Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer

Kirn, David H.; Thorne, Steve H.

doi:10.1038/nrc2545

Cited by 402Virus-based gene therapy researchPoxvirus research and outbreaksCancer Research and Treatments

Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer

Kirn, David H., Thorne, Steve H.·2009·Nature Reviews Cancer

DOI 10.1038/nrc2545

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Abstract

Viruses have been engineered for cancer therapy in a variety of ways. Approaches include non-replicating gene therapy vectors, cancer vaccines and oncolytic viruses, but the clinical efficacy of these approaches has been limited by multiple factors. However, a new therapeutic class of oncolytic poxviruses has recently been developed that combines targeted and armed approaches for treating cancer. Initial preclinical and clinical results show that products from this therapeutic class can systemically target cancers in a highly selective and potent fashion using a multi-pronged mechanism of action.

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Oncolytic viruses can be armed with vectors that encode pro-inflammatory or anti-immunosuppressive transgenes, thereby in theory promoting both immunogenicity of tumour cells and intratumoral inflammation.
“Moreover, oncolytic viruses can be armed with vectors that encode for pro-inflammatory or anti-immunosuppressive transgenes, thereby in theory promoting both the immunogenicity of the tumour cells and intratumoral inflammation.128”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [128]

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Vaccinia Virus Intermediate Stage Transcription Is Complemented by Ras-GTPase-activating Protein SH3 Domain-binding Protein (G3BP) and Cytoplasmic Activation/Proliferation-associated Protein (p137) Individually or as a Heterodimer
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Oncolytic virotherapy for ovarian carcinomatosis using a replication-selective vaccinia virus armed with a yeast cytosine deaminase gene
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The Vaccinia Virus Protein F1L Interacts with Bim and Inhibits Activation of the Pro-apoptotic Protein Bax
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Tumor-Specific Gene Delivery Using Recombinant Vaccinia Virus in a Rabbit Model of Liver Metastases
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Oncolytic Virotherapy: Approaches to Tumor Targeting and Enhancing Antitumor Effects
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Intravesical gene therapy: in vivo gene transfer using recombinant vaccinia virus vectors.
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Vaccination of Prostate Cancer Patients With Modified Vaccinia Ankara Delivering the Tumor Antigen 5T4 (TroVax)
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Selective Intratumoral Amplification of an Antiangiogenic Vector by an Oncolytic Virus Produces Enhanced Antivascular and Anti-tumor Efficacy
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Poxviruses as vectors for cancer immunotherapy.
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Pox Viral Vaccine Approaches
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THE EXPERIMENTAL LOCAL THERAPY OF CUTANEOUS METASTASES OF MALIGNANT MELANOBLASTOMAS WITH COW POX VACCINE OR COLCEMLD (DEMECOLCINE OE OMAINE)
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In Search of a Kinder, Gentler Vaccine
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Drug evaluation: Therion's rV-PSA-TRICOM + rF-PSA-TRICOM prime-boost prostate cancer vaccine.
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Nanomedicine in cancer therapy: Challenges, opportunities, and clinical applications
WICKI, A. N., Witzigmann, D., Balasubramanian, V., & Huwyler, J. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.12.030 · Cited by 1,912 · see citing works
Oncolytic virotherapy
Russell, S. J., Peng, K.-W., & Bell, J. C. (2012) · Nature Biotechnology · doi:10.1038/nbt.2287 · Cited by 1,428 · see citing works
Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer
Heo, J., Reid, T. R., Ruo, L., Breitbach, C. J., Rose, S. C., Bloomston, M., Cho, M., Lim, H. Y., Chung, H. C., Kim, C. W., et al. (2013) · Nature Medicine · doi:10.1038/nm.3089 · Cited by 781 · see citing works
Self-citation
Oncolytic virus therapy: A new era of cancer treatment at dawn
Fukuhara, H., Ino, Y., & Todo, T. (2016) · Cancer Science · doi:10.1111/cas.13027 · Cited by 776 · see citing works
Oncolytic Viruses in Cancer Treatment
Lawler, S. E., Speranza, M. C., Cho, C., & Chiocca, E. A. (2016) · JAMA Oncology · doi:10.1001/jamaoncol.2016.2064 · Cited by 602 · see citing works
Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans
Breitbach, C. J., Burke, J., Jonker, D. J., Stephenson, J., Haas, A. R., Chow, L. Q. M., Nieva, J. J., Hwang, T.-H., Moon, A., Patt, R. H., et al. (2011) · Nature · doi:10.1038/nature10358 · Cited by 552 · see citing works
Self-citation
Treatment of Liver CancerPreprint
Liu, C., Chen, K., & Chen, P. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a021535 · Cited by 401 · see citing works
Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity
Smith, G. L., Benfield, C. T. O., de Motes, C. M., Mazzon, M., Ember, S. W., Ferguson, B. J., & Sumner, R. P. (2013) · Journal of General Virology · doi:10.1099/vir.0.055921-0 · Cited by 359 · see citing works
Rational combination of oncolytic vaccinia virus and PD-L1 blockade works synergistically to enhance therapeutic efficacy
Liu, Z., Ravindranathan, R., Kaliński, P., Guo, Z. S., & Bartlett, D. L. (2017) · Nature Communications · doi:10.1038/ncomms14754 · Cited by 348 · see citing works
“These mice were injected with a -CD8 Ab on days 10, 11, 12, or a -CD4 Ab injection at 10, 15, 20 post tumour cell inoculations.”
