Review
. 2019 Jul;18(9).
doi: 10.1038/s41573-019-0029-0.

Optimizing oncolytic virotherapy in cancer treatment

Kevin Harrington 1 Daniel J Freeman 2 Beth Kelly 2 James Harper 3 Jean-Charles Soria 2 
Affiliations
  • PMID: 31292532
  •     64 citations

Abstract

In the wake of the success of modern immunotherapy, oncolytic viruses (OVs) are currently seen as a potential therapeutic option for patients with cancer who do not respond or fail to achieve durable responses following treatment with immune checkpoint inhibitors. OVs offer a multifaceted therapeutic platform because they preferentially replicate in tumour cells, can be engineered to express transgenes that augment their cytotoxic and immunostimulatory activities, and modulate the tumour microenvironment to optimize immune-mediated tumour eradication, both at locoregional and systemic sites of disease. Lysis of tumour cells releases tumour-specific antigens that trigger both the innate and adaptive immune systems. OVs also represent attractive combination partners with other systemically delivered agents by virtue of their highly favourable safety profiles. Rational combinations of OVs with different immune modifiers and/or antitumour agents, based on mechanisms of tumour resistance to immune-mediated attack, may benefit the large, currently underserved, population of patients who respond poorly to immune checkpoint inhibition.

Immunomodulatory Drugs Encoded by Oncolytic Viruses: Is the Whole Greater Than the Sum?
Dmitriy Zamarin.
Mol Ther, 2019 Oct 07; 27(11). PMID: 31586519    Free PMC article.
Immunological Effects and Viral Gene Expression Determine the Efficacy of Oncolytic Measles Vaccines Encoding IL-12 or IL-15 Agonists.
Paul S Backhaus, Rūta Veinalde, +8 authors, Christine E Engeland.
Viruses, 2019 Oct 19; 11(10). PMID: 31623390    Free PMC article.
Virotherapy as a Potential Therapeutic Approach for the Treatment of Aggressive Thyroid Cancer.
Anna Maria Malfitano, Sarah Di Somma, Nella Prevete, Giuseppe Portella.
Cancers (Basel), 2019 Oct 23; 11(10). PMID: 31636245    Free PMC article.
Review.
Oncolytic Adenovirus-A Nova for Gene-Targeted Oncolytic Viral Therapy in HCC.
Mubalake Abudoureyimu, Yongting Lai, +3 authors, Xiaoyuan Chu.
Front Oncol, 2019 Nov 30; 9. PMID: 31781493    Free PMC article.
Review.
The reciprocal regulation between host tissue and immune cells in pancreatic ductal adenocarcinoma: new insights and therapeutic implications.
Xiaomeng Liu, Jin Xu, +6 authors, Si Shi.
Mol Cancer, 2019 Dec 14; 18(1). PMID: 31831007    Free PMC article.
Review.
Gene Therapy for Liver Cancers: Current Status from Basic to Clinics.
Kenya Kamimura, Takeshi Yokoo, Hiroyuki Abe, Shuji Terai.
Cancers (Basel), 2019 Nov 27; 11(12). PMID: 31769427    Free PMC article.
Review.
Engineering Newcastle Disease Virus as an Oncolytic Vector for Intratumoral Delivery of Immune Checkpoint Inhibitors and Immunocytokines.
Gayathri Vijayakumar, Stephen McCroskery, Peter Palese.
J Virol, 2019 Nov 07; 94(3). PMID: 31694938    Free PMC article.
Oncolytic Viruses and the Immune System: The Dynamic Duo.
Ana Lemos de Matos, Lina S Franco, Grant McFadden.
Mol Ther Methods Clin Dev, 2020 Feb 20; 17. PMID: 32071927    Free PMC article.
Review.
Immunotherapies for pediatric cancer: current landscape and future perspectives.
Brian Hutzen, Siddhi Nath Paudel, +3 authors, Timothy P Cripe.
Cancer Metastasis Rev, 2019 Dec 13; 38(4). PMID: 31828566    Free PMC article.
Review.
Embelin Promotes Oncolytic Vaccinia Virus-Mediated Antitumor Immunity Through Disruption of IL-6/STAT3 Signaling in Lymphoma.
