Reciprocal cellular cross-talk within the tumor microenvironment promotes oncolytic virus activity
Abstract
Tumors are complex ecosystems composed of networks of interacting 'normal' and malignant cells. It is well recognized that cytokine-mediated cross-talk between normal stromal cells, including cancer-associated fibroblasts (CAFs), vascular endothelial cells, immune cells, and cancer cells, influences all aspects of tumor biology. Here we demonstrate that the cross-talk between CAFs and cancer cells leads to enhanced growth of oncolytic virus (OV)-based therapeutics. Transforming growth factor-β (TGF-β) produced by tumor cells reprogrammed CAFs, dampened their steady-state level of antiviral transcripts and rendered them sensitive to virus infection. In turn, CAFs produced high levels of fibroblast growth factor 2 (FGF2), initiating a signaling cascade in cancer cells that reduced retinoic acid-inducible gene I (RIG-I) expression and impeded the ability of malignant cells to detect and respond to virus. In xenografts derived from individuals with pancreatic cancer, the expression of FGF2 correlated with the susceptibility of the cancer cells to OV infection, and local application of FGF2 to resistant tumor samples sensitized them to virotherapy both in vitro and in vivo. An OV engineered to express FGF2 was safe in tumor-bearing mice, showed improved therapeutic efficacy compared to parental virus and merits consideration for clinical testing.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
FGF2-rich and CAF-rich tumours might be particularly susceptible to oncolytic viral therapy.
“suggesting that FGF2-rich and CAF-rich tumours might be particularly susceptible to oncolytic viral therapy.131”
From Current and emerging concepts for systemic treatment of metastatic colorectal cancer (2025) · cites this paper as [131]
Cites
A new mathematical model for relative quantification in real-time RT-PCR
Pfaffl, M. W. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.9.e45 · Cited by 34,610 · see citing works
PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989 · see citing works
Accessories to the Crime: Functions of Cells Recruited to the Tumor Microenvironment
Hanahan, D., & Coussens, L. M. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.022 · Cited by 4,632 · see citing works
Kalluri, R., & Zeisberg, M. (2006) · Nature Reviews Cancer · doi:10.1038/nrc1877 · Cited by 4,538 · see citing works
Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K., Akira, S., & Fujita, T. (2004) · Nature Immunology · doi:10.1038/ni1087 · Cited by 3,935 · see citing works
Orimo, A., Gupta, P. B., Sgroi, D. C., Arenzana-Seisdedos, F., Delaunay, T., Naeem, R., Carey, V. J., Richardson, A. L., & Weinberg, R. A. (2005) · Cell · doi:10.1016/j.cell.2005.02.034 · Cited by 3,759 · see citing works
GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists
Eden, E., Navon, R., Steinfeld, I., Lipson, D., & Yakhini, Z. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-48 · Cited by 3,356 · see citing works
Determination of subcutaneous tumor size in athymic (nude) mice
Tomayko, M. M., & Reynolds, C. P. (1989) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00300234 · Cited by 1,830 · see citing works
Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion
Straussman, R., Morikawa, T., Shee, K., Barzily-Rokni, M., Qian, Z. R., Du, J., Davis, A., Mongare, M. M., Gould, J., Frederick, D. T., et al. (2012) · Nature · doi:10.1038/nature11183 · Cited by 1,771 · see citing works
Erez, N., Truitt, M., Olson, P., & Hanahan, D. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.041 · Cited by 1,515 · see citing works
RNA Polymerase III Detects Cytosolic DNA and Induces Type I Interferons through the RIG-I Pathway
Chiu, Y., MacMillan, J. B., & Chen, Z. J. (2009) · Cell · doi:10.1016/j.cell.2009.06.015 · Cited by 1,185 · see citing works
Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors
Wilson, T. R., Fridlyand, J., Yan, Y., Penuel, E., Burton, L., Chan, E., Peng, J., Lin, E., Wang, Y., Sosman, J., et al. (2012) · Nature · doi:10.1038/nature11249 · Cited by 1,134 · see citing works
Cancer-Associated Stromal Fibroblasts Promote Pancreatic Tumor Progression
Hwang, R. F., Moore, T. T., Arumugam, T., Ramachandran, V., Amos, K. D., Rivera, A. M., Ji, B., Evans, D. B., & Logsdon, C. D. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5714 · Cited by 1,093 · see citing works
Cancer immunoediting from immune surveillance to immune escape
Kim, R., Emi, M., & Tanabe, K. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02587.x · Cited by 1,078 · see citing works
Stojdl, D., Lichty, B., TENOEVER, B., Paterson, J., Power, A., Knowles, S., Marius, R., Reynard, J., Poliquin, L., Atkins, H., et al. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00241-1 · Cited by 894 · see citing works
Self-citationAblasser, A., Bauernfeind, F. G., Hartmann, G., Latz, E., Fitzgerald, K. A., & Hornung, V. (2009) · Nature Immunology · doi:10.1038/ni.1779 · Cited by 892 · see citing works
Spaeth, E. L., Dembinski, J. L., Sasser, A. K., Watson, K., Klopp, A., Hall, B., Andreeff, M., & Marini, F. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004992 · Cited by 807 · see citing works
Sun, Y., Campisi, J., Higano, C., Beer, T. M., Porter, P., Coleman, I., True, L., & Nelson, P. S. (2012) · Nature Medicine · doi:10.1038/nm.2890 · Cited by 793 · see citing works
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-citationDell, R. B., Holleran, S., & Ramakrishnan, R. (2002) · ILAR Journal · doi:10.1093/ilar.43.4.207 · Cited by 746 · see citing works
The role of stroma in pancreatic cancer: Diagnostic and therapeutic implications
Erkan, M., Hausmann, S., Michalski, C. W., Fingerle, A. A., Dobritz, M., Kleeff, J., & Friess, H. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.115 · Cited by 662 · see citing works
Going viral with cancer immunotherapy
Lichty, B. D., Breitbach, C. J., Stojdl, D. F., & Bell, J. C. (2014) · Nature reviews. Cancer · doi:10.1038/nrc3770 · Cited by 590 · see citing works
Self-citationIntravenous 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-citationCancer-associated fibroblasts and tumor growth – bystanders turning into key players
Östman, A., & Augsten, M. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.01.003 · Cited by 542 · see citing works
Rønnov‐Jessen, L., & PETERSEN, O. W. (1993) · PubMed · Cited by 514 · see citing works
Cancer associated fibroblasts: the dark side of the coin.