The Oncolytic Poxvirus JX-594 Selectively Replicates in and Destroys Cancer Cells Driven by Genetic Pathways Commonly Activated in Cancers
Parato, K. A., Breitbach, C. J., Boeuf, F. L., Wang, J., Storbeck, C. J., Ilkow, C. S., Diallo, J., Falls, T. J., Burns, J. K., Garcia, V., et al. (2011) · Molecular Therapy · doi:10.1038/mt.2011.276 · Cited by 305 · see citing works
Self-citation
Oncolytic Vaccinia Virus Disrupts Tumor-Associated Vasculature in Humans
Breitbach, C. J., Arulanandam, R., Silva, N. D., Thorne, S. H., Patt, R. H., Daneshmand, M., Moon, A., Ilkow, C. S., Burke, J., Hwang, T.-H., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-2687 · Cited by 258 · see citing works
Self-citation
Preventing Postoperative Metastatic Disease by Inhibiting Surgery-Induced Dysfunction in Natural Killer Cells
Tai, L., de Souza, C. T., Bélanger, S., Ly, L., Alkayyal, A. A., Zhang, J., Rintoul, J. L., Ananth, A. A., Lam, T., Breitbach, C. J., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1993 · Cited by 241 · see citing works
“Oncolytic virus has shown several mechanisms of action including direct tumor cell cytotoxicity, tumor-specific vascular shutdown, and induction of innate and adaptive immune responses (28).”
BackgroundSelf-citation
Thunder and Lightning: Immunotherapy and Oncolytic Viruses Collide
Melcher, A. A., Parato, K. A., Rooney, C. M., & Bell, J. C. (2011) · Molecular Therapy · doi:10.1038/mt.2011.65 · Cited by 232 · see citing works
The Evolution of Poxvirus Vaccines
Sánchez-Sampedro, L., Perdiguero, B., Mejías‐Pérez, E., García‐Arriaza, J., Pilato, M. D., & Estéban, M. (2015) · Viruses · doi:10.3390/v7041726 · Cited by 217 · see citing works
“In this way, poxviruses have been engineered by the deletion of specific genes involved in nucleotide metabolism, interferon response, the cell cycle and other cell functions abnormally regulated in tumor cells (e.g., J2R, C11R, B18R [574] ).”
Background
Immune modulation of the tumor microenvironment for enhancing cancer immunotherapy
Devaud, C., John, L. B., Westwood, J. A., Darcy, P. K., & Kershaw, M. H. (2013) · OncoImmunology · doi:10.4161/onci.25961 · Cited by 207 · see citing works
“They can induce inflammatory mediators attracting myeloid cells and lymphocytes.(76) In addition, they can lyse a proportion of tumor cells, thereby releasing immunogenic antigens.”
Background
Targeting Tumor Vasculature With an Oncolytic Virus
Breitbach, C. J., Silva, N. S. D., Falls, T. J., Aladl, U. E., Evgin, L., Paterson, J. M., Sun, Y., Roy, D. G., Rintoul, J. L., Daneshmand, M., et al. (2011) · Molecular Therapy · doi:10.1038/mt.2011.26 · Cited by 204 · see citing works
Self-citation
Intratumoral expression of IL-7 and IL-12 using an oncolytic virus increases systemic sensitivity to immune checkpoint blockade
Nakao, S., Arai, Y., Tasaki, M., YAMASHITA, M., Murakami, R., Kawase, T., Amino, N., Nakatake, M., Kurosaki, H., Mori, M., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aax7992 · Cited by 191 · see citing works
Oncolytic Viruses for Cancer Therapy: Overcoming the Obstacles
Wong, H. H., Lemoine, N. R., & Wang, Y. (2010) · Viruses · doi:10.3390/v2010078 · Cited by 182 · see citing works
“Gene-manipulated oncolytic viruses such as Ad, herpes virus and vaccinia virus are being developed as a new class of anti-tumoral agent [23,40,41].”
Background
Vaccinia Virus Protein C6 Is a Virulence Factor that Binds TBK-1 Adaptor Proteins and Inhibits Activation of IRF3 and IRF7
Unterholzner, L., Sumner, R. P., Baran, M., Ren, H., Mansur, D. S., Bourke, N. M., Randow, F., Smith, G. L., & Bowie, A. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002247 · Cited by 171 · see citing works
“Furthermore, VACV strains are in development as vaccine delivery systems against smallpox and other pathogens (reviewed in [62]), and as vectors for the targeting of tumours and for gene therapy (reviewed in [63]).”