Peng Wang, Yi Wu, +4 authors, Shibing Wang.
Onco Targets Ther, 2020 Feb 29; 13. PMID: 32110041    Free PMC article.
Oncolytic Virotherapy with Myxoma Virus.
Masmudur M Rahman, Grant McFadden.
J Clin Med, 2020 Jan 16; 9(1). PMID: 31936317    Free PMC article.
Review.
STAT3/5 Inhibitors Suppress Proliferation in Bladder Cancer and Enhance Oncolytic Adenovirus Therapy.
Sruthi V Hindupur, Sebastian C Schmid, +8 authors, Roman Nawroth.
Int J Mol Sci, 2020 Feb 13; 21(3). PMID: 32046095    Free PMC article.
Repurposing infectious disease vaccines for intratumoral immunotherapy.
Ignacio Melero, Maria Gato, +6 authors, Aurelien Marabelle.
J Immunother Cancer, 2020 Feb 28; 8(1). PMID: 32102830    Free PMC article.
Replicative conditioning of Herpes simplex type 1 virus by Survivin promoter, combined to ERBB2 retargeting, improves tumour cell-restricted oncolysis.
Emanuele Sasso, Guendalina Froechlich, +9 authors, Nicola Zambrano.
Sci Rep, 2020 Mar 11; 10(1). PMID: 32152425    Free PMC article.
Immunotherapy for mesothelioma: a critical review of current clinical trials and future perspectives.
Steven G Gray, Luciano Mutti.
Transl Lung Cancer Res, 2020 Mar 25; 9(Suppl 1). PMID: 32206576    Free PMC article.
Review.
Oncolytic Herpes Simplex Virus Encoding IL12 Controls Triple-Negative Breast Cancer Growth and Metastasis.
Shanawaz M Ghouse, Hong-My Nguyen, +2 authors, Dipongkor Saha.
Front Oncol, 2020 Apr 09; 10. PMID: 32266155    Free PMC article.
Therapeutic Advances of Stem Cell-Derived Extracellular Vesicles in Regenerative Medicine.
Lei Yin, Xiaotian Liu, +6 authors, Hui Qian.
Cells, 2020 Mar 19; 9(3). PMID: 32183102    Free PMC article.
Review.
Oncolytic Adenovirus Armed with BiTE, Cytokine, and Checkpoint Inhibitor Enables CAR T Cells to Control the Growth of Heterogeneous Tumors.
Caroline E Porter, Amanda Rosewell Shaw, +8 authors, Masataka Suzuki.
Mol Ther, 2020 Mar 08; 28(5). PMID: 32145203    Free PMC article.
Overcoming resistance to anti-PD1 and anti-PD-L1 treatment in gastrointestinal malignancies.
Alberto Puccini, Francesca Battaglin, +2 authors, Mohamed E Salem.
J Immunother Cancer, 2020 May 13; 8(1). PMID: 32393474    Free PMC article.
Review.
Combining Oncolytic Viruses With Cancer Immunotherapy: Establishing a New Generation of Cancer Treatment.
Tao Shi, Xueru Song, +2 authors, Jia Wei.
Front Immunol, 2020 May 16; 11. PMID: 32411132    Free PMC article.
Review.
Oncolytic Newcastle disease virus activation of the innate immune response and priming of antitumor adaptive responses in vitro.
Shannon Burke, Amy Shergold, +6 authors, Danielle K Carroll.
Cancer Immunol Immunother, 2020 Feb 24; 69(6). PMID: 32088771    Free PMC article.
Effective Treatment of Glioblastoma Multiforme With Oncolytic Virotherapy: A Case-Series.
Benjamin Gesundheit, Eliel Ben-David, +9 authors, Arno Thaller.
Front Oncol, 2020 Jun 02; 10. PMID: 32477944    Free PMC article.
Temozolomide antagonizes oncolytic immunovirotherapy in glioblastoma.
Dipongkor Saha, Samuel D Rabkin, Robert L Martuza.
J Immunother Cancer, 2020 May 28; 8(1). PMID: 32457126    Free PMC article.
