Seminars in Radiation Oncology
Volume 19, Issue 3 , Pages 163-170 , July 2009

Therapeutic Targets in Malignant Glioblastoma Microenvironment

References 

  1. Folkman J, Hahnfeldt P, Hlatky L. Cancer: Looking outside the genome. Nat Rev Mol Cell Biol. 2000;1:76–79
  2. Barcellos-Hoff MH. It takes a tissue to make a tumor: Epigenetics, cancer and the microenvironment. J Mammary Gland Biol Neoplasia. 2001;6:213–221
  3. Moran JM, Elshaikh MA, Lawrence TS. Radiotherapy: What can be achieved by technical improvements in dose delivery?. Lancet Oncol. 2005;6:51–58
  4. Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment—Tumorigenesis and therapy. Nat Rev Cancer. 2005;5:867–875
  5. Derynck R, Akhurst RJ, Balmain A. TGFβ signaling in tumor suppression and cancer progression. Nat Genet. 2001;29:117–129
  6. Teicher BA. Malignant cells, directors of the malignant process: Role of transforming growth factor-beta. Cancer Metastasis Rev. 2001;20:133–143
  7. Anscher MS, Peters WP, Reisenbichler H, et al. Transforming growth factor β as a predictor of liver and lung fibrosis after autologous bone marrow transplantation for advanced breast cancer. N Engl J Med. 1993;328:1592–1598
  8. Kong F-M, Anscher MS, Murase T, et al. Elevated plasma transforming gorwth factor-β1 levels in breast cancer patients decrease after surgical removal of tumor. Ann Surg. 1995;222:155–162
  9. Miettinen PJ, Ebner R, Lopez AR, et al. TGFβ induced transdifferentiation of mammary epithelial cells to mesenchymal cells: Involvement of type I receptors. J Cell Biol. 1994;127:2021–2036
  10. Ronnov-Jessen L, Petersen OW. Induction of α-smooth muscle actin by transforming growth factor-β1 in quiescent human breast gland fibroblasts. Lab Invest. 1993;68:696–707
  11. Yingling JM, Blanchard KL, Sawyer JS. Development of TGF-beta signaling inhibitors for cancer therapy. Nat Rev Drug Discov. 2004;3:1011–1022
  12. Jachimczak P, Hessdörfer B, Fabel-Schulte K, et al. Transforming growth factor-beta-mediated autocrine growth regulation of gliomas as detected with phosphorothioate antisense oligonucleotides. Int J Cancer. 1996;65:332–337
  13. Weller M, Fontana A. The failure of current immunotherapy for malignant glioma (Tumor-derived TGF-beta, T-cell apoptosis, and the immune privilege of the brain). Brain Res Brain Res Rev. 1995;21:128–151
  14. Letterio JJ, Roberts AB. Regulation of immune responses by TGFβ. Annu Rev Immunol. 1998;16:137–161
  15. Naumann U, Maass P, Gleske AK, et al. Glioma gene therapy with soluble transforming growth factor-beta receptors II and III. Int J Oncol. 2008;33:759–765
  16. Pepper MS. Transforming growth factor-beta: Vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 1997;8:21–43
  17. Koochekpour S, Merzak A, Pilkington GJ. Vascular endothelial growth factor production is stimulated by gangliosides and TGF-beta isoforms in human glioma cells in vitro. Cancer Lett. 1996;102:209–215
  18. Wyss-Coray T, Feng L, Masliah E, et al. Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am J Pathol. 1995;147:53–67
  19. Hau P, Kunz-Schughart LA, Rümmele P, et al. Tenascin-C protein is induced by transforming growth factor-beta1 but does not correlate with time to tumor progression in high-grade gliomas. J Neurooncol. 2006;77:1–7
  20. Aigner L, Bogdahn U. TGF-beta in neural stem cells and in tumors of the central nervous system. Cell Tissue Res. 2008;331:225–241
