431
Views
23
CrossRef citations to date
0
Altmetric
Review

Immunotherapy for Medulloblastoma: Current Perspectives

, , &
Pages 57-77 | Published online: 20 Apr 2020

References

  • Pollack IF, Agnihotri S, Broniscer A. Childhood brain tumors: current management, biological insights, and future directions. J Neurosurg Pediatr. 2019;23(3):261–273. doi:10.3171/2018.10.PEDS1837730835699
  • Sonabend AM, Ogden AT, Maier LM, et al. Medulloblasoma: challenges for effective immunotherapy. J Neurooncol. 2012;108(1):1–10. doi:10.1007/s11060-011-0776-122173741
  • Thurnher MM. 2007 World Health Organization classification of tumours of the central nervous system. Cancer Imaging. 2009;9(Spec No A):S1–S3. doi:10.1102/1470-7330.2009.9001
  • Archer TC, Mahoney EL, Pomeroy SL. Medulloblastoma: molecular classification-based personal therapeutics. Neurotherapeutics. 2017;14(2):265–273. doi:10.1007/s13311-017-0526-y28386677
  • Packer RJ, Finlay JL. Chemotherapy for childhood medulloblastoma and primitive neuroectodermal tumors. Oncologist. 1996;1(6):381–393. doi:10.1634/theoncologist.1-6-38110388020
  • Ostrom QT, Cioffi G, Gittleman H, et al. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2012–2016. Neuro Oncol. 2019;21(Supplement_5):v1–v100. doi:10.1093/neuonc/noz15031675094
  • Zeltzer PM, Boyett JM, Finlay JL, et al. Metastasis stage, adjuvant treatment, and residual tumor are prognostic factors for medulloblastoma in children: conclusions from the children’s cancer group 921 randomized phase III study. J Clin Oncol. 1999;17(3):832–845. doi:10.1200/JCO.1999.17.3.83210071274
  • Ris MD, Packer R, Goldwein J, Jones-Wallace D, Boyett JM. Intellectual outcome after reduced-dose radiation therapy plus adjuvant chemotherapy for medulloblastoma: a children’s cancer group study. J Clin Oncol. 2001;19(15):3470–3476. doi:10.1200/JCO.2001.19.15.347011481352
  • Taylor RE, Bailey CC, Robinson K, et al. Results of a randomized study of preradiation chemotherapy versus radiotherapy alone for nonmetastatic medulloblastoma: the International Society of Paediatric Oncology/United Kingdom children’s cancer study group PNET-3 study. J Clin Oncol. 2003;21(8):1581–1591. doi:10.1200/JCO.2003.05.11612697884
  • Sayour EJ, Mitchell DA. Immunotherapy for pediatric brain tumors. Brain Sci. 2017;7(10)137.
  • Louis DN, Perry A, Reifenberger G, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–820. doi:10.1007/s00401-016-1545-127157931
  • Cavalli FMG, Remke M, Rampasek L, et al. Intertumoral heterogeneity within medulloblastoma subgroups. Cancer Cell. 2017;31(6):737–754 e736. doi:10.1016/j.ccell.2017.05.00528609654
  • Gibson P, Tong Y, Robinson G, et al. Subtypes of medulloblastoma have distinct developmental origins. Nature. 2010;468(7327):1095–1099. doi:10.1038/nature0958721150899
  • Grammel D, Warmuth-Metz M, von Bueren AO, et al. Sonic hedgehog-associated medulloblastoma arising from the cochlear nuclei of the brainstem. Acta Neuropathol. 2012;123(4):601–614. doi:10.1007/s00401-012-0961-022349907
  • Hooper CM, Hawes SM, Kees UR, Gottardo NG, Dallas PB, Alsina B. Gene expression analyses of the spatio-temporal relationships of human medulloblastoma subgroups during early human neurogenesis. PLoS One. 2014;9(11):e112909. doi:10.1371/journal.pone.011290925412507
  • Northcott PA, Jones DT, Kool M, et al. Medulloblastomics: the end of the beginning. Nat Rev Cancer. 2012;12(12):818–834. doi:10.1038/nrc341023175120
  • Taylor MD, Northcott PA, Korshunov A, et al. Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol. 2012;123(4):465–472. doi:10.1007/s00401-011-0922-z22134537
  • Wood GW, Morantz RA. In vitro reversal of depressed T-lymphocyte function in the peripheral blood of brain tumor patients. J Natl Cancer Inst. 1982;68(1):27–33.6172627
