Oncolytic virus immunotherapy induces immunogenic cell death and overcomes STING deficiency in melanoma

References

• Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359:1350–1355. doi:10.1126/science.aar4060.
   PubMed Web of Science ®Google Scholar
• Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell. 2017;168:707–723. doi:10.1016/j.cell.2017.01.017.
   PubMed Web of Science ®Google Scholar
• Gajewski TF, Louahed J, Brichard VG. Gene signature in melanoma associated with clinical activity: a potential clue to unlock cancer immunotherapy. Cancer J. 2010;16:399–403. doi:10.1097/PPO.0b013e3181eacbd8.
   PubMed Web of Science ®Google Scholar
• Vilain RE, Menzies AM, Wilmott JS, Kakavand H, Madore J, Guminski A, Liniker E, Kong BY, Cooper AJ, Howle JR, et al. Dynamic changes in PD-L1 expression and immune infiltrates early during treatment predict response to PD-1 blockade in melanoma. Clin Cancer Res. 2017;23:5024–5033. doi:10.1158/1078-0432.CCR-16-0698.
   PubMed Web of Science ®Google Scholar
• Colli LM, Machiela MJ, Myers TA, Jessop L, Yu K, Chanock SJ. Burden of nonsynonymous mutations among TCGA cancers and candidate immune checkpoint inhibitor responses. Cancer Res. 2016;76:3767–3772. doi:10.1158/0008-5472.CAN-16-0170.
   PubMed Web of Science ®Google Scholar
• Erdag G, Schaefer JT, Smolkin ME, Deacon DH, Shea SM, Dengel LT, Patterson JW, Slingluff CL Jr. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 2012;72:1070–1080. doi:10.1158/0008-5472.CAN-11-3218.
   PubMed Web of Science ®Google Scholar
• Yi M, Qin S, Zhao W, Yu S, Chu Q, Wu K. The role of neoantigen in immune checkpoint blockade therapy. Exp Hematol Oncol. 2018;7:28. doi:10.1186/s40164-018-0120-y.
   PubMed Web of Science ®Google Scholar
• Spranger S, Dai D, Horton B, Gajewski TF. Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy. Cancer Cell. 2017;31:711–723. doi:10.1016/j.ccell.2017.04.003.
   PubMed Web of Science ®Google Scholar
• Ayers M, Lunceford J, Nebozhyn M, Murphy E, Loboda A, Kaufman DR, Albright A, Cheng JD, Kang SP, Shankaran V, et al. IFN-gamma-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 2017;127:2930–2940. doi:10.1172/JCI91190.
   PubMed Web of Science ®Google Scholar
• Woo SR, Fuertes MB, Corrales L, Spranger S, Furdyna MJ, Leung MY, Duggan R, Wang Y, Barber GN, Fitzgerald KA, et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity. 2014;41:830–842. doi:10.1016/j.immuni.2014.10.017.
   PubMed Web of Science ®Google Scholar
• Li T, Chen ZJ. The cGAS-cGAMP-STING pathway connects DNA damage to inflammation, senescence, and cancer. J Exp Med. 2018;215:1287–1299. doi:10.1084/jem.20180139.
   PubMed Web of Science ®Google Scholar
• Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, Slingluff C, McKee M, Gajewski TF. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009;69:3077–3085. doi:10.1158/0008-5472.CAN-08-2281.
   PubMed Web of Science ®Google Scholar
• Bommareddy PK, Shettigar M, Kaufman HL. Integrating oncolytic viruses in combination cancer immunotherapy. Nat Rev Immunol. 2018;18:498–513. doi:10.1038/s41577-018-0014-6.
   PubMed Web of Science ®Google Scholar
• Corrales L, Glickman LH, McWhirter SM, Kanne DB, Sivick KE, Katibah GE, Woo SR, Lemmens E, Banda T, Leong JJ, et al. Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep. 2015;11:1018–1030. doi:10.1016/j.celrep.2015.04.031.
