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Original Research

Intra-tumoral delivery of CXCL11 via a vaccinia virus, but not by modified T cells, enhances the efficacy of adoptive T cell therapy and vaccines

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Article: e1395997 | Received 16 Oct 2017, Accepted 19 Oct 2017, Published online: 09 Jan 2018

References

  • Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, et al. Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer. N Engl J Med. 2015;373:1627–39. doi:10.1056/NEJMoa1507643.
  • Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372:2018–28. doi:10.1056/NEJMoa1501824.
  • Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell. 2015;27:450–61. doi:10.1016/j.ccell.2015.03.001.
  • June CH. Adoptive T cell therapy for cancer in the clinic. J Clin Invest. 2007;117:1466–76. doi:10.1172/JCI32446.
  • Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, Teachey DT, Chew A, Hauck B, Wright JF, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368:1509–18. doi:10.1056/NEJMoa1215134.
  • Porter DL, Hwang WT, Frey NV, Lacey SF, Shaw PA, Loren AW, Bagg A, Marcucci KT, Shen A, Gonzalez V, et al. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med. 2015;7:303ra139. doi:10.1126/scitranslmed.aac5415.
  • Sadelain M. CAR therapy: the CD19 paradigm. J Clin Invest. 2015;125:3392–400. doi:10.1172/JCI80010.
  • Zhang T, Cao L, Xie J, Shi N, Zhang Z, Luo Z, Yue D, Zhang Z, Wang L, Han W, et al. Efficiency of CD19 chimeric antigen receptor-modified T cells for treatment of B cell malignancies in phase I clinical trials: a meta-analysis. Oncotarget. 2015;6:33961–71. doi:10.18632/oncotarget.5582.
  • Moon EK, Wang LC, Dolfi DV, Wilson CB, Ranganathan R, Sun J, Kapoor V, Scholler J, Puré E, Milone MC. et al. Multifactorial T-cell hypofunction that is reversible can limit the efficacy of chimeric antigen receptor-transduced human T cells in solid tumors. Clin Cancer Res. 2014;20:4262–73. doi:10.1158/1078-0432.CCR-13-2627.
  • Newick K, O'Brien S, Sun J, Kapoor V, Maceyko S, Lo A, Puré E, Moon E, Albelda SM. Augmentation of CAR T-cell Trafficking and Antitumor Efficacy by Blocking Protein Kinase A Localization. Cancer Immunol Res. 2016;4:541–51. doi:10.1158/2326-6066.CIR-15-0263.
  • Ager A, Watson HA, Wehenkel SC, Mohammed RN. Homing to solid cancers: a vascular checkpoint in adoptive cell therapy using CAR T-cells. Biochem Soc Trans. 2016;44:377–85. doi:10.1042/BST20150254.
  • Moon EK, Carpenito C, Sun J, Wang LC, Kapoor V, Predina J, Powell DJ Jr, Riley JL, June CH, Albelda SM.. Expression of a functional CCR2 receptor enhances tumor localization and tumor eradication by retargeted human T cells expressing a mesothelin-specific chimeric antibody receptor. Clin Cancer Res. 2011;17:4719–30. doi:10.1158/1078-0432.CCR-11-0351.
  • Hong M, Puaux AL, Huang C, Loumagne L, Tow C, Mackay C, Kato M, Prévost-Blondel A, Avril MF, Nardin A, et al. Chemotherapy induces intratumoral expression of chemokines in cutaneous melanoma, favoring T-cell infiltration and tumor control. Cancer Res. 2011;71:6997–7009. doi:10.1158/0008-5472.CAN-11-1466.
  • 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;69:3077–85. doi:10.1158/0008-5472.CAN-08-2281.
  • Craddock JA, Lu A, Bear A, Pule M, Brenner MK, Rooney CM, Foster AE. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J Immunother. 2010;33:780–8. doi:10.1097/CJI.0b013e3181ee6675.
  • Heissmeyer V, Macian F, Im SH, Varma R, Feske S, Venuprasad K, Gu H, Liu YC, Dustin ML, Rao A. Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nat Immunol. 2004;5:255–65. doi:10.1038/ni1047.
