The Current State of Potential Therapeutic Modalities for Glioblastoma Multiforme: A Clinical Review

Author(s): Elmira Mohtashami, Negar Shafaei-Bajestani, Hamid Mollazadeh, Seyed Hadi Mousavi, Mohammad Jalili-Nik, Amirhossein Sahebkar*, Amir R. Afshari*

Journal Name: Current Drug Metabolism

Volume 21 , Issue 8 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Glioblastoma multiforme (GBM), as the most lethal brain tumor, continues to be incurable. Considering the high mortality rate of GBM, it is crucial to develop new treatment approaches. Conventional therapies, including maximal surgical resection, radiation therapy, and chemotherapy (typically temozolomide), have not led to significant changes in the survival rates of GBM patients. However, emerging modalities, such as the use of tyrosine kinase inhibitors, mTOR inhibitors, NF-κB modulators, nitrosoureas, and immunotherapeutic agents have shown promising in improving GBM outcomes. In this context, we reviewed the current status of GBM treatment, the efficacy of existing standard therapies in improving disease outcomes, and future therapeutic directions.

Keywords: Glioblastoma multiforme, tyrosine kinase inhibitor, mTOR inhibitor, NF-κB modulator, immunotherapy, nitrosoureas.

[1]
Afshari, A.R.; Jalili-Nik, M.; Soukhtanloo, M.; Ghorbani, A.; Sadeghnia, H.R.; Mollazadeh, H.; Karimi Roshan, M.; Rahmani, F.; Sabri, H.; Vahedi, M.M.; Mousavi, S.H. Auraptene-induced cytotoxicity mechanisms in human malignant glioblastoma (U87) cells: role of reactive oxygen species (ROS). EXCLI J., 2019, 18, 576-590.
[PMID: 31611741]
[2]
Chinot, O.L.; Wick, W.; Mason, W.; Henriksson, R.; Saran, F.; Nishikawa, R.; Carpentier, A.F.; Hoang-Xuan, K.; Kavan, P.; Cernea, D.; Brandes, A.A.; Hilton, M.; Abrey, L.; Cloughesy, T. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med., 2014, 370(8), 709-722.
[http://dx.doi.org/10.1056/NEJMoa1308345] [PMID: 24552318]
[3]
Barbagallo, G.M.; Jenkinson, M.D.; Brodbelt, A.R. ‘Recurrent’ glioblastoma multiforme, when should we reoperate? Br. J. Neurosurg., 2008, 22(3), 452-455.
[http://dx.doi.org/10.1080/02688690802182256] [PMID: 18568742]
[4]
Hou, L.C.; Veeravagu, A.; Hsu, A.R.; Tse, V.C. Recurrent glioblastoma multiforme: a review of natural history and management options. Neurosurg. Focus, 2006, 20(4)E5
[http://dx.doi.org/10.3171/foc.2006.20.4.2] [PMID: 16709036]
[5]
Tavana, E.; Mollazadeh, H.; Mohtashami, E.; Modaresi, S.M.S.; Hosseini, A.; Sabri, H.; Soltani, A.; Javid, H.; Afshari, A.R.; Sahebkar, A. Quercetin: A promising phytochemical for the treatment of glioblastoma multiforme. Biofactors, 2019.
[http://dx.doi.org/10.1002/biof.1605] [PMID: 31880372]
[6]
Afshari, A.R.; Mollazadeh, H.; Mohtashami, E.; Soltani, A.; Soukhtanloo, M.; Hosseini, A.; Jalili-Nik, M.; Vahedi, M.M.; Roshan, M.K.; Sahebkar, A. Protective role of natural products in glioblastoma multiforme: A focus on nitric oxide pathway. Curr. Med. Chem., 2020.
[http://dx.doi.org/10.2174/0929867327666200130104757] [PMID: 32000638]
[7]
Vredenburgh, J.J.; Desjardins, A.; Herndon, J.E., II; Marcello, J.; Reardon, D.A.; Quinn, J.A.; Rich, J.N.; Sathornsumetee, S.; Gururangan, S.; Sampson, J.; Wagner, M.; Bailey, L.; Bigner, D.D.; Friedman, A.H.; Friedman, H.S. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J. Clin. Oncol., 2007, 25(30), 4722-4729.
[http://dx.doi.org/10.1200/JCO.2007.12.2440] [PMID: 17947719]
[8]
Martínez-Garcia, M.; Álvarez-Linera, J.; Carrato, C.; Ley, L.; Luque, R.; Maldonado, X.; Martínez-Aguillo, M.; Navarro, L.M.; Vaz-Salgado, M.A.; Gil-Gil, M. SEOM clinical guidelines for diagnosis and treatment of glioblastoma (2017). Clin. Transl. Oncol., 2018, 20(1), 22-28.
[http://dx.doi.org/10.1007/s12094-017-1763-6] [PMID: 29086250]
[9]
McCracken, D.J.; Celano, E.C.; Voloschin, A.D.; Read, W.L.; Olson, J.J. Phase I trial of dose-escalating metronomic temozolomide plus bevacizumab and bortezomib for patients with recurrent glioblastoma. J. Neurooncol., 2016, 130(1), 193-201.
[http://dx.doi.org/10.1007/s11060-016-2234-6] [PMID: 27502784]
[10]
Zheng, S.; Alfaro-Munoz, K.; Wei, W.; Wang, X.; Wang, F.; Eterovic, A.K.; Shaw, K.R.M.; Meric-Bernstam, F.; Fuller, G.N.; Chen, K.; Verhaak, R.G.; Mills, G.B.; Yung, W.K.A.; Weathers, S.P.; de Groot, J.F. Prospective Clinical Sequencing of Adult Glioma. Mol. Cancer Ther., 2019, 18(5), 991-1000.
[http://dx.doi.org/10.1158/1535-7163.MCT-18-1122] [PMID: 30926639]
[11]
Preusser, M.; Lim, M.; Hafler, D.A.; Reardon, D.A.; Sampson, J.H. Prospects of immune checkpoint modulators in the treatment of glioblastoma. Nat. Rev. Neurol., 2015, 11(9), 504-514.
[http://dx.doi.org/10.1038/nrneurol.2015.139] [PMID: 26260659]
[12]
Paw, I.; Carpenter, R.C.; Watabe, K.; Debinski, W.; Lo, H-W. Mechanisms regulating glioma invasion. Cancer Lett., 2015, 362(1), 1-7.
[http://dx.doi.org/10.1016/j.canlet.2015.03.015] [PMID: 25796440]
[13]
Li, X.; Wu, C.; Chen, N.; Gu, H.; Yen, A.; Cao, L.; Wang, E.; Wang, L. PI3K/Akt/mTOR signaling pathway and targeted therapy for glioblastoma. Oncotarget, 2016, 7(22), 33440-33450.
[http://dx.doi.org/10.18632/oncotarget.7961] [PMID: 26967052]
[14]
Srivastava, C; Gupta, Y; Irshad, K; Chattopadhaya, P; Sarkar, C; Suri, A 123P Curcumin downregulates FAT1 expression via NFkB in glioblastoma. Annals of Oncology, 2017, 28(suppl_10) , mdx657. 005.
[15]
Soukhtanloo, M.; Mohtashami, E.; Maghrouni, A.; Mollazadeh, H.; Mousavi, S.H.; Roshan, M.K.; Tabatabaeizadeh, S.A.; Hosseini, A.; Vahedi, M.M.; Jalili-Nik, M.; Afshari, A.R. Natural products as promising targets in glioblastoma multiforme: a focus on NF-κB signaling pathway. Pharmacol. Rep., 2020, 72(2), 285-295.
[http://dx.doi.org/10.1007/s43440-020-00081-7] [PMID: 32152926]
[16]
Chen, R.; Cohen, A.L.; Colman, H. Targeted therapeutics in patients with high-grade gliomas: past, present, and future. Curr. Treat. Options Oncol., 2016, 17(8), 42.
[http://dx.doi.org/10.1007/s11864-016-0418-0] [PMID: 27334978]
[17]
Driehuis, E.; Spelier, S.; Beltrán Hernández, I.; de Bree, R.; M Willems, S. Clevers, H.; Oliveira, S. Patient-Derived Head and Neck Cancer Organoids Recapitulate EGFR Expression Levels of Respective Tissues and Are Responsive to EGFR-Targeted Photodynamic Therapy. J. Clin. Med., 2019, 8(11), 1880.
[http://dx.doi.org/10.3390/jcm8111880] [PMID: 31694307]
[18]
Binder, ZA; Thorne, AH; Bakas, S; Wileyto, EP; Bilello, M; Akbari, H Epidermal growth factor receptor extracellular domain mutations in glioblastoma present opportunities for clinical imaging and therapeutic development. Cancer cell., 2018, 34(1), 163-77. e7.
[http://dx.doi.org/10.1016/j.ccell.2018.06.006]
[19]
Felsberg, J.; Hentschel, B.; Kaulich, K.; Gramatzki, D.; Zacher, A.; Malzkorn, B.; Kamp, M.; Sabel, M.; Simon, M.; Westphal, M.; Schackert, G.; Tonn, J.C.; Pietsch, T.; von Deimling, A.; Loeffler, M.; Reifenberger, G.; Weller, M. German Glioma Network. Epidermal growth factor receptor variant III (EGFRvIII) positivity in EGFR-amplified glioblastomas: prognostic role and comparison between primary and recurrent tumors. Clin. Cancer Res., 2017, 23(22), 6846-6855.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-0890] [PMID: 28855349]
[20]
Faulkner, C.; Palmer, A.; Williams, H.; Wragg, C.; Haynes, H.R.; White, P.; DeSouza, R.M.; Williams, M.; Hopkins, K.; Kurian, K.M. EGFR and EGFRvIII analysis in glioblastoma as therapeutic biomarkers. Br. J. Neurosurg., 2015, 29(1), 23-29.
[http://dx.doi.org/10.3109/02688697.2014.950631] [PMID: 25141189]
[21]
Park, S.Y.; Piao, Y.; Martinez-Ledesma, E.; Dong, J.; Khan, S.; Mittal, S. Targeting MEK in EGFR amplified glioma stem like cells induces differentiation; AACR, 2019.
