Targeting Glioma with Oncolytic Viruses: Emerging Possibility in Overcoming Treatment Limitations – A Review
Tasbir Amin 1, Nusrat Jerin 1, Md Fakruddin 1, Jinath Sultana Jime 1, Nayeema Bulbul 1, Sadaf Saaz Siddiqi 2, S M Bakhtiar UL Islam 1*
Journal of Angiotherapy 8(6) 1-14 https://doi.org/10.25163/angiotherapy.869685
Submitted: 02 May 2024 Revised: 29 May 2024 Published: 02 June 2024
Diffuse glioma, notably glioblastoma, poses immense treatment challenges due to its invasiveness, genetic variability, and resistance, necessitating innovative therapeutic strategies.
Abstract
Glioma tumors are considered to be an aggressive and lethal type of cancer. Malignant gliomas continue to have a poor prognosis; the five-year survival rate for the patients with early-stage diagnosis is only 5%, despite the fact that vigorous standard therapy is provided, such as surgical resection and chemo-radiotherapy. In light of this, recent developments using new immunotherapeutic techniques aim to address the treatment of glioblastoma. Oncolytic immunotherapy (OVT) is a recent advancement for the treatment of these types of cancers. OVT is an anticancer therapeutic approach in which viruses reproduce and propagate across tumors, while killing tumor cells in a selective and preferential manner. Administering OVTs can cause an increased number of immune cells to enter into the center of tumors to reshape their microenvironment and synchronize with other immunotherapies better. By causing apoptosis or eliciting an immune response against the tumor, a number of oncolytic viruses have shown a capacity to selectively infect and kill glioma cells. In the subsequent sections, we explored the function of oncolytic virotherapy in malignant gliomas, emphasizing recently completed and continuing clinical investigations, as well as obstacles faced using this therapeutic approach. Effectual treatment modalities for malignant gliomas are made challenging by the fact that they are heterogeneous tumors as well as due to the tumor microenvironment (TME) and the blood-brain barrier (BBB). Therefore, the potential advancements that could occur in the context of this area have been reviewed.
Keywords: Glioma, Immunotherapy, Treatment, Limitation, Oncolytic Virotherapy.
References
Anderson, B. D., Nakamura, T., Russell, S. J., & Peng, K.-W. (2004). High CD46 Receptor Density Determines Preferential Killing of Tumor Cells by Oncolytic Measles Virus. Cancer Research, 64(14), 4919–4926. https://doi.org/10.1158/0008-5472.can-04-0884
Banerjee, K., Núñez, F. J., Haase, S., McClellan, B. L., Faisal, S. M., Carney, S. V., Yu, J., Alghamri, M. S., Asad, A. S., Candia, A. J. N., Varela, M. L., Candolfi, M., Lowenstein, P. R., & Castro, M. G. (2021). Current Approaches for Glioma Gene Therapy and Virotherapy. Frontiers in Molecular Neuroscience, 14. https://doi.org/10.3389/fnmol.2021.621831
Bommareddy, P. K., Patel, A., Hossain, S., & Kaufman, H. L. (2017). Talimogene Laherparepvec (T-VEC) and Other Oncolytic Viruses for the Treatment of Melanoma. American Journal of Clinical Dermatology, 18(1), 1–15. https://doi.org/10.1007/s40257-016-0238-9
Bommareddy, P. K., Shettigar, M., & Kaufman, H. L. (2018). Integrating oncolytic viruses in combination cancer immunotherapy. Nature Reviews Immunology, 18(8), 498–513. https://doi.org/10.1038/s41577-018-0014-6
Breitbach, C. J., Arulanandam, R., Silva, N. D., Thorne, S. H., Patt, R., Daneshmand, M., Moon, A., Ilkow, C., Burke, J., Hwang, T.-H., Heo, J., Cho, M., Chen, H., Angarita, F. A., Addison, C., McCart, J. A., Bell, J. C., & Kirn, D. H. (2013). Oncolytic Vaccinia Virus Disrupts Tumor-Associated Vasculature in Humans. Cancer Research, 73(4), 1265–1275. https://doi.org/10.1158/0008-5472.CAN-12-2687