  • Wood GW, Morantz RA. Depressed T lymphocyte function in brain tumor patients: monocytes as suppressor cells. J Neurooncol. 1983;1(2):87–94. doi:10.1007/BF001829536236289
  • Yamasaki T, Handa H, Yamashita J, Namba Y, Hanaoka M. Characteristic immunological responses to an experimental mouse brain tumor. Cancer Res. 1983;43(10):4610–4617.6603902
  • Gerosa M, Amadori G, Semenzato C, et al. Immunobiology of paediatric intracranial tumours. A preliminary report. Acta Neurochir (Wien). 1979;50(1–2):49–54. doi:10.1007/BF01813548316267
  • Gerosa MA, Amadori G, Semenzato P, Gasparotto G, Carteri A. Immunobiology of primary CNS tumors in infancy and childhood. B- and T-cell dependent immunity and cytotoxicity and cell kinetic evaluation. Childs Brain. 1980;6(2):92–102. doi:10.1159/0001198906965475
  • Mitchell DA, Cui X, Schmittling RJ, et al. Monoclonal antibody blockade of IL-2 receptor α during lymphopenia selectively depletes regulatory T cells in mice and humans. Blood. 2011;118(11):3003–3012. doi:10.1182/blood-2011-02-33456521768296
  • Mitchell DA, Batich KA, Gunn MD, et al. Tetanus toxoid and CCL3 improve dendritic cell vaccines in mice and glioblastoma patients. Nature. 2015;519(7543):366–369. doi:10.1038/nature1432025762141
  • Batich KA, Swartz AM, Sampson JH. Preconditioning vaccine sites for mRNA-transfected dendritic cell therapy and antitumor efficacy. Methods Mol Biol. 2016;1403:819–838.27076169
  • Sampson JH, Maus MV, June CH. Immunotherapy for brain tumors. J Clin Oncol. 2017;35(21):2450–2456. doi:10.1200/JCO.2017.72.808928640704
  • Hao C, Tian J, Liu H, Li F, Niu H, Zhu B. Efficacy and safety of anti-PD-1 and anti-PD-1 combined with anti-CTLA-4 immunotherapy to advanced melanoma: a systematic review and meta-analysis of randomized controlled trials. Medicine (Baltimore). 2017;96(26):e7325. doi:10.1097/MD.000000000000732528658143
  • Alizadeh AA, Aranda V, Bardelli A, et al. Toward understanding and exploiting tumor heterogeneity. Nat Med. 2015;21(8):846–853. doi:10.1038/nm.391526248267
  • Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature. 2013;500(7463):415–421. doi:10.1038/nature1247723945592
  • Fontebasso AM, Gayden T, Nikbakht H, et al. Epigenetic dysregulation: a novel pathway of oncogenesis in pediatric brain tumors. Acta Neuropathol. 2014;128(5):615–627. doi:10.1007/s00401-014-1325-825077668
  • Pham CD, Flores C, Yang C, et al. Differential immune microenvironments and response to immune checkpoint blockade among molecular subtypes of murine medulloblastoma. Clin Cancer Res. 2016;22(3):582–595. doi:10.1158/1078-0432.CCR-15-071326405194
  • Schlager C, Korner H, Krueger M, et al. Effector T-cell trafficking between the leptomeninges and the cerebrospinal fluid. Nature. 2016;530(7590):349–353. doi:10.1038/nature1693926863192
  • Kipnis J. Multifaceted interactions between adaptive immunity and the central nervous system. Science. 2016;353(6301):766–771. doi:10.1126/science.aag263827540163
  • Hu X, Deng Q, Ma L, et al. Meningeal lymphatic vessels regulate brain tumor drainage and immunity. Cell Res. 2020. doi:10.1038/s41422-020-0287-8
  • Woroniecka K, Chongsathidkiet P, Rhodin K, et al. T-cell exhaustion signatures vary with tumor type and are severe in glioblastoma. Clin Cancer Res. 2018;24(17):4175–4186. doi:10.1158/1078-0432.CCR-17-184629437767
  • Weller M, Butowski N, Tran DD, 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(10):1373–1385. doi:10.1016/S1470-2045(17)30517-X28844499
  • Mueller S, Chang S. Pediatric brain tumors: current treatment strategies and future therapeutic approaches. Neurotherapeutics. 2009;6(3):570–586. doi:10.1016/j.nurt.2009.04.00619560746
  • Packer RJ, Gajjar A, Vezina G, et al. Phase III study of craniospinal radiation therapy followed by adjuvant chemotherapy for newly diagnosed average-risk medulloblastoma. J Clin Oncol. 2006;24(25):4202–4208. doi:10.1200/JCO.2006.06.498016943538
