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Review

Strategies for enhancing adoptive T-cell immunotherapy against solid tumors using engineered cytokine signaling and other modalities

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Pages 653-664 | Received 08 Nov 2017, Accepted 16 Apr 2018, Published online: 14 May 2018

References

  • Rosenberg SA, Packard BS, Aebersold PM, et al. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med. 1988;319:1676–1680.
  • Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci. 1989;86:10024–10028.
  • Brocker T, Karjalainen K. Signals through T cell receptor-zeta chain alone are insufficient to prime resting T lymphocytes. J Exp Med. 1995;181:1653–1659.
  • Chimeric BT. Fv-zeta or Fv-epsilon receptors are not sufficient to induce activation or cytokine production in peripheral T cells. Blood. 2000;96:1999–2001.
  • Kershaw MH, Westwood JA, Parker LL, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res. 2006;12:6106–6115.
  • Pule MA, Savoldo B, Myers GD, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med. 2008;14:1264–1270.
  • Louis CU, Savoldo B, Dotti G, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood. 2011;118:6050–6056.
  • Finney H, Lawson A, Bebbington C, et al. Chimeric receptors providing both primary and costimulatory signaling in T cells from a single gene product. J Immunol. 1998;161:2791–2797.
  • Zhong XS, Matsushita M, Plotkin J, et al. Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI3kinase/AKT/Bcl-XL activation and CD8+ T cell-mediated tumor eradication. Mol Ther. 2010;18:413–420.
  • Pule MA, Straathof KC, Dotti G, et al. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther. 2005;12:933–941.
  • Dotti G, Gottschalk S, Savoldo B, et al. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev. 2014;257:107–126.
  • Porter DL, Levine BL, Kalos M, et al. Chimeric antigen receptor–modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365:725–733.
  • Kalos M, Levine BL, Porter DL, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3:95a73.
  • Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371:1507–1517.
  • Brentjens RJ, Davila ML, Riviere I, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5:177ra38.
  • Sotillo E, Barrett DM, Black KL, et al. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov. 2015;5:1282–1295.
  • Dudley ME, Wunderlich JR, Robbins PF, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science. 2002;298:850–854.
  • Straathof KCM, Bollard CM, Popat U, et al. Treatment of nasopharyngeal carcinoma with Epstein-Barr virus-specific T lymphocytes. Blood. 2005;105:1898–1904.
  • Louis CU, Straathof K, Bollard CM, et al. Adoptive transfer of EBV-specific T cells results in sustained clinical responses in patients with locoregional nasopharyngeal carcinoma. J Immunother. 2010;33:983–990.
  • Chia W-K, Teo M, Wang W-W, et al. Adoptive T-cell transfer and chemotherapy in the first-line treatment of metastatic and/or locally recurrent nasopharyngeal carcinoma. Mol Ther. 2014;22:132–139.
  • Kakarla S, Gottschalk S. CAR T cells for solid tumors: armed and ready to go? Cancer J. 2014;20:151–155.
  • Ahmed N, Brawley VS, Hegde M, et al. Human epidermal growth factor receptor 2 (HER2)-specific chimeric antigen receptor-modified T cells for the immunotherapy of HER2-positive sarcoma. J Clin Oncol. 2015;33:1688–1696.
  • Ahmed N, Brawley V, Hegde M, et al. HER2-specific chimeric antigen receptor-modified virus-specific T cells for progressive glioblastoma. JAMA Oncol. 2017;3:1094–1101.
  • Rourke DMO, Nasrallah MP, Desai A, et al. A single dose of peripherally infused EGFRvIII-directed CAR T cells mediates antigen loss and induces adaptive resistance in patients with recurrent glioblastoma. Sci Transl Med. 2017;9:eaaa0984.
  • Brown CE, Alizadeh D, Starr, R, et al. Regression of glioblastoma after chimeric antigen receptor T-cell therapy. N Engl J Med. 2016;375:2561–2569.
  • Bielamowicz K, Fousek K, Byrd TT, et al. Trivalent CAR T cells overcome interpatient antigenic variability in glioblastoma. Neuro Oncol. 2018;Epub ahead:1–13.
  • Kershaw MH, Westwood JA, Darcy PK. Gene-engineered T cells for cancer therapy. Nat Rev Cancer. 2013;13:525–541.
  • Carsetti R. The development of B cells in the bone marrow is controlled by the balance between cell-autonomous mechanisms and signals from the microenvironment. J Exp Med. 2000;191:5–8.
  • Jiang Q, Wen QL, Aiello FB, et al. Cell biology of IL-7, a key lymphotrophin. Cytokine Growth Factor Rev. 2005;16:513–533.
