Current and emerging EGFR therapies for glioblastoma

References

• Serban, F.; Daianu, O.; Tataranu, L.G.; Artene, S.A.; Emami, G.; Georgescu, A.M.; Sfredel, V. Silencing of Epidermal Growth Factor, Latrophilin and Seven Transmembrane Domain-Containing Protein 1 (ELTD1) via siRNA-induced Cell Death in Glioblastoma. J. Immunoassay. Immunochem. 2017, 38, 21–33. DOI:10.1080/15321819.2016.1209217.
   PubMedGoogle Scholar
• Taylor, T.E.; Furnari, F.B.; Cavenee, W.K. Targeting EGFR for Treatment of Glioblastoma: Molecular Basis to Overcome Resistance. Curr. Cancer Drug Targets. 2012, 12, 197–209. DOI:10.2174/156800912799277557.
   PubMed Web of Science ®Google Scholar
• Krakstad, C.; Chekenya, M. Survival Signalling and Apoptosis Resistance in Glioblastomas: Opportunities for Targeted Therapeutics. Mol. Cancer. 2010, 9, 135. DOI:10.1186/1476-4598-9-135.
   PubMed Web of Science ®Google Scholar
• Nicolaidis, S. Biomarkers of Glioblastoma Multiforme. Metabolism. 2015, 64, S22–S27. DOI:10.1016/j.metabol.2014.10.031.
   PubMed Web of Science ®Google Scholar
• Szopa, W.; Burley, T.A.; Kramer-Marek, Kaspera, W. Diagnostic and Therapeutic Biomarkers in Glioblastoma: Current Status and Future Perspectives. Bio. Med. Res. Inter. 2017, Article ID 8013575, 13. DOI:10.1155/2017/8013575.
   Google Scholar
• Sangwan, V.; Park, M. Receptor Tyrosine Kinases: Role in Cancer Progression. Curr Oncol. 2006, 13, 191–193.
   PubMedGoogle Scholar
• Lemmon, M.A.; Schlessinger, J. Cell Signaling by Receptor-Tyrosine Kinases. Cell. 2010, 141, 1117–1134. DOI:10.1016/j.cell.2010.06.011.
   PubMed Web of Science ®Google Scholar
• Popescu, A.M.; Alexandru, O.; Brindusa, C.; Purcaru, Ş.O.; Tache, D.E.; Tataranu, L.G.; Taisescu, C.; Dricu, A. Targeting the VEGF and PDGF Signaling Pathway in Glioblastoma Treatment. Int. J. Clin. Exp. Pathol. 2015, 8, 7825–7837.
   PubMed Web of Science ®Google Scholar
• Zahonero, C.; Sanchez-Gomez, P. EGFR-dependent Mechanisms in Glioblastoma: Towards a Better Therapeutic Strategy. Cell. Mol. Life. Sci. 2014, 71, 3465–3488. DOI:10.1007/s00018-014-1608-1.
   PubMed Web of Science ®Google Scholar
• Wheeler, D.L.; Dunn, E.F.; Harari, P.M. Understanding Resistance to EGFR Inhibitors-Impact on Future Treatment Strategies. Nature Rev. Clin. Oncol. 2010, 9, 493–507. DOI:10.1038/nrclinonc.2010.97.
   Web of Science ®Google Scholar
• Capietto, A.H.; Keirallah, S.; Gross, E.; Dauguet, N.; Laprevotte, E.; Jean, C.; Gertner-Dardenne J.; Bezombes C.; Quillet-Mary A.; Poupot M. Emerging Concepts for the Treatment of Hematological Malignancies with Therapeutic Monoclonal Antibodies. Curr. Drug Targets. 2010, 11, 790–800. DOI:10.2174/138945010791320845.
   PubMed Web of Science ®Google Scholar
• Cella, D.; Beaumont, J.L. Pazopanib in the Treatment of Advanced Renal Cell Carcinoma. Ther. Adv. Urol. 2016, 8, 61–69. DOI:10.1177/1756287215614236.
