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Research Article

Local therapy with an engineered oncolytic adenovirus enables antitumor response in non-injected melanoma tumors in mice treated with aPD-1

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Article: 2028960 | Received 15 Oct 2021, Accepted 10 Jan 2022, Published online: 22 Jan 2022

References

  • Robert C, Ribas A, Schachter J, Arance A, Grob -J-J, Mortier L, Daud A, Carlino MS, McNeil CM, Lotem M, et al. Pembrolizumab versus ipilimumab in advanced melanoma (KEYNOTE-006): post-hoc 5-year results from an open-label, multicentre, randomised, controlled, phase 3 study. Lancet Oncol. 2019;20(9):1239–14. doi:10.1016/S1470-2045(19)30388-2.
  • Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph R, Weber JS, et al. Five-year survival outcomes for patients with advanced melanoma treated with pembrolizumab in KEYNOTE-001. Ann Oncol. 2019;30(4):582–588. doi:10.1093/annonc/mdz011.
  • Gutzmer R, Stroyakovskiy D, Gogas H, Robert C, Lewis K, Protsenko S, Pereira RP, Eigentler T, Rutkowski P, Demidov L, et al. Atezolizumab, vemurafenib, and cobimetinib as first-line treatment for unresectable advanced BRAFV600 mutation-positive melanoma (IMspire150): primary analysis of the randomised, double-blind, placebo-controlled, phase 3 trial. The Lancet. 2020;395(10240):1835–1844. doi:10.1016/S0140-6736(20)30934-X.
  • Gershenwald JE, Scolyer RA. Melanoma staging: American Joint Committee on Cancer (AJCC) 8th edition and beyond. Ann Surg Oncol. 2018;25(8):2105–2110. doi:10.1245/s10434-018-6513-7.
  • Tan S, Li D, Zhu X. Cancer immunotherapy: pros, cons and beyond. Biomed Pharmacother. 2020;124:109821. doi:10.1016/j.biopha.2020.109821.
  • Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell. 2017;168(4):707–723. doi:10.1016/j.cell.2017.01.017.
  • Jenkins RW, Barbie DA, Flaherty KT. Mechanisms of resistance to immune checkpoint inhibitors. Br J Cancer. 2018;118(1):9–16. doi:10.1038/bjc.2017.434.
  • Middleton MR, Hoeller C, Michielin O, Robert C, Caramella C, Öhrling K, Hauschild A. Intratumoural immunotherapies for unresectable and metastatic melanoma: current status and future perspectives. Br J Cancer. 2020;123(6):885–897. doi:10.1038/s41416-020-0994-4.
  • Aznar MA, Planelles L, Perez-Olivares M, Molina C, Garasa S, Etxeberría I, Perez G, Rodriguez I, Bolaños E, Lopez-Casas P, et al. Immunotherapeutic effects of intratumoral nanoplexed poly I:C. J Immunother Cancer. 2019;7(1):116. doi:10.1186/s40425-019-0568-2.
  • 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(6):1109–1119.e10. doi:10.1016/j.cell.2017.08.027.
  • Koski A, Bramante S, Kipar A, Oksanen M, Juhila J, Vassilev L, Joensuu T, Kanerva A, Hemminki A. Biodistribution analysis of oncolytic adenoviruses in patient autopsy samples reveals vascular transduction of noninjected tumors and tissues. Mol Therapy. 2015;23(10):1641–1652. doi:10.1038/mt.2015.125.
  • Ahmed J, Chard LS, Yuan M, Wang J, Howells A, Li Y, Li H, Zhang Z, Lu S, Gao D, et al. A new oncolytic Vaccinia virus augments antitumor immune responses to prevent tumor recurrence and metastasis after surgery. J Immunother Cancer. 2020;8(1):e000415. doi:10.1136/jitc-2019-000415.
  • 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(17):1658–1667. doi:10.1200/JCO.2017.73.7379.
  • Bai Y, Hui P, Du X, Su X. Updates to the antitumor mechanism of oncolytic virus. Thoracic Cancer. 2019;10(5):1031–1035. doi:10.1111/1759-7714.13043.