  • Merchant TE, Kun LE, Krasin MJ, et al. Multi-institution prospective trial of reduced-dose craniospinal irradiation (23.4 Gy) followed by conformal posterior fossa (36 Gy) and primary site irradiation (55.8 Gy) and dose-intensive chemotherapy for average-risk medulloblastoma. Int J Radiat Oncol Biol Phys. 2008;70(3):782–787. doi:10.1016/j.ijrobp.2007.07.234217892918
  • Gajjar A, Chintagumpala M, Ashley D, et al. Risk-adapted craniospinal radiotherapy followed by high-dose chemotherapy and stem-cell rescue in children with newly diagnosed medulloblastoma (St Jude medulloblastoma-96): long-term results from a prospective, multicentre trial. Lancet Oncol. 2006;7(10):813–820. doi:10.1016/S1470-2045(06)70867-117012043
  • Wahba HA, Abu-Hegazy M, Wasel Y, Ismail EI, Zidan AS. Adjuvant chemotherapy after reduced craniospinal irradiation dose in children with average-risk medulloblastoma: a 5-year follow-up study. J BUON. 2013;18(2):425–429.23818356
  • Packer RJ, Goldwein J, Nicholson HS, et al. Treatment of children with medulloblastomas with reduced-dose craniospinal radiation therapy and adjuvant chemotherapy: a children’s cancer group study. J Clin Oncol. 1999;17(7):2127–2136. doi:10.1200/JCO.1999.17.7.212710561268
  • Tamburrini G, Frassanito P, Chieffo D, Massimi L, Caldarelli M, Di Rocco C. Cerebellar mutism. Childs Nerv Syst. 2015;31(10):1841–1851. doi:10.1007/s00381-015-2803-626351234
  • Merchant TE, Kiehna EN, Li C, et al. Modeling radiation dosimetry to predict cognitive outcomes in pediatric patients with CNS embryonal tumors including medulloblastoma. Int J Radiat Oncol Biol Phys. 2006;65(1):210–221. doi:10.1016/j.ijrobp.2005.10.03816472938
  • Bansal LR, Belair J, Cummings D, Zuccoli G. Late-onset radiation-induced vasculopathy and stroke in a child with medulloblastoma. J Child Neurol. 2015;30(6):800–802. doi:10.1177/088307381453850125015672
  • Benson PJ, Sung JH. Cerebral aneurysms following radiotherapy for medulloblastoma. J Neurosurg. 1989;70(4):545–550. doi:10.3171/jns.1989.70.4.05452926494
  • Neglia JP, Robison LL, Stovall M, et al. New primary neoplasms of the central nervous system in survivors of childhood cancer: a report from the childhood cancer survivor study. J Natl Cancer Inst. 2006;98(21):1528–1537. doi:10.1093/jnci/djj41117077355
  • Ullrich NJ, Pomeroy SL. Molecular genetics of pediatric central nervous system tumors. Curr Oncol Rep. 2006;8(6):423–429. doi:10.1007/s11912-006-0070-017040620
  • Wang X, Dubuc AM, Ramaswamy V, et al. Medulloblastoma subgroups remain stable across primary and metastatic compartments. Acta Neuropathol. 2015;129(3):449–457. doi:10.1007/s00401-015-1389-025689980
  • Morrissy AS, Garzia L, Shih DJ, et al. Divergent clonal selection dominates medulloblastoma at recurrence. Nature. 2016;529(7586):351–357. doi:10.1038/nature1647826760213
  • Wang J, Garancher A, Ramaswamy V, Wechsler-Reya RJ. Medulloblastoma: from molecular subgroups to molecular targeted therapies. Annu Rev Neurosci. 2018;41(1):207–232. doi:10.1146/annurev-neuro-070815-01383829641939
  • Das A, McDonald D, Lowe S, et al. Immunological low-dose radiation modulates the pediatric medulloblastoma antigens and enhances antibody-dependent cellular cytotoxicity. Childs Nerv Syst. 2017;33(3):429–436. doi:10.1007/s00381-016-3305-x27942918
  • Li K, Duan WC, Zhao HB, et al. Preoperative neutrophil to lymphocyte ratio and platelet to lymphocyte ratio are associated with the prognosis of group 3 and group 4 medulloblastoma. Sci Rep. 2019;9(1):13239. doi:10.1038/s41598-019-49733-631519974
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi:10.1016/j.cell.2011.02.01321376230
  • Jahnisch H, Fussel S, Kiessling A, et al. Dendritic cell-based immunotherapy for prostate cancer. Clin Dev Immunol. 2010;2010:517493. doi:10.1155/2010/51749321076523