  • Mazzucchelli RI, Warming S, Lawrence SM, et al. Visualization and identification of IL-7 producing cells in reporter mice. PLoS One. 2009;4:e7637.
  • Cui G, Hara T, Simmons S, et al. Characterization of the IL-15 niche in primary and secondary lymphoid organs in vivo. Proc Natl Acad Sci. 2014;111:1915–1920.
  • Surh CD, Sprent J. Homeostasis of naive and memory T cells. Immunity. 2008;29:848–862.
  • Takada K, Jameson SC. Naive T cell homeostasis: from awareness of space to a sense of place. Nat Rev Immunol. 2009;9:823–832.
  • Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor–modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368:1509–1518.
  • Liu RB, Engels B, Schreiber K, et al. IL-15 in tumor microenvironment causes rejection of large established tumors by T cells in a noncognate T cell receptor-dependent manner. Proc Natl Acad Sci U S A. 2013;110:8158–8163.
  • Joyce JA, Fearon DT. T cell exclusion, immune privilege, and the tumor microenvironment. Science. 2015;348:74–79.
  • Heczey A, Louis CU, Savoldo B, et al. CAR T cells administered in combination with lymphodepletion and PD-1 inhibition to patients with neuroblastoma. Mol Ther. 2017;25:1–11.
  • Melchionda F, Fry TJ, Milliron MJ, et al. Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8+ memory cell pool. J Clin Invest. 2005;115:1177–1187.
  • Mackall CL, Fry TJ, Gress RE. Harnessing the biology of IL-7 for therapeutic application. Nat Rev Immunol. 2011;11:330–342.
  • Markley JC, Sadelain M. IL-7 and IL-21 are superior to IL-2 and IL-15 in promoting human T cell-mediated rejection of systemic lymphoma in immunodeficient mice. Blood. 2010;115:3508–3519.
  • Zhang L, Kerkar SP, Yu Z, et al. Improving adoptive T cell therapy by targeting and controlling IL-12 expression to the tumor environment. Mol Ther. 2011;19:751–759.
  • Zeng R, Spolski R, Finkelstein SE, et al. Synergy of IL-21 and IL-15 in regulating CD8 + T cell expansion and function. J Exp Med. 2005;201:139–148.
  • Rosenberg SA. IL-2 the first effective immunotherapy for human cancer. J Immunol. 2014;192:5451–5458.
  • Sportès C, Babb RR, Krumlauf MC, et al. Phase I study of recombinant human interleukin-7 administration in subjects with refractory malignancy. Clin Cancer Res. 2010;16:727–735.
  • Conlon KC, Lugli E, Welles HC, et al. Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer. J Clin Oncol. 2015;33:74–82.
  • Xu W, Jones M, Liu B, et al. Efficacy and mechanism-of-action of a novel superagonist interleukin-15: interleukin-15 receptor αSu/Fc fusion complex in syngeneic murine models of multiple myeloma. Cancer Res. 2013;73:3075–3086.
  • Thompson JA, Curti BD, Redman BG, et al. Phase I study of recombinant interleukin-21 in patients with metastatic melanoma and renal cell carcinoma. J Clin Oncol. 2008;26:2034–2039.
  • Leonard JP, Sherman ML, Fisher GL, et al. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-g production. Blood. 1997;90:2541–2548.
  • Hurton LV, Singh H, Najjar AM, et al. Tethered IL-15 augments antitumor activity and promotes a stem-cell memory subset in tumor-specific T cells. Proc Natl Acad Sci. 2016;113:E7788–E7797.
  • Zhang L, Morgan RA, Beane JD, et al. Tumor-infiltrating lymphocytes genetically engineered with an inducible gene encoding interleukin-12 for the immunotherapy of metastatic melanoma. Clin Cancer Res. 2015;21:2278–2288.
  • Shochat C, Tal N, Gryshkova V, et al. Novel activating mutations lacking cysteine in type I cytokine receptors in acute lymphoblastic leukemia. Blood. 2014;124:106–110.
  • Shum T, Omer B, Tashiro H, et al. Constitutive signaling from an engineered IL-7 receptor promotes durable tumor elimination by tumor redirected T-cells. Cancer Discov. 2017;7:1238–1247.
  • Leen AM, Sukumaran S, Watanabe N, et al. Reversal of tumor immune inhibition using a chimeric cytokine receptor. Mol Ther. 2014;22:1211–1220.
  • Mohammed S, Sukumaran S, Bajgain P, et al. Improving chimeric antigen receptor-modified T cell function by reversing the immunosuppressive tumor microenvironment of pancreatic cancer. Mol Ther. 2017;25:249–258.
  • Wilkie S, Burbridge SE, Chiapero-Stanke L, et al. Selective expansion of chimeric antigen receptor-targeted T-cells with potent effector function using interleukin-4. J Biol Chem. 2010;285:25538–25544.
