The evolving role of antiangiogenic therapies in glioblastoma multiforme: current clinical significance and future potential

References

• Rulseh A, Keller J, Klener J, et al. Long-term survival of patients suffering from glioblastoma multiforme treated with tumor-treating fields. World J Surg Oncol. 2012;10:220.
   PubMed Web of Science ®Google Scholar
• Krex D, Klink B, Hartmann C, et al. Long-term survival with glioblastoma multiforme. Brain. 2007;130:2596–2606.
   PubMed Web of Science ®Google Scholar
• Yabroff K, Harlan L, Zeruto C, et al. Patterns of care and survival for patients with glioblastoma multiforme diagnosed during 2006. Neuro Oncol. 2012;14:351–359.
   PubMed Web of Science ®Google Scholar
• Koshy M, Villano J, Dolecek T, et al. Improved survival time trends for glioblastoma using the SEER 17 population-based registries. J Neurooncol. 2012;107:207–212.
   PubMed Web of Science ®Google Scholar
• Stupp R, Mason W, van Den Bent M, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–996.
   PubMed Web of Science ®Google Scholar
• Louis D, Ohgaki H, Wiestler O, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114(2):97–109.
   PubMed Web of Science ®Google Scholar
• André T, Chastre E, Kotelevets L, et al. Tumoral angiogenesis: physiopathology, prognostic value and therapeutic perspectives. Rev Méd Int. 1998;19:904–913.
   PubMed Web of Science ®Google Scholar
• Li WW. Tumor angiogenesis: molecular pathology, therapeutic targeting, and imaging. Acad Radiol. 2000;7:800–811.
   PubMed Web of Science ®Google Scholar
• Plate K, Scholz A, Dumont D. Tumor angiogenesis and anti-angiogenic therapy in malignant gliomas revisited. Acta Neuropathol. 2012;124:763–775.
   PubMed Web of Science ®Google Scholar
• Reardon D, Turner S, Peters K, et al. A review of VEGF/VEGFR-targeted therapeutics for recurrent glioblastoma. J Natl Compr Canc Netw. 2011;9:414–427.
   PubMed Web of Science ®Google Scholar
• Tung J, Tattersall I, Kitajewski J. Tips, stalks, tubes: notch-mediated cell fate determination and mechanisms of tubulogenesis during angiogenesis. Cold Spring Harb Perspect Med. 2012;2:a006601-a006601.
   PubMed Web of Science ®Google Scholar
• Baeriswyl V, Christofori G. The angiogenic switch in carcinogenesis. Semin Cancer Biol. 2009;19:329–337.
   PubMed Web of Science ®Google Scholar
• Viallard C, Larrivee B. Tumor angiogenesis and vascular normalization: alternative therapeutic targets. Angiogenesis. 2017;20(4):409–426.
   PubMed Web of Science ®Google Scholar
• Ferrara N, Hillan K, Gerber H, et al. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov. 2004;3:391–400.
   PubMed Web of Science ®Google Scholar
• Melder R, Koenig G, Witwer B, et al. During angiogenesis, vascular endothelial growth factor regulate natural killer cell adhesion to tumor endothelium. Nat Med. 1996;2:992–997.
   PubMed Web of Science ®Google Scholar
• Gupta K, Kshirsagar S, Li W, et al. EGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp Cell Res. 1999;247:495–504.
   PubMed Web of Science ®Google Scholar
• Plate KH, Breier G, Weich HA, et al. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature. 1992;359:845–848.
   PubMed Web of Science ®Google Scholar
• Takano S, Yoshii Y, Kondo S, et al. Concentration of vascular endothelial growth factor in the serum and tumor tissue of brain tumor patients. Cancer Res. 1996;56:2185–2190.
   PubMed Web of Science ®Google Scholar
• Nam D, Park K, Suh Y, et al. Expression of VEGF and brain specific angiogenesis inhibitor-1 in glioblastoma: prognostic significance. Oncol Rep. 2004;11:863–869.