[22]
Padfield, E.; Ellis, H.P.; Kurian, K.M. Current therapeutic advances targeting EGFR and EGFRvIII in glioblastoma. Front. Oncol., 2015, 5, 5.
[http://dx.doi.org/10.3389/fonc.2015.00005] [PMID: 25688333]
[23]
Reardon, D.A.; Groves, M.D.; Wen, P.Y.; Nabors, L.; Mikkelsen, T.; Rosenfeld, S.; Raizer, J.; Barriuso, J.; McLendon, R.E.; Suttle, A.B.; Ma, B.; Curtis, C.M.; Dar, M.M.; de Bono, J. A phase I/II trial of pazopanib in combination with lapatinib in adult patients with relapsed malignant glioma. Clin. Cancer Res., 2013, 19(4), 900-908.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-1707] [PMID: 23363814]
[24]
Reardon, D.A.; Nabors, L.B.; Mason, W.P.; Perry, J.R.; Shapiro, W.; Kavan, P.; Mathieu, D.; Phuphanich, S.; Cseh, A.; Fu, Y.; Cong, J.; Wind, S.; Eisenstat, D.D. BI 1200 36 Trial Group and the Canadian Brain Tumour Consortium. Phase I/randomized phase II study of afatinib, an irreversible ErbB family blocker, with or without protracted temozolomide in adults with recurrent glioblastoma. Neuro-oncol., 2015, 17(3), 430-439.
[PMID: 25140039]
[25]
Sepúlveda-Sánchez, J.M.; Vaz, M.Á.; Balañá, C.; Gil-Gil, M.; Reynés, G.; Gallego, Ó.; Martínez-García, M.; Vicente, E.; Quindós, M.; Luque, R.; Ramos, A.; Ruano, Y.; Pérez-Segura, P.; Benavides, M.; Sánchez-Gómez, P.; Hernández-Laín, A. Phase II trial of dacomitinib, a pan-human EGFR tyrosine kinase inhibitor, in recurrent glioblastoma patients with EGFR amplification. Neuro-oncol., 2017, 19(11), 1522-1531.
[http://dx.doi.org/10.1093/neuonc/nox105] [PMID: 28575464]
[26]
Sequist, L.V.; Piotrowska, Z.; Niederst, M.J.; Heist, R.S.; Digumarthy, S.; Shaw, A.T.; Engelman, J.A. Osimertinib responses after disease progression in patients who had been receiving rociletinib. JAMA Oncol., 2016, 2(4), 541-543.
[http://dx.doi.org/10.1001/jamaoncol.2015.5009] [PMID: 26720284]
[27]
Batchelor, T.T.; Gerstner, E.R.; Ye, X.; Desideri, S.; Duda, D.G.; Peereboom, D.; Lesser, G.J.; Chowdhary, S.; Wen, P.Y.; Grossman, S.; Supko, J.G. Feasibility, phase I, and phase II studies of tandutinib, an oral platelet-derived growth factor receptor-β tyrosine kinase inhibitor, in patients with recurrent glioblastoma. Neuro-oncol., 2017, 19(4), 567-575.
[PMID: 27663390]
[28]
Odia, Y.; Sul, J.; Shih, J.H.; Kreisl, T.N.; Butman, J.A.; Iwamoto, F.M.; Fine, H.A. A Phase II trial of tandutinib (MLN 518) in combination with bevacizumab for patients with recurrent glioblastoma. CNS Oncol., 2016, 5(2), 59-67.
[http://dx.doi.org/10.2217/cns-2015-0010] [PMID: 26860632]
[29]
Nghiemphu, P.L.; Ebiana, V.A.; Wen, P.; Gilbert, M.; Abrey, L.E.; Lieberman, F.; DeAngelis, L.M.; Robins, H.I.; Yung, W.K.A.; Chang, S.; Drappatz, J.; Mehta, M.P.; Levin, V.A.; Aldape, K.; Dancey, J.E.; Wright, J.J.; Prados, M.; Kuhn, J.; Cloughesy, T.F. Phase I study of sorafenib and tipifarnib for recurrent glioblastoma: NABTC 05-02. J. Neurooncol., 2018, 136(1), 79-86.
[http://dx.doi.org/10.1007/s11060-017-2624-4] [PMID: 28988377]
[30]
Pitz, M.W.; Eisenhauer, E.A.; MacNeil, M.V.; Thiessen, B.; Easaw, J.C.; Macdonald, D.R.; Eisenstat, D.D.; Kakumanu, A.S.; Salim, M.; Chalchal, H.; Squire, J.; Tsao, M.S.; Kamel-Reid, S.; Banerji, S.; Tu, D.; Powers, J.; Hausman, D.F.; Mason, W.P. Phase II study of PX-866 in recurrent glioblastoma. Neuro-oncol., 2015, 17(9), 1270-1274.
[http://dx.doi.org/10.1093/neuonc/nou365] [PMID: 25605819]
[31]
Wen, P.Y.; Touat, M.; Alexander, B.M.; Mellinghoff, I.K.; Ramkissoon, S.; McCluskey, C.S.; Pelton, K.; Haidar, S.; Basu, S.S.; Gaffey, S.C.; Brown, L.E.; Martinez-Ledesma, J.E.; Wu, S.; Kim, J.; Wei, W.; Park, M.A.; Huse, J.T.; Kuhn, J.G.; Rinne, M.L.; Colman, H.; Agar, N.Y.R.; Omuro, A.M.; DeAngelis, L.M.; Gilbert, M.R.; de Groot, J.F.; Cloughesy, T.F.; Chi, A.S.; Roberts, T.M.; Zhao, J.J.; Lee, E.Q.; Nayak, L.; Heath, J.R.; Horky, L.L.; Batchelor, T.T.; Beroukhim, R.; Chang, S.M.; Ligon, A.H.; Dunn, I.F.; Koul, D.; Young, G.S.; Prados, M.D.; Reardon, D.A.; Yung, W.K.A.; Ligon, K.L. Buparlisib in patients with recurrent glioblastoma harboring phosphatidylinositol 3-kinase pathway activation: An open-label, multicenter, multi-arm, phase II trial. J. Clin. Oncol., 2019, 37(9), 741-750.
[http://dx.doi.org/10.1200/JCO.18.01207] [PMID: 30715997]
[32]
Karimi Roshan, M.; Soltani, A.; Soleimani, A.; Rezaie Kahkhaie, K.; Afshari, A.R.; Soukhtanloo, M. Role of AKT and mTOR signaling pathways in the induction of epithelial-mesenchymal transition (EMT) process. Biochimie, 2019, 165, 229-234.
[http://dx.doi.org/10.1016/j.biochi.2019.08.003] [PMID: 31401189]
[33]
Batsios, G.; Viswanath, P.; Subramani, E.; Najac, C.; Gillespie, A.M.; Santos, R.D.; Molloy, A.R.; Pieper, R.O.; Ronen, S.M. PI3K/mTOR inhibition of IDH1 mutant glioma leads to reduced 2HG production that is associated with increased survival. Sci. Rep., 2019, 9(1), 10521.
[http://dx.doi.org/10.1038/s41598-019-47021-x] [PMID: 31324855]
[34]
Fan, Q.; Aksoy, O.; Wong, R.A.; Ilkhanizadeh, S.; Novotny, C.J.; Gustafson, W.C.; Truong, A.Y.; Cayanan, G.; Simonds, E.F.; Haas-Kogan, D.; Phillips, J.J.; Nicolaides, T.; Okaniwa, M.; Shokat, K.M.; Weiss, W.A. A kinase inhibitor targeted to mTORC1 drives regression in glioblastoma. Cancer Cell, 2017, 31(3), 424-435.
[http://dx.doi.org/10.1016/j.ccell.2017.01.014] [PMID: 28292440]
[35]
Wahl, M.; Chang, S.M.; Phillips, J.J.; Molinaro, A.M.; Costello, J.F.; Mazor, T. Probing the PI3K/mTOR Pathway in Gliomas: A Phase II Study of Everolimus for Recurrent Adult Low Grade Gliomas. Cancer, 2017, 123(23), 4631.
[http://dx.doi.org/10.1002/cncr.30909] [PMID: 28759109]
[36]
Chinnaiyan, P.; Won, M.; Wen, P.Y.; Rojiani, A.M.; Werner-Wasik, M.; Shih, H.A.; Ashby, L.S.; Michael Yu, H.H.; Stieber, V.W.; Malone, S.C.; Fiveash, J.B.; Mohile, N.A.; Ahluwalia, M.S.; Wendland, M.M.; Stella, P.J.; Kee, A.Y.; Mehta, M.P. A randomized phase II study of everolimus in combination with chemoradiation in newly diagnosed glioblastoma: results of NRG Oncology RTOG 0913. Neuro-oncol., 2018, 20(5), 666-673.
[http://dx.doi.org/10.1093/neuonc/nox209] [PMID: 29126203]
[37]
Chheda, M.G.; Wen, P.Y.; Hochberg, F.H.; Chi, A.S.; Drappatz, J.; Eichler, A.F.; Yang, D.; Beroukhim, R.; Norden, A.D.; Gerstner, E.R.; Betensky, R.A.; Batchelor, T.T. Vandetanib plus sirolimus in adults with recurrent glioblastoma: results of a phase I and dose expansion cohort study. J. Neurooncol., 2015, 121(3), 627-634.
[http://dx.doi.org/10.1007/s11060-014-1680-2] [PMID: 25503302]
[38]
Schiff, D.; Jaeckle, K.A.; Anderson, S.K.; Galanis, E.; Giannini, C.; Buckner, J.C.; Stella, P.; Flynn, P.J.; Erickson, B.J.; Schwerkoske, J.F.; Kaluza, V.; Twohy, E.; Dancey, J.; Wright, J.; Sarkaria, J.N. Phase 1/2 trial of temsirolimus and sorafenib in the treatment of patients with recurrent glioblastoma: North Central Cancer Treatment Group Study/Alliance N0572. Cancer, 2018, 124(7), 1455-1463.
