Innovative therapies for malignant brain tumors: the road to a tailored cure

Innovative therapies for malignant brain tumors: the road to a tailored cure

Authors

  • Alice Giotta Lucifero University of Pavia, Pavia, Italy
  • Sabino Luzzi Neurosurgery Unit, Department of Clinical-Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy; Neurosurgery Unit, Department of Surgical Sciences, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy
  • Ilaria Brambilla Pediatric Clinic, Department of Pediatrics, Fondazione IRCCS Policlinico San Matteo, Uni-versity of Pavia, Pavia, Italy
  • Chiara Trabatti Pediatric Clinic, Department of Pediatrics, Fondazione IRCCS Policlinico San Matteo, Uni-versity of Pavia, Pavia, Italy
  • Mario Mosconi Orthopaedic and Traumatology Unit, Department of Clinical-Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy
  • Salvatore Savasta Pediatric Clinic, Department of Pediatrics, Fondazione IRCCS Policlinico San Matteo, Uni-versity of Pavia, Pavia, Italy
  • Thomas Foiadelli Pediatric Clinic, Department of Pediatrics, Fondazione IRCCS Policlinico San Matteo, Uni-versity of Pavia, Pavia, Italy

Keywords:

Cell-based Therapy; Glioblastoma; Immunotherapy Malignant Brain Tumor, Target Therapy.

Abstract

Background: Immune tolerance, immune escape, neoangiogenesis, phenotypic changes, and glioma stem cells are all responsible for the resistance of malignant brain tumors to current therapies and persistent recurrence. The present study provides a panoramic view of innovative therapies for malignant brain tumors, especially glioblastoma, aimed at achieving a tailored approach. Methods: PubMed/Medline and ClinicalTrials.gov were the main sources of an extensive literature review in which “Regenerative Medicine,” “Cell-Based Therapy,” “Chemotherapy,” “Vaccine,” “Cell Engineering,” “Immunotherapy, Active,” “Immunotherapy, Adoptive,” “Stem Cells,” “Gene Therapy,” “Target Therapy,” “Brain Cancer,” “Glioblastoma,” and “Malignant Brain Tumor” were the search terms. Only articles in English published in the last 5 years were included. A further selection was made according to the quality of the studies and level of evidence. Results: Cell-based and targeted therapies represent the newest frontiers of brain cancer treatment. Active and adoptive immunotherapies, stem cell therapies, and gene therapies represent a tremendous evolution in recent years due to many preclinical and clinical studies. Clinical trials have validated the effectiveness of antibody-based immunotherapies, including an in-depth study of bevacizumab, in combination with standard of care. Preclinical data highlights the role of vaccines, stem cells, and gene therapies to prevent recurrence. Conclusion: Monoclonal antibodies strengthen the first-line therapy for high grade gliomas. Vaccines, engineered cells, stem cells, and gene and targeted therapies are good candidates for second-line treatment of both newly diagnosed and recurrent gliomas. Further data are necessary to validate this tailored approach at the bedside.

References

Ahmed N, Salsman VS, Kew Y, Shaffer D, Powell S, Zhang YJ, Grossman RG, Heslop HE, Gottschalk S (2010) HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin Cancer Res 16:474-485. doi:10.1158/1078-0432.CCR-09-1322

Attenello FJ, Mukherjee D, Datoo G, McGirt MJ, Bohan E, Weingart JD, Olivi A, Quinones-Hinojosa A, Brem H (2008) Use of Gliadel (BCNU) wafer in the surgical treatment of malignant glioma: a 10-year institutional experience. Ann Surg Oncol 15:2887-2893. doi:10.1245/s10434-008-0048-2

Auffinger B, Spencer D, Pytel P, Ahmed AU, Lesniak MS (2015) The role of glioma stem cells in chemotherapy resistance and glioblastoma multiforme recurrence. Expert Rev Neurother 15:741-752. doi:10.1586/14737175.2015.1051968

Baldini C, Romano PM, Varga A, Champiat S, Dumont S, Dhermain F, Louvel G, Marabelle A, Postel-Vinay S, Angevin E, Gazzah A, Ribrag V, Bahleda R, Michot JM, Hollebecque A, Soria JC, Massard C (2018). Bull Cancer 105 Suppl 1:S59-S67. doi:10.1016/S0007-4551(18)30391-6