   PubMed Web of Science ®Google Scholar
• Sharma A, Bendre A, Mondal A, et al. Angiogenic gene signature derived from subtype specific cell models segregate proneural and mesenchymal glioblastoma. Front Oncol. 2017;7:146.
   PubMed Web of Science ®Google Scholar
• Phillips H, Kharbanda S, Chen R, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006;9(3):157–173.
   PubMed Web of Science ®Google Scholar
• Salmaggi A, Eoli M, Frigerio S, et al. Intracavitary VEGF, bFGF, IL-8, IL-12 levels in primary and recurrent malignant glioma. J Neurooncol. 2003;62:297–303.
   PubMed Web of Science ®Google Scholar
• Stefanik D, Fellows W, Rizkalla L, 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kerber M, Reiss Y, Wickersheim A, et al. Flt-1 signaling in macrophages promotes glioma growth in vivo. Cancer Res. 2008;68:7342–7351.
   PubMed Web of Science ®Google Scholar
• Peterson T, Kirkpatrick N, Huang Y, et al. Dual inhibition of Ang-2 and VEGF receptors normalizes tumor vasculature and prolongs survival in glioblastoma by altering macrophages. Proc Natl Acad Sci U S A. 2016;113:4470–4475.
   PubMed Web of Science ®Google Scholar
• Liu K, Zhang X, Xu W, et al. Targeting the vasculature in hepatocellular carcinoma treatment: starving versus normalizing blood supply. Clin Transl Gastroenterol. 2017;8(6):e98. doi: 10.1038/ctg.2017.28.
   Google Scholar
• Al-Husein B, Abdalla M, Trepte M, et al. Antiangiogenic therapy for cancer: an update. Pharmacotherapy. 1012;32(12):1095–1111.
   Google Scholar
• Batchelor T, Gerstner E, Emblem K, et al. Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc Natl Acad Sci USA. 2013;110(47):19059–19064.
   PubMed Web of Science ®Google Scholar
• Batchelor T, Mulholland P, Neyns B, et al. Phase III randomized trial comparing the efficacy of cediranib as monotherapy, and in combination with lomustine, versus lomustine alone in patients with recurrent glioblastoma. J Clin Oncol. 2013;31:3212–3218.
   PubMed Web of Science ®Google Scholar
• Gomez-Manzano C, Holash J, Fueyo J, et al. VEGF Trap induces antiglioma effect at different stages of disease. Neuro Oncol. 2008;10:940–945.
   PubMed Web of Science ®Google Scholar
• De Groot J, Lamborn K, Chang S, et al. Phase II study of aflibercept in recurrent malignant glioma: a North American brain tumor consortium study. J Clin Oncol. 2011;29:2689–2695.
   PubMed Web of Science ®Google Scholar
• Raymond E, Brandes A, Dittrich C, et al. Phase II study of imatinib in patients with recurrent gliomas of various histologies: a European Organisation for Research and Treatment of Cancer Brain Tumor Group Study. J Clin Oncol. 2008;26:4659–4665.
   PubMed Web of Science ®Google Scholar
• Reardon D, Dresemann G, Taillibert S, et al. Multicentre phase II studies evaluating imatinib plus hydroxyurea in patients with progressive glioblastoma. Br J Cancer. 2009;101:1995–2004.
   PubMed Web of Science ®Google Scholar
• Dresemann G, Weller M, Rosenthal M, et al. Imatinib in combination with hydroxyurea versus hydroxyurea alone as oral therapy in patients with progressive pretreated glioblastoma resistant to standard dose temozolomide. J Neurooncol. 2010;96:393–402.
   PubMed Web of Science ®Google Scholar
• Reardon DJ, Pan E, Fan J, et al. A phase 2 trial of the multitargeted Kinase Inhibitor Lenvatinib (E7080) in patients with recurrent glioblastoma and disease progression following prior bevacizumab treatment. In: Fabrice André (ed). Abstract book of the 37th ESMO Congress Vienna, Austria, 28 September – 2 October 2012. Vienna, Austria.: Presented at the ESMO 2012; 2012:417p.