Background
Cell Carriers for Oncolytic Viruses: Fed Ex for Cancer Therapy
Willmon, C. L., Harrington, K. J., Kottke, T. J., Prestwich, R. J. D., Melcher, A. A., & Vile, R. G. (2009) · Molecular Therapy · doi:10.1038/mt.2009.194 · Cited by 167 · see citing works
A Mechanistic Proof-of-concept Clinical Trial With JX-594, a Targeted Multi-mechanistic Oncolytic Poxvirus, in Patients With Metastatic Melanoma
Hwang, T.-H., Moon, A., Burke, J., Ribas, A., Stephenson, J., Breitbach, C. J., Daneshmand, M., Silva, N. D., Parato, K. A., Diallo, J., et al. (2011) · Molecular Therapy · doi:10.1038/mt.2011.132 · Cited by 159 · see citing works
Self-citation
Tumor Microenvironment Remodeling by Intratumoral Oncolytic Vaccinia Virus Enhances the Efficacy of Immune-Checkpoint Blockade
Chon, H. J., Lee, W. S., Yang, H., Kong, S. J., Lee, N. K., Moon, E. S., Choi, J., Han, E. C., Kim, J. H., Ahn, J. B., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-1932 · Cited by 158 · see citing works
“7 JX-594 (pexastimogene devacirepvec, Pexa-vec) is an oncolytic vaccinia virus that is engineered to express an immune-activating transgene, GM-CSF, and that has the viral thymidine kinase gene disrupted (26,27).”
Background
CXCL12/CXCR4 Blockade by Oncolytic Virotherapy Inhibits Ovarian Cancer Growth by Decreasing Immunosuppression and Targeting Cancer-Initiating Cells
Gil, M., Komorowski, M. P., Seshadri, M., Rokita, H., McGray, A. R., Opyrchal, M., Odunsi, K. O., & Kozbor, D. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400201 · Cited by 151 · see citing works
“elevation, and type-1 IFN resistance (36).”
Targeting CXCL12/CXCR4 signaling with oncolytic virotherapy disrupts tumor vasculature and inhibits breast cancer metastases
Gil, M., Seshadri, M., Komorowski, M. P., Abrams, S. I., & Kozbor, D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220580110 · Cited by 148 · see citing works
“Discussion Although engineered OVVs have demonstrated promising results in the treatment of cancer in preclinical models and early clinical trials (21, 51), systemic efficacy against metastatic disease needs to be improved to have a major impact on cancer patient survival.”
Background
Vaccinia-based oncolytic immunotherapy Pexastimogene Devacirepvec in patients with advanced hepatocellular carcinoma after sorafenib failure: a randomized multicenter Phase IIb trial (TRAVERSE)
Moehler, M. H., Heo, J., Lee, H. C., Tak, W. Y., Chao, Y., Paik, S. W., Yim, H. J., Byun, K. S., Baron, A. D., Ungerechts, G., et al. (2019) · OncoImmunology · doi:10.1080/2162402x.2019.1615817 · Cited by 133 · see citing works
“Prior non-systemic therapies – n (%) Surgical resection 33 (38) 17 (40) TACE 49 (57) 27 (63) RFA 16 (19) 9 (21) Radiation Therapy 19 (22) 6 (14) Macroscopic vascular invasion – n (%) 20 (23) 10 (23) Tumor burden (SLD) in the liver (mm), Median (Range) 105 (15–257) 102 (34–314) e1615817-4 M.”
Self-citation
Targeting 4-1BB Costimulation to Disseminated Tumor Lesions With Bi-specific Oligonucleotide Aptamers
Pastor, F., Kolonias, D. S., McNamara, J. O., & Gilboa, E. (2011) · Molecular Therapy · doi:10.1038/mt.2011.145 · Cited by 132 · see citing works
Chemokine Expression From Oncolytic Vaccinia Virus Enhances Vaccine Therapies of Cancer
Li, J., O’Malley, M. E., Urban, J. A., Sampath, P., Guo, Z. S., Kaliński, P., Thorne, S. H., & Bartlett, D. L. (2011) · Molecular Therapy · doi:10.1038/mt.2010.312 · Cited by 131 · see citing works
Self-citation
Intratumoral delivery of inactivated modified vaccinia virus Ankara (iMVA) induces systemic antitumor immunity via STING and Batf3-dependent dendritic cells
Dai, P., Wang, W., Yang, N., Serna‐Tamayo, C., Ricca, J. M., Zamarin, D., Shuman, S., Merghoub, T., Wolchok, J. D., & Deng, L. (2017) · Science Immunology · doi:10.1126/sciimmunol.aal1713 · Cited by 123 · see citing works
Bridging the gap between traditional Chinese medicine and systems biology: the connection of Cold Syndrome and NEI network
Ma, T., Tan, C., Zhang, H., Wang, M., Ding, W., & Li, S. (2010) · Molecular BioSystems · doi:10.1039/b914024g · Cited by 119 · see citing works
Dendritic Cell and T Cell Crosstalk in Liver Fibrogenesis and Hepatocarcinogenesis: Implications for Prevention and Therapy of Liver Cancer
Lurje, I., Hammerich, L., & Tacke, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197378 · Cited by 118 · see citing works
“GM-CSF production from infected tumor cells has been suggested as an additional immunostimulatory mechanism [151,152].”
