Preclinical And Clinical Development Of Oncolytic Adenovirus For The Treatment Of Malignant Glioma

References

• Louis D, von Deimling A, Cavenee W 1. Disffuse astrocytic and oligodendroglial tumors. WHO classifivation of tumours of the central nervous system Revised 4th IARC; 2016; Lyon, France:15–78.
   Google Scholar
• Stupp R, Mason WP, van Den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–996. doi:10.1056/NEJMoa04333015758009
   PubMed Web of Science ®Google Scholar
• Larson C, Oronsky B, Scicinski J, et al. Going viral: a review of replication-selective oncolytic adenoviruses. Oncotarget. 2015;6(24):19976–19989. doi:10.18632/oncotarget.511626280277
   PubMed Web of Science ®Google Scholar
• Kelly E, Russell SJ. History of oncolytic viruses: genesis to genetic engineering. Mol Ther. 2007;15(4):651–659. doi:10.1038/sj.mt.630010817299401
   PubMed Web of Science ®Google Scholar
• Alemany R. Viruses in cancer treatment. Clin Transl Oncol. 2013;15(3):182–188. doi:10.1007/s12094-012-0951-723143950
   PubMed Web of Science ®Google Scholar
• Bell J, McFadden G. Viruses for tumor therapy. Cell Host Microbe. 2014;15(3):260–265. doi:10.1016/j.chom.2014.01.00224629333
   PubMed Web of Science ®Google Scholar
• Andtbacka RH, Kaufman HL, Collichio F, et al. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol. 2015;33(25):2780–2788. doi:10.1200/JCO.2014.58.337726014293
   PubMed Web of Science ®Google Scholar
• Cervera-Carrascon V, Havunen R, Hemminki A. Oncolytic adenoviruses: a game changer approach in the battle between cancer and the immune system. Expert Opin Biol Ther. 2019;19(5):443–455. doi:10.1080/14712598.2019.159558230905206
   PubMed Web of Science ®Google Scholar
• Alemany R. Oncolytic adenoviruses in cancer treatment. Biomedicines. 2014;2(1):36–49. doi:10.3390/biomedicines201003628548059
   PubMedGoogle Scholar
• Niemann J, Kuhnel F. Oncolytic viruses: adenoviruses. Virus Genes. 2017;53(5):700–706. doi:10.1007/s11262-017-1488-128702840
   PubMed Web of Science ®Google Scholar
• Baker AT, Aguirre-Hernandez C, Hallden G, Parker AL. Designer oncolytic adenovirus: coming of age. Cancers (Basel). 2018;10(6). doi:10.3390/cancers10110400
   Web of Science ®Google Scholar
• Bischoff JR, Kirn DH, Williams A, et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science. 1996;274(5286):373–376. doi:10.1126/science.274.5286.3738832876
   PubMed Web of Science ®Google Scholar
• Edwards SJ, Dix BR, Myers CJ, et al. Evidence that replication of the antitumor adenovirus ONYX-015 is not controlled by the p53 and p14(ARF) tumor suppressor genes. J Virol. 2002;76(24):12483–12490. doi:10.1128/jvi.76.24.12483-12490.200212438574
   PubMed Web of Science ®Google Scholar
• Rothmann T, Hengstermann A, Whitaker NJ, Scheffner M, Zur Hausen H. Replication of ONYX-015, a potential anticancer adenovirus, is independent of p53 status in tumor cells. J Virol. 1998;72(12):9470–9478.9811680
   PubMed Web of Science ®Google Scholar
• Geoerger B, Grill J, Opolon P, et al. Oncolytic activity of the E1B-55 kDa-deleted adenovirus ONYX-015 is independent of cellular p53 status in human malignant glioma xenografts. Cancer Res. 2002;62(3):764–772.11830531
   PubMed Web of Science ®Google Scholar
• O’Shea CC, Johnson L, Bagus B, et al. Late viral RNA export, rather than p53 inactivation, determines ONYX-015 tumor selectivity. Cancer Cell. 2004;6(6):611–623. doi:10.1016/j.ccr.2004.11.01215607965
   PubMed Web of Science ®Google Scholar
• O’Shea CC, Soria C, Bagus B, McCormick F. Heat shock phenocopies E1B-55K late functions and selectively sensitizes refractory tumor cells to ONYX-015 oncolytic viral therapy. Cancer Cell. 2005;8(1):61–74. doi:10.1016/j.ccr.2005.06.00916023599