Cirri, P., & Chiarugi, P. (2011) · Europe PMC (PubMed Central) · Cited by 501 · see citing works
Activation of fibroblasts in cancer stroma
Räsänen, K., & Vaheri, A. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.04.032 · Cited by 499 · see citing works
Nakasone, E. S., Askautrud, H. A., Kees, T., Park, J.-H., Plaks, V., Ewald, A. J., Fein, M. R., Rasch, M. G., Tan, Y.-X., Qiu, J., et al. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.017 · Cited by 477 · see citing works
An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy
Chung, A. S., Wu, X., Zhuang, G., Ngu, H., Kasman, I., Zhang, J., Vernes, J.-M., Jiang, Z., Meng, Y. G., Peale, F. V., et al. (2013) · Nature Medicine · doi:10.1038/nm.3291 · Cited by 445 · see citing works
Self-citationCancer associated fibroblasts in cancer pathogenesis
Franco, O. E., Shaw, A. K., Strand, D. W., & Hayward, S. W. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.10.010 · Cited by 395 · see citing works
AltAnalyze and DomainGraph: analyzing and visualizing exon expression data
Emig, D., Salomonis, N., Baumbach, J., Lengauer, T., Conklin, B. R., & Albrecht, M. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq405 · Cited by 324 · see citing works
Löhr, M. J., Schmidt, C., Ringel, J., Kluth, M., Müller, P., Nizze, H., & Jesnowski, R. (2001) · PubMed · Cited by 323 · see citing works
Kim, J. H., Oh, J. Y., Park, B. H., Lee, D. E., Kim, J. S., Park, H. E., Roh, M.-S., Je, J.-E., Yoon, J., Thorne, S. H., et al. (2006) · Molecular Therapy · doi:10.1016/j.ymthe.2006.05.008 · Cited by 303 · see citing works
Self-citationINTERFEROME: the database of interferon regulated genes
Samarajiwa, S., Forster, S. C., Auchettl, K., & Hertzog, P. J. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn732 · Cited by 266 · see citing works
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-citationEffect of Tumor Microenvironment Modulation on the Efficacy of Oncolytic Virus Therapy
Kurozumi, K., Hardcastle, J. J., Thakur, R., Yang, M., Christoforidis, G. A., Fulci, G., Hochberg, F. H., Weissleder, R., Carson, W. E., Chiocca, E. A., et al. (2007) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djm229 · Cited by 172 · see citing works
Identification of Genetically Modified Maraba Virus as an Oncolytic Rhabdovirus
Brun, J., McManus, D. C., Lefebvre, C. A., Hu, K., Falls, T. J., Atkins, H. L., Bell, J. C., McCart, J. A., Mahoney, D. J., & Stojdl, D. F. (2010) · Molecular Therapy · doi:10.1038/mt.2010.103 · Cited by 153 · see citing works
Self-citationLisanti, M. P., Martinez‐Outschoorn, U., & Sotgia, F. (2013) · Cell Cycle · doi:10.4161/cc.25695 · Cited by 119 · see citing works
Adaptive antiviral immunity is a determinant of the therapeutic success of oncolytic virotherapy.