   PubMed Web of Science ®Google Scholar
• Gyorki, D.E.; Spillane, J.; Speakman, D.; Shackleton, M.; Henderson, M.A. Current Management of Advanced Melanoma: A Transformed Landscape. ANZ. J. Surg. 2014, 84, 612–617. DOI:10.1111/ans.2014.84.issue-9.
   PubMed Web of Science ®Google Scholar
• Liang, W.; Wu, X.; Fang, W.; Zhao, Y.; Yang, Y.; Hu, Z.; Xue C.; Zhang J.; Zhang J.; Ma Y. Network Meta-Analysis of Erlotinib, Gefitinib, Afatinib and Icotinib in Patients with Advanced Non-Small-Cell Lung Cancer Harboring EGFR Mutations. PLoS One. 2014, 9, e85245. DOI:10.1371/journal.pone.0085245.
   PubMed Web of Science ®Google Scholar
• Eller, J.L.; Longo, S.L.; Hicklin, D.J.; Canute, G. W. Activity of Anti-Epidermal Growth Factor Receptor Monoclonal Antibody C225 against Glioblastoma Multiforme. Neurosurgery. 2002, 51, 1005–1013.
   PubMed Web of Science ®Google Scholar
• Neyns, B.; Sadones, J.; Joosens, E.; Bouttens, F.; Verbeke, L.; Baurain, J.-F.; D’Hondt, L.; Strauven, T.; Chaskis, C.; In’t Veld, P.; et al. Stratified Phase II Trial of Cetuximab in Patients with Recurrent High-Grade Glioma. Ann. Oncol. 2009, 20, 1596–1603. DOI:10.1093/annonc/mdp032.
   PubMed Web of Science ®Google Scholar
• Bode, U.; Massimino, M.; Bach, F.; Zimmermann, M.; Khuhlaeva, E.; Westphal, M.; Fleischhack, G. Nimotuzumab Treatment of Malignant Gliomas. Expert. Opin. Biol. Ther. 2012, 12, 649–659. DOI:10.1517/14712598.2012.733367.
   PubMed Web of Science ®Google Scholar
• Emrich, J.G.; Brady, L.W.; Quang, T.S.; Class, R.; Miyamoto, C.; Black, P.; Rodeck, U. Radioio- Dinated (I-125) Monoclonal Antibody 425 in the Treatment of High Grade Glioma Patients: Ten-Year synopsis of a Novel Treatment. Am. J. Clin. Oncol. 2002, 25, 541–546. DOI:10.1097/00000421-200212000-00001.
   PubMed Web of Science ®Google Scholar
• Li, L.; Quang, T.S.; Gracely, E.J.; Kim, J.H.; Emrich, J.G.; Yaeger, T.E.; Jenrette, J.M.; Cohen, S.C.; Black, P.; Brady, L.W. A Phase II Study of Anti-Epidermal Growth Factor Receptor Radioimmunotherapy in the Treatment of Glioblastoma Multiforme. J. Neurosurg. 2010, 113, 192–198. DOI:10.3171/2010.2.JNS091211.
   PubMed Web of Science ®Google Scholar
• Quang, T.S.; Brady, L.W. Radioimmunotherapy as a Novel Treatment Regimen: 125i-Labeled Monoclonal Antibody 425 in the Treatment of High-Grade Brain Gliomas. Int. J. Radiat. Oncol. Biol. Phys. 2004, 58, 972–975. DOI:10.1016/j.ijrobp.2003.09.096.
   PubMed Web of Science ®Google Scholar
• Fabry, Z.; Raine, C.S.; Hart, M.N. Nervous Tissue as an Immune Compartment: The Dialect of the Immune Response in the CNS. Immunol. Today. 1994, 15, 218–224.