Bayin NS, Modrek AS, Dietrich A, Lebowitz J, Abel T, Song HR, Schober M, Zagzag D, Buchholz CJ, Chao MV, Placantonakis DG (2014) Selective lentiviral gene delivery to CD133-expressing human glioblastoma stem cells. PLoS One 9:e116114. doi:10.1371/journal.pone.0116114

Bellantoni G, Guerrini F, Del Maestro M, Galzio R, Luzzi S (2019) Simple schwannomatosis or an incomplete Coffin-Siris? Report of a particular case. eNeurologicalSci 14:31-33. doi:10.1016/j.ensci.2018.11.021

Black ME, Newcomb TG, Wilson HM, Loeb LA (1996) Creation of drug-specific herpes simplex virus type 1 thymidine kinase mutants for gene therapy. Proc Natl Acad Sci U S A 93:3525-3529. doi:10.1073/pnas.93.8.3525

Bloch O, Crane CA, Fuks Y, Kaur R, Aghi MK, Berger MS, Butowski NA, Chang SM, Clarke JL, McDermott MW, Prados MD, Sloan AE, Bruce JN, Parsa AT (2014) Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma: a phase II, single-arm trial. Neuro Oncol 16:274-279. doi:10.1093/neuonc/not203

Bykov VJ, Zache N, Stridh H, Westman J, Bergman J, Selivanova G, Wiman KG (2005) PRIMA-1(MET) synergizes with cisplatin to induce tumor cell apoptosis. Oncogene 24:3484-3491. doi:10.1038/sj.onc.1208419

Chen L, Han X (2015) Anti-PD-1/PD-L1 therapy of human cancer: past, present, and future. J Clin Invest 125:3384-3391. doi:10.1172/JCI80011

Chow KK, Naik S, Kakarla S, Brawley VS, Shaffer DR, Yi Z, Rainusso N, Wu MF, Liu H, Kew Y, Grossman RG, Powell S, Lee D, Ahmed N, Gottschalk S (2013) T cells redirected to EphA2 for the immunotherapy of glioblastoma. Mol Ther 21:629-637. doi:10.1038/mt.2012.210

Daniela F, Vescovi AL, Bottai D (2007) The stem cells as a potential treatment for neurodegeneration. Methods Mol Biol 399:199-213. doi:10.1007/978-1-59745-504-6_14

Das M, Zhu C, Kuchroo VK (2017) Tim-3 and its role in regulating anti-tumor immunity. Immunol Rev 276:97-111. doi:10.1111/imr.12520

Del Maestro M, Luzzi S, Gallieni M, Trovarelli D, Giordano AV, Gallucci M, Ricci A, Galzio R (2018) Surgical Treatment of Arteriovenous Malformations: Role of Preoperative Staged Embolization. Acta Neurochir Suppl 129:109-113. doi:10.1007/978-3-319-73739-3_16

Del Vecchio CA, Li G, Wong AJ (2012) Targeting EGF receptor variant III: tumor-specific peptide vaccination for malignant gliomas. Expert Rev Vaccines 11:133-144. doi:10.1586/erv.11.177

Dhodapkar KM, Cirignano B, Chamian F, Zagzag D, Miller DC, Finlay JL, Steinman RM (2004) Invariant natural killer T cells are preserved in patients with glioma and exhibit antitumor lytic activity following dendritic cell-mediated expansion. Int J Cancer 109:893-899. doi:10.1002/ijc.20050

Diaz RJ, Ali S, Qadir MG, De La Fuente MI, Ivan ME, Komotar RJ (2017) The role of bevacizumab in the treatment of glioblastoma. J Neurooncol 133:455-467. doi:10.1007/s11060-017-2477-x

Dolecek TA, Propp JM, Stroup NE, Kruchko C (2012) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2005-2009. Neuro Oncol 14 Suppl 5:v1-49. doi:10.1093/neuonc/nos218

Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096. doi:10.1126/science.1258096

Fang C, Wang K, Stephen ZR, Mu Q, Kievit FM, Chiu DT, Press OW, Zhang M (2015) Temozolomide nanoparticles for targeted glioblastoma therapy. ACS Appl Mater Interfaces 7:6674-6682. doi:10.1021/am5092165

Foiadelli T, Piccorossi A, Sacchi L, De Amici M, Tucci M, Brambilla I, Marseglia GL, Savasta S, Verrotti A (2018) Clinical characteristics of headache in Italian adolescents aged 11-16 years: a cross-sectional questionnaire school-based study. Ital J Pediatr 44:44. doi:10.1186/s13052-018-0486-9