  • Adachi Y, Hattori M, Yoshida T. Regulation of T cell activation and anergy by the intensity of the Ca(2)+ signal in cooperation with other signals. Biosci Biotechnol Biochem. 2010;74:1788–93. doi:10.1271/bbb.100107.
  • Hensbergen PJ, Wijnands PG, Schreurs MW, Scheper RJ, Willemze R, Tensen CP. The CXCR3 targeting chemokine CXCL11 has potent antitumor activity in vivo involving attraction of CD8+ T lymphocytes but not inhibition of angiogenesis. J Immunother. 2005;28:343–51. doi:10.1097/01.cji.0000165355.26795.27.
  • Berencsi K, Meropol NJ, Hoffman JP, Sigurdson E, Giles L, Rani P, Somasundaram R, Zhang T, Kalabis J, Caputo L, et al. Colon carcinoma cells induce CXCL11-dependent migration of CXCR3-expressing cytotoxic T lymphocytes in organotypic culture. Cancer Immunol Immunother. 2007;56:359–70. doi:10.1007/s00262-006-0190-2.
  • Flier J, Boorsma DM, van Beek PJ, Nieboer C, Stoof TJ, Willemze R, Tensen CP. Differential expression of CXCR3 targeting chemokines CXCL10, CXCL9, and CXCL11 in different types of skin inflammation. J Pathol. 2001;194:398–405. doi:10.1002/1096-9896(200108)194:4%3c397::AID-PATH899%3e3.0.CO;2-S.
  • Cole KE, Strick CA, Paradis TJ, Ogborne KT, Loetscher M, Gladue RP, Lin W, Boyd JG, Moser B, Wood DE, et al. Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J Exp Med 1998;187:2009–21. doi:10.1084/jem.187.12.2009.
  • Thorne SH. Immunotherapeutic potential of oncolytic vaccinia virus. Front Oncol. 2014;4:155. doi:10.3389/fonc.2014.00155.
  • Kim M. Replicating poxviruses for human cancer therapy. J Microbiol. 2015;53:209–18. doi:10.1007/s12275-015-5041-4.
  • Liu TC, Hwang T, Park BH, Bell J, Kirn DH. The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma. Mol Ther. 2008;16:1637–42. doi:10.1038/mt.2008.143.
  • Park BH, Hwang T, Liu TC, Sze DY, Kim JS, Kwon HC, Oh SY, Han SY, Yoon JH, Hong SH, et al. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol. 2008;9:533–42. doi:10.1016/S1470-2045(08)70107-4.
  • Heo J, Breitbach CJ, Moon A, Kim CW, Patt R, Kim MK, Lee YK, Oh SY, Woo HY, Parato K, et al. Sequential therapy with JX-594, a targeted oncolytic poxvirus, followed by sorafenib in hepatocellular carcinoma: preclinical and clinical demonstration of combination efficacy. Mol Ther. 2011;19:1170–9. doi:10.1038/mt.2011.39.
  • Sampath P, Thorne SH. Arming viruses in multi-mechanistic oncolytic viral therapy: current research and future developments, with emphasis on poxviruses. Oncolytic Virother. 2014;3:1–9.
  • Kirn DH, Wang Y, Le Boeuf F, Bell J, Thorne SH. Targeting of interferon-beta to produce a specific, multi-mechanistic oncolytic vaccinia virus. PLoS Med. 2007;4:e353. doi:10.1371/journal.pmed.0040353.
  • Wang LC, Lynn RC, Cheng G, Alexander E, Kapoor V, Moon EK, Sun J, Fridlender ZG, Isaacs SN, Thorne SH, et al. Treating tumors with a vaccinia virus expressing IFNbeta illustrates the complex relationships between oncolytic ability and immunogenicity. Mol Ther. 2012;20:736–48. doi:10.1038/mt.2011.228.
  • Li J, O'Malley M, Urban J, Sampath P, Guo ZS, Kalinski P, Thorne SH, Bartlett DL. Chemokine expression from oncolytic vaccinia virus enhances vaccine therapies of cancer. Mol Ther. 2011;19:650–7. doi:10.1038/mt.2010.312.
  • Nishio N, Diaconu I, Liu H, Cerullo V, Caruana I, Hoyos V, Bouchier-Hayes L, Savoldo B, Dotti G. Armed oncolytic virus enhances immune functions of chimeric antigen receptor-modified T cells in solid tumors. Cancer Res. 2014;74:5195–205. doi:10.1158/0008-5472.CAN-14-0697.
  • Liu Z, Ravindranathan R, Li J, Kalinski P, Guo ZS, Bartlett DL. CXCL11-Armed oncolytic poxvirus elicits potent antitumor immunity and shows enhanced therapeutic efficacy. Oncoimmunology. 2016;5:e1091554. doi:10.1080/2162402X.2015.1091554.