[http://dx.doi.org/10.1002/cncr.31219] [PMID: 29313954]
[39]
Wick, W.; Gorlia, T.; Bady, P.; Platten, M.; van den Bent, M.J.; Taphoorn, M.J.; Steuve, J.; Brandes, A.A.; Hamou, M.F.; Wick, A.; Kosch, M.; Weller, M.; Stupp, R.; Roth, P.; Golfinopoulos, V.; Frenel, J.S.; Campone, M.; Ricard, D.; Marosi, C.; Villa, S.; Weyerbrock, A.; Hopkins, K.; Homicsko, K.; Lhermitte, B.; Pesce, G.; Hegi, M.E. Phase II study of radiotherapy and temsirolimus versus radiochemotherapy with temozolomide in patients with newly diagnosed glioblastoma without MGMT promoter hypermethylation (EORTC 26082). Clin. Cancer Res., 2016, 22(19), 4797-4806.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-3153] [PMID: 27143690]
[40]
Wen, P.Y.; Omuro, A.; Ahluwalia, M.S.; Fathallah-Shaykh, H.M.; Mohile, N.; Lager, J.J.; Laird, A.D.; Tang, J.; Jiang, J.; Egile, C.; Cloughesy, T.F. Phase I dose-escalation study of the PI3K/mTOR inhibitor voxtalisib (SAR245409, XL765) plus temozolomide with or without radiotherapy in patients with high-grade glioma. Neuro-oncol., 2015, 17(9), 1275-1283.
[http://dx.doi.org/10.1093/neuonc/nov083] [PMID: 26019185]
[41]
Wen, P.Y.; Cloughesy, T.F.; Olivero, A.; Lu, X.; Mueller, L.; Fernandez Coimbra, A. A first-in-human phase 1 study to evaluate the brain-penetrant PI3K/mTOR inhibitor GDC-0084 in patients with progressive or recurrent high-grade glioma; American Society of Clinical Oncology, 2016.
[http://dx.doi.org/10.1200/JCO.2016.34.15_suppl.2012]
[42]
Das, S.; Marsden, P.A. Angiogenesis in glioblastoma. N. Engl. J. Med., 2013, 369(16), 1561-1563.
[http://dx.doi.org/10.1056/NEJMcibr1309402] [PMID: 24131182]
[43]
Jain, R.K.; di Tomaso, E.; Duda, D.G.; Loeffler, J.S.; Sorensen, A.G.; Batchelor, T.T. Angiogenesis in brain tumours. Nat. Rev. Neurosci., 2007, 8(8), 610-622.
[http://dx.doi.org/10.1038/nrn2175] [PMID: 17643088]
[44]
Morbidelli, L.; Donnini, S.; Ziche, M. Therapeutic implications of the nitric oxide pathway in the angiogenesis of tumors and inflammatory-related disorders. Therapeutic Application of Nitric Oxide in Cancer and Inflammatory Disorders; Elsevier, 2019, pp. 65-91.
[http://dx.doi.org/10.1016/B978-0-12-816545-4.00004-9]
[45]
Keunen, O.; Johansson, M.; Oudin, A.; Sanzey, M.; Rahim, S.A.A.; Fack, F.; Thorsen, F.; Taxt, T.; Bartos, M.; Jirik, R.; Miletic, H.; Wang, J.; Stieber, D.; Stuhr, L.; Moen, I.; Rygh, C.B.; Bjerkvig, R.; Niclou, S.P. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc. Natl. Acad. Sci. USA, 2011, 108(9), 3749-3754.
[http://dx.doi.org/10.1073/pnas.1014480108] [PMID: 21321221]
[46]
Moustakas, A.; Kreisl, T.N. New treatment options in the management of glioblastoma multiforme: a focus on bevacizumab. OncoTargets Ther., 2010, 3, 27-38.
[PMID: 20616955 ]
[47]
Zhang, X.; Zhang, W.; Cao, W-D.; Cheng, G.; Zhang, Y-Q. Glioblastoma multiforme: Molecular characterization and current treatment strategy (Review). Exp. Ther. Med., 2012, 3(1), 9-14.
[http://dx.doi.org/10.3892/etm.2011.367] [PMID: 22969836]
[48]
Brown, N.; McBain, C.; Nash, S.; Hopkins, K.; Sanghera, P.; Saran, F.; Phillips, M.; Dungey, F.; Clifton-Hadley, L.; Wanek, K.; Krell, D.; Jeffries, S.; Khan, I.; Smith, P.; Mulholland, P. Multi-center randomized phase II study comparing cediranib plus gefitinib with cediranib plus placebo in subjects with recurrent/progressive glioblastoma. PLoS One, 2016, 11(5)e0156369
[http://dx.doi.org/10.1371/journal.pone.0156369] [PMID: 27232884]
[49]
Taylor, J.W.; Dietrich, J.; Gerstner, E.R.; Norden, A.D.; Rinne, M.L.; Cahill, D.P.; Stemmer-Rachamimov, A.; Wen, P.Y.; Betensky, R.A.; Giorgio, D.H.; Snodgrass, K.; Randall, A.E.; Batchelor, T.T.; Chi, A.S. Phase 2 study of bosutinib, a Src inhibitor, in adults with recurrent glioblastoma. J. Neurooncol., 2015, 121(3), 557-563.
[http://dx.doi.org/10.1007/s11060-014-1667-z] [PMID: 25411098]
[50]
Schäfer, N.; Gielen, G.H.; Kebir, S.; Wieland, A.; Till, A.; Mack, F.; Schaub, C.; Tzaridis, T.; Reinartz, R.; Niessen, M.; Fimmers, R.; Simon, M.; Coch, C.; Fuhrmann, C.; Herrlinger, U.; Scheffler, B.; Glas, M. Phase I trial of dovitinib (TKI258) in recurrent glioblastoma. J. Cancer Res. Clin. Oncol., 2016, 142(7), 1581-1589.
[http://dx.doi.org/10.1007/s00432-016-2161-0] [PMID: 27100354]
[51]
Wen, P.Y.; Drappatz, J.; de Groot, J.; Prados, M.D.; Reardon, D.A.; Schiff, D.; Chamberlain, M.; Mikkelsen, T.; Desjardins, A.; Holland, J.; Ping, J.; Weitzman, R.; Cloughesy, T.F. Phase II study of cabozantinib in patients with progressive glioblastoma: subset analysis of patients naive to antiangiogenic therapy. Neuro-oncol., 2018, 20(2), 249-258.
[http://dx.doi.org/10.1093/neuonc/nox154] [PMID: 29016998]
[52]
Wang, L.; Liang, L.; Yang, T.; Qiao, Y.; Xia, Y.; Liu, L.; Li, C.; Lu, P.; Jiang, X. A pilot clinical study of apatinib plus irinotecan in patients with recurrent high-grade glioma: Clinical Trial/Experimental Study. Medicine (Baltimore), 2017, 96(49)e9053
[http://dx.doi.org/10.1097/MD.0000000000009053] [PMID: 29245310]
[53]
Gerstner, E.R.; Ye, X.; Duda, D.G.; Levine, M.A.; Mikkelsen, T.; Kaley, T.J.; Olson, J.J.; Nabors, B.L.; Ahluwalia, M.S.; Wen, P.Y.; Jain, R.K.; Batchelor, T.T.; Grossman, S. A phase I study of cediranib in combination with cilengitide in patients with recurrent glioblastoma. Neuro-oncol., 2015, 17(10), 1386-1392.
[http://dx.doi.org/10.1093/neuonc/nov085] [PMID: 26008604]
[54]
Nabors, L.B.; Fink, K.L.; Mikkelsen, T.; Grujicic, D.; Tarnawski, R.; Nam, D.H.; Mazurkiewicz, M.; Salacz, M.; Ashby, L.; Zagonel, V.; Depenni, R.; Perry, J.R.; Hicking, C.; Picard, M.; Hegi, M.E.; Lhermitte, B.; Reardon, D.A. Two cilengitide regimens in combination with standard treatment for patients with newly diagnosed glioblastoma and unmethylated MGMT gene promoter: results of the open-label, controlled, randomized phase II CORE study. Neuro-oncol., 2015, 17(5), 708-717.
[http://dx.doi.org/10.1093/neuonc/nou356] [PMID: 25762461]
[55]
Stupp, R.; Hegi, M.E.; Gorlia, T.; Erridge, S.C.; Perry, J.; Hong, Y-K.; Aldape, K.D.; Lhermitte, B.; Pietsch, T.; Grujicic, D.; Steinbach, J.P.; Wick, W.; Tarnawski, R.; Nam, D.H.; Hau, P.; Weyerbrock, A.; Taphoorn, M.J.; Shen, C.C.; Rao, N.; Thurzo, L.; Herrlinger, U.; Gupta, T.; Kortmann, R.D.; Adamska, K.; McBain, C.; Brandes, A.A.; Tonn, J.C.; Schnell, O.; Wiegel, T.; Kim, C.Y.; Nabors, L.B.; Reardon, D.A.; van den Bent, M.J.; Hicking, C.; Markivskyy, A.; Picard, M.; Weller, M. European Organisation for Research and Treatment of Cancer (EORTC); Canadian Brain Tumor Consortium; CENTRIC study team. Cilengitide combined with standard treatment for patients with newly diagnosed glioblastoma with methylated MGMT promoter (CENTRIC EORTC 26071-22072 study): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol., 2014, 15(10), 1100-1108.