   PubMedGoogle Scholar
• Artene, S.A.; Turcu-Stiolica, A.; Hartley, R.; Ciurea, M.E.; Daianu, O.; Brindusa, C.; Alexandru, O.; Tataranu, L.G.; Purcaru, S.O.; Dricu, A. Dendritic Cell Immunotherapy versus Bevacizumab Plus Irinotecan in Recurrent Malignant Glioma Patients: A Survival Gain Analysis. Onco. Targets. Ther. 2016, 9, 6669–6677. DOI:10.2147/OTT.S112842.
   PubMed Web of Science ®Google Scholar
• Sagar, D.; Foss, C.; Baz, E.R.; Pomper, M.G.; Khan, Z.K.; Jain, P. Mechanisms of Dendritic Cell Trafficking across the Blood-Brain Barrier. J. Neuro. Immune. Pharmacol. 2012, 7, 74–94. DOI:10.1007/s11481-011-9302-7.
   PubMed Web of Science ®Google Scholar
• Xu, X.; Stockhammer, F.; Schmitt, M. Cellular-Based Immunotherapies for Patients with Glioblastoma Multiforme. Clin. Dev. Immunol. 2012, 2012, 764213.
   PubMedGoogle Scholar
• Cheng, C.; Qu, Q.X.; Shen, Y.; Lv, Y.T.; Zhu, Y.B.; Zhang, X.G.; Huang, J.A. Overexpression of B7-H4 in Tumor Infiltrated Dendritic Cells. J. Immunoassay. Immunochem. 2011, 32, 353–364. DOI:10.1080/15321819.2011.578190.
   PubMed Web of Science ®Google Scholar
• Palucka, K.; Banchereau, J. Cancer Immunotherapy via Dendritic Cells. Nat. Rev. Cancer. 2012, 12, 265–277. DOI:10.1038/nrc3258.
   PubMed Web of Science ®Google Scholar
• Oh, T.; Sayegh, E.T.; Fakurnejad, S.; Oyon, D.; Balquiedra Lamano, J.; DiDomenico, J.D.; Bloch, O.; Parsa, A.T. Vaccine Therapies in Malignant Glioma. Curr. Neurol. Neurosci. Rep. 2015, 15, 508. DOI:10.1007/s11910-014-0508-y.
   PubMed Web of Science ®Google Scholar
• Broker, M.;. Potential Protective Immunogenicity of Tetanus Toxoid, Diphtheria Toxoid and Cross Reacting Material 197 (CRM197) When Used as Carrier Proteins in Glycoconjugates. Hum. Vaccin. Immunother. 2016, 12, 664–667. DOI:10.1080/21645515.2015.1086048.
   PubMed Web of Science ®Google Scholar
• Sampson, J.H.; Archer, G.E.; Mitchell, D.A.; Heimberger, A.B.; Herndon, J.E.; Lally-Goss, D.; McGehee-Norman, S.; Paolino, A.; Reardon, D.A.; Friedman, A. H.; et al. An Epidermal Growth Factor Receptor Variant III-targeted Vaccine Is Safe and Immunogenic in Patients with Glioblastoma Multiforme. Mol. Cancer. Ther. 2009, 8, 2773–2779. DOI:10.1158/1535-7163.MCT-09-0124.
   PubMed Web of Science ®Google Scholar
• Heimberger, A.B.; Hussain, S.F.; Aldape, K.; Sawaya, R.; Archer, G.A.; Friedman, H.; Reardon D.; Friedman A.; Bigner D.; Sampson J.H. Tumor-Specific Peptide Vaccination in Newly-Diagnosed Patients with GBM. J. Clin. Oncol. 2006, 24, 107S–107S.
   Web of Science ®Google Scholar
• Gatson, N.T.; Weathers, S.P.; De Groot, J.F. ReACT Phase II Trial: A Critical Evaluation of the Use of Rindopepimut Plus Bevacizumab to Treat EGFRvIII-positive Recurrent Glioblastoma. CNS Oncol. 2016, 5, 11–26. DOI:10.2217/cns.15.38.