Sobol, P. T., Boudreau, J., Stephenson, K., Wan, Y., Lichty, B., & Mossman, K. (2011) · Molecular Therapy · doi:10.1038/mt.2010.264 · Cited by 104 · see citing works
Self-citationErkan, M., Reiser–Erkan, C., Michalski, C. W., Kong, B., Esposito, I., Frieß, H., & Kleeff, J. H. (2012) · Current Molecular Medicine · doi:10.2174/156652412799218921 · Cited by 88 · see citing works
ICP0 Gene Expression Is a Herpes Simplex Virus Type 1 Apoptotic Trigger
Sanfilippo, C. M., & Blaho, J. A. (2006) · Journal of Virology · doi:10.1128/jvi.00334-06 · Cited by 77 · see citing works
Dayer, A. G., Jenny, B., Sauvain, M.-O., Potter, G., Salmon, P., Zgraggen, E., Kanemitsu, M., Gascon, E., Sizonenko, S. V., Trono, D., et al. (2007) · Brain · doi:10.1093/brain/awm200 · Cited by 75 · see citing works
Abnormal properties of skin fibroblasts from patients with breast cancer
Azzarone, B. G., Mareel, M., Billard, C., Scemama, P., Chaponnier, C., & Macieira‐Coelho, A. (1984) · International Journal of Cancer · doi:10.1002/ijc.2910330608 · Cited by 74 · see citing works
Schor, S. L., Schor, A. M., & Rushton, G. (1988) · Journal of Cell Science · doi:10.1242/jcs.90.3.401 · Cited by 72 · see citing works
Innate immunity, tumor microenvironment and oncolytic virus therapy: friends or foes?
Stanford, M. M., Breitbach, C. J., Bell, J. C., & McFadden, G. (2008) · PubMed · Cited by 44 · see citing works
Self-citationFetal myofibroblast‐like cells isolated from post‐radiation fibrosis in human breast cancer
Brouty‐Boyé, D., Raux, H., Azzarone, B. G., Tamboise, A., Tamboise, E., Beranger, S., Magnien, V., Pihan, I., Zardi, L., & Israël, L. (1991) · International Journal of Cancer · doi:10.1002/ijc.2910470512 · Cited by 37 · see citing works
Pickrell, B. B., Bhadkamkar, M. A., & Hollier, L. H. (2014) · Journal of Craniofacial Surgery · doi:10.1097/scs.0000000000000688 · Cited by 32 · see citing works
Altomonte, J., & Ebert, O. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00085 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Oncolytic viruses as engineering platforms for combination immunotherapy
Twumasi‐Boateng, K., Pettigrew, J. L., Kwok, Y. Y. E., Bell, J. C., & Nelson, B. H. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0009-4 · Cited by 423 · see citing works
Self-citationTalimogene Laherparepvec (T-VEC) and Other Oncolytic Viruses for the Treatment of Melanoma
Bommareddy, P. K., Patel, A. V., Hossain, S., & Kaufman, H. L. (2016) · American Journal of Clinical Dermatology · doi:10.1007/s40257-016-0238-9 · Cited by 323 · see citing works
Engineering strategies to enhance oncolytic viruses in cancer immunotherapy
Tian, Y., Xie, D., & Li, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00951-x · Cited by 304 · see citing works
Signaling pathways in cancer‐associated fibroblasts: recent advances and future perspectives
Fang, Z., Meng, Q., Xu, J., Wang, W., Zhang, B., Liu, J., Liang, C., Hua, J., Zhao, Y., Yu, X., et al. (2022) · 癌症:英文版 · doi:10.1002/cac2.12392 · Cited by 292 · see citing works
Vacchelli, E., Eggermont, A. M. M., Sautès‐Fridman, C., Galon, J., Zitvogel, L., Kroemer, G., & Galluzzi, L. (2013) · OncoImmunology · doi:10.4161/onci.24612 · Cited by 255 · see citing works
Antitumor Benefits of Antiviral Immunity: An Underappreciated Aspect of Oncolytic Virotherapies
Gujar, S. A., Pol, J. G., Kim, Y., Lee, P. W. K., & Kroemer, G. (2017) · Trends in Immunology · doi:10.1016/j.it.2017.11.006 · Cited by 234 · see citing works
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
Lighting a Fire in the Tumor Microenvironment Using Oncolytic Immunotherapy
Achard, C., Surendran, A., Wedge, M.-È., Ungerechts, G., Bell, J. C., & Ilkow, C. S. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.04.020 · Cited by 152 · see citing works
Self-citationYu, G., Wu, Y., Wang, W., Xu, J., Lv, X., Cao, X., & Wan, T. (2018) · Cellular and Molecular Immunology · doi:10.1038/s41423-018-0026-y · Cited by 147 · see citing works
Oncolytic Virus Combination Therapy: Killing One Bird with Two Stones
Martin, N. T., & Bell, J. C. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2018.04.001 · Cited by 148 · see citing works