[http://dx.doi.org/10.1016/S1470-2045(14)70379-1] [PMID: 25163906]
[56]
Lee, E.Q.; Kaley, T.J.; Duda, D.G.; Schiff, D.; Lassman, A.B.; Wong, E.T.; Mikkelsen, T.; Purow, B.W.; Muzikansky, A.; Ancukiewicz, M.; Huse, J.T.; Ramkissoon, S.; Drappatz, J.; Norden, A.D.; Beroukhim, R.; Weiss, S.E.; Alexander, B.M.; McCluskey, C.S.; Gerard, M.; Smith, K.H.; Jain, R.K.; Batchelor, T.T.; Ligon, K.L.; Wen, P.Y. A multicenter, phase II, randomized, noncomparative clinical trial of radiation and temozolomide with or without vandetanib in newly diagnosed glioblastoma patients. Clin. Cancer Res., 2015, 21(16), 3610-3618.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-3220] [PMID: 25910950]
[57]
Duerinck, J.; Du Four, S.; Sander, W.; Van Binst, A-M.; Everaert, H.; Michotte, A.; Hau, P.; Neyns, B. Sunitinib malate plus lomustine for patients with temozolomide-refractory recurrent anaplastic or low-grade glioma. Anticancer Res., 2015, 35(10), 5551-5557.
[PMID: 26408725]
[58]
Friedmann-Morvinski, D.; Narasimamurthy, R.; Xia, Y.; Myskiw, C.; Soda, Y.; Verma, I.M. Targeting NF-κB in glioblastoma: A therapeutic approach. Sci. Adv., 2016, 2(1)e1501292
[http://dx.doi.org/10.1126/sciadv.1501292] [PMID: 26824076]
[59]
Cahill, K.E.; Morshed, R.A.; Yamini, B. Nuclear factor-κB in glioblastoma: insights into regulators and targeted therapy. Neuro-oncol., 2016, 18(3), 329-339.
[http://dx.doi.org/10.1093/neuonc/nov265] [PMID: 26534766]
[60]
Bonavia, R.; Inda, M.M.; Vandenberg, S.; Cheng, S.Y.; Nagane, M.; Hadwiger, P.; Tan, P.; Sah, D.W.; Cavenee, W.K.; Furnari, F.B. EGFRvIII promotes glioma angiogenesis and growth through the NF-κB, interleukin-8 pathway. Oncogene, 2012, 31(36), 4054-4066.
[http://dx.doi.org/10.1038/onc.2011.563] [PMID: 22139077]
[61]
Qian, C.; Li, P.; Yan, W.; Shi, L.; Zhang, J.; Wang, Y.; Liu, H.; You, Y. Downregulation of osteopontin enhances the sensitivity of glioma U251 cells to temozolomide and cisplatin by targeting the NF-κB/Bcl2 pathway. Mol. Med. Rep., 2015, 11(3), 1951-1955.
[http://dx.doi.org/10.3892/mmr.2014.2951] [PMID: 25405848]
[62]
Lan, F.; Yang, Y.; Han, J.; Wu, Q.; Yu, H.; Yue, X. Sulforaphane reverses chemo-resistance to temozolomide in glioblastoma cells by NF-κB-dependent pathway downregulating MGMT expression. Int. J. Oncol., 2016, 48(2), 559-568.
[http://dx.doi.org/10.3892/ijo.2015.3271] [PMID: 26648123]
[63]
Kong, X-T; Nguyen, N; Choi, Y; Zhang, G; Nguyen, H; Filka, E Actr-53. Safety And Efficacy Evaluation Of A Phase Ii Study Of Bortezomib In Combination With Temozolomide And Regional Radiation Therapy For Upfront Treatment Of Patients With Newlydiagnosed Glioblastoma Multiforme (gbm). Neuro-Oncology, 2017, 19(suppl_6), vi12-vi.
[64]
Raizer, J.J.; Chandler, J.P.; Ferrarese, R.; Grimm, S.A.; Levy, R.M.; Muro, K.; Rosenow, J.; Helenowski, I.; Rademaker, A.; Paton, M.; Bredel, M. A phase II trial evaluating the effects and intra-tumoral penetration of bortezomib in patients with recurrent malignant gliomas. J. Neurooncol., 2016, 129(1), 139-146.
[http://dx.doi.org/10.1007/s11060-016-2156-3] [PMID: 27300524]
[65]
Odia, Y.; Kreisl, T.N.; Aregawi, D.; Innis, E.K.; Fine, H.A. A phase II trial of tamoxifen and bortezomib in patients with recurrent malignant gliomas. J. Neurooncol., 2015, 125(1), 191-195.
[http://dx.doi.org/10.1007/s11060-015-1894-y] [PMID: 26285768]
[66]
Robe, P.A.; Bentires-Alj, M.; Bonif, M.; Rogister, B.; Deprez, M.; Haddada, H.; Khac, M.T.; Jolois, O.; Erkmen, K.; Merville, M.P.; Black, P.M.; Bours, V. In vitro and in vivo activity of the nuclear factor-kappaB inhibitor sulfasalazine in human glioblastomas. Clin. Cancer Res., 2004, 10(16), 5595-5603.
[http://dx.doi.org/10.1158/1078-0432.CCR-03-0392] [PMID: 15328202]
[67]
Robe, P.A.; Martin, D.H.; Nguyen-Khac, M.T.; Artesi, M.; Deprez, M.; Albert, A.; Vanbelle, S.; Califice, S.; Bredel, M.; Bours, V. Early termination of ISRCTN45828668, a phase 1/2 prospective, randomized study of sulfasalazine for the treatment of progressing malignant gliomas in adults. BMC Cancer, 2009, 9(1), 372.
[http://dx.doi.org/10.1186/1471-2407-9-372] [PMID: 19840379]
[68]
Kanzawa, T.; Kondo, Y.; Ito, H.; Kondo, S.; Germano, I. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res., 2003, 63(9), 2103-2108.
[PMID: 12727826]
[69]
Kumthekar, P.; Grimm, S.; Chandler, J.; Mehta, M.; Marymont, M.; Levy, R.; Muro, K.; Helenowski, I.; McCarthy, K.; Fountas, L.; Raizer, J. A phase II trial of arsenic trioxide and temozolomide in combination with radiation therapy for patients with malignant gliomas. J. Neurooncol., 2017, 133(3), 589-594.
[http://dx.doi.org/10.1007/s11060-017-2469-x] [PMID: 28510787]
[70]
Brandes, A.A.; Bartolotti, M.; Tosoni, A.; Franceschi, E. Nitrosoureas in the management of malignant gliomas. Curr. Neurol. Neurosci. Rep., 2016, 16(2), 13.
[http://dx.doi.org/10.1007/s11910-015-0611-8] [PMID: 26750128]
[71]
Chang, S.; Zhang, P.; Cairncross, J.G.; Gilbert, M.R.; Bahary, J-P.; Dolinskas, C.A.; Chakravarti, A.; Aldape, K.D.; Bell, E.H.; Schiff, D.; Jaeckle, K.; Brown, P.D.; Barger, G.R.; Werner-Wasik, M.; Shih, H.; Brachman, D.; Penas-Prado, M.; Robins, H.I.; Belanger, K.; Schultz, C.; Hunter, G.; Mehta, M. Phase III randomized study of radiation and temozolomide versus radiation and nitrosourea therapy for anaplastic astrocytoma: results of NRG Oncology RTOG 9813. Neuro-oncol., 2017, 19(2), 252-258.
[PMID: 27994066]
[72]
Herrlinger, U.; Tzaridis, T.; Mack, F.; Steinbach, J.P.; Schlegel, U.; Sabel, M.; Hau, P.; Kortmann, R.D.; Krex, D.; Grauer, O.; Goldbrunner, R.; Schnell, O.; Bähr, O.; Uhl, M.; Seidel, C.; Tabatabai, G.; Kowalski, T.; Ringel, F.; Schmidt-Graf, F.; Suchorska, B.; Brehmer, S.; Weyerbrock, A.; Renovanz, M.; Bullinger, L.; Galldiks, N.; Vajkoczy, P.; Misch, M.; Vatter, H.; Stuplich, M.; Schäfer, N.; Kebir, S.; Weller, J.; Schaub, C.; Stummer, W.; Tonn, J.C.; Simon, M.; Keil, V.C.; Nelles, M.; Urbach, H.; Coenen, M.; Wick, W.; Weller, M.; Fimmers, R.; Schmid, M.; Hattingen, E.; Pietsch, T.; Coch, C.; Glas, M. Neurooncology Working Group of the German Cancer Society. Lomustine-temozolomide combination therapy versus standard temozolomide therapy in patients with newly diagnosed glioblastoma with methylated MGMT promoter (CeTeG/NOA-09): a randomised, open-label, phase 3 trial. Lancet, 2019, 393(10172), 678-688.
[http://dx.doi.org/10.1016/S0140-6736(18)31791-4] [PMID: 30782343]
[73]
Mack, F.; Schäfer, N.; Kebir, S.; Stuplich, M.; Schaub, C.; Niessen, M.; Scheffler, B.; Herrlinger, U.; Glas, M. Carmustine (BCNU) plus Teniposide (VM26) in recurrent malignant glioma. Oncology, 2014, 86(5-6), 369-372.
[http://dx.doi.org/10.1159/000360295] [PMID: 24942787]
[74]
Brandes, A.A.; Finocchiaro, G.; Zagonel, V.; Reni, M.; Caserta, C.; Fabi, A.; Clavarezza, M.; Maiello, E.; Eoli, M.; Lombardi, G.; Monteforte, M.; Proietti, E.; Agati, R.; Eusebi, V.; Franceschi, E. AVAREG: a phase II, randomized, noncomparative study of fotemustine or bevacizumab for patients with recurrent glioblastoma. Neuro-oncol., 2016, 18(9), 1304-1312.
[http://dx.doi.org/10.1093/neuonc/now035] [PMID: 26951379]
[75]
Wick, W.; Gorlia, T.; Bendszus, M.; Taphoorn, M.; Sahm, F.; Harting, I.; Brandes, A.A.; Taal, W.; Domont, J.; Idbaih, A.; Campone, M.; Clement, P.M.; Stupp, R.; Fabbro, M.; Le Rhun, E.; Dubois, F.; Weller, M.; von Deimling, A.; Golfinopoulos, V.; Bromberg, J.C.; Platten, M.; Klein, M.; van den Bent, M.J. Lomustine and bevacizumab in progressive glioblastoma. N. Engl. J. Med., 2017, 377(20), 1954-1963.
