The employment of vaccinia virus for colorectal cancer treatment: A review of preclinical and clinical studies

References

• Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: gLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:1–13. doi:10.3322/caac.21660.
   Web of Science ®Google Scholar
• Kastrinos F, Samadder NJ, Burt RW. Use of family history and genetic testing to determine risk of colorectal cancer. Gastroenterology. 2020;158:389–403. doi:10.1053/j.gastro.2019.11.029.
   PubMed Web of Science ®Google Scholar
• Perera AP, Sajnani K, Dickinson J, Eri R, Korner H. NLRP3 inflammasome in colitis and colitis-associated colorectal cancer. Mamm Genome. 2018;29:817–30. doi:10.1007/s00335-018-9783-2.
   PubMed Web of Science ®Google Scholar
• Liang PS, Chen TY, Giovannucci E. Cigarette smoking and colorectal cancer incidence and mortality: systematic review and meta-analysis. Int J Cancer. 2009;124:2406–15. doi:10.1002/ijc.24191.
   PubMed Web of Science ®Google Scholar
• Vieira AR, Abar L, Chan DSM, Vingeliene S, Polemiti E, Stevens C, Greenwood D, Norat T. Foods and beverages and colorectal cancer risk: a systematic review and meta-analysis of cohort studies, an update of the evidence of the WCRF-AICR continuous update project. Ann Oncol. 2017;28:1788–802. doi:10.1093/annonc/mdx171.
   PubMed Web of Science ®Google Scholar
• Soltani G, Poursheikhani A, Yassi M, Hayatbakhsh A, Kerachian M, Kerachian MA. Obesity, diabetes and the risk of colorectal adenoma and cancer. BMC Endocr Disord. 2019;19:113. doi:10.1186/s12902-019-0444-6.
   PubMed Web of Science ®Google Scholar
• Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet. 2014;383:1490–502. doi:10.1016/S0140-6736(13)61649-9.
   PubMed Web of Science ®Google Scholar
• Piawah S, Venook AP. Targeted therapy for colorectal cancer metastases: a review of current methods of molecularly targeted therapy and the use of tumor biomarkers in the treatment of metastatic colorectal cancer. Cancer. 2019;125:4139–47. doi:10.1002/cncr.32163.
   PubMed Web of Science ®Google Scholar
• Van Vliet K, Mohamed MR, Zhang L, Villa NY, Werden SJ, Liu J, McFadden G. Poxvirus proteomics and virus-host protein interactions. Microbiol Mol Biol Rev. 2009;73:730–49. doi:10.1128/MMBR.00026-09.
   PubMed Web of Science ®Google Scholar
• Guse K, Cerullo V, Hemminki A. Oncolytic vaccinia virus for the treatment of cancer. Expert Opin Biol Ther. 2011;11:595–608. doi:10.1517/14712598.2011.558838.
   PubMed Web of Science ®Google Scholar
• Smith GL, Benfield CTO, Maluquer de Motes C, Mazzon M, Ember SWJ, Ferguson BJ, Sumner RP. Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. J Gen Virol. 2013;94:2367–92. doi:10.1099/vir.0.055921-0.
   PubMed Web of Science ®Google Scholar
• Guo ZS, Lu B, Guo Z, Giehl E, Feist M, Dai E, Liu W, Storkus WJ, He Y, Liu Z, et al. Vaccinia virus-mediated cancer immunotherapy: cancer vaccines and oncolytics. J Immunother Cancer. 2019;7:6. doi:10.1186/s40425-018-0495-7.
   PubMed Web of Science ®Google Scholar
• Berry J, Vreeland T, Trappey A, Hale D, Peace K, Tyler J, Walker A, Brown R, Herbert G, Yi F, et al. Cancer vaccines in colon and rectal cancer over the last decade: lessons learned and future directions. Expert Rev Clin Immunol. 2017;13:235–45. doi:10.1080/1744666X.2016.1226132.
   PubMed Web of Science ®Google Scholar
• Larocca C, Schlom J. Viral vector-based therapeutic cancer vaccines. Cancer J. 2011;17:359–71. doi:10.1097/PPO.0b013e3182325e63.