Background
Recent trends of nanomedicinal approaches in clinics
Dilnawaz, F., Acharya, S., & Sahoo, S. K. (2018) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2018.01.016 · Cited by 114 · see citing works
Engineering oncolytic viruses to exploit tumor specific defects in innate immune signaling pathways
Naik, S., & Russell, S. J. (2009) · Expert Opinion on Biological Therapy · doi:10.1517/14712590903170653 · Cited by 108 · see citing works
“Significant progress with VV oncolytics has taken place in an industrial setting with a conscious effort made to incorporate multiple mechanisms of action [56].”
Background
Oncolytic Parapoxvirus induces Gasdermin E-mediated pyroptosis and activates antitumor immunity
Lin, J., Sun, S., Zhao, K., Gao, F., Wang, R., Li, Q., Zhou, Y., Zhang, J., Li, Y., Wang, X., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-35917-2 · Cited by 110 · see citing works
Moving oncolytic viruses into the clinic: clinical-grade production, purification, and characterization of diverse oncolytic viruses
Ungerechts, G., Bossow, S., Leuchs, B., Holm, P. S., Rommelaere, J., Coffey, M. C., Coffin, R., Bell, J. C., & Nettelbeck, D. M. (2016) · Molecular Therapy — Methods & Clinical Development · doi:10.1038/mtm.2016.18 · Cited by 109 · see citing works
Targeting tumor suppressor genes for cancer therapy
Liu, Y., Hu, X., Han, C., Wang, L., Zhang, X., He, X., & Lu, X. (2015) · BioEssays · doi:10.1002/bies.201500093 · Cited by 106 · see citing works
“Onyx015 has been extensively tested in clinical trials [64].”
Background
Selective gene silencing by viral delivery of short hairpin RNA
Sliva, K., & Schnierle, B. S. (2010) · Virology Journal · doi:10.1186/1743-422x-7-248 · Cited by 107 · see citing works
“Also Reovirus [109,110], Poliovirus [111,112], Paramyxovirus [113], Vaccinia Virus [114-117] and Vesticular Stomatitis Virus [118] are being exploited.”
Background
Oncolytic vaccinia virus for the treatment of cancer
Guse, K., Cerullo, V., & Hemminki, A. (2011) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2011.558838 · Cited by 105 · see citing works
“This mechanism seems to have features of both necrosis and apoptosis [25].”
Background
Oncolytic and Immunotherapeutic Vaccinia Induces Antibody-Mediated Complement-Dependent Cancer Cell Lysis in Humans
Kim, M. K., Breitbach, C. J., Moon, A., Heo, J., Lee, Y. K., Cho, M., Lee, J. W., Kim, S.-G., Kang, D. H., Bell, J. C., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005361 · Cited by 101 · see citing works
Self-citation
Oncolytic Viruses: Therapeutics With an Identity Crisis
Breitbach, C. J., Lichty, B. D., & Bell, J. C. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.06.046 · Cited by 102 · see citing works
“OVs are multi-mechanistic therapeutics but their versatility has left them suffering from an identity crisis - are they in situ vaccines, systemically administered cancer killers, potent oncolytic vaccines, anti-vascular agents, gene therapy vectors, or loco-regional adjuvants that stimulate innate immune reactions? T…”
Background
Vectorization in an oncolytic vaccinia virus of an antibody, a Fab and a scFv against programmed cell death -1 (PD-1) allows their intratumoral delivery and an improved tumor-growth inhibition
Kleinpeter, P., Fend, L., Thioudellet, C., Geist, M., Sfrontato, N., Koerper, V., Fahrner, C., Schmitt, D., Gantzer, M., Remy‐Ziller, C., et al. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1220467 · Cited by 99 · see citing works
“These antitumoral effects of oncolytic vaccinia virus are mainly due to a combination of at least three recognized activities: (i) direct lysis or triggered apoptosis of infected tumor cells; (ii) disruption of tumor-associated vasculature by destruction of peritumoral endothelial cells and (iii) elicitation of an imm…”
Background
Oncolytic Poxviruses
Chan, W. M., & McFadden, G. (2014) · Annual Review of Virology · doi:10.1146/annurev-virology-031413-085442 · Cited by 98 · see citing works
“Such transgenes may encode cytokines to enhance the immune stimulatory effects of the virus, agents to disrupt tumor vasculature or the extracellular matrix that hinders virus spread, prodrug-converting enzymes that generate antimetabolites within the cancerous cells, and/or bioactive molecules to detect therapeutic e…”
Background
Internalization of Oncolytic Reovirus by Human Dendritic Cell Carriers Protects the Virus from Neutralization
Ilett, E. J., Bárcena, M., Errington‐Mais, F., Griffin, S. D. C., Harrington, K. J., Pandha, H., Coffey, M. C., Selby, P. J., Limpens, R. W. A. L., Mommaas, M., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-3266 · Cited by 97 · see citing works
“Recently there has been renewed interest in viral therapy for cancer and several viruses have been evaluated in clinical trials(1-3).”
Oncolytic viruses as immunotherapy: progress and remaining challenges
Aurelian, L. (2016) · OncoTargets and Therapy · doi:10.2147/ott.s63049 · Cited by 95 · see citing works
“For example, therapeutic efficacy was greatly increased in a mouse model of breast cancer by utilizing ex vivo expanded NKT cells (known as CIK) to deliver an oVV, 73 and DCs were shown to be effective cell carriers for oncolytic reovirus 74 and measles virus.”