   Google Scholar
• Nabors L, Fiveash J, Markert J, et al. A phase 1 trial of ABT-510 concurrent with standard chemoradiation for patients with newly diagnosed glioblastoma. Arch Neurol. 2010;67:313–319.
   PubMedGoogle Scholar
• Anderson JC, Grammer JR, Wang W, et al. ABT-510, a modified type 1 repeat peptide of thrombospondin, inhibits malignant glioma growth in vivo by inhibiting angiogenesis. Cancer Biol Ther. 2007;6:454–462.
   PubMed Web of Science ®Google Scholar
• Taga T, Suzuki A, Gonzalez-Gomez I, et al. alpha v-Integrin antagonist EMD 121974 induces apoptosis in brain tumor cells growing on vitronectin and tenascin. Int J Cancer. 2002;98:690–697.
   PubMed Web of Science ®Google Scholar
• Reardon D, Fink K, Mikkelsen T, et al. Randomized phase II study of cilengitide, an integrin-targeting arginine-glycine-aspartic acid peptide, in recurrent glioblastoma multiforme. J Clin Oncol. 2008;26:5610–5617.
   PubMed Web of Science ®Google Scholar
• Gilbert M, Kuhn J, Lamborn K, et al. Cilengitide in patients with recurrent glioblastoma: the results of NABTC 03–02, a phase II trial with measures of treatment delivery. J Neurooncol. 2012;106:147–153.
   PubMed Web of Science ®Google Scholar
• Nabors L, Mikkelsen T, Hegi M, et al. A safety run-in and randomized phase 2 study of cilengitide combined with chemoradiation for newly diagnosed glioblastoma. Cancer. 2012;118:5601–56607.
   PubMed Web of Science ®Google Scholar
• Stupp R, Hegi M, Neyns B, et al. Phase I/IIa study of cilengitide and temozolomide with concomitant radiotherapy followed by cilengitide and temozolomide maintenance therapy in patients with newly diagnosed glioblastoma. JCO. 2010;28:2712–2718.
   PubMed Web of Science ®Google Scholar
• Stupp R, Van Den Bent M, Erridge S, et al. Cilengitide in newly diagnosed glioblastoma with MGMT promoter methylation: protocol of a multicenter, randomized, open-label, controlled phase III trial (CENTRIC). J Clin Oncol. 2010;28:15.
   PubMed Web of Science ®Google Scholar
• Cohen M, Shen Y, Keegan P, et al. Recurrent FDASBAaTo. FDA drug approval summary: bevacizumab (Avastin®) as treatment of recurrent glioblastoma multiforme. Oncologist. 2009;14:1131–1138.
   PubMed Web of Science ®Google Scholar
• Summers J, Cohen M, Keegan P, et al. FDA drug approval summary: bevacizumab plus interferon for advanced renal cell carcinoma. Oncologist. 2010;15(1):104–111.
   PubMed Web of Science ®Google Scholar
• Hofer S, Elandt K, Greil R, et al. Clinical outcome with bevacizumab in patients with recurrent high-grade glioma treated outside clinical trials. Acta Oncologica. 2011;50:630–635.
   PubMed Web of Science ®Google Scholar
• Kreisl T, Kim L, Moore K, et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol. 2009;27:740–745.
   PubMed Web of Science ®Google Scholar
• Raizer J, Grimm S, Chamberlain M, et al. A phase 2 trial of single-agent bevacizumab given in an every-3-week schedule for patients with recurrent high-grade gliomas. Cancer. 2010;116:5297–5305.
   PubMed Web of Science ®Google Scholar
• Nagane M, Nishikawa R, Narita Y, et al. Phase II study of single-agent bevacizumab in Japanese patients with recurrent malignant glioma. Jpn J Clin Oncol. 2012;42:887–895.
   PubMed Web of Science ®Google Scholar
• Friedman H, Prados M, Wen P, et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol. 2009;27:4733–4740.
   PubMed Web of Science ®Google Scholar
• Taal W, Oosterkamp H, Walenkamp A, et al. Single-agent bevacizumab or lomustine versus a combination of bevacizumab plus lomustine in patients with recurrent glioblastoma (BELOB trial): a randomised controlled phase 2 trial. Lancet Oncol. 2014;15(9):943–953.