   PubMed Web of Science ®Google Scholar
• Kim-Schulze S, Kim HS, Wainstein A, Kim DW, Yang WC, Moroziewicz D, Mong PY, Bereta M, Taback B, Wang Q, et al. Intrarectal vaccination with recombinant vaccinia virus expressing carcinoembronic antigen induces mucosal and systemic immunity and prevents progression of colorectal cancer. J Immunol. 2008;181:8112–19. doi:10.4049/jimmunol.181.11.8112.
   PubMed Web of Science ®Google Scholar
• Lorenz MG, Kantor JA, Schlom J, Hodge JW. Anti-tumor immunity elicited by a recombinant vaccinia virus expressing CD70 (CD27L). Hum Gene Ther. 1999;10:1095–103. doi:10.1089/10430349950018094.
   PubMed Web of Science ®Google Scholar
• Uzendoski K, Kantor JA, Abrams SI, Schlom J, Hodge JW. Construction and characterization of a recombinant vaccinia virus expressing murine intercellular adhesion molecule-1: induction and potentiation of antitumor responses. Hum Gene Ther. 1997;8:851–60. doi:10.1089/hum.1997.8.7-851.
   PubMed Web of Science ®Google Scholar
• Sivanandham M, Shaw P, Bernik SF, Paoletti E, Wallack MK. Colon cancer cell vaccine prepared with replication-deficient vaccinia viruses encoding B7.1 and interleukin-2 induce antitumor response in syngeneic mice. Cancer Immunol Immunother. 1998;46:261–67. doi:10.1007/s002620050486.
   PubMed Web of Science ®Google Scholar
• Kaufman HL, Rao JB, Irvine KR, Bronte V, Rosenberg SA, Restifo NP. Interleukin-10 enhances the therapeutic effectiveness of a recombinant poxvirus-based vaccine in an experimental murine tumor model. J Immunother (1991). 1999;22:489–96. doi:10.1097/00002371-199911000-00003.
   PubMed Web of Science ®Google Scholar
• Rao JB, Chamberlain RS, Bronte V, Carroll MW, Irvine KR, Moss B, Rosenberg SA, Restifo NP. IL-12 is an effective adjuvant to recombinant vaccinia virus-based tumor vaccines: enhancement by simultaneous B7-1 expression. J Immunol. 1996;156:3357–65.
   PubMed Web of Science ®Google Scholar
• Hance KW, Rogers CJ, Zaharoff DA, Canter D, Schlom J, Greiner JW. The antitumor and immunoadjuvant effects of IFN-alpha in combination with recombinant poxvirus vaccines. Clin Cancer Res. 2009;15:2387–96. doi:10.1158/1078-0432.CCR-08-1752.
   PubMed Web of Science ®Google Scholar
• Dai P, Wang W, Yang N, Serna-Tamayo C, Ricca JM, Zamarin D, Shuman S, Merghoub T, Wolchok JD, Deng L. Intratumoral delivery of inactivated modified vaccinia virus Ankara (iMVA) induces systemic antitumor immunity via STING and Batf3-dependent dendritic cells. Sci Immunol. 2017;2. doi:10.1126/sciimmunol.aal1713.
   Web of Science ®Google Scholar
• Kudo-Saito C, Schlom J, Hodge JW. Intratumoral vaccination and diversified subcutaneous/intratumoral vaccination with recombinant poxviruses encoding a tumor antigen and multiple costimulatory molecules. Clin Cancer Res. 2004;10:1090–99. doi:10.1158/1078-0432.CCR-03-0145.
   PubMed Web of Science ®Google Scholar
• Tykodi SS, Thompson JA. Development of modified vaccinia Ankara-5T4 as specific immunotherapy for advanced human cancer. Expert Opin Biol Ther. 2008;8:1947–53. doi:10.1517/14712590802567298.
   PubMed Web of Science ®Google Scholar
• Stern PL, Harrop R. 5T4 oncofoetal antigen: an attractive target for immune intervention in cancer. Cancer Immunol Immunother. 2017;66:415–26. doi:10.1007/s00262-016-1917-3.
   PubMed Web of Science ®Google Scholar
• Harrop R, Ryan MG, Myers KA, Redchenko I, Kingsman SM, Carroll MW. Active treatment of murine tumors with a highly attenuated vaccinia virus expressing the tumor associated antigen 5T4 (TroVax) is CD4+ T cell dependent and antibody mediated. Cancer Immunol Immunother. 2006;55:1081–90. doi:10.1007/s00262-005-0096-4.