   PubMedGoogle Scholar
• 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.; et al. A Phase II, Multicenter Trial of Rindopepimut (CDX-110) in Newly Diagnosed Glioblastoma: The ACT III Study. Neuro. Oncol. 2015, 17, 854–861. DOI:10.1093/neuonc/nou348.
   PubMed Web of Science ®Google Scholar
• Weller, M.; Butowski, N.; Tran, D.D.; Recht, L.D.; Lim, M.; Hirte, H.; Ashby, L.; Mechtler, L.; Goldlust, S.A.; Iwamoto, F.; et al. Rindopepimut with Temozolomide for Patients with Newly Diagnosed, EGFRvIII-expressing Glioblastoma (ACT IV): A Randomised, Double-Blind, International Phase 3 Trial. Lancet Oncol. 2017, 18, 1373–1385. DOI:10.1016/S1470-2045(17)30517-X.
   PubMed Web of Science ®Google Scholar
• Brahmer, J.; Reckamp, K.L.; Baas, P.; Crino, L.; Eberhardt, W.E.; Poddubskaya, E.; Borghaei H.; Paz-Ares L.; Horn L.; Spigel D.R.; Steins M.; Ready N.E.; Chow L. Q.; Vokes E.E.; Felip E.; Holgado E. Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer. N. Engl. J. Med. 2015, 373, 123–135. DOI:10.1056/NEJMoa1504627.
   PubMed Web of Science ®Google Scholar
• Lynch, T.J.; Bondarenko, I.; Luft, A.; Serwatowski, P.; Barlesi, F.; Chacko, R.; Sebastian, M.; Neal, J.; Lu, H.; Cuillerot, J.-M.; Reck, M. Ipilimumab in Combination with Paclitaxel and Carboplatin as First-Line Treatment in Stage IIIB/IV Non-Small-Cell Lung Cancer: Results from a Randomized, Double-Blind, Multicenter Phase II Study. J. Clin. Oncol. 2012, 30, 2046–2054. DOI:10.1200/JCO.2011.38.4032.
   PubMed Web of Science ®Google Scholar
• Robert, C.; Long, G.V.; Brady, B.; Dutriaux, C.; Maio, M.; Mortier, L.; Hassel, J. C.; Rutkowski, P.; McNeil, C.; Kalinka-Warzocha, E.; et al. Nivolumab in Previously Untreated Melanoma without BRAF Mutation. N. Engl. J. Med. 2015, 372, 320–330. DOI:10.1056/NEJMoa1412082.
   PubMed Web of Science ®Google Scholar
• Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J.J.; Cowey, C.L.; Lao, C.D.; Schadendorf, D.; Dummer, R.; Smylie, M.; Rutkowski, P.; et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N. Engl.J.Med. 2015, 373, 23–34. DOI:10.1056/NEJMoa1504030.
   PubMed Web of Science ®Google Scholar
• Buchbinder, E.I.; Desai, A. CTLA-4 and PD-1 Pathways: Similarities, Differences, and Implications of Their Inhibition. Am.J.Clin.Oncol. 2016, 39, 98–106. DOI:10.1097/COC.0000000000000239.
   PubMed Web of Science ®Google Scholar
• La-Beck, N.M.; Jean, G.W.; Huynh, C.; Alzghari, S.K.; Lowe, D.B. Immune Checkpoint Inhibitors: New Insights and Current Place in Cancer Therapy. Pharmacotherapy. 2015, 35, 963–976. DOI:10.1002/phar.1643.
   PubMed Web of Science ®Google Scholar
• Nduom, E.K.; Wei, J.; Yaghi, N.K.; Huang, N.; Kong, L.Y.; Gabrusiewicz, K.; Ling, X.; Zhou, S.; Ivan, C.; Chen, J.Q.; et al. PD-L1 Expression and Prognostic Impact in Glioblastoma. Neuro-Oncology. 2016, 18, 195–205. DOI:10.1093/neuonc/nov172.
