Angiogenesis, Inflammation & Therapeutics | Online ISSN  2207-872X
REVIEWS   (Open Access)

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*

+ Author Affiliations

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

Full Text
Export Citation

View Dimensions


View Plumx



View Altmetric



0
Save
0
Citation
509
View
0
Share