[http://dx.doi.org/10.1056/NEJMoa1707358] [PMID: 29141164]
[76]
Aoki, T; Arakawa, Y; Ueba, T; Oda, M; Nishida, N; Akiyama, Y Phase I/II study of temozolomide plus nimustine chemotherapy for recurrent malignant gliomas: Kyoto Neuro-oncology Group. Neurologia medico-chirurgica., 2016, oa. 2016-0162.
[77]
Chamberlain, M.C.; Colman, H.; Kim, B.T.; Raizer, J. Salvage therapy with bendamustine for temozolomide refractory recurrent anaplastic gliomas: a prospective phase II trial. J. Neurooncol., 2017, 131(3), 507-516.
[http://dx.doi.org/10.1007/s11060-016-2241-7] [PMID: 28204914]
[78]
Duerinck, J.; Du Four, S.; Bouttens, F.; Andre, C.; Verschaeve, V.; Van Fraeyenhove, F.; Chaskis, C.; D’Haene, N.; Le Mercier, M.; Rogiers, A.; Michotte, A.; Salmon, I.; Neyns, B. Randomized phase II trial comparing axitinib with the combination of axitinib and lomustine in patients with recurrent glioblastoma. J. Neurooncol., 2018, 136(1), 115-125.
[http://dx.doi.org/10.1007/s11060-017-2629-z] [PMID: 28988341]
[79]
Weller, M.; Roth, P.; Preusser, M.; Wick, W.; Reardon, D.A.; Platten, M.; Sampson, J.H. Vaccine-based immunotherapeutic approaches to gliomas and beyond. Nat. Rev. Neurol., 2017, 13(6), 363-374.
[http://dx.doi.org/10.1038/nrneurol.2017.64] [PMID: 28497804]
[80]
Lim, M.; Xia, Y.; Bettegowda, C.; Weller, M. Current state of immunotherapy for glioblastoma. Nat. Rev. Clin. Oncol., 2018, 15(7), 422-442.
[http://dx.doi.org/10.1038/s41571-018-0003-5] [PMID: 29643471]
[81]
Zheng, Y.; Ma, Y.; Yue, H.; Liu, G.; Han, S. EGFRvIII epigenetically regulates ARHI to promote glioma cell proliferation and migration. Exp. Mol. Pathol., 2020.112104344
[http://dx.doi.org/10.1016/j.yexmp.2019.104344] [PMID: 31751560]
[82]
Westphal, M.; Heese, O.; Steinbach, J.P.; Schnell, O.; Schackert, G.; Mehdorn, M.; Schulz, D.; Simon, M.; Schlegel, U.; Senft, C.; Geletneky, K.; Braun, C.; Hartung, J.G.; Reuter, D.; Metz, M.W.; Bach, F.; Pietsch, T. A randomised, open label phase III trial with nimotuzumab, an anti-epidermal growth factor receptor monoclonal antibody in the treatment of newly diagnosed adult glioblastoma. Eur. J. Cancer, 2015, 51(4), 522-532.
[http://dx.doi.org/10.1016/j.ejca.2014.12.019] [PMID: 25616647]
[83]
Desjardins, A.; Randazzo, D.; Peters, K.B.; Johnson, M.O.; Massey, W.; Herndon, J.E. Actr-64. Phase 2 Study Of Sym004 For Adult Patients With Recurrent Glioblastoma (gbm). Neuro-oncol., 2017, 19(Suppl. 6), vi14.
[http://dx.doi.org/10.1093/neuonc/nox168.052]
[84]
Reardon, D.A.; Lassman, A.B.; van den Bent, M.; Kumthekar, P.; Merrell, R.; Scott, A.M.; Fichtel, L.; Sulman, E.P.; Gomez, E.; Fischer, J.; Lee, H.J.; Munasinghe, W.; Xiong, H.; Mandich, H.; Roberts-Rapp, L.; Ansell, P.; Holen, K.D.; Gan, H.K. Efficacy and safety results of ABT-414 in combination with radiation and temozolomide in newly diagnosed glioblastoma. Neuro-oncol., 2017, 19(7), 965-975.
[PMID: 28039367]
[85]
Wang, Y.; Pan, L. Sheng Xf, Chen S, Dai Jz. Nimotuzumab, a humanized monoclonal antibody specific for the EGFR, in combination with temozolomide and radiation therapy for newly diagnosed glioblastoma multiforme: First results in C hinese patients. Asia Pac. J. Clin. Oncol., 2016, 12(1), e23-e9.
[http://dx.doi.org/10.1111/ajco.12166] [PMID: 24571331]
[86]
Yu, A.; Faiq, N.; Green, S.; Lai, A.; Green, R.; Hu, J.; Cloughesy, T.F.; Mellinghoff, I.; Nghiemphu, P.L. Report of safety of pulse dosing of lapatinib with temozolomide and radiation therapy for newly-diagnosed glioblastoma in a pilot phase II study. J. Neurooncol., 2017, 134(2), 357-362.
[http://dx.doi.org/10.1007/s11060-017-2533-6] [PMID: 28669012]
[87]
Blaes, J.; Thomé, C.M.; Pfenning, P-N.; Rübmann, P.; Sahm, F.; Wick, A.; Bunse, T.; Schmenger, T.; Sykora, J.; von Deimling, A.; Wiestler, B.; Merz, C.; Jugold, M.; Haberkorn, U.; Abdollahi, A.; Debus, J.; Gieffers, C.; Kunz, C.; Bendszus, M.; Kluge, M.; Platten, M.; Fricke, H.; Wick, W.; Lemke, D. Inhibition of CD95/CD95L (FAS/FASLG) signaling with APG101 prevents invasion and enhances radiation therapy for glioblastoma. Mol. Cancer Res., 2018, 16(5), 767-776.
[http://dx.doi.org/10.1158/1541-7786.MCR-17-0563] [PMID: 29453321]
[88]
Wick, W.; Fricke, H.; Junge, K.; Kobyakov, G.; Martens, T.; Heese, O.; Wiestler, B.; Schliesser, M.G.; von Deimling, A.; Pichler, J.; Vetlova, E.; Harting, I.; Debus, J.; Hartmann, C.; Kunz, C.; Platten, M.; Bendszus, M.; Combs, S.E. A phase II, randomized, study of weekly APG101+reirradiation versus reirradiation in progressive glioblastoma. Clin. Cancer Res., 2014, 20(24), 6304-6313.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-0951-T] [PMID: 25338498]
[89]
Ahn, B.J.; Pollack, I.F.; Okada, H. Immune-checkpoint blockade and active immunotherapy for glioma. Cancers (Basel), 2013, 5(4), 1379-1412.
[http://dx.doi.org/10.3390/cancers5041379] [PMID: 24202450]
[90]
Yeo, A.T.; Charest, A. Immune checkpoint blockade biology in mouse models of glioblastoma. J. Cell. Biochem., 2017, 118(9), 2516-2527.
[http://dx.doi.org/10.1002/jcb.25948] [PMID: 28230277]
[91]
Caccese, M.; Indraccolo, S.; Zagonel, V.; Lombardi, G. PD-1/PD-L1 immune-checkpoint inhibitors in glioblastoma: A concise review. Crit. Rev. Oncol. Hematol., 2019, 135, 128-134.
[http://dx.doi.org/10.1016/j.critrevonc.2018.12.002] [PMID: 30819441]
[92]
Zhang, X.; Zhu, S.; Li, T.; Liu, Y-J.; Chen, W.; Chen, J. Targeting immune checkpoints in malignant glioma. Oncotarget, 2017, 8(4), 7157-7174.
[http://dx.doi.org/10.18632/oncotarget.12702] [PMID: 27756892]
[93]
Tan, A.C.; Heimberger, A.B.; Khasraw, M. Immune checkpoint inhibitors in gliomas. Curr. Oncol. Rep., 2017, 19(4), 23.
[http://dx.doi.org/10.1007/s11912-017-0586-5] [PMID: 28303490]
[94]
Lakin, N.; Rulach, R.; Nowicki, S.; Kurian, K.M. Current advances in checkpoint inhibitors: lessons from non-central nervous system cancers and potential for glioblastoma. Front. Oncol., 2017, 7, 141.
[http://dx.doi.org/10.3389/fonc.2017.00141] [PMID: 28730140]
[95]
Zeng, J; See, AP; Phallen, J; Jackson, CM; Belcaid, Z; Ruzevick, J Anti-PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas. International Journal of Radiation Oncology* Biology* Physics., 2013, 86(2), 343-9.
[http://dx.doi.org/10.1016/j.ijrobp.2012.12.025]
[96]
Nduom, E.K.; Wei, J.; Yaghi, N.K.; Huang, N.; Kong, L-Y.; Gabrusiewicz, K.; Ling, X.; Zhou, S.; Ivan, C.; Chen, J.Q.; Burks, J.K.; Fuller, G.N.; Calin, G.A.; Conrad, C.A.; Creasy, C.; Ritthipichai, K.; Radvanyi, L.; Heimberger, A.B. PD-L1 expression and prognostic impact in glioblastoma. Neuro-oncol., 2016, 18(2), 195-205.
[http://dx.doi.org/10.1093/neuonc/nov172] [PMID: 26323609]
[97]
Lowther, D.E.; Goods, B.A.; Lucca, L.E.; Lerner, B.A.; Raddassi, K.; van Dijk, D.; Hernandez, A.L.; Duan, X.; Gunel, M.; Coric, V.; Krishnaswamy, S.; Love, J.C.; Hafler, D.A. PD-1 marks dysfunctional regulatory T cells in malignant gliomas. JCI Insight, 2016, 1(5)e85935
[http://dx.doi.org/10.1172/jci.insight.85935] [PMID: 27182555]
[98]
Omuro, A.; Vlahovic, G.; Lim, M.; Sahebjam, S.; Baehring, J.; Cloughesy, T.; Voloschin, A.; Ramkissoon, S.H.; Ligon, K.L.; Latek, R.; Zwirtes, R.; Strauss, L.; Paliwal, P.; Harbison, C.T.; Reardon, D.A.; Sampson, J.H. Nivolumab with or without ipilimumab in patients with recurrent glioblastoma: results from exploratory phase I cohorts of CheckMate 143. Neuro-oncol., 2018, 20(5), 674-686.