Oncolytic virotherapy meets the human organoid technology for pancreatic cancers.
Elena Fiorini, Vincenzo Corbo.
EBioMedicine, 2020 Jun 24; 57. PMID: 32574953    Free PMC article.
Efficacy and Safety of Oncolytic Viruses in Randomized Controlled Trials: A Systematic Review and Meta-Analysis.
Zengbin Li, Zeju Jiang, +2 authors, Qiong Liu.
Cancers (Basel), 2020 Jun 04; 12(6). PMID: 32486227    Free PMC article.
Review.
Stem cell programs in cancer initiation, progression, and therapy resistance.
Tianzhi Huang, Xiao Song, +6 authors, Shi-Yuan Cheng.
Theranostics, 2020 Aug 06; 10(19). PMID: 32754274    Free PMC article.
Review.
Bi- and Tri-Specific T Cell Engager-Armed Oncolytic Viruses: Next-Generation Cancer Immunotherapy.
Zong Sheng Guo, Michael T Lotze, +2 authors, Xiao-Tong Song.
Biomedicines, 2020 Jul 16; 8(7). PMID: 32664210    Free PMC article.
Review.
Safety studies and viral shedding of intramuscular administration of oncolytic vaccinia virus TG6002 in healthy beagle dogs.
Jérémy Béguin, Virginie Nourtier, +9 authors, Philippe Erbs.
BMC Vet Res, 2020 Aug 28; 16(1). PMID: 32843040    Free PMC article.
Recombinant viruses delivering the necroptosis mediator MLKL induce a potent antitumor immunity in mice.
Lien Van Hoecke, Stephanie Riederer, +2 authors, Juan José Rojas.
Oncoimmunology, 2020 Sep 15; 9(1). PMID: 32923163    Free PMC article.
Absent in melanoma 2 enhances anti-tumour effects of CAIX promotor controlled conditionally replicative adenovirus in renal cancer.
Dafei Chai, Dong Qiu, +7 authors, Junnian Zheng.
J Cell Mol Med, 2020 Jul 30; 24(18). PMID: 32725966    Free PMC article.
Viruses of protozoan parasites and viral therapy: Is the time now right?
Paul Barrow, Jean Claude Dujardin, +7 authors, Marco Lalle.
Virol J, 2020 Oct 01; 17(1). PMID: 32993724    Free PMC article.
Review.
Oncolytic Virotherapy in Glioma Tumors.
Sergio Rius-Rocabert, Noemí García-Romero, +2 authors, Estanislao Nistal-Villan.
Int J Mol Sci, 2020 Oct 18; 21(20). PMID: 33066689    Free PMC article.
Review.
From Conventional Therapies to Immunotherapy: Melanoma Treatment in Review.
Lukasz Kuryk, Laura Bertinato, +5 authors, Mariangela Garofalo.
Cancers (Basel), 2020 Oct 24; 12(10). PMID: 33092131    Free PMC article.
Review.
Immunotherapy of hepatocellular carcinoma with infection of hepatitis B or C virus.
Cecilia Monge Bonilla, Nicole A McGrath, Jianyang Fu, Changqing Xie.
Hepatoma Res, 2020 Nov 03; 6. PMID: 33134550    Free PMC article.
Oncolytic immunotherapy for metastatic cancer: lessons and future strategies.
Zong-Sheng Guo.
Ann Transl Med, 2020 Nov 05; 8(17). PMID: 33145332    Free PMC article.
Simultaneous Tumor and Stroma Targeting by Oncolytic Viruses.
Anne Everts, Melissa Bergeman, Grant McFadden, Vera Kemp.
Biomedicines, 2020 Nov 11; 8(11). PMID: 33167307    Free PMC article.
Review.
Design and Engineering of Deimmunized Vaccinia Viral Vectors.
Kevin Song, Mariya Viskovska.
Biomedicines, 2020 Nov 15; 8(11). PMID: 33187060    Free PMC article.
Review.
Precision Approaches in the Management of Colorectal Cancer: Current Evidence and Latest Advancements Towards Individualizing the Treatment.
Rebecca A Shuford, Ashley L Cairns, Omeed Moaven.