   PubMed Web of Science ®Google Scholar
• Wick W, Gorlia T, Bendszus M, et al. Lomustine and bevacizumab in progressive glioblastoma. N Engl J Med. 2017;377(20):1954–1963.
   PubMed Web of Science ®Google Scholar
• Lai A, Kharbanda S, Pope W, et al. Evidence for sequenced molecular evolution of IDH1 mutant glioblastoma from a distinct cell of origin. JCO. 2011;29:4482–4490.
   PubMed Web of Science ®Google Scholar
• Vredenburgh J, Desjardins A, Kirkpatrick J, et al. Addition of bevacizumab to standard radiation therapy and daily temozolomide is associated with minimal toxicity in newly diagnosed glioblastoma multiforme. Int J Radiat Oncol Biol Phys. 2012;82:58–66.
   PubMed Web of Science ®Google Scholar
• Narayana A, Gruber D, Kunnakkat S, et al. A clinical trial of bevacizumab, temozolomide, and radiation for newly diagnosed glioblastoma. J Neurosurg. 2012;116:341–345.
   PubMed Web of Science ®Google Scholar
• Chinot O, Wick W, Mason W, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med. 2014;370:709–722.
   PubMed Web of Science ®Google Scholar
• Gilbert M, Dignam J, Armstrong T, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370:699–708.
   Web of Science ®Google Scholar
• Schaub C, Schafer N, Mack F, et al. The earlier the better? Bevacizumab in the treatment of recurrent MGMT-non-methylated glioblastoma. J Cancer Res Clin Oncol. 2016;142:1825–1829.
   PubMed Web of Science ®Google Scholar
• Chinot O, Nishikawa R, Mason W, et al. Upfront bevacizumab may extend survival for glioblastoma patients who do not receive second-line therapy: an exploratory analysis of AVAglio. Neuro Oncol. 2016;18(9):1313–1318.
   PubMed Web of Science ®Google Scholar
• Huang R, Neagu M, Reardon D, et al. Pitfalls in the neuroimaging of glioblastoma in the era of antiangiogenic and immuno/targeted therapy – detecting illusive disease, defining response. Front Neurol. 2015;6:33.
   PubMed Web of Science ®Google Scholar
• Hegi ME, Diserens A-C, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997–1003.
   PubMed Web of Science ®Google Scholar
• Labussière M, Cheneau C, Prahst C, et al. Angiopoietin-2 may be involved in the resistance to bevacizumab in recurrent glioblastoma. Cancer Invest. 2016;34:39–44.
   PubMed Web of Science ®Google Scholar
• Piao Y, Liang J, Holmes L, et al. Acquired resistance to anti-VEGF therapy in glioblastoma is associated with a mesenchymal transition. Clin Cancer Res. 2013;19(16):4392–4403.
   PubMed Web of Science ®Google Scholar
• Reardon D, Lassman A, Schiff D, et al. Phase 2 and biomarker study of trebananib, an angiopoietin-blocking peptibody with and without bevacizumab for patients with recurrent glioblastoma. Cancer. 2018;124(7):1438–1448.
   PubMed Web of Science ®Google Scholar
• D’Alessandris Q, Montano N, Cenci T, et al. Targeted therapy with bevacizumab and erlotinib tailored to the molecular profile of patients with recurrent glioblastoma. Preliminary experience. Acta Neurochir (Wien). 2013;155:33–40.
   PubMed Web of Science ®Google Scholar
• Neal J, Nguyen K. First-line treatment of EGFR-mutant non-small-cell lung cancer: the role of erlotinib and other tyrosine kinase inhibitors. Biologics. 2012;6:337.
   PubMedGoogle Scholar
• Sathornsumetee S, Desjardins A, Vredenburgh J, et al. Phase II trial of bevacizumab and erlotinib in patients with recurrent malignant glioma. Neuro Oncol. 2010;12:1300–1310.
   PubMed Web of Science ®Google Scholar
• Mladkova N, Chakravarti A. Molecular profiling in glioblastoma: prelude to personalized treatment. Curr Oncol Rep. 2009;11:53–61.