   PubMed Web of Science ®Google Scholar
• Mulryan K, Ryan MG, Myers KA, Shaw D, Wang W, Kingsman SM, Stern PL, Carroll MW. Attenuated recombinant vaccinia virus expressing oncofetal antigen (tumor-associated antigen) 5T4 induces active therapy of established tumors. Mol Cancer Ther. 2002;1:1129–37.
   PubMed Web of Science ®Google Scholar
• Hammarstrom S. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin Cancer Biol. 1999;9:67–81. doi:10.1006/scbi.1998.0119.
   PubMed Web of Science ®Google Scholar
• Beauchemin N, Arabzadeh A. Carcinoembryonic antigen-related cell adhesion molecules (CEACAMs) in cancer progression and metastasis. Cancer Metastasis Rev. 2013;32:643–71. doi:10.1007/s10555-013-9444-6.
   PubMed Web of Science ®Google Scholar
• Jacobs J, Deschoolmeester V, Zwaenepoel K, Rolfo C, Silence K, Rottey S, Lardon F, Smits E, Pauwels P. CD70: an emerging target in cancer immunotherapy. Pharmacol Ther. 2015;155:1–10. doi:10.1016/j.pharmthera.2015.07.007.
   PubMed Web of Science ®Google Scholar
• Zheng J, Mo J, Zhu T, Zhuo W, Yi Y, Hu S, Yin J, Zhang W, Zhou H, Liu Z. Comprehensive elaboration of the cGAS-STING signaling axis in cancer development and immunotherapy. Mol Cancer. 2020;19:133. doi:10.1186/s12943-020-01250-1.
   PubMed Web of Science ®Google Scholar
• Timiryasova TM, Li J, Chen B, Chong D, Langridge WH, Gridley DS, Fodor I. Antitumor effect of vaccinia virus in glioma model. Oncol Res. 1999;11:133–44.
   PubMed Web of Science ®Google Scholar
• Ferguson MS, Chard Dunmall LS, Gangeswaran R, Marelli G, Tysome JR, Burns E, Whitehead MA, Aksoy E, Alusi G, Hiley C, et al. Transient inhibition of PI3Kδ enhances the therapeutic effect of intravenous delivery of oncolytic vaccinia virus. Mol Ther. 2020;28:1263–75. doi:10.1016/j.ymthe.2020.02.017.
   PubMed Web of Science ®Google Scholar
• Ottolino-Perry K, Tang N, Head R, Ng C, Arulanandam R, Angarita FA, Acuna SA, Chen Y, Bell J, DaCosta RS, et al. Tumor vascularization is critical for oncolytic vaccinia virus treatment of peritoneal carcinomatosis. Int J Cancer. 2014;134:717–30. doi:10.1002/ijc.28395.
   PubMed Web of Science ®Google Scholar
• Badrinath N, Jeong YI, Woo HY, Bang SY, Kim C, Heo J, Kang DH, Yoo SY. Local delivery of a cancer-favoring oncolytic vaccinia virus via poly (lactic-co-glycolic acid) nanofiber for theranostic purposes. Int J Pharm. 2018;552:437–42. doi:10.1016/j.ijpharm.2018.10.020.
   PubMedGoogle Scholar
• Nakatake M, Kuwano N, Kaitsurumaru E, Kurosaki H, Nakamura T. Fusogenic oncolytic vaccinia virus enhances systemic antitumor immune response by modulating the tumor microenvironment. Mol Ther. 2021;29:1782–93. doi:10.1016/j.ymthe.2020.12.024.
   PubMed Web of Science ®Google Scholar
• Ho TY, Mealiea D, Okamoto L, Stojdl DF, McCart JA. Deletion of immunomodulatory genes as a novel approach to oncolytic vaccinia virus development. Mol Ther Oncolytics. 2021;22:85–97. doi:10.1016/j.omto.2021.05.007.
   PubMed Web of Science ®Google Scholar
• Thirunavukarasu P, Sathaiah M, Gorry MC, O’Malley ME, Ravindranathan R, Austin F, Thorne SH, Guo ZS, Bartlett DL. A rationally designed A34R mutant oncolytic poxvirus: improved efficacy in peritoneal carcinomatosis. Mol Ther. 2013;21:1024–33. doi:10.1038/mt.2013.27.