Carolien A.M. Koks, Garg, A. D., Ehrhardt, M. C., Matteo Dalla Riva, Vandenberk, L., Boon, L., Steven De Vleeschouwer, Patrizia Agostinis, Graf, N., & Stefaan Van Gool. (2014). Newcastle disease virotherapy induces long-term survival and tumor-specific immune memory in orthotopic glioma through the induction of immunogenic cell death. 136(5). https://doi.org/10.1002/ijc.29202
Ceccarelli, M., Barthel, Floris P., Malta, Tathiane M., Sabedot, Thais S., Salama, Sofie R., Murray, Bradley A., Morozova, O., Newton, Y., Radenbaugh, A., Pagnotta, Stefano M., Anjum, S., Wang, J., Manyam, G., Zoppoli, P., Ling, S., Rao, Arjun A., Grifford, M., Cherniack, Andrew D., Zhang, H., & Poisson, L. (2016). Molecular Profiling Reveals Biologically Discrete Subsets and Pathways of Progression in Diffuse Glioma. Cell, 164(3), 550–563. https://doi.org/10.1016/j.cell.2015.12.028
Cheema, T. A., Wakimoto, H., Fecci, P. E., Ning, J., Kuroda, T., Jeyaretna, D. S., Martuza, R. L., & Rabkin, S. D. (2013). Multifaceted oncolytic virus therapy for glioblastoma in an immunocompetent cancer stem cell model. Proceedings of the National Academy of Sciences, 110(29), 12006–12011. https://doi.org/10.1073/pnas.1307935110
Cloughesy, T. F., Landolfi, J., Vogelbaum, M. A., Ostertag, D., Elder, J. B., Bloomfield, S., Carter, B., Chen, C. C., Kalkanis, S. N., Kesari, S., Lai, A., Lee, I. Y., Liau, L. M., Mikkelsen, T., Nghiemphu, P., Piccioni, D., Accomando, W., Diago, O. R., Hogan, D. J., & Gammon, D. (2018). Durable complete responses in some recurrent high-grade glioma patients treated with Toca 511 + Toca FC. Neuro-Oncology, 20(10), 1383–1392. https://doi.org/10.1093/neuonc/noy075
Cloughesy, T. F., Petrecca, K., Walbert, T., Butowski, N., Salacz, M., Perry, J., Damek, D., Bota, D., Bettegowda, C., Zhu, J.-J., Iwamoto, F., Placantonakis, D., Kim, L., Elder, B., Kaptain, G., Cachia, D., Moshel, Y., Brem, S., Piccioni, D., & Landolfi, J. (2020). Effect of Vocimagene Amiretrorepvec in Combination With Flucytosine vs Standard of Care on Survival Following Tumor Resection in Patients With Recurrent High-Grade Glioma. JAMA Oncology, 6(12), 1–8. https://doi.org/10.1001/jamaoncol.2020.3161
Crespo, I., Vital, A. L., Gonzalez-Tablas, M., Patino, M. del C., Otero, A., Lopes, M. C., de Oliveira, C., Domingues, P., Orfao, A., & Tabernero, M. D. (2015). Molecular and Genomic Alterations in Glioblastoma Multiforme. The American Journal of Pathology, 185(7), 1820–1833. https://doi.org/10.1016/j.ajpath.2015.02.023
Daneman, R., & Prat, A. (2015). The Blood–Brain Barrier. Cold Spring Harbor Perspectives in Biology, 7(1). https://doi.org/10.1101/cshperspect.a020412
Davis, F. G., Smith, T. R., Gittleman, H. R., Ostrom, Q. T., Kruchko, C., & Barnholtz-Sloan, J. S. (2019). Glioblastoma incidence rate trends in Canada and the United States compared with England, 1995–2015. Neuro-Oncology. https://doi.org/10.1093/neuonc/noz203
Davola, M. E., & Mossman, K. L. (2019). Oncolytic viruses: how “lytic” must they be for therapeutic efficacy?. OncoImmunology, 8(6), e1581528. https://doi.org/10.1080/2162402x.2019.1596006
Delgado-López, P. D., Corrales-García, E. M., Martino, J., Lastra-Aras, E., & Dueñas-Polo, M. T. (2017). Diffuse low-grade glioma: a review on the new molecular classification, natural history and current management strategies. Clinical and Translational Oncology, 19(8), 931–944. https://doi.org/10.1007/s12094-017-1631-4
Desjardins, A., Gromeier, M., Herndon, J. E., Beaubier, N., Bolognesi, D. P., Friedman, A. H., Friedman, H. S., McSherry, F., Muscat, A. M., Nair, S., Peters, K. B., Randazzo, D., Sampson, J. H., Vlahovic, G., Harrison, W. T., McLendon, R. E., Ashley, D., & Bigner, D. D. (2018). Recurrent Glioblastoma Treated with Recombinant Poliovirus. New England Journal of Medicine, 379(2), 150–161. https://doi.org/10.1056/nejmoa1716435