   PubMed Web of Science ®Google Scholar
• Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discov. 2015;14:642–662. doi:10.1038/nrd4663.
   PubMed Web of Science ®Google Scholar
• Ribas A, Dummer R, Puzanov I, VanderWalde A, Andtbacka RHI, Michielin O, Olszanski AJ, Malvehy J, Cebon J, Fernandez E, et al. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell. 2017;170:1109–1119. e10. doi:10.1016/j.cell.2017.08.027.
   PubMed Web of Science ®Google Scholar
• Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, Delman KA, Spitler LE, Puzanov I, Agarwala SS, et al. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol. 2015;33:2780–2788.
   PubMed Web of Science ®Google Scholar
• Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS, Kim-Schulze S. Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage IIIc and IV melanoma. Ann Surg Oncol. 2010;17:718–730. doi:10.1245/s10434-009-0809-6.
   PubMed Web of Science ®Google Scholar
• Reinert LS, Lopusna K, Winther H, Sun C, Thomsen MK, Nandakumar R, Mogensen TH, Meyer M, Vaegter C, Nyengaard JR, et al. Sensing of HSV-1 by the cGAS-STING pathway in microglia orchestrates antiviral defence in the CNS. Nat Commun. 2016;7:13348. doi:10.1038/ncomms13348.
   PubMed Web of Science ®Google Scholar
• Bedoui S, Whitney PG, Waithman J, Eidsmo L, Wakim L, Caminschi I, Allan RS, Wojtasiak M, Shortman K, Carbone FR, et al. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol. 2009;10:488–495. doi:10.1038/ni.1724.
   PubMed Web of Science ®Google Scholar
• Bommareddy PK, Aspromonte S, Zloza A, Rabkin SD, Kaufman HL. MEK inhibition enhances oncolytic virus immunotherapy through increased tumor cell killing and T cell activation. Sci Transl Med. 2018;10. doi:10.1126/scitranslmed.aao4496.
   PubMed Web of Science ®Google Scholar
• Jenkins MH, Steinberg SM, Alexander MP, Fisher JL, Ernstoff MS, Turk MJ, Mullins DW, Brinckerhoff CE. Multiple murine BRaf(V600E) melanoma cell lines with sensitivity to PLX4032. Pigment Cell Melanoma Res. 2014;27:495–501. doi:10.1111/pcmr.12220.
   PubMed Web of Science ®Google Scholar
• Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034. doi:10.1186/gb-2002-3-7-research0034.
   PubMed Web of Science ®Google Scholar
• Yu Z, Adusumilli PS, Eisenberg DP, Darr E, Ghossein RA, Li S, Liu S, Singh B, Shah JP, Fong Y, et al. Nectin-1 expression by squamous cell carcinoma is a predictor of herpes oncolytic sensitivity. Mol Ther. 2007;15:103–113. doi:10.1038/sj.mt.6300009.
   PubMed Web of Science ®Google Scholar
• Friedman GK, Bernstock JD, Chen D, Nan L, Moore BP, Kelly VM, Youngblood SL, Langford CP, Han X, Ring EK, et al. Enhanced sensitivity of patient-derived pediatric high-grade brain tumor xenografts to oncolytic HSV-1 virotherapy correlates with nectin-1 expression. Sci Rep. 2018;8:13930. doi:10.1038/s41598-018-32353-x.
   PubMed Web of Science ®Google Scholar
• Kepp O, Senovilla L, Vitale I, Vacchelli E, Adjemian S, Agostinis P, Apetoh L, Aranda F, Barnaba V, Bloy N, et al. Consensus guidelines for the detection of immunogenic cell death. Oncoimmunology. 2014;3:e955691. doi:10.4161/21624011.2014.955691.
   PubMed Web of Science ®Google Scholar
• Zhang J, Zhao J, Xu S, Li J, He S, Zeng Y, Xie L, Xie N, Liu T, Lee K, et al. Species-specific deamidation of cGAS by herpes simplex virus UL37 protein facilitates viral replication. Cell Host Microbe. 2018;24:234–248. e5. doi:10.1016/j.chom.2018.07.004.
