Abstract
Oncolytic therapy is a treatment method used to directly combat tumor cells by modifying the genes of naturally occurring low pathogenic viruses to form "rhizobia" virus. By taking the advantage of abnormal signal pathways in cancer cells, it selectively replicates in tumor cells leading to tumor cell lysis and death. At present, clinical studies widely employ biomolecular technology to transform oncolytic viruses to exert stronger oncolytic effects and reduce their adverse reactions. This review summarizes the current progresses and the molecular mechanism of oncolytic viruses towards tumor treatment and management.
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References
Bell JC, McFadden G (2015) Editorial overview: oncolytic viruses-replicating virus therapeutics for the treatment of cancer. Curr Opin Virol 13:viii–ix
Bommareddy PK, Shettigar M, Kaufman HL (2018) Integrating oncolytic viruses in combination cancer immunotherapy. Nat Rev Immunol 18(8):498–513
Boutros C, Tarhini A, Routier E et al (2016) Safety profiles of anti-CTLA-4 and anti-PD-1 antibodies alone and in combination. Nat Rev Clin Oncol 13(8):473–486
Card PB, Hogg RT, Gil Del Alcazar CR, Gerard RD (2012) MicroRNA silencing improves the tumor specificity of adenoviral transgene expression. Cancer Gene Ther 19(7):451–459
Chaurasiya S, Fong Y, Warner SG (2020) Optimizing oncolytic viral design to enhance antitumor efficacy: progress and challenges. Cancers (Basel) 12(6):1699
Chen R, Ganesan A, Okoye I, Arutyunova E, Elahi S, Lemieux MJ, Barakat K (2020) Targeting B7–1 in immunotherapy. Med Res Rev 40(2):654–682
Chesney J, Puzanov I, Collichio F et al (2018) Randomized, open-label phase II study evaluating the efficacy and safety of talimogene laherparepvec in combination with ipilimumab versus ipilimumab alone in patients with advanced. Unresectable Melanoma J Clin Oncol 36(17):1658–1667
Ch’ng WC, Stanbridge EJ, Yusoff K, Shafee N (2013) The oncolytic activity of Newcastle disease virus in clear cell renal carcinoma cells in normoxic and hypoxic conditions: the interplay between von Hippel-Lindau and interferon-β signaling. J Interferon Cytokine Res 33(7):346–354
Dalio RJD, Magalhães DM, Rodrigues CM et al (2017) PAMPs, PRRs, effectors and R-genes associated with citrus-pathogen interactions. Ann Bot 119(5):749–774
Davydova J, Gavrikova T, Brown EJ et al (2010) In vivo bioimaging tracks conditionally replicative adenoviral replication and provides an early indication of viral antitumor efficacy. Cancer Sci 101(2):474–481
Di Piazza M, Mader C, Geletneky K et al (2007) Cytosolic activation of cathepsins mediates parvovirus H-1-induced killing of cisplatin and TRAIL-resistant glioma cells. J Virol 81(8):4186–4198
Elankumaran S, Chavan V, Qiao D et al (2010) Type I interferon-sensitive recombinant newcastle disease virus for oncolytic virotherapy. J Virol 84(8):3835–3844
Fuerer C, Iggo R (2004) 5-Fluorocytosine increases the toxicity of Wnt-targeting replicating adenoviruses that express cytosine deaminase as a late gene. Gene Ther 11(2):142–151
Garg AD, Galluzzi L, Apetoh L et al (2015) Molecular and translational classifications of DAMPs in immunogenic cell death. Front Immunol 6:588
Guedan S, Alemany R (2018) CAR-T cells and oncolytic viruses: joining forces to overcome the solid tumor challenge. Front Immunol 9:2460
Gujar SA, Clements D, Dielschneider R, Helson E, Marcato P, Lee PW (2014) Gemcitabine enhances the efficacy of reovirus-based oncotherapy through anti-tumour immunological mechanisms. Br J Cancer 110(1):83–93