Self-citationPast, Present and Future of Oncolytic Reovirus
Müller, L. M. E., Berkeley, R. A., Barr, T., Ilett, E. J., & Errington‐Mais, F. (2020) · Cancers · doi:10.3390/cancers12113219 · Cited by 129 · see citing works
Yang, J., Yang, L., Lin, Y., Zheng, Z., Fang, J., He, S., & Zhuang, S. (2016) · Cancer Letters · doi:10.1016/j.canlet.2016.09.012 · Cited by 127 · see citing works
Oncolytic viruses: overcoming translational challenges
Martínez‐Quintanilla, J., Seah, I. Y. J., Chua, M. M. J., & Shah, K. (2019) · Journal of Clinical Investigation · doi:10.1172/jci122287 · Cited by 119 · see citing works
Prospects for combined use of oncolytic viruses and CAR T-cells
Ajina, A., & Maher, J. F. (2017) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-017-0294-6 · Cited by 117 · see citing works
Hou, W., Sampath, P., Rojas, J. J., & Thorne, S. H. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.05.012 · Cited by 115 · see citing works
Self-citationTrial Watch—Oncolytic viruses and cancer therapy
Pol, J. G., Buqué, A., Aranda, F., Bloy, N., Cremer, I., Eggermont, A. M. M., Erbs, P., Fucikova, J. P., Galon, J., Limacher, J., et al. (2015) · OncoImmunology · doi:10.1080/2162402x.2015.1117740 · Cited by 111 · see citing works
Oncolytic Viruses: Exploiting Cancer's Deal with the Devil
Pikor, L. A., Bell, J. C., & Diallo, J. (2015) · Trends in cancer · doi:10.1016/j.trecan.2015.10.004 · Cited by 109 · see citing works
Self-citationOncolytic viruses encoding bispecific T cell engagers: a blueprint for emerging immunovirotherapies
Heidbuechel, J. P. W., & Engeland, C. E. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01075-5 · Cited by 109 · see citing works
Zhong, L., Gan, L., Wang, B., Wu, T., Yao, F., Gong, W., Peng, H., Deng, Z., Xiao, G., Liu, X., et al. (2025) · Cell · doi:10.1016/j.cell.2024.12.010 · Cited by 107 · see citing works
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
Self-citationJang, J., Kim, D.-H., Lim, J. M., Lee, J. W., Jeong, S. J., Kim, K. P., & Surh, Y. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-2288 · Cited by 105 · see citing works
Wang, L., Chard, L. S., Cheng, Z., & Wang, Y. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-004167 · Cited by 100 · see citing works
Combination therapy with CAR T cells and oncolytic viruses: a new era in cancer immunotherapy
Rezaei, R., Ghaleh, H. E. G., Farzanehpour, M., Dorostkar, R., Ranjbar, R., Bolandian, M., Nodooshan, M. M., & Alvanegh, A. G. (2021) · Cancer Gene Therapy · doi:10.1038/s41417-021-00359-9 · Cited by 98 · see citing works
Oncolytic virotherapy in cancer treatment: challenges and optimization prospects
Chen, L., Zuo, M., Zhou, Q., & Wang, Y. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1308890 · Cited by 92 · see citing works
Oncolytic Immunotherapy: Conceptual Evolution, Current Strategies, and Future Perspectives
Guo, Z. S., Liu, Z., Kowalsky, S. J., Feist, M., Kaliński, P., Lu, B., Storkus, W. J., & Bartlett, D. L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00555 · Cited by 90 · see citing works
Arwert, E. N., Milford, E. L., Rullan, A., Derzsi, S., Hooper, S., Kato, T., Mansfield, D., Melcher, A., Harrington, K. J., & Sahai, E. (2020) · Nature Cell Biology · doi:10.1038/s41556-020-0527-7 · Cited by 90 · see citing works
Multi-modal Potentiation of Oncolytic Virotherapy by Vanadium Compounds
Selman, M., Rousso, C., Bergeron, A., Son, H. H., Krishnan, R., El-Sayes, N., Varette, O., Chen, A., Bœuf, F. L., Tzelepis, F., et al. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.10.014 · Cited by 90 · see citing works
Self-citationMarchini, A., Daeffler, L., Pozdeev, V. I., Angelova, A. L., & Rommelaere, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01848 · Cited by 91 · see citing works
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
Computer‐assisted engineering of hyperstable fibroblast growth factor 2
Dvořák, P., Bednář, D., Vaňáček, P., Bálek, L., Eiselleová, L., Štěpánková, V., Šebestová, E., Bosakova, M. K., Konečná, Ž., Mazurenko, S., et al. (2017) · Biotechnology and Bioengineering · doi:10.1002/bit.26531 · Cited by 77 · see citing works