  • Wang SS, Bandopadhayay P, Jenkins MR. Towards immunotherapy for pediatric brain tumors. Trends Immunol. 2019;40(8):748–761. doi:10.1016/j.it.2019.05.00931229353
  • Kantoff PW, Higano CS, Shore ND, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363(5):411–422. doi:10.1056/NEJMoa100129420818862
  • Holtkamp S, Kreiter S, Selmi A, et al. Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood. 2006;108(13):4009–4017. doi:10.1182/blood-2006-04-01502416940422
  • Kranz LM, Diken M, Haas H, et al. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature. 2016;534(7607):396–401. doi:10.1038/nature1830027281205
  • Kreiter S, Selmi A, Diken M, et al. Intranodal vaccination with naked antigen-encoding RNA elicits potent prophylactic and therapeutic antitumoral immunity. Cancer Res. 2010;70(22):9031–9040. doi:10.1158/0008-5472.CAN-10-069921045153
  • Coban C, Kobiyama K, Aoshi T, et al. Novel strategies to improve DNA vaccine immunogenicity. Curr Gene Ther. 2011;11(6):479–484. doi:10.2174/15665231179819281522023477
  • Nair SK, Driscoll T, Boczkowski D, et al. Ex vivo generation of dendritic cells from cryopreserved, post-induction chemotherapy, mobilized leukapheresis from pediatric patients with medulloblastoma. J Neurooncol. 2015;125(1):65–74. doi:10.1007/s11060-015-1890-226311248
  • Majd N, Penas-Prado M. Updates on management of adult medulloblastoma. Curr Treat Options Oncol. 2019;20(8):64. doi:10.1007/s11864-019-0663-031236711
  • Ardon H, De Vleeschouwer S, Van Calenbergh F, et al. Adjuvant dendritic cell-based tumour vaccination for children with malignant brain tumours. Pediatr Blood Cancer. 2010;54(4):519–525. doi:10.1002/pbc.2231919852061
  • Sampson JH, Archer GE, Mitchell DA, 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(10):2773–2779. doi:10.1158/1535-7163.MCT-09-012419825799
  • Kim W, Liau LM. Dendritic cell vaccines for brain tumors. Neurosurg Clin N Am. 2010;21(1):139–157. doi:10.1016/j.nec.2009.09.00519944973
  • Liau LM, Black KL, Martin NA, et al. Treatment of a patient by vaccination with autologous dendritic cells pulsed with allogeneic major histocompatibility complex class I-matched tumor peptides: case report. Neurosurg Focus. 2000;9(6):e8. doi:10.3171/foc.2000.9.6.9
  • Liau LM, Prins RM, Kiertscher SM, et al. 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. doi:10.1158/1078-0432.CCR-05-046416061868
  • Heimberger AB, Archer GE, Crotty LE, et al. Dendritic cells pulsed with a tumor-specific peptide induce long-lasting immunity and are effective against murine intracerebral melanoma. Neurosurgery. 2002;50(1):158–164; discussion 164–156. doi:10.1097/00006123-200201000-00024
  • Felsberg J, Hentschel B, Kaulich K, et al. 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. doi:10.1158/1078-0432.CCR-17-089028855349
  • van den Bent MJ, Gao Y, Kerkhof M, et al. Changes in the EGFR amplification and EGFRvIII expression between paired primary and recurrent glioblastomas. Neuro Oncol. 2015;17(7):935–941. doi:10.1093/neuonc/nov01325691693
  • Aurelian L. Oncolytic viruses as immunotherapy: progress and remaining challenges. Onco Targets Ther. 2016;9:2627–2637. doi:10.2147/OTT.S6304927226725
  • Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discov. 2015;14(9):642–662. doi:10.1038/nrd466326323545
  • Killock D. Skin cancer: T-VEC oncolytic viral therapy shows promise in melanoma. Nat Rev Clin Oncol. 2015;12(8):438. doi:10.1038/nrclinonc.2015.10626077044
  • Kohlhapp FJ, Kaufman HL. Molecular pathways: mechanism of action for talimogene laherparepvec, a new oncolytic virus immunotherapy. Clin Cancer Res. 2016;22(5):1048–1054. doi:10.1158/1078-0432.CCR-15-266726719429
  • Kanerva A, Nokisalmi P, Diaconu I, et al. Antiviral and antitumor T-cell immunity in patients treated with GM-CSF-coding oncolytic adenovirus. Clin Cancer Res. 2013;19(10):2734–2744. doi:10.1158/1078-0432.CCR-12-254623493351