E. Antonio Chiocca, Solomon, I. H., Nakashima, H., Lawler, S. E., Triggs, D., Zhang, A., Grant, J. K., Reardon, D. A., Wen, P. Y., Eudocia Quant Lee, Ligon, K. L., Pisano, W., Rodig, S. J., Suvà, M. L., Wucherpfennig, K. W., Gritsch, S., Mathewson, N. D., Krisky, D., Estuardo Aguilar-Cordova, & Aguilar, L. K. (2021). First-in-human CAN-3110 (ICP-34.5 expressing HSV-1 oncolytic virus) in patients with recurrent high-grade glioma. Journal of Clinical Oncology, 39(15_suppl), 2009–2009. https://doi.org/10.1200/jco.2021.39.15_suppl.2009
Fares, J., Ahmed, A. U., Ulasov, I. V., Sonabend, A. M., Miska, J., Lee-Chang, C., Balyasnikova, I. V., Chandler, J. P., Portnow, J., Tate, M. C., Kumthekar, P., Lukas, R. V., Grimm, S. A., Adams, A. K., Hébert, C. D., Strong, T. V., Amidei, C., Arrieta, V. A., Zannikou, M., & Horbinski, C. (2021). Neural stem cell delivery of an oncolytic adenovirus in newly diagnosed malignant glioma: a first-in-human, phase 1, dose-escalation trial. The Lancet. Oncology, 22(8), 1103–1114. https://doi.org/10.1016/S1470-2045(21)00245-X
Fong, Y., Ady, J., Heffner, J., & Klein, E. (2014). Oncolytic viral therapy for pancreatic cancer: current research and future directions. Oncolytic Virotherapy, 35. https://doi.org/10.2147/ov.s53858
Forrester, J. V., McMenamin, P. G., & Dando, S. J. (2018). CNS infection and immune privilege. Nature Reviews Neuroscience, 19(11), 655–671. https://doi.org/10.1038/s41583-018-0070-8
Gambini, E., Reisoli, E., Appolloni, I., Gatta, V., Campadelli-Fiume, G., Menotti, L., & Malatesta, P. (2012). Replication-competent Herpes Simplex Virus Retargeted to HER2 as Therapy for High-grade Glioma. 20(5), 994–1001. https://doi.org/10.1038/mt.2012.22
Geletneky, K., Hajda, J., Angelova, A. L., Leuchs, B., Capper, D., Bartsch, A. J., Neumann, J.-O., Schöning, T., Hüsing, J., Beelte, B., Kiprianova, I., Roscher, M., Bhat, R., von Deimling, A., Brück, W., Just, A., Frehtman, V., Löbhard, S., Terletskaia-Ladwig, E., & Fry, J. (2017). Oncolytic H-1 Parvovirus Shows Safety and Signs of Immunogenic Activity in a First Phase I/IIa Glioblastoma Trial. Molecular Therapy, 25(12), 2620–2634. https://doi.org/10.1016/j.ymthe.2017.08.016
Gersey, Z., Osiason, A. D., Bloom, L., Shah, S., Thompson, J. W., Bregy, A., Agarwal, N., & Komotar, R. J. (2019). Therapeutic Targeting of the Notch Pathway in Glioblastoma Multiforme. World Neurosurgery, 131, 252-263.e2. https://doi.org/10.1016/j.wneu.2019.07.180
Gujar, S., Pol, J. G., Kim, Y., Lee, P. W., & Kroemer, G. (2018). Antitumor Benefits of Antiviral Immunity: An Underappreciated Aspect of Oncolytic Virotherapies. Trends in Immunology, 39(3), 209–221. https://doi.org/10.1016/j.it.2017.11.006
Hardcastle, J., Mills, L., Malo, C. S., Jin, F., Kurokawa, C., Geekiyanage, H., Schroeder, M., Sarkaria, J., Johnson, A. J., & Galanis, E. (2016). Immunovirotherapy with measles virus strains in combination with anti–PD-1 antibody blockade enhances antitumor activity in glioblastoma treatment. Neuro-Oncology, now179. https://doi.org/10.1093/neuonc/now179
Hegi, M. E., Diserens, A.-C., Gorlia, T., Hamou, M.-F., de Tribolet, N., Weller, M., Kros, J. M., Hainfellner, J. A., Mason, W., Mariani, L., Bromberg, J. E. C., Hau, P., Mirimanoff, R. O., Cairncross, J. G., Janzer, R. C., & Stupp, R. (2005). MGMT gene silencing and benefit from temozolomide in glioblastoma. The New England Journal of Medicine, 352(10), 997–1003. https://doi.org/10.1056/NEJMoa043331
Hong Jae Chon, Won Young Lee, Yang, H. P., So Yeon Kong, Na Mi Lee, Eun Sun Moon, Choi, J.-W., Eun Hee Han, Joo Sung Kim, & Joong Bae Ahn. (2018). Tumor Microenvironment Remodeling by Intratumoral Oncolytic Vaccinia Virus Enhances the Efficacy of Immune-Checkpoint Blockade. Clinical Cancer Research, 25(5), 1612–1623. https://doi.org/10.1158/1078-0432.ccr-18-1932