[http://dx.doi.org/10.1093/neuonc/nox208] [PMID: 29106665]
[99]
Reardon, D; Omuro, A; Brandes, A; Rieger, J; Wick, A; Sepulveda, J OS10. 3 randomized phase 3 study evaluating the efficacy and safety of nivolumab vs. bevacizumab in patients with recurrent glioblastoma: CheckMate 143. Neuro-oncology, 2017, 19(suppl_3), iii21-iii.
[100]
Reardon, D.A.; Kaley, T.J.; Dietrich, J.; Lim, M.; Dunn, G.P.; Gan, H.K. Phase 2 study to evaluate the clinical efficacy and safety of MEDI4736 (durvalumab) in patients with glioblastoma (GBM); American Society of Clinical Oncology, 2016.
[http://dx.doi.org/10.1200/JCO.2016.34.15_suppl.TPS2080]
[101]
Sahebjam, S. Forsyth, P; Arrington, J; Jaglal, M; Tran, ND; Etame, AB ATIM-18. A phase I trial of hypofractionated stereotactic irradiation (HFSRT) with pembrolizumab and bevacizumab in patients with recurrent high grade glioma (NCT02313272). Neurooncology., 2017, 19(suppl_6), pp. vi30-vi.
[102]
Wheeler, C.J.; Das, A.; Liu, G.; Yu, J.S.; Black, K.L. Clinical responsiveness of glioblastoma multiforme to chemotherapy after vaccination. Clin. Cancer Res., 2004, 10(16), 5316-5326.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-0497] [PMID: 15328167]
[103]
Liau, L.M.; Prins, R.M.; Kiertscher, S.M.; Odesa, S.K.; Kremen, T.J.; Giovannone, A.J.; Lin, J.W.; Chute, D.J.; Mischel, P.S.; Cloughesy, T.F.; Roth, M.D. Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin. Cancer Res., 2005, 11(15), 5515-5525.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-0464] [PMID: 16061868]
[104]
Huang, X.; Ginwala, R.; Karabudak, A.; Jain, P.; Philip, R. Targeted multi-epitope therapeutic vaccine for the treatment of invasive glioblastoma multiforme. J. Immunother. Cancer, 2015, 3(S2), 436.
[http://dx.doi.org/10.1186/2051-1426-3-S2-P436]
[105]
Srinivasan, V.M.; Ferguson, S.D.; Lee, S.; Weathers, S-P.; Kerrigan, B.C.P.; Heimberger, A.B. Tumor vaccines for malignant gliomas. Neurotherapeutics, 2017, 14(2), 345-357.
[http://dx.doi.org/10.1007/s13311-017-0522-2] [PMID: 28389997]
[106]
Schuster, J.; Lai, R.K.; Recht, L.D.; Reardon, D.A.; Paleologos, N.A.; Groves, M.D.; Mrugala, M.M.; Jensen, R.; Baehring, J.M.; Sloan, A.; Archer, G.E.; Bigner, D.D.; Cruickshank, S.; Green, J.A.; Keler, T.; Davis, T.A.; Heimberger, A.B.; Sampson, J.H. A phase II, multicenter trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma: the ACT III study. Neuro-oncol., 2015, 17(6), 854-861.
[http://dx.doi.org/10.1093/neuonc/nou348] [PMID: 25586468]
[107]
Reardon, D.A.; Desjardins, A.; Vredenburgh, J.J.; O’Rourke, D.M.; Tran, D.D.; Fink, K.L.; Nabors, L.B.; Li, G.; Bota, D.A.; Lukas, R.V.; Ashby, L.S.; Duic, J.P.; Mrugala, M.M.; Cruickshank, S.; Vitale, L.; He, Y.; Green, J.A.; Yellin, M.J.; Turner, C.D.; Keler, T.; Davis, T.A.; Sampson, J.H. ReACT trial investigators. Rindopepimut with Bevacizumab for Patients with Relapsed EGFRvIII-Expressing Glioblastoma (ReACT): Results of a Double-Blind Randomized Phase II Trial. Clin. Cancer Res., 2020, 26(7), 1586-1594.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-1140] [PMID: 32034072]
[108]
Elsamadicy, A.A.; Chongsathidkiet, P.; Desai, R.; Woroniecka, K.; Farber, S.H.; Fecci, P.E.; Sampson, J.H. Prospect of rindopepimut in the treatment of glioblastoma. Expert Opin. Biol. Ther., 2017, 17(4), 507-513.
[http://dx.doi.org/10.1080/14712598.2017.1299705] [PMID: 28274144]
[109]
Fenstermaker, R.A.; Ciesielski, M.J.; Qiu, J.; Yang, N.; Frank, C.L.; Lee, K.P.; Mechtler, L.R.; Belal, A.; Ahluwalia, M.S.; Hutson, A.D. Clinical study of a survivin long peptide vaccine (SurVaxM) in patients with recurrent malignant glioma. Cancer Immunol. Immunother., 2016, 65(11), 1339-1352.
[http://dx.doi.org/10.1007/s00262-016-1890-x] [PMID: 27576783]
[110]
Ahluwalia, M.S.; Reardon, D.A.; Abad, A.P.; Curry, W.T.; Wong, E.T.; Belal, A. SurVaxM with standard therapy in newly diagnosed glioblastoma: Phase II trial update; American Society of Clinical Oncology, 2019.
[111]
Reardon, D; Nabors, B; Kumthekar, P; Badruddoja, M; Fink, K; Lieberman, F Atim-10. 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. Neuro-Oncology, 2017, 19(suppl_6), vi28-vi.
[112]
Peereboom, D; Nabors, L; Kumthekar, P; Badruddoja, M; Fink, K; Lieberman, F 373O Results of phase II trial of SL-701, a novel immunotherapy targeting IL-13Ra2, EphA2, and survivin, in adults with second-line recurrent glioblastoma (GBM). Annals of Oncology., 2018, 29(suppl_8), mdy273-361.
[113]
Peereboom, D.M.; Nabors, L.B.; Kumthekar, P.; Badruddoja, M.A.; Fink, K.L.; Lieberman, F.S. Phase 2 trial of SL-701 in relapsed/refractory (r/r) glioblastoma (GBM): Correlation of immune response with longer-term survival; American Society of Clinical Oncology, 2018.
[114]
Wick, W.; Dietrich, P-Y.; Kuttruff, S.; Hilf, N.; Frenzel, K.; Admon, A. GAPVAC-101: First-in-human trial of a highly personalized peptide vaccination approach for patients with newly diagnosed glioblastoma; American Society of Clinical Oncology, 2018.
[115]
Rampling, R.; Peoples, S.; Mulholland, P.J.; James, A.; Al-Salihi, O.; Twelves, C.J.; McBain, C.; Jefferies, S.; Jackson, A.; Stewart, W.; Lindner, J.; Kutscher, S.; Hilf, N.; McGuigan, L.; Peters, J.; Hill, K.; Schoor, O.; Singh-Jasuja, H.; Halford, S.E.; Ritchie, J.W. A cancer research UK first time in human phase I trial of IMA950 (novel multipeptide therapeutic vaccine) in patients with newly diagnosed glioblastoma. Clin. Cancer Res., 2016, 22(19), 4776-4785.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-0506] [PMID: 27225692]
[116]
Vandenberk, L.; Garg, A.D.; Verschuere, T.; Koks, C.; Belmans, J.; Beullens, M.; Agostinis, P.; De Vleeschouwer, S.; Van Gool, S.W. Irradiation of necrotic cancer cells, employed for pulsing dendritic cells (DCs), potentiates DC vaccine-induced antitumor immunity against high-grade glioma. OncoImmunology, 2015, 5(2)e1083669
[http://dx.doi.org/10.1080/2162402X.2015.1083669] [PMID: 27057467]
[117]
Ludewig, P.; Gallizioli, M.; Urra, X.; Behr, S.; Brait, V.H.; Gelderblom, M. Dendritic cells in brain diseases. Biochimica et Biophysica Acta (BBA)-. Molecular Basis of Disease., 2016, 1862(3), 352-367.
[http://dx.doi.org/10.1016/j.bbadis.2015.11.003]
[118]
Wen, P.Y.; Reardon, D.A.; Armstrong, T.S.; Phuphanich, S.; Aiken, R.D.; Landolfi, J.C.; Curry, W.T.; Zhu, J.J.; Glantz, M.; Peereboom, D.M.; Markert, J.M.; LaRocca, R.; O’Rourke, D.M.; Fink, K.; Kim, L.; Gruber, M.; Lesser, G.J.; Pan, E.; Kesari, S.; Muzikansky, A.; Pinilla, C.; Santos, R.G.; Yu, J.S. A Randomized Double-Blind Placebo-Controlled Phase II Trial of Dendritic Cell Vaccine ICT-107 in Newly Diagnosed Patients with Glioblastoma. Clin. Cancer Res., 2019, 25(19), 5799-5807.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-0261] [PMID: 31320597]
[119]
Inogés, S.; Tejada, S.; de Cerio, A.L-D.; Gállego Pérez-Larraya, J.; Espinós, J.; Idoate, M.A.; Domínguez, P.D.; de Eulate, R.G.; Aristu, J.; Bendandi, M.; Pastor, F.; Alonso, M.; Andreu, E.; Cardoso, F.P.; Valle, R.D. A phase II trial of autologous dendritic cell vaccination and radiochemotherapy following fluorescence-guided surgery in newly diagnosed glioblastoma patients. J. Transl. Med., 2017, 15(1), 104.