Gallieni M, Del Maestro M, Luzzi S, Trovarelli D, Ricci A, Galzio R (2018) Endoscope-Assisted Microneurosurgery for Intracranial Aneurysms: Operative Technique, Reliability, and Feasibility Based on 14 Years of Personal Experience. Acta Neurochir Suppl 129:19-24. doi:10.1007/978-3-319-73739-3_3

Garone G, Reale A, Vanacore N, Parisi P, Bondone C, Suppiej A, Brisca G, Calistri L, Cordelli DM, Savasta S, Grosso S, Midulla F, Falsaperla R, Verrotti A, Bozzola E, Vassia C, Da Dalt L, Maggiore R, Masi S, Maltoni L, Foiadelli T, Rossetti A, Greco C, Marino S, Di Paolantonio C, Papetti L, Urbino AF, Rossi R, Raucci U (2019) Acute ataxia in paediatric emergency departments: a multicentre Italian study. Arch Dis Child 104:768-774. doi:10.1136/archdischild-2018-315487

Gras Navarro A, Kmiecik J, Leiss L, Zelkowski M, Engelsen A, Bruserud O, Zimmer J, Enger PO, Chekenya M (2014) NK cells with KIR2DS2 immunogenotype have a functional activation advantage to efficiently kill glioblastoma and prolong animal survival. J Immunol 193:6192-6206. doi:10.4049/jimmunol.1400859

Hardee ME, Zagzag D (2012) Mechanisms of glioma-associated neovascularization. Am J Pathol 181:1126-1141. doi:10.1016/j.ajpath.2012.06.030

Hartmann J, Schussler-Lenz M, Bondanza A, Buchholz CJ (2017) Clinical development of CAR T cells-challenges and opportunities in translating innovative treatment concepts. EMBO Mol Med 9:1183-1197. doi:10.15252/emmm.201607485

Hasselbalch B, Lassen U, Hansen S, Holmberg M, Sorensen M, Kosteljanetz M, Broholm H, Stockhausen MT, Poulsen HS (2010) Cetuximab, bevacizumab, and irinotecan for patients with primary glioblastoma and progression after radiation therapy and temozolomide: a phase II trial. Neuro Oncol 12:508-516. doi:10.1093/neuonc/nop063

Hegde M, Corder A, Chow KK, Mukherjee M, Ashoori A, Kew Y, Zhang YJ, Baskin DS, Merchant FA, Brawley VS, Byrd TT, Krebs S, Wu MF, Liu H, Heslop HE, Gottschalk S, Yvon E, Ahmed N (2013) Combinational targeting offsets antigen escape and enhances effector functions of adoptively transferred T cells in glioblastoma. Mol Ther 21:2087-2101. doi:10.1038/mt.2013.185

Hofland KF, Hansen S, Sorensen M, Engelholm S, Schultz HP, Muhic A, Grunnet K, Ask A, Costa JC, Kristiansen C, Thomsen C, Poulsen HS, Lassen U (2014) Neoadjuvant bevacizumab and irinotecan versus bevacizumab and temozolomide followed by concomitant chemoradiotherapy in newly diagnosed glioblastoma multiforme: A randomized phase II study. Acta Oncol 53:939-944. doi:10.3109/0284186X.2013.879607

Izquierdo M, Martin V, de Felipe P, Izquierdo JM, Perez-Higueras A, Cortes ML, Paz JF, Isla A, Blazquez MG (1996) Human malignant brain tumor response to herpes simplex thymidine kinase (HSVtk)/ganciclovir gene therapy. Gene Ther 3:491-495

Izumoto S, Tsuboi A, Oka Y, Suzuki T, Hashiba T, Kagawa N, Hashimoto N, Maruno M, Elisseeva OA, Shirakata T, Kawakami M, Oji Y, Nishida S, Ohno S, Kawase I, Hatazawa J, Nakatsuka S, Aozasa K, Morita S, Sakamoto J, Sugiyama H, Yoshimine T (2008) Phase II clinical trial of Wilms tumor 1 peptide vaccination for patients with recurrent glioblastoma multiforme. J Neurosurg 108:963-971. doi:10.3171/JNS/2008/108/5/0963

Jiang X, Reardon DA, Desjardins A, Vredenburgh JJ, Quinn JA, Austin AD, Herndon JE, 2nd, McLendon RE, Friedman HS (2013) O6-methylguanine-DNA methyltransferase (MGMT) immunohistochemistry as a predictor of resistance to temozolomide in primary CNS lymphoma. J Neurooncol 114:135-140. doi:10.1007/s11060-013-1162-y