Gujar S, Pol JG, Kim Y, Lee PW, Kroemer G (2018) Antitumor benefits of antiviral immunity: an underappreciated aspect of oncolytic virotherapies. Trends Immunol 39(3):209–221
Güler A, Lopez Venegas M, Adankwah E, Mayatepek E, Nausch N, Jacobsen M (2020) Suppressor of cytokine signalling 3 is crucial for interleukin-7 receptor re-expression after T-cell activation and interleukin-7 dependent proliferation. Eur J Immunol 50(2):234–244
Heo SK, Ju SA, Kim GY et al (2012) The presence of high level soluble herpes virus entry mediator in sera of gastric cancer patients. Exp Mol Med 44(2):149–158
Huajun J, Saiqun L, Jiahe Y et al (2011) Use of MicroRNA Let-7 to control the replication specificity of oncolytic adenovirus in hepatocellular carcinoma cells. PLoS ONE 6(7):21307
Ip WH, Dobner T (2020) Cell transformation by the adenovirus oncogenes E1 and E4. FEBS Lett 594(12):1848–1860
Jain RK, Stylianopoulos T (2010) Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol 7(11):653–664
Johnson DB, Puzanov I, Kelley MC (2015) Talimogene laherparepvec (T-VEC) for the treatment of advanced melanoma. Immunotherapy 7(6):611–619
Kelly E, Russell SJ (2007) History of oncolytic viruses: genesis to genetic engineering. Mol Ther 15:651–659
Keppler SJ, Rosenits K, Koegl T, Vucikuja S, Aichele P (2012) Signal 3 cytokines as modulators of primary immune responses during infections: the interplay of type I IFN and IL-12 in CD8 T cell responses. PLoS ONE 7(7):e40865
Kim M, Chung YH, Johnston RN (2007) Reovirus and tumor oncolysis. J Microbiol 45(3):187–192
Kuczynski EA, Vermeulen PB, Pezzella F, Kerbel RS, Reynolds AR (2019) Vessel co-option in cancer. Nat Rev Clin Oncol 16(8):469–493
Lichty BD, Breitbach CJ, Stojdl DF, Bell JC (2014) Going viral with cancer immunotherapy. Nat Rev Cancer 14(8):559–567
Lolkema MP, Arkenau HT, Harrington K et al (2011) A phase I study of the combination of intravenous reovirus type 3 Dearing and gemcitabine in patients with advanced cancer. Clin Cancer Res 17(3):581–588
Mahalingam D, Goel S, Aparo S et al (2018) A phase II study of pelareorep (REOLYSIN®) in combination with gemcitabine for patients with advanced pancreatic adenocarcinoma. Cancers (Basel) 10(6):160
Marchini A, Daeffler L, Pozdeev VI, Angelova A, Rommelaere J (2019) Immune conversion of tumor microenvironment by oncolytic viruses: the protoparvovirus H-1PV case study. Front Immunol 10:1848
Melero I, Hervas-Stubbs S, Glennie M, Pardoll DM, Chen L (2007) Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer 7(2):95–106
Navarro SA, Carrillo E, Griñán-Lisón C, Martín A, Perán M, Marchal JA, Boulaiz H (2016) Cancer suicide gene therapy: a patent review. Expert Opin Ther Pat 26(9):1095–1104
Oh E, Hong J, Kwon OJ, Yun CO (2018) A hypoxia- and telomerase-responsive oncolytic adenovirus expressing secretable trimeric TRAIL triggers tumour-specific apoptosis and promotes viral dispersion in TRAIL-resistant glioblastoma. Sci Rep 8(1):1420
Ontiveros F, Wilson EB, Livingstone AM (2011) Type I interferon supports primary CD8+T-cell responses to peptide-pulsed dendritic cells in the absence of CD4+T-cell help. Immunology 132(4):549–558
Pesonen S, Nokisalmi P, Ristimaki A et al (2008) Treatment of cancer patients with capsid modified double controlled oncolytic adenovirus Ad5/3-Cox2L-D24. Can Res 68(9):2818
Puzanov I, Milhem MM, Minor D et al (2016) Talimogene laherparepvec in combination with ipilimumab in previously untreated, unresectable stage IIIB-IV melanoma. J Clin Oncol 34(22):2619–2626
Ribas A, Dummer R, Puzanov I et al (2017) Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell 170(6):1109-1119.e10