  • Matos ALD, Franco LS, McFadden G. Oncolytic viruses and the immune system: the dynamic duo. Mol Ther Methods Clin Dev. 2020;17:349–358. doi:10.1016/j.omtm.2020.01.001.
  • Quixabeira DCA, Zafar S, Santos JM, Cervera-Carrascon V, Havunen R, Kudling TV, Basnet S, Anttila M, Kanerva A, Hemminki A, et al. Oncolytic adenovirus coding for a variant Interleukin 2 (vIL-2) cytokine re-programs the tumor microenvironment and confers enhanced tumor control. Front Immunol. 2021;12. doi:10.3389/fimmu.2021.674400
  • Ranki T, Pesonen S, Hemminki A, Partanen K, Kairemo K, Alanko T, Lundin J, Linder N, Turkki R, Ristimäki A, et al. Phase I study with ONCOS-102 for the treatment of solid tumors - an evaluation of clinical response and exploratory analyses of immune markers. J Immunother Cancer. 2016;4(1):17. doi:10.1186/s40425-016-0121-5.
  • Ramelyte E, Tastanova A, Balázs Z, Ignatova D, Turko P, Menzel U, Guenova E, Beisel C, Krauthammer M, Levesque MP, et al. Oncolytic virotherapy-mediated anti-tumor response: a single-cell perspective. Cancer Cell. 2021;39(3):394–406.e4. doi:10.1016/j.ccell.2020.12.022.
  • Heiniö C, Havunen R, Santos J, de Lint K, Cervera-Carrascon V, Kanerva A, Hemminki A. TNFa and IL2 encoding oncolytic adenovirus activates pathogen and danger-associated immunological signaling. Cells. 2020;9(4):798. doi:10.3390/cells9040798.
  • Kanerva A, Nokisalmi P, Diaconu I, Koski A, Cerullo V, Liikanen I, Tähtinen S, Oksanen M, Heiskanen R, Pesonen S, et al. Antiviral and antitumor T-cell immunity in patients treated with GM-CSF–coding oncolytic adenovirus. Clin Cancer Res. 2013;19(10):2734–2744. doi:10.1158/1078-0432.CCR-12-2546.
  • Havunen R, Siurala M, Sorsa S, Grönberg-Vähä-Koskela S, Behr M, Tähtinen S, Santos JM, Karell P, Rusanen J, Nettelbeck DM, et al. Oncolytic adenoviruses armed with tumor necrosis factor alpha and Interleukin-2 enable successful adoptive cell therapy. Mol Ther Oncolytics. 2017;4:77–86. doi:10.1016/j.omto.2016.12.004.
  • Jiang H, Shin DH, Nguyen TT, Fueyo J, Fan X, Henry V, Carrillo CC, Yi Y, Alonso MM, Collier TL, et al. Localized treatment with oncolytic adenovirus delta-24-RGDOX induces systemic immunity against disseminated subcutaneous and intracranial melanomas. Clin Cancer Res. 2019;25(22):6801–6814. doi:10.1158/1078-0432.CCR-19-0405.
  • Cervera-Carrascon V, Siurala M, Santos JM, Havunen R, Tähtinen S, Karell P, Sorsa S, Kanerva A, Hemminki A. TNFa and IL-2 armed adenoviruses enable complete responses by anti-PD-1 checkpoint blockade. OncoImmunology. 2018;7(5):e1412902. doi:10.1080/2162402X.2017.1412902.
  • Kaluza KM, Thompson JM, Kottke TJ, Flynn Gilmer HC, Knutson DL, Vile RG. Adoptive T cell therapy promotes the emergence of genomically altered tumor escape variants. Int J Cancer. 2012;131(4):844–854. doi:10.1002/ijc.26447.
  • Siurala M, Havunen R, Saha D, Lumen D, Airaksinen A.J, Tähtinen S, Cervera-Carrascon V, Bramante S, Parviainen S, Vähä-Koskela M, et al. Adenoviral delivery of tumor necrosis factor-α and Interleukin-2 enables successful adoptive cell therapy of immunosuppressive melanoma. Mol Ther. 2016;24(8):1435–1443. doi:10.1038/mt.2016.137.