Kim JE, Patel MA, Mangraviti A, Kim ES, Theodros D, Velarde E, Liu A, Sankey EW, Tam A, Xu H, Mathios D, Jackson CM, Harris-Bookman S, Garzon-Muvdi T, Sheu M, Martin AM, Tyler BM, Tran PT, Ye X, Olivi A, Taube JM, Burger PC, Drake CG, Brem H, Pardoll DM, Lim M (2017) Combination Therapy with Anti-PD-1, Anti-TIM-3, and Focal Radiation Results in Regression of Murine Gliomas. Clin Cancer Res 23:124-136. doi:10.1158/1078-0432.CCR-15-1535

Kim Y, Wu Q, Hamerlik P, Hitomi M, Sloan AE, Barnett GH, Weil RJ, Leahy P, Hjelmeland AB, Rich JN (2013) Aptamer identification of brain tumor-initiating cells. Cancer Res 73:4923-4936. doi:10.1158/0008-5472.CAN-12-4556

Kmiecik J, Poli A, Brons NH, Waha A, Eide GE, Enger PO, Zimmer J, Chekenya M (2013) Elevated CD3+ and CD8+ tumor-infiltrating immune cells correlate with prolonged survival in glioblastoma patients despite integrated immunosuppressive mechanisms in the tumor microenvironment and at the systemic level. J Neuroimmunol 264:71-83. doi:10.1016/j.jneuroim.2013.08.013

Koukourakis GV (2015) Bevacizumab for Malignant Brain Gliomas. Which is the Current Evidence? Recent Pat Inflamm Allergy Drug Discov 9:136-143. doi:10.2174/1872213x09666150807110031

Kreisl TN, Lassman AB, Mischel PS, Rosen N, Scher HI, Teruya-Feldstein J, Shaffer D, Lis E, Abrey LE (2009) A pilot study of everolimus and gefitinib in the treatment of recurrent glioblastoma (GBM). J Neurooncol 92:99-105. doi:10.1007/s11060-008-9741-z

Kuhnt D, Becker A, Ganslandt O, Bauer M, Buchfelder M, Nimsky C (2011) Correlation of the extent of tumor volume resection and patient survival in surgery of glioblastoma multiforme with high-field intraoperative MRI guidance. Neuro Oncol 13:1339-1348. doi:10.1093/neuonc/nor133

Kwatra MM (2017) A Rational Approach to Target the Epidermal Growth Factor Receptor in Glioblastoma. Curr Cancer Drug Targets 17:290-296. doi:10.2174/1568009616666161227091522

Lang FF, Bruner JM, Fuller GN, Aldape K, Prados MD, Chang S, Berger MS, McDermott MW, Kunwar SM, Junck LR, Chandler W, Zwiebel JA, Kaplan RS, Yung WK (2003) Phase I trial of adenovirus-mediated p53 gene therapy for recurrent glioma: biological and clinical results. J Clin Oncol 21:2508-2518. doi:10.1200/JCO.2003.21.13.2508

Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, Ferrucci PF, Hill A, Wagstaff J, Carlino MS, Haanen JB, Maio M, Marquez-Rodas I, McArthur GA, Ascierto PA, Long GV, Callahan MK, Postow MA, Grossmann K, Sznol M, Dreno B, Bastholt L, Yang A, Rollin LM, Horak C, Hodi FS, Wolchok JD (2015) Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med 373:23-34. doi:10.1056/NEJMoa1504030

Longo DL, Baden LR (2018) Exploiting Viruses to Treat Diseases. N Engl J Med 379:194-196. doi:10.1056/NEJMe1807181

Lukas RV, Rodon J, Becker K, Wong ET, Shih K, Touat M, Fasso M, Osborne S, Molinero L, O'Hear C, Grossman W, Baehring J (2018) Clinical activity and safety of atezolizumab in patients with recurrent glioblastoma. J Neurooncol 140:317-328. doi:10.1007/s11060-018-2955-9

Luzzi S, Crovace AM, Del Maestro M, Giotta Lucifero A, Elbabaa SK, Cinque B, Palumbo P, Lombardi F, Cimini A, Cifone MG, Crovace A, Galzio R (2019) The cell-based approach in neurosurgery: ongoing trends and future perspectives. Heliyon 5:e02818. doi:10.1016/j.heliyon.2019.e02818