Huang, J., Zheng, M., Zhang, Z., Tang, X., Chen, Y., Peng, A., Peng, X., Tong, A., & Zhou, L. (2021). Interleukin-7-loaded oncolytic adenovirus improves CAR-T cell therapy for glioblastoma. 70(9), 2453–2465. https://doi.org/10.1007/s00262-021-02856-0
Islam, S. M. B. U., Lee, B., Jiang, F., Kim, E.-K., Ahn, S. C., & Hwang, T.-H. (2020). Engineering and Characterization of Oncolytic Vaccinia Virus Expressing Truncated Herpes Simplex Virus Thymidine Kinase. Cancers, 12(1), 228. https://doi.org/10.3390/cancers12010228
Jackson, C. M., Choi, J., & Lim, M. (2019). Mechanisms of immunotherapy resistance: lessons from glioblastoma. Nature Immunology, 20(9), 1100–1109. https://doi.org/10.1038/s41590-019-0433-y
Jafari, M., Kadkhodazadeh, M., Mina Bahrololoumi Shapourabadi, Nasser Hashemi Goradel, Mohammad Ali Shokrgozar, Arash Arashkia, Shahriyar Abdoli, & Zahra Sharifzadeh. (2022). Immunovirotherapy: The role of antibody based therapeutics combination with oncolytic viruses. Frontiers in Immunology, 13. https://doi.org/10.3389/fimmu.2022.1012806
Jahan, N., Lee, J. M., Shah, K., & Wakimoto, H. (2017). Therapeutic targeting of chemoresistant and recurrent glioblastoma stem cells with a proapoptotic variant of oncolytic herpes simplex virus. International Journal of Cancer, 141(8), 1671–1681. https://doi.org/10.1002/ijc.30811
Ji, N., Weng, D., Liu, C., Gu, Z., Chen, S., Guo, Y., Fan, Z., Wang, X., Chen, J., Zhao, Y., Zhou, J., Wang, J., Ma, D., & Li, N. (2015). Adenovirus-mediated delivery of herpes simplex virus thymidine kinase administration improves outcome of recurrent high-grade glioma. Oncotarget, 7(4), 4369–4378. https://doi.org/10.18632/oncotarget.6737
Jiang, H., McCormick, F., Lang, F. F., Gomez-Manzano, C., & Fueyo, J. (2006). Oncolytic adenoviruses as antiglioma agents. 6(5), 697–708. https://doi.org/10.1586/14737140.6.5.697
Jiang, H., Rivera-Molina, Y., Gomez-Manzano, C., Clise-Dwyer, K., Bover, L., Vence, L. M., Yuan, Y., Lang, F. F., Toniatti, C., Hossain, M. B., & Fueyo, J. (2017). Oncolytic Adenovirus and Tumor-Targeting Immune Modulatory Therapy Improve Autologous Cancer Vaccination. Cancer Research, 77(14), 3894–3907. https://doi.org/10.1158/0008-5472.CAN-17-0468
Juri Kiyokawa, Kawamura, Y., Ghouse, S. M., Acar, S., Erinç Barçin, Jordi Martinez-Quintanilla, Martuza, R. L., Alemany, R., Rabkin, S. D., Shah, K., & Hiroaki Wakimoto. (2021). Modification of Extracellular Matrix Enhances Oncolytic Adenovirus Immunotherapy in Glioblastoma. 27(3), 889–902. https://doi.org/10.1158/1078-0432.ccr-20-2400
Karsten Geletneky, Kiprianova, I., Ayache, A., Koch, R. M., Herrero, M., Laurent Deleu, Sommer, C., Thomas, N., Rommelaere, J., & Schlehofer, J. R. (2010). Regression of advanced rat and human gliomas by local or systemic treatment with oncolytic parvovirus H-1 in rat models. 12(8), 804–814. https://doi.org/10.1093/neuonc/noq023
Kaufman, H. L., Kohlhapp, F. J., & Zloza, A. (2016). Erratum: Oncolytic viruses: a new class of immunotherapy drugs. Nature Reviews Drug Discovery, 15(9), 660–660. https://doi.org/10.1038/nrd.2016.178
Khoonkari, M., Liang, D., Kamperman, M., Kruyt, F. A. E., & van Rijn, P. (2022). Physics of Brain Cancer: Multiscale Alterations of Glioblastoma Cells under Extracellular Matrix Stiffening. Pharmaceutics, 14(5), 1031. https://doi.org/10.3390/pharmaceutics14051031
Kleijn, A., van, Haefner, E., Zineb Belcaid, Burghoorn-Maas, C., Jenneke Kloezeman, Pas, S. D., Sieger Leenstra, Reno Debets, Jeroen de Vrij, Clemens, & Martine L.M. Lamfers. (2017). The Sequence of Delta24-RGD and TMZ Administration in Malignant Glioma Affects the Role of CD8 + T Cell Anti-tumor Activity. 5, 11–19. https://doi.org/10.1016/j.omto.2017.02.002