   PubMed Web of Science ®Google Scholar
• Chiocca EA, Abbed KM, Tatter S, et al. A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther. 2004;10(5):958–966. doi:10.1016/j.ymthe.2004.07.02115509513
   PubMed Web of Science ®Google Scholar
• Kirn D. Clinical research results with dl1520 (Onyx-015), a replication-selective adenovirus for the treatment of cancer: what have we learned? Gene Ther. 2001;8(2):89–98. doi:10.1038/sj.gt.330137711313778
   PubMed Web of Science ®Google Scholar
• Wildner O. Clinical trials: the sensitizing side of Onyx-015. Gene Ther. 2005;12(5):386–387.19202637
   PubMed Web of Science ®Google Scholar
• Xia ZJ, Chang JH, Zhang L, et al. Phase III randomized clinical trial of intratumoral injection of E1B gene-deleted adenovirus (H101) combined with cisplatin-based chemotherapy in treating squamous cell cancer of head and neck or esophagus (Article in Chinese). Ai Zheng. 2004;23(12):1666–1670.15601557
   PubMedGoogle Scholar
• Garber K. China approves world’s first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst. 2006;98(5):298–300. doi:10.1093/jnci/djj11116507823
   PubMedGoogle Scholar
• Fueyo J, Gomez-Manzano C, Alemany R, et al. A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene. 2000;19(1):2–12. doi:10.1038/sj.onc.120325110644974
   PubMed Web of Science ®Google Scholar
• Nevins JR. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science. 1992;258(5081):424–429. doi:10.1126/science.14115351411535
   PubMed Web of Science ®Google Scholar
• Heise C, Hermiston T, Johnson L, et al. An adenovirus E1A mutant that demonstrates potent and selective systemic anti-tumoral efficacy. Nat Med. 2000;6(10):1134–1139. doi:10.1038/8047411017145
   PubMed Web of Science ®Google Scholar
• Reeh M, Bockhorn M, Gorgens D, et al. Presence of the coxsackievirus and adenovirus receptor (CAR) in human neoplasms: a multitumour array analysis. Br J Cancer. 2013;109(7):1848–1858. doi:10.1038/bjc.2013.50924022195
   PubMed Web of Science ®Google Scholar
• Miller CR, Buchsbaum DJ, Reynolds PN, et al. Differential susceptibility of primary and established human glioma cells to adenovirus infection: targeting via the epidermal growth factor receptor achieves fiber receptor-independent gene transfer. Cancer Res. 1998;58(24):5738–5748.9865732
   PubMed Web of Science ®Google Scholar
• Fuxe J, Liu L, Malin S, Philipson L, Collins VP, Pettersson RF. Expression of the coxsackie and adenovirus receptor in human astrocytic tumors and xenografts. Int J Cancer. 2003;103(6):723–729. doi:10.1002/ijc.1089112516090
   PubMed Web of Science ®Google Scholar
• Suzuki K, Fueyo J, Krasnykh V, Reynolds PN, Curiel DT, Alemany R. A conditionally replicative adenovirus with enhanced infectivity shows improved oncolytic potency. Clin Cancer Res. 2001;7(1):120–126.11205899
   PubMed Web of Science ®Google Scholar
• Pasqualini R, Koivunen E, Ruoslahti E. Alpha v integrins as receptors for tumor targeting by circulating ligands. Nat Biotechnol. 1997;15(6):542–546. doi:10.1038/nbt0697-5429181576
   PubMed Web of Science ®Google Scholar
• Gladson CL, Cheresh DA. Glioblastoma expression of vitronectin and the alpha v beta 3 integrin. Adhesion mechanism for transformed glial cells. J Clin Invest. 1991;88(6):1924–1932. doi:10.1172/JCI1155161721625
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Alonso MM, Cascallo M, Gomez-Manzano C, et al. ICOVIR-5 shows E2F1 addiction and potent antiglioma effect in vivo. Cancer Res. 2007;67(17):8255–8263. doi:10.1158/0008-5472.CAN-06-467517804740
   PubMed Web of Science ®Google Scholar