Trial Watch: Oncolytic viro-immunotherapy of hematologic and solid tumors
Pol, J. G., Lévesque, S., Workenhe, S. T., Gujar, S. A., Bœuf, F. L., Clements, D. R., Fahrner, J., Fend, L., Bell, J. C., Mossman, K. L., et al. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1503032 · Cited by 77 · see citing works
Self-citationPan, M., Wang, H., Ansari, K. H., Li, X., Sun, W., & Fan, Y. (2020) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-020-01742-4 · Cited by 77 · see citing works
Bi- and Tri-Specific T Cell Engager-Armed Oncolytic Viruses: Next-Generation Cancer Immunotherapy
Guo, Z. S., Lotze, M. T., Zhu, Z., Storkus, W. J., & Song, X. (2020) · Biomedicines · doi:10.3390/biomedicines8070204 · Cited by 74 · see citing works
Targeting type I collagen for cancer treatment
Shi, R., Zhang, Z., Zhu, A.-K., Xiong, X., Zhang, J., Xu, J., Sy, M., & Li, C. (2022) · International Journal of Cancer · doi:10.1002/ijc.33985 · Cited by 71 · see citing works
Self-citationEmerging systemic delivery strategies of oncolytic viruses: A key step toward cancer immunotherapy
Ban, W., Guan, J., Huang, H., He, Z., Sun, M., Liu, F., & Sun, J. (2022) · Nano Research · doi:10.1007/s12274-021-4031-6 · Cited by 69 · see citing works
Potentiating prostate cancer immunotherapy with oncolytic viruses
Lee, P. C., & Gujar, S. A. (2018) · Nature Reviews Urology · doi:10.1038/nrurol.2018.10 · Cited by 69 · see citing works
Immunotherapeutic Potential of TGF-β Inhibition and Oncolytic Viruses
Groeneveldt, C., van Hall, T., van der Burg, S. H., ten Dijke, P., & van Montfoort, N. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.03.003 · Cited by 67 · see citing works
Liu, K., Kong, L., Cui, H., Zhang, L., Xin, Q., Zhuang, Y., Guo, C., Yao, Y., Tao, J., Gu, X., et al. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101751 · Cited by 72 · see citing works
Cytokines in oncolytic virotherapy
Pol, J. G., Workenhe, S. T., Konda, P., Gujar, S. A., & Kroemer, G. (2020) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2020.10.007 · Cited by 68 · 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
Wu, S., Liu, X., Zhou, X., Liang, X. M., Gao, D., Liu, H., Zhao, G., Zhang, Q., & Wu, X. (2016) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2015.09.024 · Cited by 64 · see citing works
Combination Immunotherapy Using Oncolytic Virus for the Treatment of Advanced Solid Tumors
Oh, C., Chon, H. J., & Kim, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207743 · Cited by 62 · see citing works
Ovarian Cancer Immunotherapy: Preclinical Models and Emerging Therapeutics
McCloskey, C. W., Rodriguez, G. M., Galpin, K. J. C., & Vanderhyden, B. C. (2018) · Cancers · doi:10.3390/cancers10080244 · Cited by 61 · see citing works
Enhancing cancer therapy: the integration of oncolytic virus therapy with diverse treatments
Yan, Z., Zhang, Z., Chen, Y., Xu, J., Wang, J., & Wang, Z. W. (2024) · Cancer Cell International · doi:10.1186/s12935-024-03424-z · Cited by 58 · see citing works
Wedge, M.-È., Jennings, V. A., Crupi, M. J. F., Poutou, J., Jamieson, T. R., Pelin, A., Pugliese, G., de Souza, C. T., Petryk, J., Laight, B. J., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29526-8 · Cited by 55 · see citing works
Self-citationAn oncolytic virus–delivered TGFβ inhibitor overcomes the immunosuppressive tumor microenvironment
DePeaux, K., Rivadeneira, D. B., Lontos, K., Dean, V. G., Gunn, W. G., Watson, M. J., Yao, T., Wilfahrt, D. N., Hinck, C. S., Wieteska, Ł., et al. (2023) · The Journal of Experimental Medicine · doi:10.1084/jem.20230053 · Cited by 54 · see citing works
Self-citationLi, M., Li, G., Kiyokawa, J., Tirmizi, Z. A., Richardson, L. G., Ning, J., Das, S., Martuza, R. L., Stemmer-Rachamimov, A. O., Rabkin, S. D., et al. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01096-0 · Cited by 54 · see citing works
Oncolytic viruses—immunotherapeutics on the rise
Keller, B. A., & Bell, J. C. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1453-9 · Cited by 52 · see citing works
Self-citationThe discovery and development of oncolytic viruses: are they the future of cancer immunotherapy?
