutin PH. (1975). Corticosteroid therapy in patients with cerebral tumors: benefits, mechanisms, problems, practicalities. Semin Oncol 2: 49-56.
49. Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K, Holland EC. (2008). PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 22: 436-448. (Pubitemid 351272752)
50. Hambardzumyan D, Parada LF, Holland EC, Charest A. (2011). Genetic modeling of gliomas in mice: New tools to tackle old problems. Glia 59: 1155-1168.
51. Hanisch UK. (2002). Microglia as a source and target of cytokines. Glia 40: 140-155.
52. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M et al. (2005). MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352: 997-1003. (Pubitemid 40349502)
53. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. (1999). Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126: 3047-3055. (Pubitemid 29378170)
54. Hellstrom NA, Lindberg OR, Stahlberg A, Swanpalmer J, Pekny M, Blomgren K et al. (2011). Unique gene expression patterns indicate microglial contribution to neural stem cell recovery following irradiation. Mol Cell Neurosci 46: 710-719.
55. Hoelzinger DB, Demuth T, Berens ME. (2007). Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment. J Natl Cancer Inst 99: 1583-1593. (Pubitemid 351767231)
56. Hong X, Jiang F, Kalkanis SN, Zhang ZG, Zhang XP, DeCarvalho AC et al. (2006). SDF-1 and CXCR4 are up-regulated by VEGF and contribute to glioma cell invasion. Cancer Lett 236: 39-45.
57. Huse JT, Holland EC. (2010). Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev 10: 319-331.
58. Huse JT, Phillips HS, Brennan CW. (2011). Molecular subclassification of diffuse gliomas: Seeing order in the chaos. Glia 59: 1190-1199.
59. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A et al. (2008). Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 68: 918-926. (Pubitemid 351206771)
60. Hwang SY, Jung JS, Kim TH, Lim SJ, Oh ES, Kim JY et al. (2006). Ionizing radiation induces astrocyte gliosis through microglia activation. Neurobiol Dis 21: 457-467.
61. Jain RK. (2005). Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307: 58-62.
62. Jones TS, Holland EC. (2011). Molecular pathogenesis of malignant glial tumors. Toxicol Pathol 39: 158-166.
63. Jordan JT, Sun W, Hussain SF, DeAngulo G, Prabhu SS, Heimberger AB. (2008). Preferential migration of regulatory T cells mediated by glioma-secreted chemokines can be blocked with chemotherapy. Cancer Immunol Immunother 57: 123-131. (Pubitemid 350043644)
64. Kalm M, Fukuda A, Fukuda H, Ohrfelt A, Lannering B, Bjork-Eriksson T et al. (2009). Transient inflammation in neurogenic regions after irradiation of the developing brain. Radiat Res 171: 66-76.
65. Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG. (2005). Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol 7: 134-153. (Pubitemid 40590514)
66. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F et al. (2011). Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci USA 108: 3749-3754.
67. Kiefer R, Kreutzberg GW. (1991). Effects of dexamethasone on microglial activation in vivo: selective downregulation of major histocompatibility complex class II expression in regenerating facial nucleus. J Neuroimmunol 34: 99-108.
68. Kim JH, Park JA, Lee SW, Kim WJ, Yu YS, Kim KW. (2006). Bloodneural barrier: intercellular communication at glio-vascular interface. J Biochem Mol Biol 39: 339-345.
69. Kim JH, Min KJ, Seol W, Jou I, Joe EH. (2010). Astrocytes in injury states rapidly produce anti-inflammatory factors and attenuate microglial inflammatory responses. J Neurochem 115: 1161-1171.
70. Kim SH, Lim DJ, Chung YG, Cho TH, Lim SJ, Kim WJ et al. (2002). Expression of TNF-alpha and TGF-beta 1 in the rat brain after a single high-dose irradiation. J Korean Med Sci 17: 242-248.
71. Kofman S, Garvin JS, Nagamani D, Taylor III SG. (1957). Treatment of cerebral metastases from breast carcinoma with prednisolone. J Am Med Assoc 163: 1473-1476.
72. Kureshi SA, Hofman FM, Schneider JH, Chin LS, Apuzzo ML, Hinton DR. (1994). Cytokine expression in radiation-induced delayed cerebral injury. Neurosurgery 35: 822-829; discussion 829-830.
73. Kyrkanides S, Olschowka JA, Williams JP, Hansen JT, O'Banion MK. (1999). TNF alpha and IL-1beta mediate intercellular adhesion molecule-1 induction via microglia-astrocyte interaction in CNS radiation injury. J Neuroimmunol 95: 95-106. (Pubitemid 29173026)
74. Lai A, Tran A, Nghiemphu PL, Pope WB, Solis OE, Selch M et al. (2011). Phase II study of bevacizumab plus temozolomide during and after radiation therapy for patients with newly diagnosed glioblastoma multiforme. J Clin Oncol 29: 142-148.