TRAIL and Noxa Are Selectively Upregulated in Prostate Cancer Cells Downstream of the RIG-I/MAVS Signaling Pathway by Nonreplicating Sendai Virus Particles
Matsushima-Miyagi, T., Hatano, K., Nomura, M., Liu, L., Nishikawa, T., Saga, K., Shimbo, T., & Kaneda, Y. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1595 · Cited by 95 · see citing works
Hepatocellular Carcinoma from an Immunologic Perspective
Greten, T. F., Duffy, A. G., & Korangy, F. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-1721 · Cited by 93 · see citing works
“followed by the induction of a GM-CSF–enhanced anticancer immunity (38).”
Background
Oncolytic myxoma virus: The path to clinic
Chan, W. M., Rahman, M. M., & McFadden, G. (2013) · Vaccine · doi:10.1016/j.vaccine.2013.05.056 · Cited by 92 · see citing works
A Phase 2, Open-Label, Randomized Study of Pexa-Vec (JX-594) Administered by Intratumoral Injection in Patients with Unresectable Primary Hepatocellular Carcinoma
Breitbach, C. J., Moon, A., Burke, J., Hwang, T.-H., & Kirn, D. H. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2727-2_19 · Cited by 92 · see citing works
Self-citation
Signal transduction therapy of cancer
Levitzki, A., & Klein, S. (2010) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2010.04.001 · Cited by 85 · see citing works
“Some of these vaccines are in clinical trials (Schlom et al., 2007; Kirn and Thorne, 2009).”
Background
A vaccinia virus renaissance
Verardi, P. H., Titong, A., & Hagen, C. J. (2012) · Human Vaccines & Immunotherapeutics · doi:10.4161/hv.21080 · Cited by 84 · see citing works
Immunotherapy for hepatocellular carcinoma
Li, S., Yang, F., & Ren, X. (2015) · Drug Discoveries & Therapeutics · doi:10.5582/ddt.2015.01054 · Cited by 83 · see citing works
“JX-594 is an artificial genetic recombination vaccinia virus vaccine (70-72).”
Background
A single intravenous injection of oncolytic picornavirus SVV-001 eliminates medulloblastomas in primary tumor-based orthotopic xenograft mouse models
Yu, L., Baxter, P. A., Zhao, X., Liu, Z., Wadhwa, L., Zhang, Y., Su, J. M. F., Tan, X., Yang, J., Adesina, A. M., et al. (2010) · Neuro-Oncology · doi:10.1093/neuonc/noq148 · Cited by 80 · see citing works
“Efforts are thus being made to develop oncolytic virus that can be systemically administered, such as oncolytic poxviruses and including vaccinia virus.(26,27) The Seneca Valley virus-001 (SVV-001) is a native single-strand RNA virus that belongs to the family Picornaviridae.”
Background
Emerging Nano-/Biotechnology Drives Oncolytic Virus-Activated and Combined Cancer Immunotherapy
Fang, C., Xiao, G., Wang, T., Li, S., Peng, B., Xu, B., & Zhang, K. (2023) · Research · doi:10.34133/research.0108 · Cited by 79 · see citing works
“0108 8 The biosafety of biomolecules such as small interfering RNA could be significantly enhanced if OVs were able to selectively replicate into higher load in tumor tissues than in normal tissues after intravenous administration [100].”
Background
Bugs and Drugs: Oncolytic Virotherapy in Combination with Chemotherapy
Wennier, S. T., Liu, J., & McFadden, G. (2012) · Current Pharmaceutical Biotechnology · doi:10.2174/138920112800958850 · Cited by 77 · see citing works
“Replication competent OVs are very diverse and belong to many different virus families (Table 1) [18-33].”
Background
Phase I/II study of PexaVec in combination with immune checkpoint inhibition in refractory metastatic colorectal cancer
Monge, C., Xie, C., Myojin, Y., Coffman, K., Hrones, D. M., Wang, S., Hernandez, J. M., Wood, B. J., Levy, E. B., Juburi, I., et al. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-005640 · Cited by 76 · see citing works
Enhancement of Vaccinia Virus Based Oncolysis with Histone Deacetylase Inhibitors
MacTavish, H., Diallo, J., Huang, B., Stanford, M. M., Bœuf, F. L., Silva, N. D., Cox, J. A., Simmons, J.-G., Guimond, T., Falls, T. J., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014462 · Cited by 76 · see citing works
“It has an extensive safety history in humans, a large cloning capacity for insertion of therapeutic transgene payloads, is active as a systemic agent, lacks any known genotoxic activity and expresses a sophisticated array of immune modulating genes that can be exploited for therapeutic benefit [1].”