   PubMed Web of Science ®Google Scholar
• Hulou, M.M.; Cho, C.F.; Chiocca, E.A.; Bjerkvig, R. Experimental Therapies: Gene Therapies and Oncolytic Viruses. Handbook. Clin. Neurol. 2016, 134, 183–197.
   PubMedGoogle Scholar
• Larocca, C.; Schlom, J. Viral Vector-Based Therapeutic Cancer Vaccines. Cancer Journal. 2011, 17, 359–371. DOI:10.1097/PPO.0b013e3182325e63.
   PubMed Web of Science ®Google Scholar
• Halloran, P.J.; Fenton, R.G. Irreversible G2-M Arrest and Cytoskeletal Reorganization Induced by Cytotoxic Nucleoside Analogues. Cancer. Res. 1998, 58, 3855–3865.
   PubMed Web of Science ®Google Scholar
• Westphal, M.; Yla-Herttuala, S.; Martin, J.; Warnke, P.; Menei, P.; Eckland, D.; Kinley, J.; Kay, R.; Ram, Z. Adenovirus-Mediated Gene Therapy with Sitimagene Ceradenovec Followed by Intravenous Ganciclovir for Patients with Operable High-Grade Glioma (ASPECT): A Randomised, Open-Label, Phase 3 Trial. Lancet. Oncol. 2013, 14, 823–833. DOI:10.1016/S1470-2045(13)70274-2.
   PubMed Web of Science ®Google Scholar
• Wheeler, L.A.; Manzanera, A.G.; Bell, S.D.; Cavaliere, R.; McGregor, J.M.; Grecula, J.C.; Newton, H.B.; Lo, S.S.; Badie, B.; Portnow, J.; et al. Phase II Multicenter Study of Gene-Mediated Cytotoxic Immunotherapy as Adjuvant to Surgical Resection for Newly Diagnosed Malignant Glioma. Neuro-Oncology. 2016, 18, 1137–1145. DOI:10.1093/neuonc/now002.
   PubMed Web of Science ®Google Scholar
• Piao, Y.; Jiang, H.; Alemany, R.; Krasnykh, V.; Marini, F.C.; Xu, J.; Alonso, M.M.; Conrad, C.A.; Aldape, K.D.; Gomez-Manzano, C.; Fueyo, J. Oncolytic Adenovirus Retargeted to Delta-EGFR Induces Selective Antiglioma Activity. Cancer. Gene. Ther. 2009, 16, 256–265. DOI:10.1038/cgt.2008.75.
   PubMed Web of Science ®Google Scholar
• Sawamura, Y.; Hosokawa, M.; Kuppner, M.C.; Kobayashi, H.; Aida, T.; Abe, H.; de Tribolet, N. Antitumor Activity and Surface Phenotypes of Human Glioma-Infiltrating Lymphocytes after in Vitro Expansion in the Presence of Interleukin 2. Cancer. Res. 1989, 49, 7, 1843–1849.
   PubMed Web of Science ®Google Scholar
• Stevens, A.; Kloter, I.; Roggendorf, W. Inflammatory Infiltrates and Natural Killer Cell Presence in Human Brain Tumors. Cancer. 1988, 61, 738–743. DOI:10.1002/1097-0142(19880215)61:4<738::AID-CNCR2820610417>3.0.CO;2-E.
   PubMed Web of Science ®Google Scholar
• Hayes, R.L.; Arbit, E.; Odaimi, M.; Pannullo, S.; Scheff, R.; Kravchinskiy, D.; Zaroulis, C. Adoptive Cellular Immunotherapy for the Treatment of Malignant Gliomas. Crit. Rev. Oncol. Hematol. 2001, 39, 31–42. DOI:10.1016/S1040-8428(01)00122-6.