Zhang, S., & Rabkin, S. D. (2020) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2021.1850689 · Cited by 52 · see citing works
Virotherapy: From single agents to combinatorial treatments
Malfitano, A. M., Somma, S. D., Iannuzzi, C. A., Pentimalli, F., & Portella, G. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.113986 · Cited by 51 · see citing works
A 3D tumor microenvironment regulates cell proliferation, peritoneal growth and expression patterns
Loessner, D., Rockstroh, A., Shokoohmand, A., Holzapfel, B. M., Wagner, F., Baldwin, J., Boxberg, M., Schmalfeldt, B., Lengyel, E. R., Clements, J. A., et al. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.10.014 · Cited by 50 · see citing works
Resistance Mechanisms Influencing Oncolytic Virotherapy, a Systematic Analysis
Bhatt, D., Chammas, R. J., & Daemen, T. (2021) · Vaccines · doi:10.3390/vaccines9101166 · Cited by 48 · see citing works
Oncolytic viruses: advanced strategies in cancer therapy
Xiao, D., Zhang, H., Liu, Y., Li, Y., Li, G., & Ning, Y. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02343-3 · Cited by 48 · see citing works
Microbiota in cancer: current understandings and future perspectives
Yao, Y., Zhu, Y., Chen, K., Chen, J., Li, Y., Li, D., & Wei, P. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02335-3 · Cited by 52 · see citing works
Oncolytic Virotherapy in Solid Tumors: The Challenges and Achievements
Jin, K., Du, W., Liu, Y., Lan, H., Si, J., & Mou, X. (2021) · Cancers · doi:10.3390/cancers13040588 · Cited by 46 · see citing works
Simultaneous Tumor and Stroma Targeting by Oncolytic Viruses
Everts, A., Bergeman, M. H., McFadden, G., & Kemp, V. (2020) · Biomedicines · doi:10.3390/biomedicines8110474 · Cited by 45 · see citing works
Oncolytic Virotherapy and the Tumor Microenvironment
Berkey, S. E., Thorne, S. H., & Bartlett, D. L. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-67577-0_11 · Cited by 43 · see citing works
Self-citationDraganov, D., Santidrián, A. F., Minev, I., Nguyen, D. H., Kilinc, M. O., Petrov, I. S., Vyalkova, A., Lander, E. B., Berman, M. H., Minev, B., et al. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-019-1829-z · Cited by 43 · see citing works
Rojas, J. J., Sampath, P., Bonilla, B., Ashley, A., Hou, W., Byrd, D., & Thorne, S. H. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.017 · Cited by 42 · see citing works
Self-citationGene Therapy for Pancreatic Cancer: Specificity, Issues and Hopes
Rouanet, M., Lebrin, M., Gross, F., Bournet, B., Cordelier, P., & Buscail, L. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18061231 · Cited by 42 · see citing works
The Interaction Between Human Papillomaviruses and the Stromal Microenvironment
Woodby, B. L., Scott, M. L., & Bodily, J. M. (2016) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2016.09.003 · Cited by 41 · see citing works
Human CAFs promote lymphangiogenesis in ovarian cancer via the Hh-VEGF-C signaling axis
Wei, R., Lv, M., Li, F., Cheng, T., Zhang, Z., Jiang, G., Zhou, Y., Gao, R., Xiao, W., Lou, J., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.18621 · Cited by 41 · see citing works
Esaki, S., Nigim, F., Moon, E., Luk, S. O., Kiyokawa, J., Curry, W. T., Cahill, D. P., Chi, A. S., Iafrate, A. J., Martuza, R. L., et al. (2017) · International Journal of Cancer · doi:10.1002/ijc.30929 · Cited by 41 · see citing works
TGF-β Inhibition Improves Oncolytic Herpes Viroimmunotherapy in Murine Models of Rhabdomyosarcoma
Hutzen, B. J., Chen, C., Wang, P.-Y., Sprague, L., Swain, H. M., Love, J., Conner, J., Boon, L., & Cripe, T. P. (2017) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2017.09.001 · Cited by 40 · see citing works
Yang, T., Huang, T., Zhang, D., Wang, M., Wu, B., Shang, Y., Sattar, S., Ding, L., Liu, Y., Jiang, H., et al. (2019) · Aging · doi:10.18632/aging.102329 · Cited by 40 · see citing works
Current and emerging concepts for systemic treatment of metastatic colorectal cancer
Steup, C., Kennel, K. B., Neurath, M. F., Fichtner-Feigl, S., & Greten, F. R. (2025) · Gut · doi:10.1136/gutjnl-2025-335412 · Cited by 39 · see citing works
Tong, J., Valdés, Y. R., Sivapragasam, M., Barrett, J. W., Bell, J. C., Stojdl, D. F., DiMattia, G. E., & Shepherd, T. G. (2017) · BMC Cancer · doi:10.1186/s12885-017-3600-2 · Cited by 38 · see citing works
Self-citationImmunovirotherapy: The role of antibody based therapeutics combination with oncolytic viruses
Jafari, M., Kadkhodazadeh, M., Shapourabadi, M. B., Goradel, N. H., Shokrgozar, M. A., Arashkia, A., Abdoli, S., & Sharifzadeh, Z. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1012806 · Cited by 35 · see citing works
Viruses as nanomedicine for cancer
Yoo, S. Y., Badrinath, N., & Heo, J. (2016) · International Journal of Nanomedicine · doi:10.2147/ijn.s116447 · Cited by 35 · see citing works
Molecular Effects of Stromal-Selective Targeting by uPAR-Retargeted Oncolytic Virus in Breast Cancer
Jing, Y., Chavez, V. A., Ban, Y. J., Acquavella, N., El-Ashry, D., Pronin, A. N., Chen, X., & Merchan, J. R. (2017) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-17-0016 · Cited by 34 · see citing works
Concise Review: Targeting Cancer Stem Cells and Their Supporting Niche Using Oncolytic Viruses
Crupi, M. J. F., Bell, J. C., & Singaravelu, R. (2019) · Stem Cells · doi:10.1002/stem.3004 · Cited by 35 · see citing works
Self-citationDobson, C. C., Naing, T., Beug, S. T., Faye, M. D., Chabot, J., St‐Jean, M., Walker, D. E., LaCasse, E. C., Stojdl, D. F., Korneluk, R. G., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.13849 · Cited by 34 · see citing works