Kumar, V., Patel, S., Tcyganov, E., & Gabrilovich, D. I. (2016). The Nature of Myeloid-Derived Suppressor Cells in the Tumor Microenvironment. Trends in Immunology, 37(3), 208–220. https://doi.org/10.1016/j.it.2016.01.004
Lang, F. F., Conrad, C., Gomez-Manzano, C., Yung, W. K. A., Sawaya, R., Weinberg, J. S., Prabhu, S. S., Rao, G., Fuller, G. N., Aldape, K. D., Gumin, J., Vence, L. M., Wistuba, I., Rodriguez-Canales, J., Villalobos, P. A., Dirven, C. M. F., Tejada, S., Valle, R. D., Alonso, M. M., & Ewald, B. (2018). Phase I Study of DNX-2401 (Delta-24-RGD) Oncolytic Adenovirus: Replication and Immunotherapeutic Effects in Recurrent Malignant Glioma. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology, 36(14), 1419–1427. https://doi.org/10.1200/JCO.2017.75.8219
Lang, F. F., Tran, N. D., Puduvalli, V. K., Elder, J. B., Fink, K. L., Conrad, C. A., Yung, W. K. A., Penas-Prado, M., Gomez-Manzano, C., Peterkin, J., & Fueyo, J. (2017). Phase 1b open-label randomized study of the oncolytic adenovirus DNX-2401 administered with or without interferon gamma for recurrent glioblastoma. Journal of Clinical Oncology, 35(15_suppl), 2002–2002. https://doi.org/10.1200/jco.2017.35.15_suppl.2002
Le, D. T., Durham, J. N., Smith, K. N., Wang, H., Bartlett, B. R., Aulakh, L. K., Lu, S., Kemberling, H., Wilt, C., Luber, B. S., Wong, F., Azad, N. S., Rucki, A. A., Laheru, D., Donehower, R., Zaheer, A., Fisher, G. A., Crocenzi, T. S., Lee, J. J., & Greten, T. F. (2017). Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science, 357(6349), 409–413. https://doi.org/10.1126/science.aan6733
Li, X., Wang, P., Li, H., Du, X., Liu, M., Huang, Q., Wang, Y., & Wang, S. (2016). The Efficacy of Oncolytic Adenovirus Is Mediated by T-cell Responses against Virus and Tumor in Syrian Hamster Model. Clinical Cancer Research, 23(1), 239–249. https://doi.org/10.1158/1078-0432.ccr-16-0477
Liu, T.-C., Galanis, E., & Kirn, D. (2007). Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nature Clinical Practice Oncology, 4(2), 101–117. https://doi.org/10.1038/ncponc0736
Liu, Z., Zhao, X., Mao, H., Baxter, P., Huang, Y., Yu, L., Wadhwa, L., Su, J., Adesina, A. M., Lazlo Perlaky, Hurwitz, M. Y., Neeraja Idamakanti, Hallenbeck, P. L., Hurwitz, R. L., Lau, C. C., Murali Chintagumpala, Blaney, S. M., & Li, X.-N. (2013). Intravenous injection of oncolytic picornavirus SVV-001 prolongs animal survival in a panel of primary tumor–based orthotopic xenograft mouse models of pediatric glioma. 15(9), 1173–1185. https://doi.org/10.1093/neuonc/not065
Louveau, A., Harris, T. H., & Kipnis, J. (2015). Revisiting the concept of CNS immune privilege. Trends in Immunology, 36(10), 569–577. https://doi.org/10.1016/j.it.2015.08.006
Lundstrom, K. (2019). RNA Viruses as Tools in Gene Therapy and Vaccine Development. Genes, 10(3), 189. https://doi.org/10.3390/genes10030189
Mackay, A., Burford, A., Carvalho, D., Izquierdo, E., Fazal-Salom, J., Taylor, K. R., Bjerke, L., Clarke, M., Vinci, M., Nandhabalan, M., Temelso, S., Popov, S., Molinari, V., Raman, P., Waanders, A. J., Han, H. J., Gupta, S., Marshall, L., Zacharoulis, S., & Vaidya, S. (2017). Integrated Molecular Meta-Analysis of 1,000 Pediatric High-Grade and Diffuse Intrinsic Pontine Glioma. Cancer Cell, 32(4), 520-537.e5. https://doi.org/10.1016/j.ccell.2017.08.017
Marelli, G., Howells, A., Lemoine, N. R., & Wang, Y. (2018). Oncolytic Viral Therapy and the Immune System: A Double-Edged Sword Against Cancer. Frontiers in Immunology, 9. https://doi.org/10.3389/fimmu.2018.00866
Martikainen, M., & Essand, M. (2019). Virus-Based Immunotherapy of Glioblastoma. Cancers, 11(2), 186. https://doi.org/10.3390/cancers11020186