• Rojas JJ, Guedan S, Searle PF, et al. Minimal RB-responsive E1A promoter modification to attain potency, selectivity, and transgene-arming capacity in oncolytic adenoviruses. Mol Ther. 2010;18(11):1960–1971. doi:10.1038/mt.2010.17320808288
   PubMed Web of Science ®Google Scholar
• Guedan S, Rojas JJ, Gros A, Mercade E, Cascallo M, Alemany R. Hyaluronidase expression by an oncolytic adenovirus enhances its intratumoral spread and suppresses tumor growth. Mol Ther. 2010;18(7):1275–1283. doi:10.1038/mt.2010.7920442708
   PubMed Web of Science ®Google Scholar
• Martinez-Quintanilla J, He D, Wakimoto H, Alemany R, Shah K. Encapsulated stem cells loaded with hyaluronidase-expressing oncolytic virus for brain tumor therapy. Mol Ther. 2015;23(1):108–118. doi:10.1038/mt.2014.20425352242
   PubMed Web of Science ®Google Scholar
• Vera B, Martinez-Velez N, Xipell E, et al. Characterization of the antiglioma effect of the oncolytic adenovirus VCN-01. PLoS One. 2016;11(1):e0147211. doi:10.1371/journal.pone.014721126808201
   PubMed Web of Science ®Google Scholar
• Bayo-Puxan N, Gimenez-Alejandre M, Lavilla-Alonso S, et al. Replacement of adenovirus type 5 fiber shaft heparan sulfate proteoglycan-binding domain with RGD for improved tumor infectivity and targeting. Hum Gene Ther. 2009;20(10):1214–1221. doi:10.1089/hum.2009.03819537946
   PubMed Web of Science ®Google Scholar
• Jiang H, Rivera-Molina Y, Gomez-Manzano C, et al. Oncolytic adenovirus and tumor-targeting immune modulatory therapy improve autologous cancer vaccination. Cancer Res. 2017;77(14):3894–3907. doi:10.1158/0008-5472.CAN-17-046828566332
   PubMed Web of Science ®Google Scholar
• Ma Q, Long W, Xing C, et al. Cancer stem cells and immunosuppressive microenvironment in glioma. Front Immunol. 2018;9:2924. doi:10.3389/fimmu.2018.0292430619286
   PubMed Web of Science ®Google Scholar
• Ochs K, Sahm F, Opitz CA, et al. Immature mesenchymal stem cell-like pericytes as mediators of immunosuppression in human malignant glioma. J Neuroimmunol. 2013;265(1–2):106–116. doi:10.1016/j.jneuroim.2013.09.01124090655
   PubMed Web of Science ®Google Scholar
• Sokratous G, Polyzoidis S, Ashkan K. Immune infiltration of tumor microenvironment following immunotherapy for glioblastoma multiforme. Hum Vaccin Immunother. 2017;13(11):2575–2582. doi:10.1080/21645515.2017.130358228362548
   PubMed Web of Science ®Google Scholar
• Becker JC, Andersen MH, Schrama D, Thor Straten P. Immune-suppressive properties of the tumor microenvironment. Cancer Immunol Immunother. 2013;62(7):1137–1148. doi:10.1007/s00262-013-1434-623666510
   PubMed Web of Science ®Google Scholar
• Renfrow JJ, Weller M, Strowd RE. Meeting update-world federation of neuro-oncology societies (WFNOS) meeting 2017. Neuro Oncol. 2017;19(11):1457–1459. doi:10.1093/neuonc/nox18429059448
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Jiang H, Clise-Dwyer K, Ruisaard KE, et al. Delta-24-RGD oncolytic adenovirus elicits anti-glioma immunity in an immunocompetent mouse model. PLoS One. 2014;9(5):e97407. doi:10.1371/journal.pone.009740724827739
   PubMed Web of Science ®Google Scholar
• Kleijn A, Kloezeman J, Treffers-Westerlaken E, et al. The in vivo therapeutic efficacy of the oncolytic adenovirus Delta24-RGD is mediated by tumor-specific immunity. PLoS One. 2014;9(5):e97495. doi:10.1371/journal.pone.009749524866126
   PubMed Web of Science ®Google Scholar
• Kleijn A, Kloezeman J, Treffers-Westerlaken E, et al. The therapeutic efficacy of the oncolytic virus Delta24-RGD in a murine glioma model depends primarily on antitumor immunity. Oncoimmunology. 2014;3(9):e955697. doi:10.4161/21624011.2014.95569725941622
   PubMed Web of Science ®Google Scholar