  • Francis L, Guo ZS, Liu Z, Ravindranathan R, Urban JA, Sathaiah M, Magge D, Kalinski P, Bartlett DL. Modulation of chemokines in the tumor microenvironment enhances oncolytic virotherapy for colorectal cancer. Oncotarget. 2016;7:22174–85. doi:10.18632/oncotarget.7907.
  • Carpenito C, Milone MC, Hassan R, Simonet JC, Lakhal M, Suhoski MM, Varela-Rohena A, Haines KM, Heitjan DF, Albelda SM, et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci U S A. 2009;106:3360–5. doi:10.1073/pnas.0813101106.
  • Lin KY, Guarnieri FG, Staveley-O'Carroll KF, Levitsky HI, August JT, Pardoll DM, Wu TC. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 1996;56:21–6.
  • Riese MJ, Wang LC, Moon EK, Joshi RP, Ranganathan A, June CH, Koretzky GA, Albelda SM. Enhanced effector responses in activated CD8+ T cells deficient in diacylglycerol kinases. Cancer Res. 2013;73:3566–77. doi:10.1158/0008-5472.CAN-12-3874.
  • Haas AR, Sun J, Vachani A, Wallace AF, Silverberg M, Kapoor V, Albelda SM. Cycloxygenase-2 inhibition augments the efficacy of a cancer vaccine. Clin Cancer Res. 2006;12:214–22. doi:10.1158/1078-0432.CCR-05-1178.
  • Quatromoni JG, Singhal S, Bhojnagarwala P, Hancock WW, Albelda SM, Eruslanov E. An optimized disaggregation method for human lung tumors that preserves the phenotype and function of the immune cells. J Leukoc Biol. 2015;97:201–9. doi:10.1189/jlb.5TA0814-373.
  • Sampath P, Li J, Hou W, Chen H, Bartlett DL, Thorne SH. Crosstalk between immune cell and oncolytic vaccinia therapy enhances tumor trafficking and antitumor effects. Mol Ther. 2013;21:620–8. doi:10.1038/mt.2012.257.
  • 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.
  • Chmielewski M, Hombach AA, Abken H. Of CARs and TRUCKs: chimeric antigen receptor (CAR) T cells engineered with an inducible cytokine to modulate the tumor stroma. Immunol Rev. 2014;257:83–90. doi:10.1111/imr.12125.
  • Chinnasamy D, Yu Z, Kerkar SP, Zhang L, Morgan RA, Restifo NP, Rosenberg SA. Local delivery of interleukin-12 using T cells targeting VEGF receptor-2 eradicates multiple vascularized tumors in mice. Clin Cancer Res. 2012;18:1672–83. doi:10.1158/1078-0432.CCR-11-3050.
  • Santoni M, Bracarda S, Nabissi M, Massari F, Conti A, Bria E, Tortora G, Santoni G, Cascinu S. CXC and CC chemokines as angiogenic modulators in nonhaematological tumors. Biomed Res Int. 2014;2014:768758. doi:10.1155/2014/768758.
  • Huang H, Liu Y, Xiang J. Synergistic effect of adoptive T-cell therapy and intratumoral interferon gamma-inducible protein-10 transgene expression in treatment of established tumors. Cellular Immunology. 2002; 217: 12–22. doi:10.1016/S0008-8749(02)00508-7.
  • Rodriguez MMB, Ryu S-M, Qian C, Geissler M, Grimm C, Preito J, Blum H, Mohr L, Immunotherapy of murine hepatocellular carcinoma by DNA vaccination combined with adenovirus-mediated chemokine and cytokine expression. Human Gene Therapy. 2008; 19:753–759, 2008. doi:10.1089/hum.2007.130.
  • Dotti G, Gottschalk S, Savoldo B, Brenner MK. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev. 2014;257:107–26. doi:10.1111/imr.12131.
  • Nishio N, Dotti G. Oncolytic virus expressing RANTES and IL-15 enhances function of CAR-modified T cells in solid tumors. Oncoimmunology. 2015;4:e988098. doi:10.4161/21505594.2014.988098.
  • 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;19:2734–44. doi:10.1158/1078-0432.CCR-12-2546.
  • Breitbach CJ, Moon A, Burke J, Hwang TH, Kirn DH. A phase 2, open-label, randomized study of pexa-vec (JX-594) administered by intratumoral injection in patients with unresectable primary hepatocellular carcinoma. Methods Mol Biol. 2015;1317:343–57. doi:10.1007/978-1-4939-2727-2_19.

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