Mendez, F., Kadiyala, P., Nunez, F. J., Carney, S. V., Nunez, F. M., Gauss, J. C., Ravindran, R., Pawar, S., Edwards, M., Maria Belen Garcia-Fabiani, Haase, S., & Lowenstein, P. R. (2020). Therapeutic Efficacy of Immune Stimulatory Thymidine Kinase and fms-like Tyrosine Kinase 3 Ligand (TK/Flt3L) Gene Therapy in a Mouse Model of High-Grade Brainstem Glioma. 26(15), 4080–4092. https://doi.org/10.1158/1078-0432.ccr-19-3714
Muik, A., Stubbert, L. J., Jahedi, R. Z., Geiβ, Y., Kimpel, J., Dold, C., Tober, R., Volk, A., Klein, S., Dietrich, U., Yadollahi, B., Falls, T., Miletic, H., Stojdl, D., Bell, J. C., & Laer, D. von. (2014). Re-engineering Vesicular Stomatitis Virus to Abrogate Neurotoxicity, Circumvent Humoral Immunity, and Enhance Oncolytic Potency. Cancer Research, 74(13), 3567–3578. https://doi.org/10.1158/0008-5472.CAN-13-3306
Nazarenko, I., Hede, S.-M., He, X., Hedrén, A., Thompson, J., Lindström, M. S., & Nistér, M. (2012). PDGF and PDGF receptors in glioma. Upsala Journal of Medical Sciences, 117(2), 99–112. https://doi.org/10.3109/03009734.2012.665097
Nishikawa, R., Ji, X. D., Harmon, R. C., Lazar, C. S., Gill, G. N., Cavenee, W. K., & Huang, H. J. (1994). A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proceedings of the National Academy of Sciences, 91(16), 7727–7731. https://doi.org/10.1073/pnas.91.16.7727
Nishio, N., & Dotti, G. (2015). Oncolytic virus expressing RANTES and IL-15 enhances function of CAR-modified T cells in solid tumors. OncoImmunology, 4(2), e988098. https://doi.org/10.4161/21505594.2014.988098
Oddrun Elise Olsen, Karin Fahl Wader, Misund, K., Thea Kristin Våtsveen, Torstein Baade Rø, Anne Kærsgaard Mylin, Ingemar Turesson, Berit Fladvad Størdal, Siv Helen Moen, Standal, T., Waage, A., Anders Sundan, & Holien, T. (2014). Bone morphogenetic protein-9 suppresses growth of myeloma cells by signaling through ALK2 but is inhibited by endoglin. 4(3), e196–e196. https://doi.org/10.1038/bcj.2014.16
Omuro, A., Vlahovic, G., Lim, M., Sahebjam, S., Baehring, J., Cloughesy, T., Voloschin, A., Ramkissoon, S. H., Ligon, K. L., Latek, R., Zwirtes, R., Strauss, L., Paliwal, P., Harbison, C. T., Reardon, D. A., & Sampson, J. H. (2017). Nivolumab with or without ipilimumab in patients with recurrent glioblastoma: results from exploratory phase I cohorts of CheckMate 143. Neuro-Oncology, 20(5), 674–686. https://doi.org/10.1093/neuonc/nox208
Ostrand-Rosenberg, S., & Fenselau, C. (2018). Myeloid-Derived Suppressor Cells: Immune-Suppressive Cells That Impair Antitumor Immunity and Are Sculpted by Their Environment. The Journal of Immunology, 200(2), 422–431. https://doi.org/10.4049/jimmunol.1701019
Ostrom, Q. T., Cioffi, G., Gittleman, H., Patil, N., Waite, K., Kruchko, C., & Barnholtz-Sloan, J. S. (2019). CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2012–2016. Neuro-Oncology, 21(Supplement_5), v1–v100. https://doi.org/10.1093/neuonc/noz150
Ostrom, Q. T., Gittleman, H., Truitt, G., Boscia, A., Kruchko, C., & Barnholtz-Sloan, J. S. (2018). CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2011–2015. Neuro-Oncology, 20(suppl_4), iv1–iv86. https://doi.org/10.1093/neuonc/noy131
Qi, Z., Long, X., Liu, J., & Cheng, P. (2022). Glioblastoma microenvironment and its reprogramming by oncolytic virotherapy. Frontiers in Cellular Neuroscience, 16. https://doi.org/10.3389/fncel.2022.819363
Ramachandran, M., Yu, D., Dyczynski, M., Baskaran, S., Zhang, L., Lulla, A., Lulla, V., Saul, S., Nelander, S., Dimberg, A., Merits, A., Leja-Jarblad, J., & Essand, M. (2017). Safe and Effective Treatment of Experimental Neuroblastoma and Glioblastoma Using Systemically Delivered Triple MicroRNA-Detargeted Oncolytic Semliki Forest Virus. Clinical Cancer Research, 23(6), 1519–1530. https://doi.org/10.1158/1078-0432.CCR-16-0925
Rius-Rocabert, S., García-Romero, N., García, A., Ayuso-Sacido, A., & Nistal-Villan, E. (2020). Oncolytic Virotherapy in Glioma Tumors. International Journal of Molecular Sciences, 21(20).