Self-citationOral reovirus reshapes the gut microbiome and enhances antitumor immunity in colon cancer
Lee, W. S., Lee, S. J., Lee, H. J., Yang, H., Go, E., Enkhtaivan, G., Song, K., Xiang, X., Park, D.-G., Alain, T., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-53347-6 · Cited by 32 · see citing works
Oncolytic virus driven T-cell-based combination immunotherapy platform for colorectal cancer
Crupi, M. J. F., Taha, Z., Janssen, T. J. A., Petryk, J., Boulton, S., Alluqmani, N., Jirovec, A., Kassas, O., Khan, S., Vallati, S., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1029269 · Cited by 31 · see citing works
Self-citationPeng, C., Liu, J., Yang, G., & Li, Y. (2017) · International Journal of Nanomedicine · doi:10.2147/ijn.s143871 · Cited by 31 · see citing works
Virotherapy as a Potential Therapeutic Approach for the Treatment of Aggressive Thyroid Cancer
Malfitano, A. M., Somma, S. D., Prevete, N., & Portella, G. (2019) · Cancers · doi:10.3390/cancers11101532 · Cited by 30 · see citing works
Liu, Y., Zheng, Y., Deng, T., Huang, Y., Liu, Z., Zhan, B., Zhou, X., Yan, R., Ren, J., Xing, Y., et al. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1037934 · Cited by 30 · see citing works
Kuhn, I., Bauzon, M., Green, N. H., Seymour, L. W., Fisher, K. D., & Hermiston, T. W. (2016) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2016.12.001 · Cited by 28 · see citing works
Fibroblast Growth Factor 2 Enhances Zika Virus Infection in Human Fetal Brain
Limonta, D., Jovel, J., Kumar, A., Lu, J., Hou, S., Airo, A. M., López-Orozco, J., Wong, C. P., Saito, L. B., Branton, W. G., et al. (2019) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiz073 · Cited by 26 · see citing works
Calpe, B., & Kovacs, W. J. (2020) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2020.1756769 · Cited by 25 · see citing works
Holbrook, M. C., Goad, D. W., & Grdzelishvili, V. Z. (2021) · Cancers · doi:10.3390/cancers13051171 · Cited by 24 · see citing works
Oncolytic virotherapy evolved into the fourth generation as tumor immunotherapy
Wang, X., Shen, Y., Wan, X., Hu, X., Cai, W.-Q., Wu, Z., Xin, Q., Liu, X., Gui, J., Xin, H.-Y., et al. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04360-8 · Cited by 24 · see citing works
The limiting factors of oncolytic virus immunotherapy and the approaches to overcome them
Hu, P.-Y., Fan, X., Zhang, Y.-N., Wang, S., Wan, W.-J., Pan, H., & Mou, X. (2020) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-020-10802-w · Cited by 22 · see citing works
MicroRNA-sensitive oncolytic measles virus for chemovirotherapy of pancreatic cancer
Singh, H. M., Leber, M. F., Bossow, S., Engeland, C. E., Dessila, J., Grossardt, C., Zaoui, K., Bell, J. C., Jäger, D., Kalle, C. V., et al. (2021) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2021.04.015 · Cited by 22 · see citing works
Self-citationSchirrmacher, V., Gool, S. V., & Stuecker, W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113050 · Cited by 22 · see citing works
Oncolytic Viruses and Hematological Malignancies: A New Class of Immunotherapy Drugs
Innao, V., Rizzo, V., Allegra, A. G., Musolino, C., & Allegra, A. (2020) · Current Oncology · doi:10.3390/curroncol28010019 · Cited by 22 · see citing works
Combination of Oncolytic Virotherapy with Different Antitumor Approaches against Glioblastoma
Ageenko, A. B., Vasileva, N. S., Richter, V. A., & Kuligina, E. V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042042 · Cited by 21 · see citing works
Chen, J., Madina, B. R., Ahmadi, E., Yarovinsky, T. O., Krady, M. M., Meehan, E. V., Wang, I. C., Ye, X., Pitmon, E., Ma, X., et al. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2023.08.034 · Cited by 20 · see citing works
Müller, L. M. E., Migneco, G., Scott, G. B., Down, J. M., King, S., Askar, B., Jennings, V. A., Oyajobi, B. O., Scott, K. J., West, E. J., et al. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001803 · Cited by 20 · see citing works
Self-citationEnhancing the Efficacy of Tumor Vaccines Based on Immune Evasion Mechanisms
Chen, J., Zhang, H., Zhou, L., Hu, Y., Li, M., He, Y., & Li, Y. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2020.584367 · Cited by 19 · see citing works
Synergistic combination of oncolytic virotherapy with CAR T-cell therapy
Ajina, A., & Maher, J. F. (2019) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2019.06.015 · Cited by 20 · see citing works
Harryvan, T. J., Golo, M., van Dam, N. M., Schoonderwoerd, M. J. A., Farshadi, E. A., Hornsveld, M., Hoeben, R. C., Hawinkels, L. J. A. C., & Kemp, V. (2022) · Cancer Gene Therapy · doi:10.1038/s41417-022-00507-9 · Cited by 17 · see citing works
Zhao, J., Wang, H., Wang, C., Li, F., Chen, J., Zhou, F., Zhu, Y., Chen, J., Liu, J., Zheng, H., et al. (2024) · Molecular Therapy · doi:10.1016/j.ymthe.2024.12.017 · Cited by 17 · see citing works
Viro-immune therapy: A new strategy for treatment of pancreatic cancer
Ibrahim, A. M. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i2.748 · Cited by 17 · see citing works
Advances and Challenges of Nanoparticle-Based Macrophage Reprogramming for Cancer Immunotherapy
Kapitanova, K., Naumenko, V., Garanina, A. S., Melnikov, P., Abakumov, M. A., & Alieva, I. B. (2019) · Biochemistry (Moscow) · doi:10.1134/s0006297919070058 · Cited by 17 · see citing works
Infection of non-cancer cells: A barrier or support for oncolytic virotherapy?