Schenk EL, Mandrekar SJ, Dy GK, Aubry MC, Tan AD, Dakhil SR, Sachs BA, Nieva JJ, Bertino E, Lee Hann C, Schild SE, Wadsworth TW, Adjei AA, Molina JR (2020) A randomized double-blind phase II study of the Seneca Valley Virus (NTX-010) versus placebo for patients with extensive-stage SCLC (ES SCLC) who were stable or responding after at least four cycles of platinum-based chemotherapy: north central cancer treatment group (Alliance) N0923 study. J Thorac Oncol 15(1):110–119
Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A (2017) Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell 168(4):707–723
Sharp DW, Lattime EC (2016) Recombinant poxvirus and the tumor microenvironment: oncolysis, immune regulation and immunization. Biomedicines 4(3):19
Shen Y, Nemunaitis J (2006) Herpes simplex virus 1 (HSV-1) for cancer treatment. Cancer Gene Ther 13(11):975–992
Shi Q, Zhang P, Zhang J et al (2009) Adenovirus-mediated brain-derived neurotrophic factor expression regulated by hypoxia response element protects brain from injury of transient middle cerebral artery occlusion in mice. Neurosci Lett 465(3):220–225
Shi T, Song X, Wang Y, Liu F, Wei J (2020) Combining oncolytic viruses with cancer immunotherapy: establishing a new generation of cancer treatment. Front Immunol 28(11):683
Sobhanimonfared F, Bamdad T, Sadigh ZA, Choobin H (2020) Virus specific tolerance enhanced efficacy of cancer immuno-virotherapy. Microb Pathog 140:103957
Twumasi-Boateng K, Pettigrew JL, Kwok YYE, Bell JC, Nelson BH (2018) Oncolytic viruses as engineering platforms for combination immunotherapy. Nat Rev Cancer 18(7):419–432
Vaupel P (2004) The role of hypoxia-induced factors in tumor progression. Oncologist 9(Suppl 5):10–17
Vogel I, Kasran A, Cremer J et al (2015) CD28/CTLA-4/B7 costimulatory pathway blockade affects regulatory T-cell function in autoimmunity. Eur J Immunol 45(6):1832–1841
Wing A, Fajardo CA, Posey AD Jr et al (2018) Improving CART-cell therapy of solid tumors with oncolytic virus-driven production of a bispecific T-cell engager. Cancer Immunol Res 6(5):605–616
Yamaguchi S, Maida Y, Yasukawa M, Kato T, Yoshida M, Masutomi K (2014) Eribulin mesylate targets human telomerase reverse transcriptase in ovarian cancer cells. PLoS ONE 9(11):e112438
Zhang Y, Thai V, McCabe A, Jones M, MacNamara KC (2014) Type I interferons promote severe disease in a mouse model of lethal ehrlichiosis. Infect Immun 82(4):1698–1709
Zhang W, Ge K, Zhao Q et al (2015) A novel oHSV-1 targeting telomerase reverse transcriptase-positive cancer cells via tumor-specific promoters regulating the expression of ICP4. Oncotarget 6(24):20345–20355
Zheng X, Rao XM, Snodgrass C et al (2005) Adenoviral E1a expression levels affect virus-selective replication in human cancer cells. Cancer Biol Ther 4(11):1255–1262
Funding
This work was supported by National Natural Science Foundation of China (Grant Nos. 81870821, 82071187 Sponsor: J Xu) and by grants from the Natural Science Foundation of Jiangsu Province, China (Grant No. BK20151347, Sponsor: F Yu).
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All authors contributed to the study conception and design. FY and HS had the idea for the article, YG, YW and TH performed the literature search, data analysis and draft, and XW, JX and QX critically revised the work.
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Gao, Y., Wu, Y., Huan, T. et al. The application of oncolytic viruses in cancer therapy. Biotechnol Lett 43, 1945–1954 (2021). https://doi.org/10.1007/s10529-021-03173-3
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DOI: https://doi.org/10.1007/s10529-021-03173-3