  • Yu YA, Galanis C, Woo Y, et al. Regression of human pancreatic tumor xenografts in mice after a single systemic injection of recombinant vaccinia virus GLV-1h68. Mol Cancer Ther. 2009;8(1):141–151.19139123
  • Saha D, Martuza RL, Rabkin SD. Macrophage polarization contributes to glioblastoma eradication by combination immunovirotherapy and immune checkpoint blockade. Cancer Cell. 2017;32(2):253–267 e255. doi:10.1016/j.ccell.2017.07.00628810147
  • Lang FF, Conrad C, Gomez-Manzano C, et al. Phase I study of DNX-2401 (Delta-24-RGD) oncolytic adenovirus: replication and immunotherapeutic effects in recurrent malignant glioma. J Clin Oncol. 2018;36(14):1419–1427. doi:10.1200/JCO.2017.75.821929432077
  • Thompson EM, Brown M, Dobrikova E, et al. Poliovirus receptor (CD155) expression in pediatric brain tumors mediates oncolysis of medulloblastoma and pleomorphic xanthoastrocytoma. J Neuropathol Exp Neurol. 2018;77(8):696–702. doi:10.1093/jnen/nly04529878245
  • Hortal AM, Vermeulen JF, Van Hecke W, Bovenschen N. Oncogenic role of cytomegalovirus in medulloblastoma? Cancer Lett. 2017;408:55–59. doi:10.1016/j.canlet.2017.08.02428844716
  • Cinatl J Jr, Cinatl J, Vogel JU, Rabenau H, Kornhuber B, Doerr HW. Modulatory effects of human cytomegalovirus infection on malignant properties of cancer cells. Intervirology. 1996;39(4):259–269. doi:10.1159/0001505279078467
  • Michaelis M, Baumgarten P, Mittelbronn M, Driever PH, Doerr HW, Cinatl J Jr. Oncomodulation by human cytomegalovirus: novel clinical findings open new roads. Med Microbiol Immunol. 2011;200(1):1–5. doi:10.1007/s00430-010-0177-720967552
  • Baryawno N, Sveinbjornsson B, Eksborg S, et al. Tumor-growth-promoting cyclooxygenase-2 prostaglandin E2 pathway provides medulloblastoma therapeutic targets. Neuro Oncol. 2008;10(5):661–674. doi:10.1215/15228517-2008-03518715952
  • Taher C, Frisk G, Fuentes S, et al. High prevalence of human cytomegalovirus in brain metastases of patients with primary breast and colorectal cancers. Transl Oncol. 2014;7(6):732–740. doi:10.1016/j.tranon.2014.09.00825500083
  • Baryawno N, Rahbar A, Wolmer-Solberg N, et al. Detection of human cytomegalovirus in medulloblastomas reveals a potential therapeutic target. J Clin Invest. 2011;121(10):4043–4055. doi:10.1172/JCI5714721946257
  • Yang MY, Lee HT, Chen CM, Shen CC, Ma HI. Celecoxib suppresses the phosphorylation of STAT3 protein and can enhance the radiosensitivity of medulloblastoma-derived cancer stem-like cells. Int J Mol Sci. 2014;15(6):11013–11029. doi:10.3390/ijms15061101324945311
  • Raso A, Mascelli S, Biassoni R, et al. High levels of PROM1 (CD133) transcript are a potential predictor of poor prognosis in medulloblastoma. Neuro Oncol. 2011;13(5):500–508. doi:10.1093/neuonc/nor02221486962
  • Hwang K, Koh EJ, Choi EJ, et al. PD-1/PD-L1 and immune-related gene expression pattern in pediatric malignant brain tumors: clinical correlation with survival data in Korean population. J Neurooncol. 2018;139(2):281–291. doi:10.1007/s11060-018-2886-529730815
  • Vermeulen JF, Van Hecke W, Adriaansen EJM, et al. Prognostic relevance of tumor-infiltrating lymphocytes and immune checkpoints in pediatric medulloblastoma. Oncoimmunology. 2018;7(3):e1398877. doi:10.1080/2162402X.2017.139887729399402
  • Martin AM, Nirschl CJ, Polanczyk MJ, et al. PD-L1 expression in medulloblastoma: an evaluation by subgroup. Oncotarget. 2018;9(27):19177–19191. doi:10.18632/oncotarget.2495129721192
  • Flores CT, Wildes TJ, Drake JA, et al. Lin(-)CCR2(+) hematopoietic stem and progenitor cells overcome resistance to PD-1 blockade. Nat Commun. 2018;9(1):4313. doi:10.1038/s41467-018-06182-530333482
  • Omuro A, Vlahovic G, Lim M, et al. 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. doi:10.1093/neuonc/nox20829106665