  21. Letterio JJ, Geiser AG, Kulkarni AB, et al. Maternal rescue of transforming growth factor-β1 null mice. Science. 1994;264:1936–1938
  22. Makwana M, Jones LL, Cuthill D, et al. Endogenous transforming growth factor {beta}1 suppresses inflammation and promotes survival in adult (Child Neurology Society). J Neurosci. 2007;27:11201–11213
  23. Erickson AC, Barcellos-Hoff MH. The not-so innocent bystander: Microenvironment as a target of cancer therapy. Expert Opin Ther Targets. 2003;7:71–88
  24. Schlingensiepen K-H, Schlingensiepen R, Steinbrecher A, et al. Targeted tumor therapy with the TGF-Î22 antisense compound AP 12,009. Cytokine Growth Factor Rev. 2006;17:129–139
  25. Hau P, Jachimczak P, Schlingensiepen R, et al. Inhibition of TGFβ2 with AP 12009 (Recurrent malignant gliomas: From preclinical to phase I/II studies). Oligonucleotides. 2007;17:201–212
  26. Stefanik DF, Fellows WK, Rizkalla LR, et al. Monoclonal antibodies to vascular endothelial growth factor (VEGF) and the VEGF receptor, FLT-1, inhibit the growth of C6 glioma in a mouse xenograft. J Neurooncol. 2001;55:91–100
  27. Cha S, Knopp EA, Johnson G, et al. Intracranial mass lesions: Dynamic contrast-enhanced susceptibility-weighted echo-planar perfusion MR imaging. Radiology. 2002;223:11–29
  28. Kassner A, Roberts TP. Beyond perfusion: Cerebral vascular reactivity and assessment of microvascular permeability. Top Magn Reson Imaging. 2004;15:58–65
  29. Narayana A, Kelly P, Golfinos J, et al. Antiangiogenic therapy using bevacizumab in recurrent high-grade glioma: Impact on local control and patient survival. J Neurosurg. 2009;110:173–180
  30. Vredenburgh JJ, Desjardins A, En Herndon J, et al. Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res. 2007;13:1253–1259
  31. Chen W, Delaloye S, Silverman DH, et al. Predicting treatment response of malignant gliomas to bevacizumab and irinotecan by imaging proliferation with [18F] fluorothymidine positron emission tomography: A pilot study. J Clin Oncol. 2007;25:4714–4721
  32. Narayana A, Golfinos JG, Fischer I, et al. Feasibility of using bevacizumabwith radiation therapy and temozolomide in newly diagnosed high-grade glioma. Int J Radiat Oncol Biol Phys. 2008;72:383–389
  33. Fischer I, Cunliffe C, Bollo R, et al. High-grade glioma before and after treatment with radiation and Avastin: Initial observations. Neuro Oncol. 2008;10:700–708
  34. Norden AD, Young GS, Setayesh K, et al. Bevacizumab for recurrent malignant gliomas: Efficacy, toxicity, and patterns of recurrence. Neurology. 2008;70:779–787
  35. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008;8:592–603
  36. Bao S, Wu Q, Sathornsumetee S, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006;66:7843–7848
  37. Liu G, Yuan X, Zeng ZC, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer Res. 2006;5:67
  38. Sakariassen PØ, Prestegarden L, Wang J, et al. Angiogenesis-independent tumor growth mediated by stem-like cancer cells. Proc Natl Acad Sci U S A. 2006;101:16466–16471
  39. Nowicki MO, Dmitrieva N, Stein AM, et al. Lithium inhibits invasion of glioma cells: Possible involvement of glycogen synthase kinase-3. Neuro Oncol. 2008;10:690–699
  40. Cheon SS, Wei Q, Gurung A, et al. Beta-catenin regulates wound size and mediates the effect of TGF-beta in cutaneous healing 10.1096/fj. 05-4759com. FASEB J. 2006;20:692–701
  41. Reardon DA, Nabors LB, Stupp R, et al. Cilengitide: An integrin-targeting arginine-glycine–aspartic acid peptide with promising activity for glioblastoma multiforme. Expert Opin Investig Drugs. 2008;17:1225–1735