Self-citation
Synergistic anti-tumor effects between oncolytic vaccinia virus and paclitaxel are mediated by the IFN response and HMGB1
Huang, B., Sikorski, R. P., Kirn, D. H., & Thorne, S. H. (2010) · Gene Therapy · doi:10.1038/gt.2010.121 · Cited by 76 · see citing works
Self-citation
Complement Inhibition Prevents Oncolytic Vaccinia Virus Neutralization in Immune Humans and Cynomolgus Macaques
Evgin, L., Acuña, S. A., de Souza, C. T., Marguerie, M., Lemay, C. G., Ilkow, C. S., Findlay, C. S., Falls, T. J., Parato, K. A., Hanwell, D., et al. (2015) · Molecular Therapy · doi:10.1038/mt.2015.49 · Cited by 76 · see citing works
Self-citation
In Situ Vaccination as a Strategy to Modulate the Immune Microenvironment of Hepatocellular Carcinoma
Lurje, I., Werner, W., Mohr, R. U., Roderburg, C., Tacke, F., & Hammerich, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.650486 · Cited by 75 · see citing works
“They replicate inside and lyse cancerous cells, releasing TAAs in an immunogenic fashion with simultaneous release of DAMPs and pathogen associated molecular patterns (PAMPs) (53, 55).”
Background
HPMA copolymers for masking and retargeting of therapeutic viruses☆
Fisher, K. D., & Seymour, L. W. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.12.003 · Cited by 74 · see citing works
Novel theranostic agents for next-generation personalized medicine: small molecules, nanoparticles, and engineered mammalian cells
Kojima, R., Aubel, D., & Fussenegger, M. (2015) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2015.05.021 · Cited by 74 · see citing works
Prolonged systemic circulation of chimeric oncolytic adenovirus Ad5/3-Cox2L-D24 in patients with metastatic and refractory solid tumors
Pesonen, S. A., Nokisalmi, P., Escutenaire, S., Särkioja, M., Raki, M., Cerullo, V., Kangasniemi, L., Laasonen, L., Ribacka, C., Guse, K., et al. (2010) · Gene Therapy · doi:10.1038/gt.2010.17 · Cited by 72 · see citing works
Vaccinia virus evasion of regulated cell death
Veyer, D. L., Carrara, G., de Motes, C. M., & Smith, G. L. (2017) · Immunology Letters · doi:10.1016/j.imlet.2017.03.015 · Cited by 72 · see citing works
“Although this was the basis for the development of the first oncolytic viral agents, several clinical trials have demonstrated the need to harness the immune response associated to the oncolytic agent to guarantee optimal therapeutic activity [159].”
Background
Synthetic therapeutic gene circuits in mammalian cells
Ye, H., & Fussenegger, M. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.05.003 · Cited by 69 · see citing works
Oncolytic virus therapy for cancer
Kaufman, H. L., Goldufsky, J. W., Sivendran, Harcharik, S., Pan, M., Bernardo, S. G., Stern, R. H., Friedlander, P. A., Ruby, C. E., & Saenger, Y. M. (2013) · Oncolytic Virotherapy · doi:10.2147/ov.s38901 · Cited by 70 · see citing works
“34,35 A 36–38 Induction of antitumor immunity is likely aided by oncolytic-mediated cell death and release of tumor antigens and danger signals, such as ATP and high mobility group box-1, into the extra-cellular microenvironment.”
Oncolytic viruses in radiation oncology
Touchefeu, Y., Vassaux, G., & Harrington, K. J. (2011) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2011.05.078 · Cited by 69 · see citing works
Oncolytic VSV Primes Differential Responses to Immuno-oncology Therapy
Durham, N. M., Mulgrew, K. A., McGlinchey, K., Monks, N. R., Ji, H. T., Herbst, R., Suzich, J., Hammond, S. A., & Kelly, E. J. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.05.006 · Cited by 66 · see citing works
Development of oncolytic virotherapy: from genetic modification to combination therapy
Lan, Q., Xia, S., Wang, Q., Xu, W., Huang, H., Jiang, S., & Lu, L. (2020) · Frontiers of Medicine · doi:10.1007/s11684-020-0750-4 · Cited by 66 · see citing works
Reovirus in cancer therapy: an evidence-based review
Lee, P. C., Clements, D. R., Helson, E., & Gujar, S. A. (2014) · Oncolytic Virotherapy · doi:10.2147/ov.s51321 · Cited by 66 · see citing works
Expression of CCL19 from Oncolytic Vaccinia Enhances Immunotherapeutic Potential while Maintaining Oncolytic Activity
Li, J., O’Malley, M. E., Sampath, P., Kaliński, P., Bartlett, D. L., & Thorne, S. H. (2012) · Neoplasia · doi:10.1593/neo.121272 · Cited by 64 · see citing works
“One factor driving the advances in this next generation of oncolytic viruses has been the realization that their immunotherapeutic activity is critical for their success [5,6].”