[http://dx.doi.org/10.1186/s12967-017-1202-z] [PMID: 28499389]
[120]
Buchroithner, J.; Erhart, F.; Pichler, J.; Widhalm, G.; Preusser, M.; Stockhammer, G.; Nowosielski, M.; Iglseder, S.; Freyschlag, C.F.; Oberndorfer, S.; Bordihn, K.; von Campe, G.; Hoffermann, M.; Ruckser, R.; Rössler, K.; Spiegl-Kreinecker, S.; Fischer, M.B.; Czech, T.; Visus, C.; Krumpl, G.; Felzmann, T.; Marosi, C. Audencel Immunotherapy Based on Dendritic Cells Has No Effect on Overall and Progression-Free Survival in Newly Diagnosed Glioblastoma: A Phase II Randomized Trial. Cancers (Basel), 2018, 10(10), 372.
[http://dx.doi.org/10.3390/cancers10100372] [PMID: 30301187]
[121]
Keskin, D.B.; Anandappa, A.J.; Sun, J.; Tirosh, I.; Mathewson, N.D.; Li, S.; Oliveira, G.; Giobbie-Hurder, A.; Felt, K.; Gjini, E.; Shukla, S.A.; Hu, Z.; Li, L.; Le, P.M.; Allesøe, R.L.; Richman, A.R.; Kowalczyk, M.S.; Abdelrahman, S.; Geduldig, J.E.; Charbonneau, S.; Pelton, K.; Iorgulescu, J.B.; Elagina, L.; Zhang, W.; Olive, O.; McCluskey, C.; Olsen, L.R.; Stevens, J.; Lane, W.J.; Salazar, A.M.; Daley, H.; Wen, P.Y.; Chiocca, E.A.; Harden, M.; Lennon, N.J.; Gabriel, S.; Getz, G.; Lander, E.S.; Regev, A.; Ritz, J.; Neuberg, D.; Rodig, S.J.; Ligon, K.L.; Suvà, M.L.; Wucherpfennig, K.W.; Hacohen, N.; Fritsch, E.F.; Livak, K.J.; Ott, P.A.; Wu, C.J.; Reardon, D.A. Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial. Nature, 2019, 565(7738), 234-239.
[http://dx.doi.org/10.1038/s41586-018-0792-9] [PMID: 30568305]
[122]
Liau, L.M.; Ashkan, K.; Tran, D.D.; Campian, J.L.; Trusheim, J.E.; Cobbs, C.S.; Heth, J.A.; Salacz, M.; Taylor, S.; D’Andre, S.D.; Iwamoto, F.M.; Dropcho, E.J.; Moshel, Y.A.; Walter, K.A.; Pillainayagam, C.P.; Aiken, R.; Chaudhary, R.; Goldlust, S.A.; Bota, D.A.; Duic, P.; Grewal, J.; Elinzano, H.; Toms, S.A.; Lillehei, K.O.; Mikkelsen, T.; Walbert, T.; Abram, S.R.; Brenner, A.J.; Brem, S.; Ewend, M.G.; Khagi, S.; Portnow, J.; Kim, L.J.; Loudon, W.G.; Thompson, R.C.; Avigan, D.E.; Fink, K.L.; Geoffroy, F.J.; Lindhorst, S.; Lutzky, J.; Sloan, A.E.; Schackert, G.; Krex, D.; Meisel, H.J.; Wu, J.; Davis, R.P.; Duma, C.; Etame, A.B.; Mathieu, D.; Kesari, S.; Piccioni, D.; Westphal, M.; Baskin, D.S.; New, P.Z.; Lacroix, M.; May, S.A.; Pluard, T.J.; Tse, V.; Green, R.M.; Villano, J.L.; Pearlman, M.; Petrecca, K.; Schulder, M.; Taylor, L.P.; Maida, A.E.; Prins, R.M.; Cloughesy, T.F.; Mulholland, P.; Bosch, M.L. First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma. J. Transl. Med., 2018, 16(1), 142.
[http://dx.doi.org/10.1186/s12967-018-1507-6] [PMID: 29843811]
[123]
Bloch, O.; Lim, M.; Sughrue, M.E.; Komotar, R.J.; Abrahams, J.M.; O’Rourke, D.M.; D’Ambrosio, A.; Bruce, J.N.; Parsa, A.T. Autologous heat shock protein peptide vaccination for newly diagnosed glioblastoma: impact of peripheral PD-L1 expression on response to therapy. Clin. Cancer Res., 2017, 23(14), 3575-3584.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-1369] [PMID: 28193626]
[124]
Ji, N.; Zhang, Y.; Liu, Y.; Xie, J.; Wang, Y.; Hao, S.; Gao, Z. Heat shock protein peptide complex-96 vaccination for newly diagnosed glioblastoma: a phase I, single-arm trial. JCI Insight, 2018, 3(10), 99145.
[http://dx.doi.org/10.1172/jci.insight.99145] [PMID: 29769450]
[125]
Bloch, O.; Crane, C.A.; Fuks, Y.; Kaur, R.; Aghi, M.K.; Berger, M.S.; Butowski, N.A.; Chang, S.M.; Clarke, J.L.; McDermott, M.W.; Prados, M.D.; Sloan, A.E.; Bruce, J.N.; Parsa, A.T. Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma: a phase II, single-arm trial. Neuro-oncol., 2014, 16(2), 274-279.
[http://dx.doi.org/10.1093/neuonc/not203] [PMID: 24335700]
[126]
Pellegatta, S.; Eoli, M.; Cuccarini, V.; Anghileri, E.; Pollo, B.; Pessina, S.; Frigerio, S.; Servida, M.; Cuppini, L.; Antozzi, C.; Cuzzubbo, S.; Corbetta, C.; Paterra, R.; Acerbi, F.; Ferroli, P.; DiMeco, F.; Fariselli, L.; Parati, E.A.; Bruzzone, M.G.; Finocchiaro, G. Survival gain in glioblastoma patients treated with dendritic cell immunotherapy is associated with increased NK but not CD8+ T cell activation in the presence of adjuvant temozolomide. OncoImmunology, 2018, 7(4)e1412901
[http://dx.doi.org/10.1080/2162402X.2017.1412901] [PMID: 29632727]
[127]
Maus, M.V.; June, C.H. Making better chimeric antigen receptors for adoptive T-cell therapy; AACR, 2016.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-1433]
[128]
Plautz, G.E.; Miller, D.W.; Barnett, G.H.; Stevens, G.H.; Maffett, S.; Kim, J.; Cohen, P.A.; Shu, S. T cell adoptive immunotherapy of newly diagnosed gliomas. Clin. Cancer Res., 2000, 6(6), 2209-2218.
[PMID: 10873070]
[129]
Kong, D-S.; Nam, D-H.; Kang, S-H.; Lee, J.W.; Chang, J-H.; Kim, J-H.; Lim, Y.J.; Koh, Y.C.; Chung, Y.G.; Kim, J.M.; Kim, C.H. Phase III randomized trial of autologous cytokine-induced killer cell immunotherapy for newly diagnosed glioblastoma in Korea. Oncotarget, 2017, 8(4), 7003-7013.
[http://dx.doi.org/10.18632/oncotarget.12273] [PMID: 27690294]
[130]
Brown, C.E.; Alizadeh, D.; Starr, R.; Weng, L.; Wagner, J.R.; Naranjo, A.; Ostberg, J.R.; Blanchard, M.S.; Kilpatrick, J.; Simpson, J.; Kurien, A.; Priceman, S.J.; Wang, X.; Harshbarger, T.L.; D’Apuzzo, M.; Ressler, J.A.; Jensen, M.C.; Barish, M.E.; Chen, M.; Portnow, J.; Forman, S.J.; Badie, B. Regression of glioblastoma after chimeric antigen receptor T-cell therapy. N. Engl. J. Med., 2016, 375(26), 2561-2569.
[http://dx.doi.org/10.1056/NEJMoa1610497] [PMID: 28029927]
[131]
Johnson, LA; Scholler, J; Ohkuri, T; Kosaka, A; Patel, PR; McGettigan, SE Rational development and characterization of humanized anti-EGFR variant III chimeric antigen receptor T cells for glioblastoma. Science translational medicine., 2015, 7(275), 275ra22-ra22.
[http://dx.doi.org/10.1126/scitranslmed.aaa4963]
[132]
Choi, B.D.; Suryadevara, C.M.; Gedeon, P.C.; Herndon, J.E., II; Sanchez-Perez, L.; Bigner, D.D.; Sampson, J.H. Intracerebral delivery of a third generation EGFRvIII-specific chimeric antigen receptor is efficacious against human glioma. J. Clin. Neurosci., 2014, 21(1), 189-190.
[http://dx.doi.org/10.1016/j.jocn.2013.03.012] [PMID: 24054399]
[133]
Brown, C.E.; Badie, B.; Barish, M.E.; Weng, L.; Ostberg, J.R.; Chang, W-C.; Naranjo, A.; Starr, R.; Wagner, J.; Wright, C.; Zhai, Y.; Bading, J.R.; Ressler, J.A.; Portnow, J.; D’Apuzzo, M.; Forman, S.J.; Jensen, M.C. Bioactivity and safety of IL13Rα2-redirected chimeric antigen receptor CD8+ T cells in patients with recurrent glioblastoma. Clin. Cancer Res., 2015, 21(18), 4062-4072.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0428] [PMID: 26059190]
[134]
Kong, S.; Sengupta, S.; Tyler, B.; Bais, A.J.; Ma, Q.; Doucette, S.; Zhou, J.; Sahin, A.; Carter, B.S.; Brem, H.; Junghans, R.P.; Sampath, P. Suppression of human glioma xenografts with second-generation IL13R-specific chimeric antigen receptor-modified T cells. Clin. Cancer Res., 2012, 18(21), 5949-5960.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-0319] [PMID: 22966020]
[135]
O’Rourke, D.M.; Nasrallah, M.P.; Desai, A.; Melenhorst, J.J.; Mansfield, K.; Morrissette, J.J.D.; Martinez-Lage, M.; Brem, S.; Maloney, E.; Shen, A.; Isaacs, R.; Mohan, S.; Plesa, G.; Lacey, S.F.; Navenot, J.M.; Zheng, Z.; Levine, B.L.; Okada, H.; June, C.H.; Brogdon, J.L.; Maus, M.V. A single dose of peripherally infused EGFRvIII-directed CAR T cells mediates antigen loss and induces adaptive resistance in patients with recurrent glioblastoma. Sci. Transl. Med., 2017, 9(399)eaaa0984
[http://dx.doi.org/10.1126/scitranslmed.aaa0984] [PMID: 28724573]
[136]
Ahmed, N.; Brawley, V.; Hegde, M.; Bielamowicz, K.; Kalra, M.; Landi, D.; Robertson, C.; Gray, T.L.; Diouf, O.; Wakefield, A.; Ghazi, A.; Gerken, C.; Yi, Z.; Ashoori, A.; Wu, M.F.; Liu, H.; Rooney, C.; Dotti, G.; Gee, A.; Su, J.; Kew, Y.; Baskin, D.; Zhang, Y.J.; New, P.; Grilley, B.; Stojakovic, M.; Hicks, J.; Powell, S.Z.; Brenner, M.K.; Heslop, H.E.; Grossman, R.; Wels, W.S.; Gottschalk, S. Her2-specific chimeric antigen receptor-modified virus-specific t cells for progressive glioblastoma: a phase 1 dose-escalation trial. JAMA Oncol., 2017, 3(8), 1094-1101.