Cancers (Basel), 2020 Nov 27; 12(11). PMID: 33238500    Free PMC article.
Review.
The armed oncolytic adenovirus ZD55-IL-24 eradicates melanoma by turning the tumor cells from the self-state into the nonself-state besides direct killing.
Hai-Jun Hu, Xiu Liang, +13 authors, Xin-Yuan Liu.
Cell Death Dis, 2020 Dec 02; 11(11). PMID: 33257647    Free PMC article.
Lonidamine potentiates the oncolytic efficiency of M1 virus independent of hexokinase 2 but via inhibition of antiviral immunity.
Jing Cai, Wenbo Zhu, +9 authors, Jiankai Liang.
Cancer Cell Int, 2020 Dec 10; 20(1). PMID: 33292203    Free PMC article.
Anti-viral immunity in the tumor microenvironment: implications for the rational design of herpes simplex virus type 1 oncolytic virotherapy.
Paul J F Rider, Ifeanyi K Uche, Larissa Sweeny, Konstantin G Kousoulas.
Curr Clin Microbiol Rep, 2020 Dec 22; 6(4). PMID: 33344108    Free PMC article.
Newcastle Disease Virus at the Forefront of Cancer Immunotherapy.
Bharat Burman, Giulio Pesci, Dmitriy Zamarin.
Cancers (Basel), 2020 Dec 03; 12(12). PMID: 33260685    Free PMC article.
Review.
Mutant myogenin promoter-controlled oncolytic adenovirus selectively kills PAX3-FOXO1-positive rhabdomyosarcoma cells.
Hideki Yoshida, Mizuho Sato-Dahlman, +5 authors, Masato Yamamoto.
Transl Oncol, 2020 Dec 19; 14(2). PMID: 33338875    Free PMC article.
Modification of Extracellular Matrix Enhances Oncolytic Adenovirus Immunotherapy in Glioblastoma.
Juri Kiyokawa, Yoichiro Kawamura, +8 authors, Hiroaki Wakimoto.
Clin Cancer Res, 2020 Dec 02; 27(3). PMID: 33257429    Free PMC article.
Bluetongue Viruses Act as Novel Oncolytic Viruses to Effectively Inhibit Human Renal Cancer Cell Growth In Vitro and In Vivo.
Haozhou Wang, Liming Song, +2 authors, Xiaoguang Zhou.
Med Sci Monit, 2021 Jan 29; 27. PMID: 33507885    Free PMC article.
Recombinant oncolytic adenovirus expressing a soluble PVR elicits long-term antitumor immune surveillance.
Hailin Zhang, Yonghui Zhang, +5 authors, Jiwu Wei.
Mol Ther Oncolytics, 2021 Feb 13; 20. PMID: 33575467    Free PMC article.
Mesenchymal stem cells and oncolytic viruses: joining forces against cancer.
Rafael Moreno.
J Immunother Cancer, 2021 Feb 10; 9(2). PMID: 33558278    Free PMC article.
Review.
Advantages of targeting the tumor immune microenvironment over blocking immune checkpoint in cancer immunotherapy.
Tianyu Tang, Xing Huang, +3 authors, Tingbo Liang.
Signal Transduct Target Ther, 2021 Feb 21; 6(1). PMID: 33608497    Free PMC article.
Review.
Efficient antitumor effects of a novel oncolytic adenovirus fully composed of species B adenovirus serotype 35.
Ryosuke Ono, Kosuke Takayama, Fuminori Sakurai, Hiroyuki Mizuguchi.
Mol Ther Oncolytics, 2021 Feb 23; 20. PMID: 33614920    Free PMC article.
Personalizing Oncolytic Virotherapy for Glioblastoma: In Search of Biomarkers for Response.
Eftychia Stavrakaki, Clemens M F Dirven, Martine L M Lamfers.
Cancers (Basel), 2021 Feb 10; 13(4). PMID: 33557101    Free PMC article.
Review.
Mesenchymal stem cell carriers enhance anti-tumor efficacy of oncolytic virotherapy.
Xianyao Wang, Xing Zhao, Zhixu He.
Oncol Lett, 2021 Mar 06; 21(4). PMID: 33664802    Free PMC article.