   PubMed Web of Science ®Google Scholar
• Rojas JJ, Sampath P, Hou W, Thorne SH. Defining effective combinations of immune checkpoint blockade and oncolytic virotherapy. Clin Cancer Res. 2015;21:5543–51. doi:10.1158/1078-0432.CCR-14-2009.
   PubMed Web of Science ®Google Scholar
• Liu Z, Ravindranathan R, Kalinski P, Guo ZS, Bartlett DL. Rational combination of oncolytic vaccinia virus and PD-L1 blockade works synergistically to enhance therapeutic efficacy. Nat Commun. 2017;8:14754. doi:10.1038/ncomms14754.
   PubMed Web of Science ®Google Scholar
• Yoo SY, Badrinath N, Jeong SN, Woo HY, Heo J. Overcoming tumor resistance to oncolyticvaccinia virus with anti-PD-1-based combination therapy by inducing antitumor immunity in the tumor microenvironment. Vaccines (Basel). 2020;8:321. doi:10.3390/vaccines8020321.
   PubMed Web of Science ®Google Scholar
• Yoo SY, Bang SY, Jeong SN, Kang DH, Heo J. A cancer-favoring oncolytic vaccinia virus shows enhanced suppression of stem-cell like colon cancer. Oncotarget. 2016;7:16479–89. doi:10.18632/oncotarget.7660.
   PubMedGoogle Scholar
• Liu W, Dai E, Liu Z, Ma C, Guo ZS, Bartlett DL. In Situ therapeutic cancer vaccination with an oncolytic virus expressing membrane-tethered IL-2. Mol Ther Oncolytics. 2020;17:350–60. doi:10.1016/j.omto.2020.04.006.
   PubMed Web of Science ®Google Scholar
• Ge Y, Wang H, Ren J, Liu W, Chen L, Chen H, Ye J, Dai E, Ma C, Ju S, et al. Oncolytic vaccinia virus delivering tethered IL-12 enhances antitumor effects with improved safety. J Immunother Cancer. 2020;8:e000710. doi:10.1136/jitc-2020-000710.
   PubMed Web of Science ®Google Scholar
• Chen L, Chen H, Ye J, Ge Y, Wang H, Dai E, Ren J, Liu W, Ma C, Ju S, et al. Intratumoral expression of interleukin 23 variants using oncolytic vaccinia virus elicit potent antitumor effects on multiple tumor models via tumor microenvironment modulation. Theranostics. 2021;11:6668–81. doi:10.7150/thno.56494.
   PubMed Web of Science ®Google Scholar
• Wang N, Wang J, Zhang Z, Cao H, Yan W, Chu Y, Chard Dunmall LS, Wang Y. A novel vaccinia virus enhances anti-tumor efficacy and promotes a long-term anti-tumor response in a murine model of colorectal cancer. Mol Ther Oncolytics. 2021;20:71–81. doi:10.1016/j.omto.2020.11.002.
   PubMed Web of Science ®Google Scholar
• Deng L, Yang X, Fan J, Ding Y, Peng Y, Xu D, Huang B, Hu Z. IL-24-armed oncolytic vaccinia virus exerts potent antitumor effects via multiple pathways in colorectal cancer. Oncol Res. 2021;28:579–90. doi:10.3727/096504020X15942028641011.
   PubMed Web of Science ®Google Scholar
• Lee YS, Lee WS, Kim CW, Lee SJ, Yang H, Kong SJ, Ning J, Yang K-M, Kang B, Kim WR, et al. Oncolytic vaccinia virus reinvigorates peritoneal immunity and cooperates with immune checkpoint inhibitor to suppress peritoneal carcinomatosis in colon cancer. J Immunother Cancer. 2020;8:e000857. doi:10.1136/jitc-2020-000857.
   PubMed Web of Science ®Google Scholar
• Li J, O’Malley M, Sampath P, Kalinski P, Bartlett DL, Thorne SH. Expression of CCL19 from oncolytic vaccinia enhances immunotherapeutic potential while maintaining oncolytic activity. Neoplasia. 2012;14:1115–21. doi:10.1593/neo.121272.