Luzzi S, Crovace AM, Lacitignola L, Valentini V, Francioso E, Rossi G, Invernici G, Galzio RJ, Crovace A (2018) Engraftment, neuroglial transdifferentiation and behavioral recovery after complete spinal cord transection in rats. Surg Neurol Int 9:19. doi:10.4103/sni.sni_369_17

Luzzi S, Del Maestro M, Bongetta D, Zoia C, Giordano AV, Trovarelli D, Raysi Dehcordi S, Galzio RJ (2018) Onyx Embolization Before the Surgical Treatment of Grade III Spetzler-Martin Brain Arteriovenous Malformations: Single-Center Experience and Technical Nuances. World Neurosurg 116:e340-e353. doi:10.1016/j.wneu.2018.04.203

Luzzi S, Del Maestro M, Elia A, Vincitorio F, Di Perna G, Zenga F, Garbossa D, Elbabaa S, Galzio R (2019) Morphometric and Radiomorphometric Study of the Correlation Between the Foramen Magnum Region and the Anterior and Posterolateral Approaches to Ventral Intradural Lesions. Turk Neurosurg. doi:10.5137/1019-5149.JTN.26052-19.2

Luzzi S, Gallieni M, Del Maestro M, Trovarelli D, Ricci A, Galzio R (2018) Giant and Very Large Intracranial Aneurysms: Surgical Strategies and Special Issues. Acta Neurochir Suppl 129:25-31. doi:10.1007/978-3-319-73739-3_4

McKay R (1997) Stem cells in the central nervous system. Science 276:66-71. doi:10.1126/science.276.5309.66

Mercapide J, Rappa G, Anzanello F, King J, Fodstad O, Lorico A (2010) Primary gene-engineered neural stem/progenitor cells demonstrate tumor-selective migration and antitumor effects in glioma. Int J Cancer 126:1206-1215. doi:10.1002/ijc.24809

Mitchell DA, Batich KA, Gunn MD, Huang MN, Sanchez-Perez L, Nair SK, Congdon KL, Reap EA, Archer GE, Desjardins A, Friedman AH, Friedman HS, Herndon JE, 2nd, Coan A, McLendon RE, Reardon DA, Vredenburgh JJ, Bigner DD, Sampson JH (2015) Tetanus toxoid and CCL3 improve dendritic cell vaccines in mice and glioblastoma patients. Nature 519:366-369. doi:10.1038/nature14320

Mohme M, Neidert MC (2020) Tumor-Specific T Cell Activation in Malignant Brain Tumors. Front Immunol 11:205. doi:10.3389/fimmu.2020.00205

Mount NM, Ward SJ, Kefalas P, Hyllner J (2015) Cell-based therapy technology classifications and translational challenges. Philos Trans R Soc Lond B Biol Sci 370:20150017. doi:10.1098/rstb.2015.0017

Nagpal S (2012) The role of BCNU polymer wafers (Gliadel) in the treatment of malignant glioma. Neurosurg Clin N Am 23:289-295, ix. doi:10.1016/j.nec.2012.01.004

Nosadini M, Granata T, Matricardi S, Freri E, Ragona F, Papetti L, Suppiej A, Valeriani M, Sartori S, Italian Working Group on Paediatric Anti Nm-DaRE (2019) Relapse risk factors in anti-N-methyl-D-aspartate receptor encephalitis. Dev Med Child Neurol 61:1101-1107. doi:10.1111/dmcn.14267

Omuro A, DeAngelis LM (2013) Glioblastoma and other malignant gliomas: a clinical review. JAMA 310:1842-1850. doi:10.1001/jama.2013.280319

Omuro A, Vlahovic G, Lim M, Sahebjam S, Baehring J, Cloughesy T, Voloschin A, Ramkissoon SH, Ligon KL, Latek R, Zwirtes R, Strauss L, Paliwal P, Harbison CT, Reardon DA, Sampson JH (2018) Nivolumab with or without ipilimumab in patients with recurrent glioblastoma: results from exploratory phase I cohorts of CheckMate 143. Neuro Oncol 20:674-686. doi:10.1093/neuonc/nox208

Padfield E, Ellis HP, Kurian KM (2015) Current Therapeutic Advances Targeting EGFR and EGFRvIII in Glioblastoma. Front Oncol 5:5. doi:10.3389/fonc.2015.00005