• van Den Bossche WBL, Kleijn A, Teunissen CE, et al. Oncolytic virotherapy in glioblastoma patients induces a tumor macrophage phenotypic shift leading to an altered glioblastoma microenvironment. Neuro Oncol. 2018;20(11):1494–1504. doi:10.1093/neuonc/noy08229796615
   PubMed Web of Science ®Google Scholar
• Kuryk L, Moller AW, Jaderberg M. Combination of immunogenic oncolytic adenovirus ONCOS-102 with anti-PD-1 pembrolizumab exhibits synergistic antitumor effect in humanized A2058 melanoma huNOG mouse model. Oncoimmunology. 2019;8(2):e1532763. doi:10.1080/2162402X.2018.153276330713786
   PubMed Web of Science ®Google Scholar
• Cervera-Carrascon V, Siurala M, Santos JM, et al. TNFa and IL-2 armed adenoviruses enable complete responses by anti-PD-1 checkpoint blockade. Oncoimmunology. 2018;7(5):e1412902. doi:10.1080/2162402X.2018.149085429721366
   PubMed Web of Science ®Google Scholar
• Woller N, Gurlevik E, Fleischmann-Mundt B, et al. Viral infection of tumors overcomes resistance to PD-1-immunotherapy by broadening neoantigenome-directed T-cell responses. Mol Ther. 2015;23(10):1630–1640. doi:10.1038/mt.2015.11526112079
   PubMed Web of Science ®Google Scholar
• Gea Z. Abstract – interim results of a phase II multicenter study of the conditionally replicative oncolytic adenovirus DNX-2401 with pembrolizumab(Keytruda) for recurrent glioblastoma; CAPTIVE STUDY (LEYNOTE-192). Neuro-Oncology. 2018;20(suppl_6):vi6. doi:10.1093/neuonc/noy148.019
   Google Scholar
• Lang FF, Tran ND, Puduvalli VK, et al. Phase 1b open-label randomized study of the oncolytic adenovirus DNX-2401 administered with or without interferon gamma for recurrent glioblastoma. J Clin Oncol. 2017;35(15_suppl):2002. doi:10.1200/JCO.2017.35.15_suppl.2002
   Web of Science ®Google Scholar
• Dunn J, Baborie A, Alam F, et al. Extent of MGMT promoter methylation correlates with outcome in glioblastomas given temozolomide and radiotherapy. Br J Cancer. 2009;101(1):124–131. doi:10.1038/sj.bjc.660512719536096
   PubMed Web of Science ®Google Scholar
• Alonso MM, Gomez-Manzano C, Bekele BN, Yung WK, Fueyo J. Adenovirus-based strategies overcome temozolomide resistance by silencing the O6-methylguanine-DNA methyltransferase promoter. Cancer Res. 2007;67(24):11499–11504. doi:10.1158/0008-5472.CAN-07-531218089777
   PubMed Web of Science ®Google Scholar
• Kleijn A, van Den Bossche W, Haefner ES, et al. The sequence of delta24-RGD and TMZ administration in malignant glioma affects the role of CD8(+)T cell anti-tumor activity. Mol Ther Oncolytics. 2017;5:11–19. doi:10.1016/j.omto.2017.02.00228480325
   PubMed Web of Science ®Google Scholar
• Wu G, Broniscer A, McEachron TA, et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet. 2012;44(3):251–253. doi:10.1038/ng.110222286216
   PubMed Web of Science ®Google Scholar
• Wu G, Diaz AK, Paugh BS, et al. The genomic landscape of diffuse intrinsic pontine glioma and pediatric non-brainstem high-grade glioma. Nat Genet. 2014;46(5):444–450. doi:10.1038/ng.293824705251
   PubMed Web of Science ®Google Scholar
• Warren KE. Diffuse intrinsic pontine glioma: poised for progress. Front Oncol. 2012;2:205. doi:10.3389/fonc.2012.0020523293772
   PubMedGoogle Scholar
• Martinez-Velez N, Garcia-Moure M, Marigil M, et al. The oncolytic virus Delta-24-RGD elicits an antitumor effect in pediatric glioma and DIPG mouse models. Nat Commun. 2019;10(1):2235. doi:10.1038/s41467-019-10043-031138805
   PubMed Web of Science ®Google Scholar
• Martinez-Velez N, Marigil M, Garcia-Moure M, et al. Delta-24-RGD combined with radiotherapy exerts a potent antitumor effect in diffuse intrinsic pontine glioma and pediatric high grade glioma models. Acta Neuropathol Commun. 2019;7(1):64. doi:10.1186/s40478-019-0714-631036068