   PubMed Web of Science ®Google Scholar
• Flanagan K, Glover RT, Horig H, Yang W, Kaufman HL. Local delivery of recombinant vaccinia virus expressing secondary lymphoid chemokine (SLC) results in a CD4 T-cell dependent antitumor response. Vaccine. 2004;22:2894–903. doi:10.1016/j.vaccine.2003.12.021.
   PubMed Web of Science ®Google Scholar
• Bereta M, Bereta J, Park J, Medina F, Kwak H, Kaufman HL. Immune properties of recombinant vaccinia virus encoding CD154 (CD40L) are determined by expression of virally encoded CD40L and the presence of CD40L protein in viral particles. Cancer Gene Ther. 2004;11:808–18. doi:10.1038/sj.cgt.7700762.
   PubMed Web of Science ®Google Scholar
• Warner SG, Kim SI, Chaurasiya S, O’Leary MP, Lu J, Sivanandam V, Woo Y, Chen NG, Fong Y. A novel chimeric poxvirus encoding hNIS is tumor-tropic, imageable, and synergistic with radioiodine to sustain colon cancer regression. Mol Ther Oncolytics. 2019;13:82–92. doi:10.1016/j.omto.2019.04.001.
   PubMed Web of Science ®Google Scholar
• Haddad D, Chen N, Zhang Q, Chen CH, Yu YA, Gonzalez L, Aguilar J, Li P, Wong J, Szalay AA, et al. A novel genetically modified oncolytic vaccinia virus in experimental models is effective against a wide range of human cancers. Ann Surg Oncol. 2012;19(Suppl 3):S665–74. doi:10.1245/s10434-011-2198-x.
   PubMedGoogle Scholar
• Eveno C, Mojica K, Ady JW, Thorek DL, Longo V, Belin LJ, Gholami S, Johnsen C, Zanzonico P, Chen N, et al. Gene therapy using therapeutic and diagnostic recombinant oncolytic vaccinia virus GLV-1h153 for management of colorectal peritoneal carcinomatosis. Surgery. 2015;157:331–37. doi:10.1016/j.surg.2014.09.008.
   PubMed Web of Science ®Google Scholar
• McCart JA, Mehta N, Scollard D, Reilly RM, Carrasquillo JA, Tang N, Deng H, Miller M, Xu H, Libutti SK, et al. Oncolytic vaccinia virus expressing the human somatostatin receptor SSTR2: molecular imaging after systemic delivery using 111in-pentetreotide. Mol Ther. 2004;10:553–61. doi:10.1016/j.ymthe.2004.06.158.
   PubMed Web of Science ®Google Scholar
• Ding Y, Fan J, Deng L, Huang B, Zhou B. Antitumor efficacy of cytosine deaminase-armed vaccinia virus plus 5-fluorocytosine in colorectal cancers. Cancer Cell Int. 2020;20:243. doi:10.1186/s12935-020-01340-6.
   PubMed Web of Science ®Google Scholar
• McCart JA, Puhlmann M, Lee J, Hu Y, Libutti SK, Alexander HR, Bartlett DL. Complex interactions between the replicating oncolytic effect and the enzyme/prodrug effect of vaccinia-mediated tumor regression. Gene Ther. 2000;7:1217–23. doi:10.1038/sj.gt.3301237.
   PubMed Web of Science ®Google Scholar
• Foloppe J, Kintz J, Futin N, Findeli A, Cordier P, Schlesinger Y, Hoffmann C, Tosch C, Balloul J-M, Erbs P. Targeted delivery of a suicide gene to human colorectal tumors by a conditionally replicating vaccinia virus. Gene Ther. 2008;15:1361–71. doi:10.1038/gt.2008.82.
   PubMed Web of Science ®Google Scholar
• Ziauddin MF, Guo ZS, O’Malley ME, Austin F, Popovic PJ, Kavanagh MA, Li J, Sathaiah M, Thirunavukarasu P, Fang B, et al. TRAIL gene-armed oncolytic poxvirus and oxaliplatin can work synergistically against colorectal cancer. Gene Ther. 2010;17:550–59. doi:10.1038/gt.2010.5.