[http://dx.doi.org/10.1001/jamaoncol.2017.0184] [PMID: 28426845]
[137]
Ahmed, N.; Brawley, V.; Hegde, M.; Bielamowicz, K.; Wakefield, A.; Ghazi, A. Autologous HER2 CMV bispecific CAR T cells are safe and demonstrate clinical benefit for glioblastoma in a Phase I trial. J. Immunother. Cancer, 2015, 3(S2), O11.
[http://dx.doi.org/10.1186/2051-1426-3-S2-O11]
[138]
Russell, S.J.; Peng, K-W.; Bell, J.C. Oncolytic virotherapy. Nat. Biotechnol., 2012, 30(7), 658-670.
[http://dx.doi.org/10.1038/nbt.2287] [PMID: 22781695]
[139]
Wollmann, G.; Ozduman, K.; van den Pol, A.N. Oncolytic virus therapy for glioblastoma multiforme: concepts and candidates. Cancer J., 2012, 18(1), 69-81.
[http://dx.doi.org/10.1097/PPO.0b013e31824671c9] [PMID: 22290260]
[140]
Liu, T-C.; Galanis, E.; Kirn, D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat. Clin. Pract. Oncol., 2007, 4(2), 101-117.
[http://dx.doi.org/10.1038/ncponc0736] [PMID: 17259931]
[141]
Cloughesy, T.F.; Landolfi, J.; Vogelbaum, M.A.; Ostertag, D.; Elder, J.B.; Bloomfield, S.; Carter, B.; Chen, C.C.; Kalkanis, S.N.; Kesari, S.; Lai, A.; Lee, I.Y.; Liau, L.M.; Mikkelsen, T.; Nghiemphu, P.; Piccioni, D.; Accomando, W.; Diago, O.R.; Hogan, D.J.; Gammon, D.; Kasahara, N.; Kheoh, T.; Jolly, D.J.; Gruber, H.E.; Das, A.; Walbert, T. Durable complete responses in some recurrent high-grade glioma patients treated with Toca 511 + Toca FC. Neuro-oncol., 2018, 20(10), 1383-1392.
[http://dx.doi.org/10.1093/neuonc/noy075] [PMID: 29762717]
[142]
Batich, K.A.; Reap, E.A.; Archer, G.E.; Sanchez-Perez, L.; Nair, S.K.; Schmittling, R.J.; Norberg, P.; Xie, W.; Herndon, J.E., II; Healy, P.; McLendon, R.E.; Friedman, A.H.; Friedman, H.S.; Bigner, D.; Vlahovic, G.; Mitchell, D.A.; Sampson, J.H. Long-term survival in glioblastoma with cytomegalovirus pp65-targeted vaccination. Clin. Cancer Res., 2017, 23(8), 1898-1909.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-2057] [PMID: 28411277]
[143]
Reap, E.A.; Suryadevara, C.M.; Batich, K.A.; Sanchez-Perez, L.; Archer, G.E.; Schmittling, R.J.; Norberg, P.K.; Herndon, J.E., II; Healy, P.; Congdon, K.L.; Gedeon, P.C.; Campbell, O.C.; Swartz, A.M.; Riccione, K.A.; Yi, J.S.; Hossain-Ibrahim, M.K.; Saraswathula, A.; Nair, S.K.; Dunn-Pirio, A.M.; Broome, T.M.; Weinhold, K.J.; Desjardins, A.; Vlahovic, G.; McLendon, R.E.; Friedman, A.H.; Friedman, H.S.; Bigner, D.D.; Fecci, P.E.; Mitchell, D.A.; Sampson, J.H. Dendritic cells enhance polyfunctionality of adoptively transferred T cells that target cytomegalovirus in glioblastoma. Cancer Res., 2018, 78(1), 256-264.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-0469] [PMID: 29093005]
[144]
Barrett, J.A.; Cai, H.; Miao, J.; Khare, P.D.; Gonzalez, P.; Dalsing-Hernandez, J.; Sharma, G.; Chan, T.; Cooper, L.J.N.; Lebel, F. Regulated intratumoral expression of IL-12 using a RheoSwitch Therapeutic System® (RTS®) gene switch as gene therapy for the treatment of glioma. Cancer Gene Ther., 2018, 25(5-6), 106-116.
[http://dx.doi.org/10.1038/s41417-018-0019-0] [PMID: 29755109]
[145]
Chiocca, E.A.; Nassiri, F.; Wang, J.; Peruzzi, P.; Zadeh, G. Viral and other therapies for recurrent glioblastoma: is a 24-month durable response unusual? Neuro-oncol., 2019, 21(1), 14-25.
[http://dx.doi.org/10.1093/neuonc/noy170] [PMID: 30346600]
[146]
Robins, H.I.; Zhang, P.; Gilbert, M.R.; Chakravarti, A.; de Groot, J.F.; Grimm, S.A.; Wang, F.; Lieberman, F.S.; Krauze, A.; Trotti, A.M.; Mohile, N.; Kee, A.Y.; Colman, H.; Cavaliere, R.; Kesari, S.; Chmura, S.J.; Mehta, M. A randomized phase I/II study of ABT-888 in combination with temozolomide in recurrent temozolomide resistant glioblastoma: an NRG oncology RTOG group study. J. Neurooncol., 2016, 126(2), 309-316.
[http://dx.doi.org/10.1007/s11060-015-1966-z] [PMID: 26508094]
[147]
Lassen, U.; Chinot, O.L.; McBain, C.; Mau-Sørensen, M.; Larsen, V.A.; Barrie, M.; Roth, P.; Krieter, O.; Wang, K.; Habben, K.; Tessier, J.; Lahr, A.; Weller, M. Phase 1 dose-escalation study of the antiplacental growth factor monoclonal antibody RO5323441 combined with bevacizumab in patients with recurrent glioblastoma. Neuro-oncol., 2015, 17(7), 1007-1015.
[http://dx.doi.org/10.1093/neuonc/nov019] [PMID: 25665807]
[148]
Lukas, R.V.; Rodon, J.; Becker, K.; Wong, E.T.; Shih, K.; Touat, M.; Fassò, M.; Osborne, S.; Molinero, L.; O’Hear, C.; Grossman, W.; Baehring, J. Clinical activity and safety of atezolizumab in patients with recurrent glioblastoma. J. Neurooncol., 2018, 140(2), 317-328.
[http://dx.doi.org/10.1007/s11060-018-2955-9] [PMID: 30073642]
[149]
Holdhoff, M.; Ye, X.; Supko, J.G.; Nabors, L.B.; Desai, A.S.; Walbert, T.; Lesser, G.J.; Read, W.L.; Lieberman, F.S.; Lodge, M.A.; Leal, J.; Fisher, J.D.; Desideri, S.; Grossman, S.A.; Wahl, R.L.; Schiff, D. Timed sequential therapy of the selective T-type calcium channel blocker mibefradil and temozolomide in patients with recurrent high-grade gliomas. Neuro-oncol., 2017, 19(6), 845-852.
[http://dx.doi.org/10.1093/neuonc/nox020] [PMID: 28371832]
[150]
Galanis, E.; Anderson, S.K.; Miller, C.R.; Sarkaria, J.N.; Jaeckle, K.; Buckner, J.C.; Ligon, K.L.; Ballman, K.V.; Moore, D.F., Jr; Nebozhyn, M.; Loboda, A.; Schiff, D.; Ahluwalia, M.S.; Lee, E.Q.; Gerstner, E.R.; Lesser, G.J.; Prados, M.; Grossman, S.A.; Cerhan, J.; Giannini, C.; Wen, P.Y. Alliance for Clinical Trials in Oncology and ABTC. Phase I/II trial of vorinostat combined with temozolomide and radiation therapy for newly diagnosed glioblastoma: results of Alliance N0874/ABTC 02. Neuro-oncol., 2018, 20(4), 546-556.
[http://dx.doi.org/10.1093/neuonc/nox161] [PMID: 29016887]
[151]
Butowski, N.; Colman, H.; De Groot, J.F.; Omuro, A.M.; Nayak, L.; Wen, P.Y.; Cloughesy, T.F.; Marimuthu, A.; Haidar, S.; Perry, A.; Huse, J.; Phillips, J.; West, B.L.; Nolop, K.B.; Hsu, H.H.; Ligon, K.L.; Molinaro, A.M.; Prados, M. Orally administered colony stimulating factor 1 receptor inhibitor PLX3397 in recurrent glioblastoma: an Ivy Foundation Early Phase Clinical Trials Consortium phase II study. Neuro-oncol., 2016, 18(4), 557-564.
[http://dx.doi.org/10.1093/neuonc/nov245] [PMID: 26449250]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 8
Year: 2020
Published on: 13 July, 2020
Page: [564 - 578]
Pages: 15
DOI: 10.2174/1389200221666200714101038
Price: $65

Article Metrics

PDF: 46
HTML: 2