75. Le DM, Besson A, Fogg DK, Choi KS, Waisman DM, Goodyer CG et al. (2003). Exploitation of astrocytes by glioma cells to facilitate invasiveness: a mechanism involving matrix metalloproteinase-2 and the urokinase-type plasminogen activator-plasmin cascade. J Neurosci 23: 4034-4043. (Pubitemid 36958422)
76. Leventhal C, Rafii S, Rafii D, Shahar A, Goldman SA. (1999). Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 13: 450-464. (Pubitemid 29337211)
77. Libermann TA, Nusbaum HR, Razon N, Kris R, Lax I, Soreq H et al. (1985). Amplification, enhanced expression and possible rearrangement of EGF receptor gene in primary human brain tumours of glial origin. Nature 313: 144-147. (Pubitemid 15192341)
78. Lohr J, Ratliff T, Huppertz A, Ge Y, Dictus C, Ahmadi R et al. (2011). Effector T-Cell Infiltration Positively Impacts Survival of Glioblastoma Patients and Is Impaired by Tumor-Derived TGF-\{beta\}. Clin Cancer Res 17: 4296-4308.
79. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A et al. (2007). The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathologica 114: 97-109. (Pubitemid 47103521)
80. Lu C, Shervington A. (2008). Chemoresistance in gliomas. Mol Cell Biochem 312: 71-80.
81. Markovic DS, Glass R, Synowitz M, Rooijen N, Kettenmann H. (2005). Microglia stimulate the invasiveness of glioma cells by increasing the activity of metalloprotease-2. J Neuropathol Exp Neurol 64: 754-762. (Pubitemid 41285807)
82. Markovic DS, Vinnakota K, Chirasani S, Synowitz M, Raguet H, Stock K et al. (2009). Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion. Proc Natl Acad Sci USA 106: 12530-12535.
83. Minghetti L, Levi G. (1998). Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol 54: 99-125. (Pubitemid 28049822)
84. Network CGAR. (2008). Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455: 1061-1068.
85. Okada M, Saio M, Kito Y, Ohe N, Yano H, Yoshimura S et al. (2009). Tumor-associated macrophage/microglia infiltration in human gliomas is correlated with MCP-3, but not MCP-1. Int J Oncol 34: 1621-1627.
86. Ozerdem U, Stallcup WB. (2004). Pathological angiogenesis is reduced by targeting pericytes via the NG2 proteoglycan. Angiogenesis 7: 269-276.
87. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD et al. (2006). Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9: 157-173. (Pubitemid 43357943)
88. Platten M, Kretz A, Naumann U, Aulwurm S, Egashira K, Isenmann S et al. (2003). Monocyte chemoattractant protein-1 increases microglial infiltration and aggressiveness of gliomas. Ann Neurol 54: 388-392. (Pubitemid 37072043)
89. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P et al. (2006). Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 9: 331-339. (Pubitemid 43290962)
90. Ramnarain DB, Park S, Lee DY, Hatanpaa KJ, Scoggin SO, Otu H et al. (2006). Differential gene expression analysis reveals generation of an autocrine loop by a mutant epidermal growth factor receptor in glioma cells. Cancer Res 66: 867-874. (Pubitemid 43165952)
91. Rempel SA, Dudas S, Ge S, Gutierrez JA. (2000). Identification and localization of the cytokine SDF1 and its receptor, CXC chemokine receptor 4, to regions of necrosis and angiogenesis in human glioblastoma. Clin Cancer Res 6: 102-111. (Pubitemid 30064982)
92. Rong Y, Durden DL, Van Meir EG, Brat DJ. (2006). 'Pseudopalisading'necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J Neuropathol Exp Neurol 65: 529-539. (Pubitemid 44288937)
93. Rovit RL, Hagan R. (1968). Steroids and cerebral edema: the effects of glucocorticoids on abnormal capillary permeability following cerebral injury in cats. J Neuropathol Exp Neurol 27: 277-299.
94. Sameshima T, Nabeshima K, Toole BP, Yokogami K, Okada Y, Goya T et al. (2000). Glioma cell extracellular matrix metalloproteinase inducer (EMMPRIN) (CD147) stimulates production of membranetype matrix metalloproteinases and activated gelatinase A in cocultures with brain-derived fibroblasts. Cancer Lett 157: 177-184. (Pubitemid 30629029)
95. Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M et al. (1995). Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376: 70-74.
96. Sciuscio D, Diserens AC, van Dommelen K, Martinet D, Jones G, Janzer RC et al. (2011). Extent and patterns of MGMT promoter methylation in glioblastoma- and respective glioblastoma-derived spheres. Clin Cancer Res 17: 255-266.
97. Seidel S, Garvalov BK, Wirta V, von Stechow L, Schanzer A, Meletis K et al. (2010). A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain 133: 983-995.
98. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC et al. (2009). Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10: 459-466.
99. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S et al. (1996). Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87: 1171-1180. (Pubitemid 27010101)
100. Suzuki Y, Funakoshi H, Machide M, Matsumoto K, Nakamura T. (2008). Regulation of cell migration and cytokine production by HGF-like protein (HLP) / macrophage stimulating protein (MSP) in primary microglia. Biomed Res 29: 77-84. (Pubitemid 351753466)
101. Suzumura A, Sawada M, Yamamoto H, Marunouchi T. (1993). Transforming growth factor-beta suppresses activation and proliferation of microglia in vitro. J Immunol 151: 2150-2158. (Pubitemid 23235688)
102. Vairano M, Graziani G, Tentori L, Tringali G, Navarra P, Dello Russo C. (2004). Primary cultures of microglial cells for testing toxicity of anticancer drugs. Toxicol Lett 148: 91-94. (Pubitemid 38264524)
103. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ. (2010). Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 60: 166-193.
104. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD et al. (2010). Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110.
105. Verma S, Nakaoke R, Dohgu S, Banks WA. (2006). Release of cytokines by brain endothelial cells: A polarized response to lipopolysaccharide. Brain Behav Immun 20: 449-455. (Pubitemid 44175796)
106. Villeneuve J, Galarneau H, Beaudet MJ, Tremblay P, Chernomoretz A, Vallieres L. (2008). Reduced glioma growth following dexamethasone or anti-angiopoietin 2 treatment. Brain Pathol 18: 401-414. (Pubitemid 351782849)
107. Virrey JJ, Golden EB, Sivakumar W, Wang W, Pen L, Schonthal AH et al. (2009). Glioma-associated endothelial cells are chemoresistant to temozolomide. J Neurooncol 95: 13-22.
108. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A et al. (2010). Glioblastoma stem-like cells give rise to tumour endothelium. Nature 468: 829-833.
109. Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS et al. (2009). Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res 69: 2400-2407.
110. Watling CJ, Lee DH, Macdonald DR, Cairncross JG. (1994). Corticosteroid-induced magnetic resonance imaging changes in patients with recurrent malignant glioma. J Clin Oncol 12: 1886-1889. (Pubitemid 24349391)
111. Weissenberger J, Loeffler S, Kappeler A, Kopf M, Lukes A, Afanasieva TA et al. (2004). IL-6 is required for glioma development in a mouse model. Oncogene 23: 3308-3316. (Pubitemid 38669820)
112. Wen PY, Kesari S. (2008). Malignant gliomas in adults. N Engl J Med 359: 492-507.
113. Wiesenhofer B, Weis C, Humpel C. (2000). Glial cell line-derived neurotrophic factor (GDNF) is a proliferation factor for rat C6 glioma cells: evidence from antisense experiments. Antisense Nucleic Acid Drug Dev 10: 311-321.
114. Wilhelmsson U, Bushong EA, Price DL, Smarr BL, Phung V, Terada M et al. (2006). Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc Natl Acad Sci USA 103: 17513-17518. (Pubitemid 44789000)
115. Wong AJ, Ruppert JM, Bigner SH, Grzeschik CH, Humphrey PA, Bigner DS et al. (1992). Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc Natl Acad Sci USA 89: 2965-2969.
116. Wu A, Wei J, Kong LY, Wang Y, Priebe W, Qiao W et al. (2010). Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol 12: 1113-1125.
117. Xu Q, Wang S, Jiang X, Zhao Y, Gao M, Zhang Y et al. (2007). Hypoxia-induced astrocytes promote the migration of neural progenitor cells via vascular endothelial factor, stem cell factor, stromal-derived factor-1alpha and monocyte chemoattractant protein-1 upregulation in vitro. Clin Exp Pharmacol Physiol 34: 624-631. (Pubitemid 46953102)
118. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W et al. (2009). IDH1 and IDH2 mutations in gliomas. N Engl J Med 360: 765-773.
119. Yeh WL, Lu DY, Liou HC, Fu WM. (2011). A forward loop between glioma and microglia: Glioma-derived extracellular matrix-activated microglia secrete IL-18 to enhance the migration of glioma cells. J Cell Physiol (e-pub ahead of print).
120. Zhou Y, Larsen PH, Hao C, Yong VW. (2002). CXCR4 is a major chemokine receptor on glioma cells and mediates their survival. J Biol Chem 277: 49481-49487. (Pubitemid 36014384)
121. Zhu H, Acquaviva J, Ramachandran P, Boskovitz A, Woolfenden S, Pfannl R et al. (2009). Oncogenic EGFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc Natl Acad Sci USA 106: 2712-2716.
122. Zuniga RM, Torcuator R, Jain R, Anderson J, Doyle T, Ellika S et al. (2009). Efficacy, safety and patterns of response and recurrence in patients with recurrent high-grade gliomas treated with bevacizumab plus irinotecan. J Neurooncol 91: 329-336.