  42. Guillemin K, Krasnow MA. The hypoxic response: Huffing and HIFing. Cell. 1997;89:9–12
  43. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003;3:721–732
  44. Zagzag D, Lukyanov Y, Lan L, et al. Hypoxia-inducible factor-1 and VEGF upregulate CXCR4 in glioblastoma: Implications for angiogenesis and glioma cell invasion. Lab Invest. 2006;86:1221–1232
  45. Zagzag D, Salnikow K, Chiriboga L, et al. Downregulation of major histocompatibility complex antigens in invading glioma cells: Stealth invasion of the brain. Lab Invest. 2005;85:328–341
  46. Plasswilm L, Tannapfel A, Cordes N, et al. Hypoxia-induced tumour cell migration in an in vivo chicken model. Pathobiology. 2000;68:99–105
  47. Zagzag D, Zhong H, Scalzitti JM, et al. Expression of hypoxiainducible factor 1 in brain tumors: Association with angiogenesis, invasion, and progression. Cancer. 2000;88:2606–2618
  48. Ehtesham M, Winston JA, Kabos P, et al. CXCR4 expression mediates glioma cell invasiveness. Oncogene. 2006;25:2801–2806
  49. Bleul CC, Farzan M, Choe H, et al. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusion and blocks HIV-1 entry. Nature. 1996;382:829–833
  50. Tachibana K, Hirota S, Iizasa H, et al. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature. 1998;393:591–594
  51. Zagzag D, Esencay M, Mendez O, et al. Hypoxia- and VEGF-induced SDF-1/CXCR4 expression in glioblastomas: One plausible explanation of Scherer's structures. Am J Pathol. 2008;173:545–560
  52. Singh S, Singh UP, Grizzle WE, et al. CXCL12-CXCR4 interactions modulate prostate cancer cell migration, metalloproteinase expression and invasion. Lab Invest. 2004;84:1666–1676
  53. Lakka SS, Jasti SL, Gondi C, et al. Downregulation of MMP-9 in ERK-mutated stable transfectants inhibits glioma invasion in vitro. Oncogene. 2002;21:5601–5608
  54. Cox BD, Natarajan M, Stettner MR, et al. New concepts regarding focal adhesion kinase promotion of cell migration and proliferation. J Cell Biochem. 2006;99:35–52
  55. Haskell H, Natarajan M, Hecker TP, et al. Focal adhesion kinase is expressed in the angiogenic blood vessels of malignant astrocytic tumors in vivo and promotes capillary tube formation of brain microvascular endothelial cells. Clin Cancer Res. 2003;9:2157–2165
  56. Hauck CR, Sieg DJ, Hsia DA, et al. Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res. 2001;61:7079–7090
  57. Zagzag D, Friedlander DR, Margolis B, et al. Molecular events implicated in brain tumor angiogenesis and invasion. Pediatr Neurosurg. 2000;33:49–55
  58. Rasheed BK, Stenzel TT, McLendon RE, et al. PTEN gene mutations are seen in high-grade but not in low-grade gliomas. Cancer Res. 1997;57:4187–4190
  59. Knobbe CB, Merlo A, Reifenberger G. PTEN signaling in gliomas. Neuro Oncol. 2002;4:196–211
  60. Sibilia M, Fleischmann A, Behrens A, et al. The EGF receptor provides an essential survival signal for sos-dependent skin tumor development. Cell. 2000;102:211–220
  61. Mandell JW, Hussaini IM, Zecevic M, et al. In situ visualization of intratumor growth factor signaling: Immunohistochemical localization of activated ERK/MAP kinase in glial neoplasms. Am J Pathol. 1998;153:1411–1423
  62. Hecker TP, Grammer JR, Gillespie GY, et al. Focal adhesion kinase enhances signaling through the Shc/extracellular signal-regulated kinase pathway in anaplastic astrocytoma tumor biopsy samples. Cancer Res. 2002;62:2699–2707