   PubMed Web of Science ®Google Scholar
• Jeong SN, Yoo SY. Novel oncolytic virus armed with cancer suicide gene and normal vasculogenic gene for improved anti-tumor activity. Cancers (Basel). 2020;12:1070. doi:10.3390/cancers12051070.
   PubMed Web of Science ®Google Scholar
• Wu T, Xiang Y, Liu T, Wang X, Ren X, Ye T, Li G. Oncolytic vaccinia virus expressing aphrocallistes vastus lectin as a cancer therapeutic agent. Mar Drugs. 2019;17:363. doi:10.3390/md17060363.
   PubMed Web of Science ®Google Scholar
• Horita K, Kurosaki H, Nakatake M, Ito M, Kono H, Nakamura T. Long noncoding RNA UCA1 enhances sensitivity to oncolytic vaccinia virus by sponging miR-18a/mir-182 and modulating the Cdc42/filopodia axis in colorectal cancer. Biochem Biophys Res Commun. 2019;516:831–38. doi:10.1016/j.bbrc.2019.06.125.
   PubMed Web of Science ®Google Scholar
• Ottolino-Perry K, Acuna SA, Angarita FA, Sellers C, Zerhouni S, Tang N, McCart JA. Oncolytic vaccinia virus synergizes with irinotecan in colorectal cancer. Mol Oncol. 2015;9:1539–52. doi:10.1016/j.molonc.2015.04.009.
   PubMed Web of Science ®Google Scholar
• MacTavish H, Diallo JS, Huang B, Stanford M, Le Boeuf F, De Silva N, Cox J, Simmons JG, Guimond T, Falls T, et al. Enhancement of vaccinia virus based oncolysis with histone deacetylase inhibitors. PLoS One. 2010;5:e14462. doi:10.1371/journal.pone.0014462.
   PubMed Web of Science ®Google Scholar
• Zhou J, Sun XY, Fernando GJ, Frazer IH. The vaccinia virus K2L gene encodes a serine protease inhibitor which inhibits cell-cell fusion. Virology. 1992;189:678–86. doi:10.1016/0042-6822(92)90591-C.
   PubMed Web of Science ®Google Scholar
• Wolffe EJ, Katz E, Weisberg A, Moss B. The A34R glycoprotein gene is required for induction of specialized actin-containing microvilli and efficient cell-to-cell transmission of vaccinia virus. J Virol. 1997;71:3904–15. doi:10.1128/jvi.71.5.3904-3915.1997.
   PubMed Web of Science ®Google Scholar
• Bartlett N, Symons JA, Tscharke DC, Smith GL. The vaccinia virus N1L protein is an intracellular homodimer that promotes virulence. J Gen Virol. 2002;83:1965–76. doi:10.1099/0022-1317-83-8-1965.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Abrahams MR, Hunt LA, Suttles J, Marshall W, Lahiri DK, Kotwal GJ. The vaccinia virus N1L protein influences cytokine secretion in vitro after infection. Ann N Y Acad Sci. 2005;1056:69–86. doi:10.1196/annals.1352.005.
   PubMed Web of Science ®Google Scholar
• Meng X, Jiang C, Arsenio J, Dick K, Cao J, Xiang Y. Vaccinia virus K1L and C7L inhibit antiviral activities induced by type I interferons. J Virol. 2009;83:10627–36. doi:10.1128/JVI.01260-09.
   PubMed Web of Science ®Google Scholar
• Shisler JL, Jin XL. The vaccinia virus K1L gene product inhibits host NF-kappaB activation by preventing IkappaBalpha degradation. J Virol. 2004;78:3553–60. doi:10.1128/JVI.78.7.3553-3560.2004.
   PubMed Web of Science ®Google Scholar
• Kawagishi-Kobayashi M, Silverman JB, Ung TL, Dever TE. Regulation of the protein kinase PKR by the vaccinia virus pseudosubstrate inhibitor K3L is dependent on residues conserved between the K3L protein and the PKR substrate eIf2alpha. Mol Cell Biol. 1997;17:4146–58. doi:10.1128/MCB.17.7.4146.
   PubMed Web of Science ®Google Scholar
• Stack J, Haga IR, Schroder M, Bartlett NW, Maloney G, Reading PC, Fitzgerald KA, Smith GL, Bowie AG. Vaccinia virus protein A46R targets multiple Toll-like–interleukin-1 receptor adaptors and contributes to virulence. J Exp Med. 2005;201:1007–18. doi:10.1084/jem.20041442.