  • Fusciello M, Fontana F, Tähtinen S, Capasso C, Feola S, Martins B, Chiaro J, Peltonen K, Ylösmäki L, Ylösmäki E, et al. Artificially cloaked viral nanovaccine for cancer immunotherapy. Nat Commun. 2019;10(1):5747. doi:10.1038/s41467-019-13744-8.
  • Ribot JC, Lopes N, Silva-Santos B. γδ T cells in tissue physiology and surveillance. Nat Rev Immunol. 2021;21(4):221–232. doi:10.1038/s41577-020-00452-4.
  • Sewell AK. Why must T cells be cross-reactive? Nat Rev Immunol. 2012;12(9):669–677. doi:10.1038/nri3279.
  • Dillman RO, DePriest C, McClure SE. High-dose IL2 in metastatic melanoma: better survival in patients immunized with antigens from autologous tumor cell lines. Cancer Biother Radiopharm. 2014;29(2):53–57. doi:10.1089/cbr.2013.1565.
  • Santos JM, Havunen R, Siurala M, Cervera‐Carrascon V, Tähtinen S, Sorsa S, Anttila M, Karell P, Kanerva A, Hemminki A, et al. Adenoviral production of interleukin-2 at the tumor site removes the need for systemic postconditioning in adoptive cell therapy. Int J Cancer. 2017;141(7):1458–1468. doi:10.1002/ijc.30839.
  • Cervera-Carrascon V, Quixabeira DCA, Havunen R, Santos JM, Kutvonen E, Clubb JHA, Siurala M, Heiniö C, Zafar S, Koivula T, et al. Comparison of clinically relevant oncolytic virus platforms for enhancing T cell therapy of solid tumors. Mol Ther Oncolytics. 2020;17:47–60. doi:10.1016/j.omto.2020.03.003.
  • Malvehy J, Samoylenko I, Schadendorf D, Gutzmer R, Grob J-J, Sacco JJ, Gorski KS, Anderson A, Pickett CA, Liu K, et al. Talimogene laherparepvec upregulates immune-cell populations in non-injected lesions: findings from a phase II, multicenter, open-label study in patients with stage IIIB-IVM1c melanoma. J Immunother Cancer. 2021;9(3):e001621. doi:10.1136/jitc-2020-001621.
  • Xia A, Zhang Y, Xu J, Yin T, Lu X-J. T cell dysfunction in cancer immunity and immunotherapy. Front Immunol. 2019;10:1719. doi:10.3389/fimmu.2019.01719.
  • Kaufman HL, Maciorowski D. Advancing oncolytic virus therapy by understanding the biology. Nat Rev Clin Oncol. 2021;18(4):197–198. doi:10.1038/s41571-021-00490-4.
  • Li L, Liu S, Han D, Tang B, Ma J. Delivery and biosafety of oncolytic virotherapy. Front Oncol. 2020;10:475. doi:10.3389/fonc.2020.00475.
  • Hendrickx R, Stichling N, Koelen J, Kuryk L, Lipiec A, Greber UF. Innate immunity to adenovirus. Hum Gene Ther. 2014;25(4):265–284. doi:10.1089/hum.2014.001.
  • Donnarumma T, Young GR, Merkenschlager J, Eksmond U, Bongard N, Nutt SL, Boyer C, Dittmer U, Le-Trilling VTK, Trilling M, et al. Opposing development of cytotoxic and follicular helper CD4 T cells controlled by the TCF-1-Bcl6 Nexus. Cell Rep. 2016;17(6):1571–1583. doi:10.1016/j.celrep.2016.10.013.
  • Heemskerk B, van Vreeswijk T, Veltrop-Duits LA, Sombroek CC, Franken K, Verhoosel RM, Hiemstra PS, van Leeuwen D, Ressing ME, Toes REM, et al. Adenovirus-specific CD4 + T cell clones recognizing endogenous antigen inhibit viral replication in vitro through cognate interaction. J Immunol. 2006;177(12):8851–8859. doi:10.4049/jimmunol.177.12.8851.
  • Havunen R, Santos JM, Sorsa S, Rantapero T, Lumen D, Siurala M, Airaksinen AJ, Cervera-Carrascon V, Tähtinen S, Kanerva A, et al. Abscopal effect in non-injected tumors achieved with cytokine-armed oncolytic adenovirus. Mol Ther Oncolytics. 2018;11:109–121. doi:10.1016/j.omto.2018.10.005.