  63. Olsson AK, Dimberg A, Kreuger J, et al. VEGF receptor signaling-in control of vascular function. Nat Rev Mol Cell Biol. 2006;7:359–371
  64. Woods SA, McGlade CJ, Guha A. Phosphatidylinositol 3′-kinase and MAPK/Erk kinase ½ differentially regulate expression of vascular endothelial growth factor in human malignant astrocytoma cells. Neuro Oncol. 2002;4:242–252
  65. Wei Y-S, Zhu Y-H, Du B, et al. Association of transforming growth factor-β gene polymorphisms with genetic susceptibility to nasopharyngeal carcinoma. Clinica Chim Acta. 2007;380:165–169
  66. Monje ML, Mizumatsu S, Fike JR, et al. Irradiation induces neural precursor-cell dysfunction. Nat Med. 2002;8:955–962
  67. Amundson SA, Bittner M, Chen Y, et al. Fluorescent cDNA microarray hybridization reveals complexity and heterogeneity of cellular genotoxic stress responses. Oncogene. 1999;18:3666–3672
  68. Burns TF, El-Deiry WS. Microarray analysis of p53 target gene expression patterns in the spleen and thymus in response to ionizing radiation. Cancer Biol Ther. 2003;2:431–443
  69. Rodningen OK, Overgaard J, Alsner J, et al. Microarray analysis of the transcriptional response to single or multiple doses of ionizing radiation in human subcutaneous fibroblasts. Radiother Oncol. 2005;77:231–240
  70. Barcellos-Hoff MH. Radiation-induced transforming growth factor β and subsequent extracellular matrix reorganization in murine mammary gland. Cancer Res. 1993;53:3880–3886
  71. Ehrhart EJ, Carroll A, Segarini P, et al. Transforming growth factor-β activation in situ: Quantitative and functional evidence following low dose irradiation. FASEB J. 1997;11:991–1002
  72. Wang J, Zheng H, Sung C-C, et al. Cellular sources of transforming growth factor-β isoforms in early and chronic radiation enteropathy. Am J Pathol. 1998;153:1531–1540
  73. Hauer-Jensen M, Richter KK, Wang J, et al. Changes in transforming growth factor beta1 gene expression and immunoreactivity levels during development of chronic radiation enteropathy. Radiat Res. 1998;150:673–680
  74. Becker KA, Lu S, Dickinson ES, et al. Estrogen and progesterone regulate radiation-induced p53 activity in mammary epithelium through TGF-beta-dependent pathways. Oncogene. 2005;24:6345–6353
  75. Milliat F, Francois A, Isoir M, et al. Influence of endothelial cells on vascular smooth muscle cells phenotype after irradiation: Implication in radiation-induced vascular damages. Am J Pathol. 2006;169:1484–1495
  76. Tabatabai G, Frank B, Mohle R, et al. Irradiation and hypoxia promote homing of haematopoietic progenitor cells towards gliomas by TGF-beta-dependent HIF-1alpha-mediated induction of CXCL12. Brain. 2006;129:2426–2435
  77. Anscher MS, Thrasher B, Rabbani Z, et al. Antitransforming growth factor-β antibody 1D11 ameliorates normal tissue damage caused by high-dose radiation. Int J Radiat Oncol Biol Phys. 2006;65:876–881
  78. Martin M, Lefaix J, Delanian S. TGF-beta1 and radiation fibrosis: A master switch and a specific therapeutic target?. Int J Radiat Oncol Biol Phys. 2000;47:277–290
  79. Flanders KC, Major CD, Arabshahi A, et al. Interference with transforming growth factor-{beta}/ SmadIII signaling results in accelerated healing of wounds in previously irradiated skin. Am J Pathol. 2003;163:2247–2257
  80. Rabbani ZN, Anscher MS, Zhang X, et al. Soluble TGFbeta type II receptor gene therapy ameliorates acute radiation-induced pulmonary injury in rats. Int J Radiat Oncol Biol Phys. 2003;57:563–572