Rocha Pinheiro, S. L., Lemos, F. F. B., Marques, H. S., Silva Luz, M., de Oliveira Silva, L. G., Faria Souza Mendes dos Santos, C., da Costa Evangelista, K., Calmon, M. S., Sande Loureiro, M., & Freire de Melo, F. (2023). Immunotherapy in glioblastoma treatment: Current state and future prospects. World Journal of Clinical Oncology, 14(4), 138–159. https://doi.org/10.5306/wjco.v14.i4.138
Roesch, S., Rapp, C., Dettling, S., & Herold-Mende, C. (2018). When Immune Cells Turn Bad—Tumor-Associated Microglia/Macrophages in Glioma. International Journal of Molecular Sciences, 19(2), 436. https://doi.org/10.3390/ijms19020436
Ruiz, A. J., Hadac, E. M., Nace, R. A., & Russell, S. J. (2016). MicroRNA-Detargeted Mengovirus for Oncolytic Virotherapy. Journal of Virology, 90(8), 4078–4092. https://doi.org/10.1128/jvi.02810-15
Russell, S. J., Peng, K.-W., & Bell, J. C. (2012). Oncolytic virotherapy. Nature Biotechnology, 30(7), 658–670. https://doi.org/10.1038/nbt.2287
Saha, D., Martuza, R. L., & Rabkin, S. D. (2017). Macrophage Polarization Contributes to Glioblastoma Eradication by Combination Immunovirotherapy and Immune Checkpoint Blockade. Cancer Cell, 32(2), 253-267.e5. https://doi.org/10.1016/j.ccell.2017.07.006
Schirrmacher, van Gool, & Stuecker. (2019). Breaking Therapy Resistance: An Update on Oncolytic Newcastle Disease Virus for Improvements of Cancer Therapy. Biomedicines, 7(3), 66. https://doi.org/10.3390/biomedicines7030066
Stupp, R., Mason, W. P., van den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J. B., Belanger, K., Brandes, A. A., Marosi, C., Bogdahn, U., Curschmann, J., Janzer, R. C., Ludwin, S. K., Gorlia, T., Allgeier, A., Lacombe, D., Cairncross, J. G., Eisenhauer, E., & Mirimanoff, R. O. (2005). Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma. New England Journal of Medicine, 352(10), 987–996. https://doi.org/10.1056/nejmoa043330
Suryawanshi, Y. R., & Schulze, A. J. (2021). Oncolytic Viruses for Malignant Glioma: On the Verge of Success? Viruses, 13(7), 1294. https://doi.org/10.3390/v13071294
Sweety Asija, Chatterjee, A., Goda, J. S., Yadav, S., Godhanjali Chekuri, & Rahul Purwar. (2023). Oncolytic immunovirotherapy for high-grade gliomas: A novel and an evolving therapeutic option. 14. https://doi.org/10.3389/fimmu.2023.1118246
Tian, Y., Xie, D., & Yang, L. (2022). Engineering strategies to enhance oncolytic viruses in cancer immunotherapy. Signal Transduction and Targeted Therapy, 7(1). https://doi.org/10.1038/s41392-022-00951-x
Todo, T. (2019). ATIM-14. RESULTS OF PHASE II CLINICAL TRIAL OF ONCOLYTIC HERPES VIRUS G47Δ IN PATIENTS WITH GLIOBLASTOMA. Neuro-Oncology, 21(Supplement_6), vi4–vi4. https://doi.org/10.1093/neuonc/noz175.014
Todo, T., Ino, Y., Ohtsu, H., Shibahara, J., & Tanaka, M. (2022). A phase I/II study of triple-mutated oncolytic herpes virus G47? in patients with progressive glioblastoma. Nature Communications, 13(1). https://doi.org/10.1038/s41467-022-31262-y
Topalian, S. L., Taube, J. M., Anders, R. A., & Pardoll, D. M. (2016). Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nature Reviews Cancer, 16(5), 275–287. https://doi.org/10.1038/nrc.2016.36
Trask, T. W., Trask, R. P., Aguilar-Cordova, E., Shine, H. David., Wyde, P. R., Goodman, J. Clay., Hamilton, W. J., Rojas-Martinez, A., Chen, S.-H., Woo, S. L. C., & Grossman, R. G. (2000). Phase I Study of Adenoviral Delivery of the HSV-tk Gene and Ganciclovir Administration in Patients with Recurrent Malignant Brain Tumors. Molecular Therapy, 1(2), 195–203. https://doi.org/10.1006/mthe.2000.0030