  • Moesta AK, Cooke K, Piasecki J, Mitchell P, Rottman JB, Fitzgerald K, Zhan J, Yang B, Le T, Belmontes B, et al. Local delivery of OncoVEX mGM-CSF generates systemic antitumor immune responses enhanced by cytotoxic T-lymphocyte–associated protein blockade. Clin Cancer Res. 2017;23(20):6190–6202. doi:10.1158/1078-0432.CCR-17-0681.
  • Taipale K, Liikanen I, Juhila J, Turkki R, Tähtinen S, Kankainen M, Vassilev L, Ristimäki A, Koski A, Kanerva A, et al. Chronic activation of innate immunity correlates with poor prognosis in cancer patients treated with oncolytic adenovirus. Mol Therapy. 2016;24(1):175–183. doi:10.1038/mt.2015.143.
  • Demaria S, Formenti SC. Can abscopal effects of local radiotherapy be predicted by modeling T cell trafficking? J Immunother Cancer. 2016;4(1):29. doi:10.1186/s40425-016-0133-1.
  • Ma J, Ramachandran M, Jin C, Quijano-Rubio C, Martikainen M, Yu D, Essand M. Characterization of virus-mediated immunogenic cancer cell death and the consequences for oncolytic virus-based immunotherapy of cancer. Cell Death Dis. 2020;11(1):48. doi:10.1038/s41419-020-2236-3.
  • Maier B, Leader AM, Chen ST, Tung N, Chang C, LeBerichel J, Chudnovskiy A, Maskey S, Walker L, Finnigan JP, et al. A conserved dendritic-cell regulatory program limits antitumour immunity. Nature. 2020;580(7802):257–262. doi:10.1038/s41586-020-2134-y.
  • Dammeijer F, van Gulijk M, Mulder EE, Lukkes M, Klaase L, van Den Bosch T, van Nimwegen M, Lau SP, Latupeirissa K, Schetters S, et al. The PD-1/PD-L1-checkpoint restrains T cell immunity in tumor-draining lymph nodes. Cancer Cell. 2020;38(5):685–700.e8. doi:10.1016/j.ccell.2020.09.001.
  • Oh SA, Wu D-C, Cheung J, Navarro A, Xiong H, Cubas R, Totpal K, Chiu H, Wu Y, Comps-Agrar L, et al. PD-L1 expression by dendritic cells is a key regulator of T-cell immunity in cancer. Nat Cancer. 2020;1(7):681–691. doi:10.1038/s43018-020-0075-x.
  • Mayoux M, Roller A, Pulko V, Sammicheli S, Chen S, Sum E, Jost C, Fransen MF, Buser RB, Kowanetz M, et al. Dendritic cells dictate responses to PD-L1 blockade cancer immunotherapy. Sci Transl Med. 2020;12(534). doi:10.1126/scitranslmed.aav7431.
  • Steeg PS. Targeting metastasis. Nat Rev Cancer. 2016;16(4):201–218. doi:10.1038/nrc.2016.25.
  • Schadendorf D, van Akkooi ACJ, Berking C, Griewank KG, Gutzmer R, Hauschild A, Stang A, Roesch A, Ugurel S. Melanoma. The Lancet. 2018;392(10151):971–984. doi:10.1016/S0140-6736(18)31559-9.
  • Zhao H, Wang H, Kong F, Xu W, Wang T, Xiao F, Wang L, Huang D, Seth P, Yang Y, et al. Oncolytic adenovirus rAd.DCN inhibits breast tumor growth and lung metastasis in an immune-competent orthotopic xenograft model. Hum Gene Ther. 2019;30(2):197–210. doi:10.1089/hum.2018.055.
  • Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39(1):1–10. doi:10.1016/j.immuni.2013.07.012.
  • Veiga-Fernandes H, Walter U, Bourgeois C, McLean A, Rocha B. Response of naïve and memory CD8 + T cells to antigen stimulation in vivo. Nat Immunol. 2000;1(1):47–53. doi:10.1038/76907.