   PubMed Web of Science ®Google Scholar
• Tejada S, Alonso M, Patino A, Fueyo J, Gomez-Manzano C, Diez-Valle R. Phase I trial of DNX-2401 for diffuse intrinsic pontine glioma newly diagnosed in pediatric patients. Neurosurgery. 2018;83(5):1050–1056. doi:10.1093/neuros/nyx50729088386
   PubMed Web of Science ®Google Scholar
• Tejada S, Diez-Valle R, Dominguez PD, et al. DNX-2401, an oncolytic virus, for the treatment of newly diagnosed diffuse intrinsic pontine gliomas: a case report. Front Oncol. 2018;8:61. doi:10.3389/fonc.2018.0006129594041
   PubMed Web of Science ®Google Scholar
• Aboody KS, Brown A, Rainov NG, et al. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci U S A. 2000;97(23):12846–12851. doi:10.1073/pnas.97.23.1284611070094
   PubMed Web of Science ®Google Scholar
• Lesniak MS. Targeted therapy for malignant glioma: neural stem cells. Expert Rev Neurother. 2006;6(1):1–3. doi:10.1586/14737175.6.1.116466305
   PubMedGoogle Scholar
• Martinez-Quintanilla J, Seah I, Chua M, Shah K. Oncolytic viruses: overcoming translational challenges. J Clin Invest. 2019;130:1407–1418. doi:10.1172/JCI12228730829653
   PubMed Web of Science ®Google Scholar
• Yong RL, Shinojima N, Fueyo J, et al. Human bone marrow-derived mesenchymal stem cells for intravascular delivery of oncolytic adenovirus Delta24-RGD to human gliomas. Cancer Res. 2009;69(23):8932–8940. doi:10.1158/0008-5472.CAN-08-387319920199
   PubMed Web of Science ®Google Scholar
• Sonabend AM, Ulasov IV, Tyler MA, Rivera AA, Mathis JM, Lesniak MS. Mesenchymal stem cells effectively deliver an oncolytic adenovirus to intracranial glioma. Stem Cells. 2008;26(3):831–841. doi:10.1634/stemcells.2007-075818192232
   PubMed Web of Science ®Google Scholar
• Ahmed AU, Thaci B, Tobias AL, et al. A preclinical evaluation of neural stem cell-based cell carrier for targeted antiglioma oncolytic virotherapy. J Natl Cancer Inst. 2013;105(13):968–977. doi:10.1093/jnci/djt14123821758
   PubMed Web of Science ®Google Scholar
• Tyler MA, Ulasov IV, Sonabend AM, et al. Neural stem cells target intracranial glioma to deliver an oncolytic adenovirus in vivo. Gene Ther. 2009;16(2):262–278. doi:10.1038/gt.2008.16519078993
   PubMed Web of Science ®Google Scholar
• Kim CK, Ahmed AU, Auffinger B, et al. N-acetylcysteine amide augments the therapeutic effect of neural stem cell-based antiglioma oncolytic virotherapy. Mol Ther. 2013;21(11):2063–2073. doi:10.1038/mt.2013.17923883863
   PubMed Web of Science ®Google Scholar
• Ulasov IV, Rivera AA, Sonabend AM, et al. Comparative evaluation of survivin, midkine and CXCR4 promoters for transcriptional targeting of glioma gene therapy. Cancer Biol Ther. 2007;6(5):679–685. doi:10.4161/cbt.6.5.395717404502
   PubMed Web of Science ®Google Scholar
• Ulasov IV, Zhu ZB, Tyler MA, et al. Survivin-driven and fiber-modified oncolytic adenovirus exhibits potent antitumor activity in established intracranial glioma. Hum Gene Ther. 2007;18(7):589–602. doi:10.1089/hum.2007.00217630837
   PubMed Web of Science ®Google Scholar
• Ulasov IV, Rivera AA, Han Y, Curiel DT, Zhu ZB, Lesniak MS. Targeting adenovirus to CD80 and CD86 receptors increases gene transfer efficiency to malignant glioma cells. J Neurosurg. 2007;107(3):617–627. doi:10.3171/JNS-07/09/061717886563
   PubMed Web of Science ®Google Scholar
• Staba MJ, Wickham TJ, Kovesdi I, Hallahan DE. Modifications of the fiber in adenovirus vectors increase tropism for malignant glioma models. Cancer Gene Ther. 2000;7(1):13–19. doi:10.1038/sj.cgt.770010410678351
   PubMed Web of Science ®Google Scholar