Pandith AA, Qasim I, Zahoor W, Shah P, Bhat AR, Sanadhya D, Shah ZA, Naikoo NA (2018) Concordant association validates MGMT methylation and protein expression as favorable prognostic factors in glioma patients on alkylating chemotherapy (Temozolomide). Sci Rep 8:6704. doi:10.1038/s41598-018-25169-2

Parisi P, Vanacore N, Belcastro V, Carotenuto M, Del Giudice E, Mariani R, Papetti L, Pavone P, Savasta S, Striano P, Toldo I, Tozzi E, Verrotti A, Raucci U, Pediatric Headache Commission" of Societa Italiana di Neurologia P (2014) Clinical guidelines in pediatric headache: evaluation of quality using the AGREE II instrument. J Headache Pain 15:57. doi:10.1186/1129-2377-15-57

Pascual-Castroviejo I, Lopez-Pereira P, Savasta S, Lopez-Gutierrez JC, Lago CM, Cisternino M (2008) Neurofibromatosis type 1 with external genitalia involvement presentation of 4 patients. J Pediatr Surg 43:1998-2003. doi:10.1016/j.jpedsurg.2008.01.074

Patyka M, Sharifi Z, Petrecca K, Mansure J, Jean-Claude B, Sabri S (2016) Sensitivity to PRIMA-1MET is associated with decreased MGMT in human glioblastoma cells and glioblastoma stem cells irrespective of p53 status. Oncotarget 7:60245-60269. doi:10.18632/oncotarget.11197

Peereboom DM, Ahluwalia MS, Ye X, Supko JG, Hilderbrand SL, Phuphanich S, Nabors LB, Rosenfeld MR, Mikkelsen T, Grossman SA, New Approaches to Brain Tumor Therapy C (2013) NABTT 0502: a phase II and pharmacokinetic study of erlotinib and sorafenib for patients with progressive or recurrent glioblastoma multiforme. Neuro Oncol 15:490-496. doi:10.1093/neuonc/nos322

Phuphanich S, Wheeler CJ, Rudnick JD, Mazer M, Wang H, Nuno MA, Richardson JE, Fan X, Ji J, Chu RM, Bender JG, Hawkins ES, Patil CG, Black KL, Yu JS (2013) Phase I trial of a multi-epitope-pulsed dendritic cell vaccine for patients with newly diagnosed glioblastoma. Cancer Immunol Immunother 62:125-135. doi:10.1007/s00262-012-1319-0

Polyzoidis S, Ashkan K (2014) DCVax(R)-L--developed by Northwest Biotherapeutics. Hum Vaccin Immunother 10:3139-3145. doi:10.4161/hv.29276

Prendergast GC, Malachowski WP, DuHadaway JB, Muller AJ (2017) Discovery of IDO1 Inhibitors: From Bench to Bedside. Cancer Res 77:6795-6811. doi:10.1158/0008-5472.CAN-17-2285

Raysi Dehcordi S, Ricci A, Di Vitantonio H, De Paulis D, Luzzi S, Palumbo P, Cinque B, Tempesta D, Coletti G, Cipolloni G, Cifone MG, Galzio R (2017) Stemness Marker Detection in the Periphery of Glioblastoma and Ability of Glioblastoma to Generate Glioma Stem Cells: Clinical Correlations. World Neurosurg 105:895-905. doi:10.1016/j.wneu.2017.05.099

Reardon DA, Desjardins A, Vredenburgh JJ, Gururangan S, Friedman AH, Herndon JE, 2nd, Marcello J, Norfleet JA, McLendon RE, Sampson JH, Friedman HS (2010) Phase 2 trial of erlotinib plus sirolimus in adults with recurrent glioblastoma. J Neurooncol 96:219-230. doi:10.1007/s11060-009-9950-0

Ricci A, Di Vitantonio H, De Paulis D, Del Maestro M, Raysi SD, Murrone D, Luzzi S, Galzio RJ (2017) Cortical aneurysms of the middle cerebral artery: A review of the literature. Surg Neurol Int 8:117. doi:10.4103/sni.sni_50_17

Rich JN, Reardon DA, Peery T, Dowell JM, Quinn JA, Penne KL, Wikstrand CJ, Van Duyn LB, Dancey JE, McLendon RE, Kao JC, Stenzel TT, Ahmed Rasheed BK, Tourt-Uhlig SE, Herndon JE, 2nd, Vredenburgh JJ, Sampson JH, Friedman AH, Bigner DD, Friedman HS (2004) Phase II trial of gefitinib in recurrent glioblastoma. J Clin Oncol 22:133-142. doi:10.1200/JCO.2004.08.110