   PubMed Web of Science ®Google Scholar
• Sloan, A.E.; Dansey, R.; Zamorano, L.; Barger, G.; Hamm, C.; Diaz, F.; Baynes, R.; Wood, G. Adoptive Immunotherapy in Patients with Recurrent Malignant Glioma: Preliminary Results of Using Autologous Whole-Tumor Vaccine Plus Granulocyte-Macrophage Colony-Stimulating Factor and Adoptive Transfer of anti-CD3-activated Lymphocytes. Neurosurg. Focus. 2000, 9, e9. DOI:10.3171/foc.2000.9.6.10.
   PubMedGoogle Scholar
• Dillman, R.O.; Duma, C.M.; Ellis, R.A.; Cornforth, A.N.; Schiltz, P.M.; Sharp, S.L.; DePriest, M.C. Intralesional Lymphokine-Activated Killer Cells as Adjuvant Therapy for Primary Glioblastoma. J. Immunother. 2009, 32, 914–919. DOI:10.1097/CJI.0b013e3181b2910f.
   PubMed Web of Science ®Google Scholar
• 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. Phase III Randomized Trial of Autologous Cytokine-Induced Killer Cell Immunotherapy for Newly Diagnosed Glioblastoma in Korea. Oncotarget. 2017, 8, 4, 7003–7013.
   PubMed Web of Science ®Google Scholar
• Zagzag, D.; Salnikow, K.; Chiriboga, L.; Yee, H.; Lan, L.; Ali, M.A.; Garcia, R.; Demaria, S.; Newcomb, E.W. Downregulation of Major Histocompatibility Complex Antigens in Invading Glioma Cells: Stealth Invasion of the Brain. Lab. Invest. 2005, 85, 328–341. DOI:10.1038/labinvest.3700233.
   PubMed Web of Science ®Google Scholar
• Razavi, S.M.; Lee, K.E.; Jin, B.E.; Aujla, P.S.; Gholamin, S.; Li, G. Immune Evasion Strategies of Glioblastoma. Front. Surg. 2016, 3, 11. DOI:10.3389/fsurg.2016.00011.
   PubMed Web of Science ®Google Scholar
• Sengupta, S.; Mao, G.; Gokaslan, Z.S.; Sampath, P. Chimeric Antigen Receptors for Treatment of Glioblastoma: A Practical Review of Challenges and Ways to Overcome Them. Cancer. Gene. Ther. 2017, 24, 121–129. DOI:10.1038/cgt.2016.46.
   PubMed Web of Science ®Google Scholar
• Ahmed, N.; Brawley, V.; Hegde, M.; Bielamowicz, K.; Wakefield, A.; Ghazi, A.; Ashoori, A.; Diouf, O.; Gerken, C.; Landi, D.; et al. 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, O11. DOI:10.1186/2051-1426-3-S2-O11.
   PubMedGoogle Scholar
• O’Rourke, D.M.; Nasrallah, M.; Morrissette, J.J.; Melenhorst, J.J.; Lacey, S.F.; Mansfield, K.; Martinez-Lage M.; Desai A.S.; Brem S.; Maloney E.; Mohan S. Pilot Study of T Cells Redirected to EGFRvIII with a Chimeric Antigen Receptor in Patients with EGFRvIII+ Glioblastoma. Am. Soc. Clin. Oncol. 2016, 34, 15_suppl, 2067.
   Web of Science ®Google Scholar
• Brown, C.E.; Alizadeh, D.; Starr, R.; Weng, L.; Wagner, J.R.; Naranjo, A.; Ostberg, J.R.; Blanchard, M.S.; Kilpatrick, J.; Simpson, J.; et al. Regression of Glioblastoma after Chimeric Antigen Receptor T-Cell Therapy. N. Engl. J. Med. 2016, 375, 2561–2569. DOI:10.1056/NEJMoa1610497.
   PubMed Web of Science ®Google Scholar