  81. Xavier S, Piek E, Fujii M, et al. Amelioration of radiation-induced fibrosis: Inhibition of transforming growth factor-{beta} signaling by halofuginone. J Biol Chem. 2004;279:15167–15176
  82. Anscher MS, Thrasher B, Zgonjanin L, et al. Small molecular inhibitor of transforming growth factor-β protects against development of radiation-induced lung injury. Int J Radiat Oncol Biol Phys. 2008;71:829–837
  83. Barcellos-Hoff MH. How do tissues respond to damage at the cellular level? (The role of cytokines in irradiated tissues). Radiat Res. 1998;150:S109–S120
  84. Anscher MS, Kong F, Murase T, et al. Normal tissue injury after cancer therapy is a local response exacerbated by an endocrine effect of TGFβ. Br J Radiol. 1995;68:331–333
  85. Barcellos-Hoff MH. A novel redox mechanism for TGF-beta activation. Mol Biol Cell. 1994;5:139a
  86. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGF{beta} activation. J Cell Sci. 2003;116:217–224
  87. Flaumenhaft R, Rifkin DB. The extracellular regulation of growth factor action. Mol Biol Cell. 1992;3:1057–1065
  88. Barcellos-Hoff MH, Dix TA. Redox-mediated activation of latent transforming growth factor-β1. Mol Endocrinol. 1996;10:1077–1083
  89. Jobling MF, Mott JD, Finnegan , et al. Isoform specificity of redox-mediated TGFβ activation. Radiat Res. 2006;166:839–848
  90. Pociask DA, Sime PJ, Brody AR. Asbestos-derived reactive oxygen species active TGFβ1. Lab Invest. 2004;84:1013–1023
  91. Teicher BA, Holden SA, Ara G, et al. Transforming growth factor-beta in in vivo resistance. Cancer Chemother Pharmacol. 1996;37:601–609
  92. Teicher BA, Ikebe M, Ara G, et al. Transforming growth factor-beta 1 overexpression produces drug resistance in vivo: Reversal by decorin. In Vivo. 1997;11:463–472
  93. Ohmori T, Yang JL, Price JO, et al. Blockade of tumor cell transforming growth factor-betas enhances cell cycle progression and sensitizes human breast carcinoma cells to cytotoxic chemotherapy. Exp Cell Res. 1998;245:350–359
  94. Liu P, Menon K, Alvarez E, et al. Transforming growth factor-beta and response to anticancer therapies in human liver and gastric tumors in vitro and in vivo. Int J Oncol. 2000;16:599–610
  95. Kanamoto T, Hellman U, Heldin CH, et al. Functional proteomics of transforming growth factor-beta1-stimulated Mv1Lu epithelial cells: Rad51 as a target of TGFbeta1-dependent regulation of DNA repair. EMBO J. 2002;21:1219–1230
  96. Kirshner J, Jobling MF, Pajares MJ, et al. Inhibition of TGFβ1 signaling attenuates ATM activity in response to genotoxic stress. Cancer Res. 2006;66:10861–10868
  97. Wiegman EM, Blaese MA, Loeffler H, et al. TGFbeta-1 dependent fast stimulation of ATM and p53 phosphorylation following exposure to ionizing radiation does not involve TGFbeta-receptor I signaling. Radiother Oncol. 2007;83:289–295
  98. Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nat Rev Cancer. 2003;3:155–168
  99. Buckwalter MS, Yamane M, Coleman BS, et al. Chronically increased transforming growth factor-{beta}1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol. 2006;169:154–164
  100. Wick W, Platten M, Weller M. Glioma cell invasion: Regulation of metalloproteinase activity by TGF-beta. J Neurooncol. 2001;53:177–185

PII: S1053-4296(09)00021-6

doi: 10.1016/j.semradonc.2009.02.004

Seminars in Radiation Oncology
Volume 19, Issue 3 , Pages 163-170 , July 2009