Roder C, Bisdas S, Ebner FH, Honegger J, Naegele T, Ernemann U, Tatagiba M (2014) Maximizing the extent of resection and survival benefit of patients in glioblastoma surgery: high-field iMRI versus conventional and 5-ALA-assisted surgery. Eur J Surg Oncol 40:297-304. doi:10.1016/j.ejso.2013.11.022

Roos A, Ding Z, Loftus JC, Tran NL (2017) Molecular and Microenvironmental Determinants of Glioma Stem-Like Cell Survival and Invasion. Front Oncol 7:120. doi:10.3389/fonc.2017.00120

Salpietro V, Mankad K, Kinali M, Adams A, Valenzise M, Tortorella G, Gitto E, Polizzi A, Chirico V, Nicita F, David E, Romeo AC, Squeri CA, Savasta S, Marseglia GL, Arrigo T, Johanson CE, Ruggieri M (2014) Pediatric idiopathic intracranial hypertension and the underlying endocrine-metabolic dysfunction: a pilot study. J Pediatr Endocrinol Metab 27:107-115. doi:10.1515/jpem-2013-0156

Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32:347-355. doi:10.1038/nbt.2842

Savasta S, Chiapedi S, Perrini S, Tognato E, Corsano L, Chiara A (2008) Pai syndrome: a further report of a case with bifid nose, lipoma, and agenesis of the corpus callosum. Childs Nerv Syst 24:773-776. doi:10.1007/s00381-008-0613-9

Schmidt F, Fischer J, Herrlinger U, Dietz K, Dichgans J, Weller M (2006) PCV chemotherapy for recurrent glioblastoma. Neurology 66:587-589. doi:10.1212/01.wnl.0000197792.73656.c2

Staflin K, Honeth G, Kalliomaki S, Kjellman C, Edvardsen K, Lindvall M (2004) Neural progenitor cell lines inhibit rat tumor growth in vivo. Cancer Res 64:5347-5354. doi:10.1158/0008-5472.CAN-03-1246

Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ, Group AL-GS (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392-401. doi:10.1016/S1470-2045(06)70665-9

Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiation Oncology G, National Cancer Institute of Canada Clinical Trials G (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459-466. doi:10.1016/S1470-2045(09)70025-7

Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiotherapy G, National Cancer Institute of Canada Clinical Trials G (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996. doi:10.1056/NEJMoa043330

Tang B, Wu W, Wei X, Li Y, Ren G, Fan W (2014) Activation of glioma cells generates immune tolerant NKT cells. J Biol Chem 289:34595-34600. doi:10.1074/jbc.M114.614503

Trask TW, Trask RP, Aguilar-Cordova E, Shine HD, Wyde PR, Goodman JC, Hamilton WJ, Rojas-Martinez A, Chen SH, Woo SL, Grossman RG (2000) Phase I study of adenoviral delivery of the HSV-tk gene and ganciclovir administration in patients with current malignant brain tumors. Mol Ther 1:195-203. doi:10.1006/mthe.2000.0030

Villa A, Navarro-Galve B, Bueno C, Franco S, Blasco MA, Martinez-Serrano A (2004) Long-term molecular and cellular stability of human neural stem cell lines. Exp Cell Res 294:559-570. doi:10.1016/j.yexcr.2003.11.025

Wang Y, Pan L, Sheng XF, Chen S, Dai JZ (2016) Nimotuzumab, a humanized monoclonal antibody specific for the EGFR, in combination with temozolomide and radiation therapy for newly diagnosed glioblastoma multiforme: First results in Chinese patients. Asia Pac J Clin Oncol 12:e23-29. doi:10.1111/ajco.12166

Weinmann L, Wischhusen J, Demma MJ, Naumann U, Roth P, Dasmahapatra B, Weller M (2008) A novel p53 rescue compound induces p53-dependent growth arrest and sensitises glioma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ 15:718-729. doi:10.1038/sj.cdd.4402301

Weller M, Butowski N, Tran DD, Recht LD, Lim M, Hirte H, Ashby L, Mechtler L, Goldlust SA, Iwamoto F, Drappatz J, O'Rourke DM, Wong M, Hamilton MG, Finocchiaro G, Perry J, Wick W, Green J, He Y, Turner CD, Yellin MJ, Keler T, Davis TA, Stupp R, Sampson JH, investigators AIt (2017) Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial. Lancet Oncol 18:1373-1385. doi:10.1016/S1470-2045(17)30517-X