• Zheng S, Ulasov IV, Han Y, Tyler MA, Zhu ZB, Lesniak MS. Fiber-knob modifications enhance adenoviral tropism and gene transfer in malignant glioma. J Gene Med. 2007;9(3):151–160. doi:10.1002/jgm.100817351980
   PubMed Web of Science ®Google Scholar
• Perez-Cruet MJ, Trask TW, Chen SH, et al. Adenovirus-mediated gene therapy of experimental gliomas. J Neurosci Res. 1994;39(4):506–511. doi:10.1002/jnr.4903904177884826
   PubMed Web of Science ®Google Scholar
• Chen SH, Shine HD, Goodman JC, Grossman RG, Woo SL. Gene therapy for brain tumors: regression of experimental gliomas by adenovirus-mediated gene transfer in vivo. Proc Natl Acad Sci U S A. 1994;91(8):3054–3057. doi:10.1073/pnas.91.8.30548159705
   PubMed Web of Science ®Google Scholar
• Barba D, Hardin J, Sadelain M, Gage FH. Development of anti-tumor immunity following thymidine kinase-mediated killing of experimental brain tumors. Proc Natl Acad Sci U S A. 1994;91(10):4348–4352. doi:10.1073/pnas.91.10.43488183911
   PubMed Web of Science ®Google Scholar
• Trask TW, Trask RP, Aguilar-Cordova E, et al. Phase I study of adenoviral delivery of the HSV-tk gene and ganciclovir administration in patients with current malignant brain tumors. Mol Ther. 2000;1(2):195–203. doi:10.1006/mthe.2000.003010933931
   PubMed Web of Science ®Google Scholar
• Chiocca EA, Aguilar LK, Bell SD, et al. Phase IB study of gene-mediated cytotoxic immunotherapy adjuvant to up-front surgery and intensive timing radiation for malignant glioma. J Clin Oncol. 2011;29(27):3611–3619. doi:10.1200/JCO.2011.35.522221844505
   PubMed Web of Science ®Google Scholar
• Kieran MW, Goumnerova L, Manley P, et al. Phase I study of gene-mediated cytotoxic immunotherapy with AdV-tk as adjuvant to surgery and radiation for pediatric malignant glioma and recurrent ependymoma. Neuro Oncol. 2019;21(4):537–546. doi:10.1093/neuonc/noy20230883662
   PubMed Web of Science ®Google Scholar
• Lowenstein PR, Castro MG. Evolutionary basis of a new gene- and immune-therapeutic approach for the treatment of malignant brain tumors: from mice to clinical trials for glioma patients. Clin Immunol. 2018;189:43–51. doi:10.1016/j.clim.2017.07.00628720549
   PubMed Web of Science ®Google Scholar
• Desjardins A, Gromeier M, Herndon JE 2nd, et al. Recurrent glioblastoma treated with recombinant poliovirus. N Engl J Med. 2018;379(2):150–161. doi:10.1056/NEJMoa171643529943666
   PubMed Web of Science ®Google Scholar
• Kim JW, Miska J, Young JS, et al. A comparative study of replication-incompetent and -competent adenoviral therapy-mediated immune response in a murine glioma model. Mol Ther Oncolytics. 2017;5:97–104. doi:10.1016/j.omto.2017.05.00128573184
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Curiel DT. Current issues and future directions of oncolytic adenoviruses. Mol Ther. 2010;18(2):243–250. doi:10.1038/mt.2009.26619935777
   PubMed Web of Science ®Google Scholar
• LaRocca CJ, Han J, Gavrikova T, et al. Oncolytic adenovirus expressing interferon alpha in a syngeneic Syrian hamster model for the treatment of pancreatic cancer. Surgery. 2015;157(5):888–898. doi:10.1016/j.surg.2015.01.00625731784
   PubMed Web of Science ®Google Scholar
• Koodie L, Robertson MG, Chandrashekar M, et al. Rodents versus pig model for assessing the performance of serotype chimeric Ad5/3 oncolytic adenoviruses. Cancers (Basel). 2019;11(2):198. doi:10.3390/cancers11020198
   Web of Science ®Google Scholar
• Kuryk L, Moller AW, Jaderberg M. Abscopal effect when combining oncolytic adenovirus and checkpoint inhibitor in a humanized NOG mouse model of melanoma. J Med Virol. 2019;91(9):1702–1706. doi:10.1002/jmv.2550131081549
   PubMed Web of Science ®Google Scholar