Venteicher, A. S., Tirosh, I., Hebert, C., Yizhak, K., Neftel, C., Filbin, M. G., Hovestadt, V., Escalante, L. E., Shaw, M. L., Rodman, C., Gillespie, S. M., Dionne, D., Luo, C. C., Ravichandran, H., Mylvaganam, R., Mount, C., Onozato, M. L., Nahed, B. V., Wakimoto, H., & Curry, W. T. (2017). Decoupling genetics, lineages, and microenvironment in IDH-mutant gliomas by single-cell RNA-seq. Science, 355(6332). https://doi.org/10.1126/science.aai8478
Weller, R. O., Djuanda, E., Yow, H.-Y., & Carare, R. O. (2008). Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathologica, 117(1), 1–14. https://doi.org/10.1007/s00401-008-0457-0
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., Teh, B. S., Trask, T. W., Baskin, D. S., New, P. Z., Aguilar, L. K., Aguilar-Cordova, E., & Chiocca, E. A. (2016). Phase II multicenter study of gene-mediated cytotoxic immunotherapy as adjuvant to surgical resection for newly diagnosed malignant glioma. Neuro-Oncology, 18(8), 1137–1145. https://doi.org/10.1093/neuonc/now002
Wherry, E. J., & Kurachi, M. (2015). Molecular and cellular insights into T cell exhaustion. Nature Reviews Immunology, 15(8), 486–499. https://doi.org/10.1038/nri3862
Wojton, J., & Kaur, B. (2010). Impact of tumor microenvironment on oncolytic viral therapy. Cytokine & Growth Factor Reviews, 21(2-3), 127–134. https://doi.org/10.1016/j.cytogfr.2010.02.014
Wollmann, G., Ozduman, K., & van den Pol, A. N. (2012). Oncolytic Virus Therapy for Glioblastoma Multiforme. The Cancer Journal, 18(1), 69–81. https://doi.org/10.1097/ppo.0b013e31824671c9
Woroniecka, K., Chongsathidkiet, P., Rhodin, K., Kemeny, H., Dechant, C., Farber, S. H., Elsamadicy, A. A., Cui, X., Koyama, S., Jackson, C., Hansen, L. J., Johanns, T. M., Sanchez-Perez, L., Chandramohan, V., Yu, Y.-R. A., Bigner, D. D., Giles, A., Healy, P., Dranoff, G., & Weinhold, K. J. (2018). T-Cell Exhaustion Signatures Vary with Tumor Type and Are Severe in Glioblastoma. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 24(17), 4175–4186. https://doi.org/10.1158/1078-0432.CCR-17-1846
Yoshihiko Kakiuchi, Kuroda, S., Nobuhiko Kanaya, Kento Kumon, Tsumura, T., Hashimoto, M., Yagi, C., Sugimoto, R., Hamada, Y., Kikuchi, S., Nishizaki, M., Kagawa, S., Hiroshi Tazawa, Urata, Y., & Fujiwara, T. (2021). Local oncolytic adenovirotherapy produces an abscopal effect via tumor-derived extracellular vesicles. 29(10), 2920–2930. https://doi.org/10.1016/j.ymthe.2021.05.015
Zhan, X., Guo, S., Li, Y., Ran, H., Huang, H., Mi, L., Wu, J., Wang, X., Xiao, D., Chen, L.-S., Li, D., Zhang, S., Xu, Y., Yu, Y., Li, T., Han, Q., He, K., Cui, J., Li, T., & Zhou, T. (2020). Glioma stem-like cells evade interferon suppression through MBD3/NuRD complex–mediated STAT1 downregulation. 217(5). https://doi.org/10.1084/jem.20191340
Zhang, H., Lin, Y., Li, K., Liang, J., Xiao, X., Cai, J., Tan, Y., Xing, F., Mai, J., Li, Y., Chen, W., Sheng, L., Gu, J., Zhu, W., Yin, W., Qiu, P., Su, X., Lu, B., Tian, X., & Liu, J. (2016). Naturally Existing Oncolytic Virus M1 Is Nonpathogenic for the Nonhuman Primates After Multiple Rounds of Repeated Intravenous Injections. 27(9), 700–711. https://doi.org/10.1089/hum.2016.038
Zong, H., Parada, L. F., & Baker, S. J. (2015). Cell of Origin for Malignant Gliomas and Its Implication in Therapeutic Development. Cold Spring Harbor Perspectives in Biology, 7(5). https://doi.org/10.1101/cshperspect.a020610
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