  • Castriconi R, Dondero A, Negri F, et al. Both CD133+ and CD133– medulloblastoma cell lines express ligands for triggering NK receptors and are susceptible to NK-mediated cytotoxicity. Eur J Immunol. 2007;37(11):3190–3196. doi:10.1002/eji.20073754617918205
  • Fernandez L, Portugal R, Valentin J, et al. In vitro natural killer cell immunotherapy for medulloblastoma. Front Oncol. 2013;3:94. doi:10.3389/fonc.2013.0009423626949
  • Yvon ES, Burga R, Powell A, et al. Cord blood natural killer cells expressing a dominant negative TGF-beta receptor: implications for adoptive immunotherapy for glioblastoma. Cytotherapy. 2017;19(3):408–418. doi:10.1016/j.jcyt.2016.12.00528109751
  • Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331(6013):44–49. doi:10.1126/science.119868721212348
  • Liu D, Song L, Brawley VS, et al. Medulloblastoma expresses CD1d and can be targeted for immunotherapy with NKT cells. Clin Immunol. 2013;149(1):55–64. doi:10.1016/j.clim.2013.06.00523891738
  • George RE, Loudon WG, Moser RP, Bruner JM, Steck PA, Grimm EA. In vitro cytolysis of primitive neuroectodermal tumors of the posterior fossa (medulloblastoma) by lymphokine-activated killer cells. J Neurosurg. 1988;69(3):403–409. doi:10.3171/jns.1988.69.3.04033261328
  • Okamoto Y, Shimizu K, Tamura K, et al. An adoptive immunotherapy of patients with medulloblastoma by lymphokine-activated killer cells (LAK). Acta Neurochir (Wien). 1988;94(1–2):47–52. doi:10.1007/BF014066153177046
  • Kang SG, Ryu CH, Jeun SS, et al. Lymphokine activated killer cells from umbilical cord blood show higher antitumor effect against anaplastic astrocytoma cell line (U87) and medulloblastoma cell line (TE671) than lymphokine activated killer cells from peripheral blood. Childs Nerv Syst. 2004;20(3):154–162. doi:10.1007/s00381-003-0898-714968374
  • Shimizu H, Sasaki K, Takaue Y, Ota S, Fzjimoto T. Studies of children with acute lymphoblastic leukemia (ALL) who relapsed. Relationship of site of relapse, time and prognosis. Rinsho Ketsueki. 1989;30(7):999–1004.2810802
  • Sankhla SK, Nadkarni JS, Bhagwati SN. Adoptive immunotherapy using lymphokine-activated killer (LAK) cells and interleukin-2 for recurrent malignant primary brain tumors. J Neurooncol. 1996;27(2):133–140. doi:10.1007/BF001774768699235
  • Salmaggi A, Dufour A, Silvani A, Ciusani E, Nespolo A, Boiardi A. Immunological fluctuations during intrathecal immunotherapy in three patients affected by CNS tumours disseminating via CSF. Int J Neurosci. 1994;77(1–2):117–125. doi:10.3109/002074594089860247989157
  • Garfall AL, Maus MV, Hwang WT, et al. Chimeric antigen receptor T cells against CD19 for multiple myeloma. N Engl J Med. 2015;373(11):1040–1047. doi:10.1056/NEJMoa150454226352815
  • Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368(16):1509–1518. doi:10.1056/NEJMoa121513423527958
  • Kalos M, Levine BL, Porter DL, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3(95):95ra73. doi:10.1126/scitranslmed.3002842
  • Louis CU, Savoldo B, Dotti G, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood. 2011;118(23):6050–6056. doi:10.1182/blood-2011-05-35444921984804
  • Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507–1517. doi:10.1056/NEJMoa140722225317870
  • Porter DL, Hwang WT, Frey NV, et al. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med. 2015;7(303):303ra139. doi:10.1126/scitranslmed.aac5415
  • Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci U S A. 1989;86(24):10024–10028. doi:10.1073/pnas.86.24.100242513569
  • Sadelain M, Brentjens R, Riviere I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013;3(4):388–398. doi:10.1158/2159-8290.CD-12-054823550147
  • June CH, O’Connor RS, Kawalekar OU, Ghassemi S, Milone MC. CAR T cell immunotherapy for human cancer. Science. 2018;359(6382):1361–1365. doi:10.1126/science.aar671129567707
  • Brown CE, Alizadeh D, Starr R, et al. Regression of glioblastoma after chimeric antigen receptor T-cell therapy. N Engl J Med. 2016;375(26):2561–2569. doi:10.1056/NEJMoa161049728029927