   PubMed Web of Science ®Google Scholar
• Bowie A, Kiss-Toth E, Symons JA, Smith GL, Dower SK, O’Neill LA. A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc Natl Acad Sci USA. 2000;97:10162–67. doi:10.1073/pnas.160027697.
   PubMed Web of Science ®Google Scholar
• Kleinpeter P, Remy-Ziller C, Winter E, Gantzer M, Nourtier V, Kempf J, Hortelano J, Schmitt D, Schultz H, Geist M, et al. By binding CD80 and CD86, the vaccinia virus M2 protein blocks their interactions with both CD28 and CTLA4 and potentiates CD80 binding to PD-L1. J Virol. 2019;93. doi:10.1128/JVI.00207-19.
   PubMed Web of Science ®Google Scholar
• Yan WL, Shen KY, Tien CY, Chen YA, Liu SJ. Recent progress in GM-CSF-based cancer immunotherapy. Immunotherapy. 2017;9:347–60. doi:10.2217/imt-2016-0141.
   PubMed Web of Science ®Google Scholar
• Gowhari Shabgah A, Al-Obaidi ZMJ, Sulaiman Rahman H, Kamal Abdelbasset W, Suksatan W, Bokov DO, Thangavelu L, Turki Jalil A, Jadidi-Niaragh F, Mohammadi H, et al. Does CCL19 act as a double-edged sword in cancer development? Clin Exp Immunol. 2022;207:164–75. doi:10.1093/cei/uxab039.
   PubMed Web of Science ®Google Scholar
• Hillinger S, Yang SC, Zhu L, Huang M, Duckett R, Atianzar K, Batra RK, Strieter RM, Dubinett SM, Sharma S. EBV-induced molecule 1 ligand chemokine (ELC/CCL19) promotes IFN-γ-dependent antitumor responses in a lung cancer model. J Immunol. 2003;171:6457–65. doi:10.4049/jimmunol.171.12.6457.
   PubMed Web of Science ®Google Scholar
• Lu J, Ma J, Cai W, Wangpu X, Feng H, Zhao J, Guan S, Zong Y, Lu A. CC motif chemokine ligand 19 suppressed colorectal cancer in vivo accompanied by an increase in IL-12 and IFN-γ. Biomed Pharmacother. 2015;69:374–79. doi:10.1016/j.biopha.2014.12.032.
   PubMed Web of Science ®Google Scholar
• Darrouzet E, Lindenthal S, Marcellin D, Pellequer JL, Pourcher T. The sodium/iodide symporter: state of the art of its molecular characterization. Biochim Biophys Acta. 2014;1838:244–53. doi:10.1016/j.bbamem.2013.08.013.
   PubMed Web of Science ®Google Scholar
• Gundacker D, Leys SP, Schroder HC, Muller IM, Muller WE. Isolation and cloning of a C-type lectin from the hexactinellid sponge Aphrocallistes vastus: a putative aggregation factor. Glycobiology. 2001;11:21–29. doi:10.1093/glycob/11.1.21.
   PubMed Web of Science ®Google Scholar
• Xuan W, Yu H, Zhang X, Song D. Crosstalk between the lncRNA UCA1 and microRnas in cancer. FEBS Lett. 2019;593:1901–14. doi:10.1002/1873-3468.13470.
   PubMed Web of Science ®Google Scholar
• Gatti-Mays ME, Strauss J, Donahue RN, Palena C, Del Rivero J, Redman JM, Madan RA, Marté JL, Cordes LM, Lamping E, et al. A phase I dose-escalation trial of BN-CV301, a recombinant poxviral vaccine targeting MUC1 and CEA with costimulatory molecules. Clin Cancer Res. 2019;25:4933–44. doi:10.1158/1078-0432.CCR-19-0183.
   PubMed Web of Science ®Google Scholar
• Duggan MC, Jochems C, Donahue RN, Richards J, Karpa V, Foust E, Paul B, Brooks T, Tridandapani S, Olencki T, et al. A phase I study of recombinant (r) vaccinia-CEA(6D)-TRICOM and rFowlpox-CEA(6D)-TRICOM vaccines with GM-CSF and IFN-α-2b in patients with CEA-expressing carcinomas. Cancer Immunol Immunother. 2016;65:1353–64. doi:10.1007/s00262-016-1893-7.