   PubMed Web of Science ®Google Scholar
• Tabouret E, Boudouresque F, Barrie M, et al. Association of matrix metalloproteinase 2 plasma level with response and survival in patients treated with bevacizumab for recurrent high-grade glioma. Neuro Oncol. 2014;16(3):392–399.
   PubMed Web of Science ®Google Scholar
• Sandmann T, Bourgon R, Garcia J, et al. Patients with proneural glioblastoma may derive overall survival benefit from the addition of bevacizumab to first-line radiotherapy and temozolomide: retrospective analysis of the AVAglio trial. J Clin Oncol. 2015;33(25):2735–2744.
   PubMed Web of Science ®Google Scholar
• Lu-Emerson C, Duda D, Emblem K, et al. Lessons from anti–vascular endothelial growth factor and anti-vascular endothelial growth factor receptor trials in patients with glioblastoma. J Clin Oncol. 2015;33(10):1197–1213.
   PubMed Web of Science ®Google Scholar
• Pope W, Lai A, Nghiemphu P, et al. MRI in patients with high-grade gliomas treated with bevacizumab and chemotherapy. Neurology. 2006;66:1258–1260.
   PubMed Web of Science ®Google Scholar
• Weinstein J, Varallyay C, Dosa E, et al. Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J Cereb Blood Flow Metab. 2010;30:15–35.
   PubMed Web of Science ®Google Scholar
• Imber B, Kanungo I, Braunstein S, et al. Indications and efficacy of gamma knife stereotactic radiosurgery for recurrent glioblastoma: two decades of institutional experience. Neurosurgery. 2017;80(1):129–139.
   PubMed Web of Science ®Google Scholar
• Park K, Kano H, Iyer A, et al. Salvage gamma knife stereotactic radiosurgery followed by bevacizumab for recurrent glioblastoma multiforme: a case-control study. J Neurooncol. 2012;107:323–333.
   PubMed Web of Science ®Google Scholar
• Terme M, Pernot S, Marcheteau E, et al. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res. 2013;73:539–549.
   PubMed Web of Science ®Google Scholar
• Reardon D, Mitchell D. The development of dendritic cell vaccine-based immunotherapies for glioblastoma. Semin Immunopathol. 2017;39(2):225–239.
   PubMed Web of Science ®Google Scholar
• Bota D, Chung J, Dandekar M, et al. Phase II study of ERC1671 plus bevacizumab versus bevacizumab plus placebo in recurrent glioblastoma: interim results and correlations with CD4+ T-lymphocyte counts. CNS Oncol. 2018;7(3).
   Google Scholar
• Reardon D, Nayak L, Peters K Phase II study of pembrolizumab or pembrolizumab plus bevacizumab for recurrent glioblastoma (rGBM) patients. ASCO Annual Meeting; Chicago, Illinois, United States of America. 2018.
   Google Scholar
• Ghiaseddin A, Reardon D, Massey W, et al. Phase II study of bevacizumab and vorinostat for patients with recurrent world health organization grade 4 malignant glioma. Oncologist. 2017;23(2):145.
   Web of Science ®Google Scholar
• Filley A, Henriquez M, Dey M. Recurrent glioma clinical trial, Checkmate-143: the game is not over yet. Oncotarget. 2017;8(53):91779–91794.
   PubMedGoogle Scholar
• Reardon D, Peereboom D, Nabors L. Phase 2 trial of SL-701, a novel immunotherapy comprised of synthetic short peptides against GBM targets IL-13Rα2, EphA2, and Survivin, in adults with second-line recurrent GBM: interim results. Journal of Clinical Oncology. 2016.
   Google Scholar
• Kovic B, Xie F. Economic evaluation of bevacizumab for the first-line treatment of newly diagnosed glioblastoma multiforme. J Clin Oncol. 2015;33(20):2296–2302.
   PubMed Web of Science ®Google Scholar
• Meropol N, Schulman K. Cost of cancer care: issues and implications. JCO. 2007;25:180–186.
   PubMed Web of Science ®Google Scholar