Naumenko, V., Stepanenko, A. A., Lipatova, A. V., Vishnevskiy, D. A., & Chekhonin, V. P. (2022) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2022.02.004 · Cited by 16 · see citing works
Mistarz, A., Winkler, M., Battaglia, S., Liu, S., Hutson, A. D., Rokita, H., Gambotto, A. A., Odunsi, K. O., Singh, P. K., McGray, A. R., et al. (2023) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2023.02.002 · Cited by 15 · see citing works
Surendran, A., Jamalkhah, M., Poutou, J., Birtch, R., Lawson, C., Dave, J., Crupi, M. J. F., Mayer, J., Taylor, V., Petryk, J., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1099459 · Cited by 15 · see citing works
Self-citationDailey, K. M., Allgood, J. E., Johnson, P. R., Ostlie, M. A., Schaner, K., Brooks, B. D., & Brooks, A. E. (2021) · Future Microbiology · doi:10.2217/fmb-2020-0245 · Cited by 15 · see citing works
Macrophages and their interactions with oncolytic viruses
Jakeman, P. G., Hills, T. E., Fisher, K. D., & Seymour, L. W. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.06.007 · Cited by 15 · see citing works
- Authors
- Ilkow, C. S., Marguerie, M., Batenchuk, C., Mayer, J., Ben Neriah, D., Cousineau, S., Falls, T., Jennings, V. A., Boileau, M., Bellamy, D., Bastin, D., de Souza, C. T., Alkayyal, A., Zhang, J., Le Boeuf, F., Arulanandam, R., Stubbert, L., Sampath, P., Thorne, S. H., Paramanthan, P., Chatterjee, A., Strieter, R. M., Burdick, M., Addison, C. L., Stojdl, D. F., Atkins, H. L., Auer, R. C., Diallo, J.-S., Lichty, B. D., & Bell, J. C.
- Affiliations
- University of Ottawa (CA)
- Ottawa Hospital Research Institute (CA)
- Second Hospital of Shandong University (CN)
- University of Pittsburgh (US)
- Ottawa Hospital (CA)
- University of Virginia (US)
- McMaster University (CA)
- Corresponding author
- Bell, John C
- ORCID
- Ilkow, Carolina S
- Marguerie, Monique
- Cousineau, Sophie
- Falls, Theresa
- Jennings, Victoria A
- Boileau, Meaghan
- Bastin, Donald
- Alkayyal, Almohanad
- Zhang, Jiqing
- Arulanandam, Rozanne
- Sampath, Padma
- Chatterjee, Avijit
- Strieter, Robert M
- Burdick, Marie
- Addison, Christina L
- Atkins, Harold L
- Auer, Rebecca C
- Diallo, Jean-Simon
- Lichty, Brian D
- Bell, John C
- Venue
- Nature Medicine
- Published
- 2015-04-20
- Volume
- 21
- Issue
- 5
- Pages
- 530-536
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W2000114190
- Cited by
- 165
- References
- 48
- Citations by year
- 2026: 11 · 2025: 16 · 2024: 14 · 2023: 9 · 2022: 19 · 2021: 11 · 2020: 22 · 2019: 11 · 2018: 11 · 2017: 16 · 2016: 15 · 2015: 8 · 2013: 1
- FWCI
- 11.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- McMaster University
- Ontario Institute for Cancer Research
- Université de Genève
- Canadian Institutes of Health Research (314043)
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- oncolytic virotherapy, tumor microenvironment, cancer-associated fibroblasts, TGF-beta, fibroblast growth factor 2, RIG-I, antiviral immunity, pancreatic cancer, viral susceptibility
- MeSH terms
- Aged, Animals, Antiviral Agents, Chlorocebus aethiops, Female, Fibroblasts, Humans, Lung Neoplasms, Male, Microscopy, Fluorescence, Middle Aged, Neoplasm Transplantation, Ovarian Neoplasms, Vero Cells, Signal Transduction, Transforming Growth Factor beta, Fibroblast Growth Factor 2, Stromal Cells, Coculture Techniques, Cell Line, Tumor, Green Fluorescent Proteins, Oncolytic Virotherapy, Oncolytic Viruses, Mice, Tumor Microenvironment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review