  • Petersen CT, Krenciute G. Next generation CAR T cells for the Immunotherapy of high-grade glioma. Front Oncol. 2019;9:69. doi:10.3389/fonc.2019.0006930863720
  • Chmielewski M, Abken H. TRUCKs: the fourth generation of CARs. Expert Opin Biol Ther. 2015;15(8):1145–1154. doi:10.1517/14712598.2015.104643025985798
  • Ahmed N, Brawley V, Hegde M, et al. 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. doi:10.1001/jamaoncol.2017.018428426845
  • Nellan A, Rota C, Majzner R, et al. Durable regression of medulloblastoma after regional and intravenous delivery of anti-HER2 chimeric antigen receptor T cells. J Immunother Cancer. 2018;6(1):30. doi:10.1186/s40425-018-0340-z29712574
  • Majzner RG, Theruvath JL, Nellan A, et al. CAR T cells targeting B7-H3, a pan-cancer antigen, demonstrate potent preclinical activity against pediatric solid tumors and brain tumors. Clin Cancer Res. 2019;25(8):2560–2574. doi:10.1158/1078-0432.CCR-18-043230655315
  • Tasian SK, Gardner RA. CD19-redirected chimeric antigen receptor-modified T cells: a promising immunotherapy for children and adults with B-cell acute lymphoblastic leukemia (ALL). Ther Adv Hematol. 2015;6(5):228–241. doi:10.1177/204062071558891626425336
  • Bielamowicz K, Fousek K, Byrd TT, et al. Trivalent CAR T cells overcome interpatient antigenic variability in glioblastoma. Neuro Oncol. 2018;20(4):506–518. doi:10.1093/neuonc/nox18229016929
  • Davila ML, Riviere I, Wang X, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med. 2014;6(224):224ra225. doi:10.1126/scitranslmed.3008226
  • Lee DW, Kochenderfer JN, Stetler-Stevenson M, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet. 2015;385(9967):517–528. doi:10.1016/S0140-6736(14)61403-325319501
  • Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378(5):439–448. doi:10.1056/NEJMoa170986629385370
  • Reits EA, Hodge JW, Herberts CA, et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med. 2006;203(5):1259–1271. doi:10.1084/jem.2005249416636135
  • Vermeer DW, Spanos WC, Vermeer PD, Bruns AM, Lee KM, Lee JH. Radiation-induced loss of cell surface CD47 enhances immune-mediated clearance of human papillomavirus-positive cancer. Int J Cancer. 2013;133(1):120–129. doi:10.1002/ijc.2801523292955
  • Qian JM, Yu JB, Kluger HM, Chiang VL. Timing and type of immune checkpoint therapy affect the early radiographic response of melanoma brain metastases to stereotactic radiosurgery. Cancer. 2016;122(19):3051–3058. doi:10.1002/cncr.3013827285122
  • Antonia SJ, Villegas A, Daniel D, et al. Durvalumab after chemoradiotherapy in stage iii non-small-cell lung cancer. N Engl J Med. 2017;377(20):1919–1929. doi:10.1056/NEJMoa170993728885881
  • Shaverdian N, Lisberg AE, Bornazyan K, et al. Previous radiotherapy and the clinical activity and toxicity of pembrolizumab in the treatment of non-small-cell lung cancer: a secondary analysis of the KEYNOTE-001 phase 1 trial. Lancet Oncol. 2017;18(7):895–903. doi:10.1016/S1470-2045(17)30380-728551359
  • Blaeschke F, Paul MC, Schuhmann MU, et al. Low mutational load in pediatric medulloblastoma still translates into neoantigens as targets for specific T-cell immunotherapy. Cytotherapy. 2019;21(9):973–986. doi:10.1016/j.jcyt.2019.06.00931351799
  • Hashimoto Y, Penas-Prado M, Zhou S, et al. Rethinking medulloblastoma from a targeted therapeutics perspective. J Neurooncol. 2018;139(3):713–720. doi:10.1007/s11060-018-2917-229869738
  • Orlando D, Miele E, De Angelis B, et al. Adoptive immunotherapy using PRAME-specific T cells in medulloblastoma. Cancer Res. 2018;78(12):3337–3349. doi:10.1158/0008-5472.CAN-17-314029615432
  • Vulcani-Freitas TM, Saba-Silva N, Cappellano A, Cavalheiro S, Toledo SR. PRAME gene expression profile in medulloblastoma. Arq Neuropsiquiatr. 2011;69(1):9–12. doi:10.1590/S0004-282X201100010000321359415