BackgroundSelf-citation
Genetically Engineered Microorganisms and Their Impact on Human Health
Mahdizade Ari, M., Dadgar, L., Elahi, Z., Ghanavati, R., & Taheri, B. (2024) · International Journal of Clinical Practice · doi:10.1155/2024/6638269 · Cited by 67 · see citing works
Synthetic Genomics and Synthetic Biology Applications Between Hopes and Concerns
König, H., Frank, D. O., Heil, R., & Coenen, C. (2013) · Current Genomics · doi:10.2174/1389202911314010003 · Cited by 63 · see citing works
“Similarly, a pox virus that shows tumorspecific replication (in clinical trials) based on targeting multiple mechanisms [35] was rationally constructed by simple genetic engineering, involving viral thymidine kinase gene inactivation and expression of a human transgene for granulocyte-macrophage colony stimulating fac…”
Background
Current status of gene therapy for brain tumors
Murphy, A. M., & Rabkin, S. D. (2012) · Translational research · doi:10.1016/j.trsl.2012.11.003 · Cited by 62 · see citing works
Oncolytic Viruses in the Treatment of Cancer: A Review of Current Strategies
Zeyaullah, M., Patro, M., Ahmad, I., Ibraheem, K., Sultan, P., Nehal, M., & Ali, A. (2012) · Pathology & Oncology Research · doi:10.1007/s12253-012-9548-2 · Cited by 62 · see citing works
“One advantage of oncolytic viruses is that they are known to destroy tumors by several distinct mechanisms, which typically do not overlap with the mechanisms induced by traditional therapies [12, 28, 31].”
Background
Amplification of Oncolytic Vaccinia Virus Widespread Tumor Cell Killing by Sunitinib through Multiple Mechanisms
Kim, M., Nitschké, M., Sennino, B., Murer, P., Schriver, B. J., Bell, A., Subramanian, A., McDonald, C. E., Wang, J., Cha, H., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-15-3308 · Cited by 62 · see citing works
“WR is a Wyeth strain vaccinia virus isolated through serial passage in mice to select for replication in mouse cells (34).”
BackgroundSelf-citation
Application of oncolytic virus in tumor therapy
Huang, Z., Guo, H., Lin, L., Li, S., Yang, Y., Han, Y., Huang, W., & Yang, J. (2023) · Journal of Medical Virology · doi:10.1002/jmv.28729 · Cited by 61 · see citing works
“Furthermore, OVs can damage tumor blood vessels and activate antitumor immunity in addition to killing cancer cells.(149) As most OVs”
Background
Oncolytic vaccinia virus demonstrates antiangiogenic effects mediated by targeting of VEGF
Hou, W., Chen, H., Rojas, J. J., Sampath, P., & Thorne, S. H. (2014) · International Journal of Cancer · doi:10.1002/ijc.28747 · Cited by 61 · see citing works
“One reason for the success of oncolytic virotherapy is the capacity of the agents to target the tumor through multiple mechanisms independent from those typically utilized by more traditional chemotherapies and radiotherapy.(2) This includes direct tumor cell destruction resulting from viral replication as well as the…”
BackgroundSelf-citation
Synergistic Combination of Oncolytic Virotherapy and Immunotherapy for Glioma
Tang, B., Guo, Z. S., Bartlett, D. L., Yan, D. Z., Schane, C. P., Thomas, D., Liu, J., McFadden, G., Shisler, J. L., & Roy, E. J. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-3626 · Cited by 61 · see citing works
The emerging therapeutic potential of the oncolytic immunotherapeutic Pexa-Vec (JX-594)
Breitbach, C. J., Bell, J. C., Hwang, T.-H., Kirn, D. H., & Burke, J. (2015) · Oncolytic Virotherapy · doi:10.2147/ov.s59640 · Cited by 60 · see citing works
Self-citation
Antiangiogenic Arming of an Oncolytic Vaccinia Virus Enhances Antitumor Efficacy in Renal Cell Cancer Models
Guse, K., Słoniecka, M., Diaconu, I., Ottolino‐Perry, K., Tang, N., Ng, C. S. H., Boeuf, F. L., Bell, J. C., McCart, J. A., Ristimäki, A., et al. (2009) · Journal of Virology · doi:10.1128/jvi.00692-09 · Cited by 59 · see citing works
“Moreover, good safety and preliminary evidence of antitumor efficacy were seen in phase 1 clinical trials (22, 26, 32).”
Background
Virosome: A novel vector to enable multi-modal strategies for cancer therapy
Kaneda, Y. (2011) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2011.03.007 · Cited by 59 · see citing works
Oncolytic vaccinia virus and cancer immunotherapy
Xu, L., Sun, H., Lemoine, N. R., Xuan, Y., & Wang, P. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1324744 · Cited by 58 · see citing works
“VACV is an enveloped double stranded DNA orthopoxvirus, in which the most widely used experimental strains include Lister, Western Reserve (WR), Wyeth strains, Copenhagen strains, Ankara (also known as MVA), and Tiantan stains etc (10).”
Background
DNA-PK Is Targeted by Multiple Vaccinia Virus Proteins to Inhibit DNA Sensing
Scutts, S. R., Ember, S. W., Ren, H., Ye, C., Lovejoy, C. A., Mazzon, M., Veyer, D. L., Sumner, R. P., & Smith, G. L. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.034 · Cited by 57 · see citing works
“, 1983a, 1983b) and as an oncolytic agent (Buller et al., 1985; Heo et al., 2013; Kirn and Thorne, 2009).”