Wen PY, Kesari S (2008) Malignant gliomas in adults. N Engl J Med 359:492-507. doi:10.1056/NEJMra0708126

Wen PY, Touat M, Alexander BM, Mellinghoff IK, Ramkissoon S, McCluskey CS, Pelton K, Haidar S, Basu SS, Gaffey SC, Brown LE, Martinez-Ledesma JE, Wu S, Kim J, Wei W, Park MA, Huse JT, Kuhn JG, Rinne ML, Colman H, Agar NYR, Omuro AM, DeAngelis LM, Gilbert MR, de Groot JF, Cloughesy TF, Chi AS, Roberts TM, Zhao JJ, Lee EQ, Nayak L, Heath JR, Horky LL, Batchelor TT, Beroukhim R, Chang SM, Ligon AH, Dunn IF, Koul D, Young GS, Prados MD, Reardon DA, Yung WKA, Ligon KL (2019) Buparlisib in Patients With Recurrent Glioblastoma Harboring Phosphatidylinositol 3-Kinase Pathway Activation: An Open-Label, Multicenter, Multi-Arm, Phase II Trial. J Clin Oncol 37:741-750. doi:10.1200/JCO.18.01207

Wenger A, Werlenius K, Hallner A, Thoren FB, Farahmand D, Tisell M, Smits A, Rydenhag B, Jakola AS, Caren H (2018) Determinants for Effective ALECSAT Immunotherapy Treatment on Autologous Patient-Derived Glioblastoma Stem Cells. Neoplasia 20:25-31. doi:10.1016/j.neo.2017.10.006

Wick W, Gorlia T, Bady P, Platten M, van den Bent MJ, Taphoorn MJ, Steuve J, Brandes AA, Hamou MF, Wick A, Kosch M, Weller M, Stupp R, Roth P, Golfinopoulos V, Frenel JS, Campone M, Ricard D, Marosi C, Villa S, Weyerbrock A, Hopkins K, Homicsko K, Lhermitte B, Pesce G, Hegi ME (2016) 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 22:4797-4806. doi:10.1158/1078-0432.CCR-15-3153

Wintterle S, Schreiner B, Mitsdoerffer M, Schneider D, Chen L, Meyermann R, Weller M, Wiendl H (2003) Expression of the B7-related molecule B7-H1 by glioma cells: a potential mechanism of immune paralysis. Cancer Res 63:7462-7467

Wood AJ, Lo TW, Zeitler B, Pickle CS, Ralston EJ, Lee AH, Amora R, Miller JC, Leung E, Meng X, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Meyer BJ (2011) Targeted genome editing across species using ZFNs and TALENs. Science 333:307. doi:10.1126/science.1207773

Yu W, Zhang L, Wei Q, Shao A (2019) O(6)-Methylguanine-DNA Methyltransferase (MGMT): Challenges and New Opportunities in Glioma Chemotherapy. Front Oncol 9:1547. doi:10.3389/fonc.2019.01547

Yvon ES, Burga R, Powell A, Cruz CR, Fernandes R, Barese C, Nguyen T, Abdel-Baki MS, Bollard CM (2017) Cord blood natural killer cells expressing a dominant negative TGF-beta receptor: Implications for adoptive immunotherapy for glioblastoma. Cytotherapy 19:408-418. doi:10.1016/j.jcyt.2016.12.005

Zhai L, Ladomersky E, Lauing KL, Wu M, Genet M, Gritsina G, Gyorffy B, Brastianos PK, Binder DC, Sosman JA, Giles FJ, James CD, Horbinski C, Stupp R, Wainwright DA (2017) Infiltrating T Cells Increase IDO1 Expression in Glioblastoma and Contribute to Decreased Patient Survival. Clin Cancer Res 23:6650-6660. doi:10.1158/1078-0432.CCR-17-0120

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30-06-2020

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1.
Giotta Lucifero A, Luzzi S, Brambilla I, Trabatti C, Mosconi M, Savasta S, et al. Innovative therapies for malignant brain tumors: the road to a tailored cure. Acta Biomed [Internet]. 2020 Jun. 30 [cited 2024 Jul. 27];91(7-S):5-17. Available from: https://www.mattioli1885journals.com/index.php/actabiomedica/article/view/9951