Review.
Oncolytic vaccinia virus induces a novel phenotype of CD8+ effector T cells characterized by high ICOS expression.
Midori Yamashita, Mamoru Tasaki, +3 authors, Shinsuke Nakao.
Mol Ther Oncolytics, 2021 Mar 06; 20. PMID: 33665362    Free PMC article.
Novel Oncolytic Herpes Simplex Virus 1 VC2 Promotes Long-Lasting, Systemic Anti-melanoma Tumor Immune Responses and Increased Survival in an Immunocompetent B16F10-Derived Mouse Melanoma Model.
Ifeanyi Kingsley Uche, Natalie Fowlkes, +7 authors, Paul J F Rider.
J Virol, 2020 Nov 13; 95(3). PMID: 33177208    Free PMC article.
Oncolytic Viruses and Hematological Malignancies: A New Class of Immunotherapy Drugs.
Vanessa Innao, Vincenzo Rizzo, +2 authors, Alessandro Allegra.
Curr Oncol, 2021 Mar 12; 28(1). PMID: 33704184    Free PMC article.
Review.
The discovery and development of oncolytic viruses: are they the future of cancer immunotherapy?
Shunchuan Zhang, Samuel D Rabkin.
Expert Opin Drug Discov, 2020 Nov 25; 16(4). PMID: 33232188    Free PMC article.
Oncolytic adeno-immunotherapy modulates the immune system enabling CAR T-cells to cure pancreatic tumors.
Amanda Rosewell Shaw, Caroline E Porter, +7 authors, Masataka Suzuki.
Commun Biol, 2021 Mar 21; 4(1). PMID: 33742099    Free PMC article.
Delivery of cancer therapies by synthetic and bio-inspired nanovectors.
Tina Briolay, Tacien Petithomme, +3 authors, Nicolas Boisgerault.
Mol Cancer, 2021 Mar 26; 20(1). PMID: 33761944    Free PMC article.
Review.
Oncolytic Adenoviruses for Cancer Therapy.
Lorella Tripodi, Maria Vitale, Vincenzo Cerullo, Lucio Pastore.
Int J Mol Sci, 2021 Apr 04; 22(5). PMID: 33802281    Free PMC article.
Review.
Antibody-drug conjugates, cancer immunotherapy, and metronomic chemotherapy as novel approaches in cancer management.
Sudhir Chandra Sarangi, Pranav Sopory, Soumya Sucharita Pattnaik, K H Reeta.
Indian J Pharmacol, 2020 Dec 08; 52(5). PMID: 33283772    Free PMC article.
Review.
Low-dose ipilimumab plus nivolumab combined with IL-2 and hyperthermia in cancer patients with advanced disease: exploratory findings of a case series of 131 stage IV cancers - a retrospective study of a single institution.
R Kleef, R Nagy, +7 authors, T Bakacs.
Cancer Immunol Immunother, 2020 Nov 06; 70(5). PMID: 33151369
Oncolytic herpesvirus expressing PD-L1 BiTE for cancer therapy: exploiting tumor immune suppression as an opportunity for targeted immunotherapy.
Hena Khalique, Richard Baugh, +5 authors, Leonard W Seymour.
J Immunother Cancer, 2021 Apr 07; 9(4). PMID: 33820820    Free PMC article.
Intratumoral Virotherapy with Wild-Type Newcastle Disease Virus in Carcinoma Krebs-2 Cancer Model.
Kseniya S Yurchenko, Alexandra V Glushchenko, +5 authors, Alexander M Shestopalov.
Viruses, 2021 Apr 04; 13(4). PMID: 33806229    Free PMC article.
Is immunotherapy in the future of therapeutic management of sarcomas?
Ottavia Clemente, Alessandro Ottaiano, +9 authors, Salvatore Tafuto.
J Transl Med, 2021 Apr 28; 19(1). PMID: 33902630
Review.
Therapeutic cancer vaccines.
Mansi Saxena, Sjoerd H van der Burg, Cornelis J M Melief, Nina Bhardwaj.
Nat Rev Cancer, 2021 Apr 29;. PMID: 33907315
Review.