   PubMed Web of Science ®Google Scholar
• Park SH, Breitbach CJ, Lee J, Park JO, Lim HY, Kang WK, Moon A, Mun J-H, Sommermann EM, Maruri Avidal L, et al. Phase 1b trial of biweekly intravenous Pexa-Vec (JX-594), an oncolytic and immunotherapeutic vaccinia virus in colorectal cancer. Mol Ther. 2015;23:1532–40. doi:10.1038/mt.2015.109.
   PubMed Web of Science ®Google Scholar
• Zeh HJ, Downs-Canner S, McCart JA, Guo ZS, Rao UN, Ramalingam L, Thorne SH, Jones HL, Kalinski P, Wieckowski E, et al. First-in-man study of western reserve strain oncolytic vaccinia virus: safety, systemic spread, and antitumor activity. Mol Ther. 2015;23:202–14. doi:10.1038/mt.2014.194.
   PubMed Web of Science ®Google Scholar
• Downs-Canner S, Guo ZS, Ravindranathan R, Breitbach CJ, O’Malley ME, Jones HL, Moon A, McCart JA, Shuai Y, Zeh HJ, et al. Phase 1 study of intravenous oncolytic poxvirus (vvDD) in patients with advanced solid cancers. Mol Ther. 2016;24:1492–501. doi:10.1038/mt.2016.101.
   PubMed Web of Science ®Google Scholar
• Scurr M, Pembroke T, Bloom A, Roberts D, Thomson A, Smart K, Bridgeman H, Adams R, Brewster A, Jones R, et al. Effect of modified vaccinia Ankara–5T4 and low-dose cyclophosphamide on antitumor immunity in metastatic colorectal cancer. JAMA Oncol. 2017;3:e172579. doi:10.1001/jamaoncol.2017.2579.
   PubMed Web of Science ®Google Scholar
• Harrop R, Connolly N, Redchenko I, Valle J, Saunders M, Ryan MG, Myers KA, Drury N, Kingsman SM, Hawkins RE, et al. Vaccination of colorectal cancer patients with modified vaccinia Ankara delivering the tumor antigen 5T4 (TroVax) induces immune responses which correlate with disease control: a phase I/II trial. Clin Cancer Res. 2006;12:3416–24. doi:10.1158/1078-0432.CCR-05-2732.
   PubMed Web of Science ®Google Scholar
• Harrop R, Drury N, Shingler W, Chikoti P, Redchenko I, Carroll MW, Kingsman SM, Naylor S, Melcher A, Nicholls J, et al. Vaccination of colorectal cancer patients with modified vaccinia ankara encoding the tumor antigen 5T4 (TroVax) given alongside chemotherapy induces potent immune responses. Clin Cancer Res. 2007;13:4487–94. doi:10.1158/1078-0432.CCR-07-0704.
   PubMed Web of Science ®Google Scholar
• Harrop R, Drury N, Shingler W, Chikoti P, Redchenko I, Carroll MW, Kingsman SM, Naylor S, Griffiths R, Steven N, et al. Vaccination of colorectal cancer patients with TroVax given alongside chemotherapy (5-fluorouracil, leukovorin and irinotecan) is safe and induces potent immune responses. Cancer Immunol Immunother. 2008;57:977–86. doi:10.1007/s00262-007-0428-7.
   PubMed Web of Science ®Google Scholar
• Morse MA. Virus-based therapies for colon cancer. Expert Opin Biol Ther. 2005;5:1627–33. doi:10.1517/14712598.5.12.1627.
   PubMed Web of Science ®Google Scholar
• Hill C, Grundy M, Bau L, Wallington S, Balkaran J, Ramos V, Fisher K, Seymour L, Coussios C, Carlisle R. Polymer stealthing and mucin-1 retargeting for enhanced pharmacokinetics of an oncolytic vaccinia virus. Mol Ther Oncolytics. 2021;21:47–61. doi:10.1016/j.omto.2021.03.011.
   PubMed Web of Science ®Google Scholar