  • Kasuga C, Nakahara Y, Ueda S, et al. Expression of MAGE and GAGE genes in medulloblastoma and modulation of resistance to chemotherapy. Laboratory investigation. J Neurosurg Pediatr. 2008;1(4):305–313. doi:10.3171/PED/2008/1/4/30518377306
  • Oba-Shinjo SM, Caballero OL, Jungbluth AA, et al. Cancer-testis (CT) antigen expression in medulloblastoma. Cancer Immun. 2008;8:7.18426187
  • Atanackovic D, Altorki NK, Stockert E, et al. Vaccine-induced CD4+ T cell responses to MAGE-3 protein in lung cancer patients. J Immunol. 2004;172(5):3289–3296. doi:10.4049/jimmunol.172.5.328914978137
  • Kim SH, Castro F, Gonzalez D, Maciag PC, Paterson Y, Gravekamp C. Mage-b vaccine delivered by recombinant listeria monocytogenes is highly effective against breast cancer metastases. Br J Cancer. 2008;99(5):741–749. doi:10.1038/sj.bjc.660452618728665
  • Sypniewska RK, Hoflack L, Tarango M, et al. Prevention of metastases with a mage-b DNA vaccine in a mouse breast tumor model: potential for breast cancer therapy. Breast Cancer Res Treat. 2005;91(1):19–28. doi:10.1007/s10549-004-6454-715868428
  • Toh HC, Wang WW, Chia WK, et al. Clinical benefit of allogeneic melanoma cell lysate-pulsed autologous dendritic cell vaccine in MAGE-positive colorectal cancer patients. Clin Cancer Res. 2009;15(24):7726–7736. doi:10.1158/1078-0432.CCR-09-153719996212
  • Gholamin S, Mitra SS, Feroze AH, et al. Disrupting the CD47-SIRPalpha anti-phagocytic axis by a humanized anti-CD47 antibody is an efficacious treatment for malignant pediatric brain tumors. Sci Transl Med. 2017;9(381). doi:10.1126/scitranslmed.aaf2968
  • Snuderl M, Batista A, Kirkpatrick ND, et al. Targeting placental growth factor/neuropilin 1 pathway inhibits growth and spread of medulloblastoma. Cell. 2013;152(5):1065–1076. doi:10.1016/j.cell.2013.01.03623452854
  • Xu J, Erdreich-Epstein A, Gonzalez-Gomez I, et al. Novel cell lines established from pediatric brain tumors. J Neurooncol. 2012;107(2):269–280. doi:10.1007/s11060-011-0756-522120608
  • Wei SC, Duffy CR, Allison JP. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 2018;8(9):1069–1086. doi:10.1158/2159-8290.CD-18-036730115704
  • Weiss WA, Burns MJ, Hackett C, et al. Genetic determinants of malignancy in a mouse model for oligodendroglioma. Cancer Res. 2003;63(7):1589–1595.12670909
  • Pardridge WM. Brain drug development and brain drug targeting. Pharm Res. 2007;24(9):1729–1732. doi:10.1007/s11095-007-9387-017629776
  • Filley AC, Henriquez M, Dey M. Recurrent glioma clinical trial, CheckMate-143: the game is not over yet. Oncotarget. 2017;8(53):91779–91794. doi:10.18632/oncotarget.2158629207684
  • Margolin K, Ernstoff MS, Hamid O, et al. Ipilimumab in patients with melanoma and brain metastases: an open-label, Phase 2 trial. Lancet Oncol. 2012;13(5):459–465. doi:10.1016/S1470-2045(12)70090-622456429
  • Goldberg SB, Gettinger SN, Mahajan A, et al. Pembrolizumab for patients with melanoma or non-small-cell lung cancer and untreated brain metastases: early analysis of a non-randomised, open-label, phase 2 trial. Lancet Oncol. 2016;17(7):976–983. doi:10.1016/S1470-2045(16)30053-527267608
  • Tiwary S, Morales JE, Kwiatkowski SC, Lang FF, Rao G, McCarty JH. Metastatic brain tumors disrupt the blood-brain barrier and alter lipid metabolism by inhibiting expression of the endothelial cell fatty acid transporter Mfsd2a. Sci Rep. 2018;8(1):8267. doi:10.1038/s41598-018-26636-629844613
  • Razpotnik R, Novak N, Curin Serbec V, Rajcevic U. Targeting malignant brain tumors with antibodies. Front Immunol. 2017;8:1181. doi:10.3389/fimmu.2017.0118128993773
  • Regina A, Demeule M, Tripathy S, et al. ANG4043, a novel brain-penetrant peptide-mAb conjugate, is efficacious against HER2-positive intracranial tumors in mice. Mol Cancer Ther. 2015;14(1):129–140. doi:10.1158/1535-7163.MCT-14-039925492620