Background
Combination therapy with oncolytic viruses and immune checkpoint inhibitors in head and neck squamous cell carcinomas: an approach of complementary advantages
Dong, H., Li, M., Yang, C., Wei, W., He, X., Cheng, G., & Wang, S. (2023) · Cancer Cell International · doi:10.1186/s12935-022-02846-x · Cited by 57 · see citing works
“Induce systemic anti‐tumor immunity (1) Adaptive immunity activation: neoplastic cells release threat-associated molecular pattern molecules, pathogen-associated molecular pattern molecules, and a multiplicity of tumor-associated antigens (TAAs) after lysis to recruit immune cells, which infiltrate the tumor and activ…”
Background
The role of signalling and the cytoskeleton during Vaccinia Virus egress
Leite, F. G. G., & Way, M. (2015) · Virus Research · doi:10.1016/j.virusres.2015.01.024 · Cited by 57 · see citing works
Bioinspired Artificial Tobacco Mosaic Virus with Combined Oncolytic Properties to Completely Destroy Multidrug‐Resistant Cancer
Wu, H., Zhong, D., Zhang, Z., Li, Y., Zhang, X., Li, Y., Zhang, Z., Xu, X., Yang, J., & Gu, Z. (2020) · Advanced Materials · doi:10.1002/adma.201904958 · Cited by 57 · see citing works
Recent advances of nanomedicines for liver cancer therapy
Chi, X., Liu, K., Luo, X., Yin, Z., Lin, H., & Gao, J. (2020) · Journal of Materials Chemistry B · doi:10.1039/c9tb02871d · Cited by 57 · see citing works
Immunotherapeutic potential of oncolytic vaccinia virus
Thorne, S. H. (2011) · Immunologic Research · doi:10.1007/s12026-011-8211-4 · Cited by 55 · see citing works
“It has also become apparent (especially when viruses capable of replicating in mouse cells were studied, so facilitating the pre-clinical study of immunocompetent animal tumor models) that the immune response induced by the virus can provide a beneficial anti-tumor effect [ 2 , 25].”
BackgroundSelf-citation
Evolution of Oncolytic Viruses: Novel Strategies for Cancer Treatment
Atherton, M. J., & Lichty, B. D. (2013) · Immunotherapy · doi:10.2217/imt.13.123 · Cited by 55 · see citing works
Viral gene therapy for breast cancer: progress and challenges
Asad, A. S., Ayala, M. A. M., Gottardo, M. F., Zuccato, C. F., Candia, A. J. N., Zanetti, F., Seilicovich, A., & Candolfi, M. (2017) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2017.1338684 · Cited by 55 · see citing works
“) stability and efficient delivery to metastatic tumors through blood vessels, (7) rapid spread within tumors, and (8) good safety in humans [66,67].”
Background
Crosstalk Between Immune Cell and Oncolytic Vaccinia Therapy Enhances Tumor Trafficking and Antitumor Effects
Sampath, P., Li, J., Hou, W., Chen, H., Bartlett, D. L., & Thorne, S. H. (2012) · Molecular Therapy · doi:10.1038/mt.2012.257 · Cited by 53 · see citing works
Self-citation
The combination of immunosuppression and carrier cells significantly enhances the efficacy of oncolytic poxvirus in the pre-immunized host
Guo, Z. S., Parimi, V., O’Malley, M. E., Thirunavukarasu, P., Sathaiah, M., Austin, F., & Bartlett, D. L. (2010) · Gene Therapy · doi:10.1038/gt.2010.104 · Cited by 53 · see citing works
Dendritic Cells in Oncolytic Virus-Based Anti-Cancer Therapy
Kim, Y., Clements, D. R., Sterea, A. M., Jang, H. G., Gujar, S. A., & Lee, P. C. (2015) · Viruses · doi:10.3390/v7122953 · Cited by 53 · see citing works
Host Lymphodepletion Enhances the Therapeutic Activity of an Oncolytic Vaccinia Virus Expressing 4-1BB Ligand
Kim, H. S., Kim‐Schulze, S., Kim, D. W., & Kaufman, H. L. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-2522 · Cited by 52 · see citing works
Oncolytic adenovirus research evolution: from cell-cycle checkpoints to immune checkpoints
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Background
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Authors: Kirn, D. H., & Thorne, S. H.
ORCID: Kirn, David H.
Venue: Nature Reviews Cancer
Publisher: Springer Science and Business Media LLC
Published: 2009-01
Volume: 9
Issue: 1
Pages: 64-71
ISSN: 1474-175X (ISSN-L)
1474-1768
DOI: 10.1038/nrc2545
OpenAlex: W2079647238
Cited by: 402
References: 134
Citations by year: 2026: 7 · 2025: 7 · 2024: 19 · 2023: 14 · 2022: 16 · 2021: 16 · 2020: 20 · 2019: 14 · 2018: 16 · 2017: 24 · 2016: 25 · 2015: 29 · 2014: 29 · 2013: 49 · 2012: 36
FWCI: 2.47
Type: journal article
Language: en
Open access: closed
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature reviews. Cancer (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Life Sciences › Immunology and Microbiology › Virology › Poxvirus research and outbreaks
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
Keywords: vaccinia virus, cancer gene therapy, cancer vaccines, viral vectors
MeSH terms: Animals, Forecasting, Humans, Immunity, Cellular, Inflammation, Neoplasm Metastasis, Neoplasms, Poxviridae, Vaccinia virus, Virus Replication, Gene Expression Regulation, Viral, Cancer Vaccines, Oncolytic Virotherapy, Oncolytic Viruses, Mice, Host-Pathogen Interactions

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Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer

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