   PubMed Web of Science ®Google Scholar
• Cai X, Chiu YH, Chen ZJ. The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol Cell. 2014;54:289–296. doi:10.1016/j.molcel.2014.03.040.
   PubMed Web of Science ®Google Scholar
• Barber GN. STING: infection, inflammation and cancer. Nat Rev Immunol. 2015;15:760–770. doi:10.1038/nri3921.
   PubMed Web of Science ®Google Scholar
• Deken MA, Gadiot J, Jordanova ES, Lacroix R, van Gool M, Kroon P, Pineda C, Geukes Foppen MH, Scolyer R, Song JY, et al. Targeting the MAPK and PI3K pathways in combination with PD1 blockade in melanoma. Oncoimmunology. 2016;5:e1238557. doi:10.1080/2162402X.2016.1238557.
   PubMed Web of Science ®Google Scholar
• Chesney J, Puzanov I, Collichio F, Singh P, Milhem MM, Glaspy J, Hamid O, Ross M, Friedlander P, Garbe C, et al. 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. 2018;36:1658–1667. doi:10.1200/JCO.2017.73.7379.
   PubMed Web of Science ®Google Scholar
• Minami M, Kita M, Yan XQ, Yamamoto T, Iida T, Sekikawa K, Iwakura Y, Imanishi J. Role of IFN-gamma and tumor necrosis factor-alpha in herpes simplex virus type 1 infection. J Interferon Cytokine Res. 2002;22:671–676. doi:10.1089/10799900260100150.
   PubMed Web of Science ®Google Scholar
• Ye T, Jiang K, Wei L, Barr MP, Xu Q, Zhang G, Ding C, Meng S, Piao H. Oncolytic Newcastle disease virus induces autophagy-dependent immunogenic cell death in lung cancer cells. Am J Cancer Res. 2018;8:1514–1527.
   PubMed Web of Science ®Google Scholar
• Ma Z, Damania B. The cGAS-STING defense pathway and its counteraction by viruses. Cell Host Microbe. 2016;19:150–158. doi:10.1016/j.chom.2016.01.010.
   PubMed Web of Science ®Google Scholar
• Xia T, Konno H, Barber GN. Recurrent loss of STING signaling in melanoma correlates with susceptibility to viral oncolysis. Cancer Res. 2016;76:6747–6759. doi:10.1158/0008-5472.CAN-16-1404.
   PubMed Web of Science ®Google Scholar
• Barber GN, Gual Pimenta de Queiroz NM, Xia T, Konno H. Ovarian cancer cells commonly exhibit defective STING signaling which affects sensitivity to viral oncolysis. Mol Cancer Res. 2018. doi:10.1158/1541-7786.MCR-18-0504. [Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Weiss JM, Guerin MV, Regnier F, Renault G, Galy-Fauroux I, Vimeux L, Feuillet V, Peranzoni E, Thoreau M, Trautmann A, et al. The STING agonist DMXAA triggers a cooperation between T lymphocytes and myeloid cells that leads to tumor regression. Oncoimmunology. 2017;6:e1346765. doi:10.1080/2162402X.2017.1346765.
   PubMed Web of Science ®Google Scholar
• Yuka Maeda HN, Sakaguchi S. Self-tumor-antigen-specific CD8 T cells were suppressed by regulatory T cells. Presented at AACR; Cancer Immunol Res; 2016.
   Google Scholar
• Rosenberg SA, Sherry RM, Morton KE, Scharfman WJ, Yang JC, Topalian SL, Royal RE, Kammula U, Restifo NP, Hughes MS, et al. Tumor progression can occur despite the induction of very high levels of self/tumor antigen-specific CD8+ T cells in patients with melanoma. J Immunol. 2005;175:6169–6176.
   PubMed Web of Science ®Google Scholar