  • Kagoya Y, Tanaka S, Guo T, et al. A novel chimeric antigen receptor containing a JAK–STAT signaling domain mediates superior antitumor effects. Nat Med. 2018; Epub ahead.
  • Stephan MT, Moon JJ, Um SH, et al. Therapeutic cell engineering with surface-conjugated synthetic nanoparticles. Nat Med. 2010;16:1035–1041.
  • Stephan SB, Taber AM, Jileaeva I, et al. Biopolymer implants enhance the efficacy of adoptive T-cell therapy. Nat Biotechnol. 2015;33:97–101.
  • Scharping NE, Delgoffe GM. Tumor microenvironment metabolism: a new checkpoint for anti-tumor immunity. Vaccines. 2016;4:46.
  • Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369:122–133.
  • Topalian SL, Hodi S, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366:2443–2454.
  • Kakarla S, Chow KKH, Mata M, et al. Antitumor effects of chimeric receptor engineered human T cells directed to tumor stroma. Mol Ther. 2013;21:1611–1620.
  • Bollard CM, Rössig C, Calonge MJ, et al. Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood. 2002;99:3179–3187.
  • Tripic TCruz CR, et al. Tumor-specific t-cells engineered to overcome tumor immune evasion induce clinical responses in patients with relapsed hodgkin lymphoma. J Clin Oncol. 2018;36:1128-1139.
  • Yvon ES, Burga R, Powell A, et al. Cord blood natural killer cells expressing a dominant negative TGF-β receptor: implications for adoptive immunotherapy for glioblastoma. Cytotherapy. 2017;19:408–418.
  • Salmon H, Franciskiewicz K, Damotte D, et al. Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J Clin Invest. 2012;122:899–910.
  • Bougherara H, Mansuet-Lupo A, Alifano M, et al. Real-time imaging of resident T cells in human lung and ovarian carcinomas reveals how different tumor microenvironments control T lymphocyte migration. Front Immunol. 2015;6:1–12.
  • Caruana I, Savoldo B, Hoyos V, et al. Heparanase promotes tumor infiltration and antitumor activity of CAR-redirected T lymphocytes. Nat Med. 2015;21:524–529.
  • Craddock JA, Lu A, Bear A, et al. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J Immunother. 2010;33:780–788.
  • Di Stasi A, De Angelis B, Savoldo B. Gene therapy to improve migration of T cells to the tumor site. Immunother Cancer Methods Protoc. 2010;651:103–118.
  • Nishio N, Diaconu I, Liu H, et al. Armed oncolytic virus enhances immune functions of chimeric antigen receptor-modified T cells in solid tumors. Cancer Res. 2014;74:5195–5205.
  • Postow MA, Chesney J, Pavlick AC, et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med. 2015;372:2006–2017.
  • Sharma P, Allison JP. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell. 2015;161:205–214.
  • Tanoue K, Shaw AR, Watanabe N, et al. Armed oncolytic adenovirus-expressing PD-L1 mini-body enhances antitumor effects of chimeric antigen receptor t cells in solid tumors. Cancer Res. 2017;77:2040–2051.
  • Rupp LJ, Schumann K, Roybal KT, et al. CRISPR/Cas9-mediated PD-1 disruption enhances anti-tumor efficacy of human chimeric antigen receptor T cells. Sci Rep. 2017;7:737.
  • Hu Y, Sun J, Wu Z, et al. Predominant cerebral cytokine release syndrome in CD19-directed chimeric antigen receptor-modified T cell therapy. J Hematol Oncol. 2016;9:1–5.
  • Morgan RA, Yang JC, Kitano M, et al. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther. 2010;18:843–851.
  • Lamers CHJ, Sleijfer S, Vulto AG, et al. Treatment of metastatic renal cell carcinoma with autologous t-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol. 2006;24:e20–e22.
  • June CH, Warshauer JT, Bluestone JA. Is autoimmunity the Achilles’ heel of cancer immunotherapy? Nat. Med. 2017;23:540–547.
  • Bonini C, Ferrari G, Verzeletti S, et al. HSV-TK gene transfer into donor lymphocytes for control of allogeneic graft-versus-leukemia. Science. 1997;276:1719–1724.
  • Straathof KC, Pulè MA, Yotnda P, et al. An inducible caspase 9 safety switch for T-cell therapy. Blood. 2005;105:4247–4254.
  • Fan L, Freeman KW, Khan T, et al. Improved artificial death switches based on caspases and FADD. Hum Gene Ther. 1999;10:2273–2285.
  • Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med. 2011;365:1673–1683.
  • Zhou X, Di Stasi A, Tey S-K, et al. Long-term outcome and immune reconstitution after haploidentical stem cell transplant in recipients of allodepleted-T-cells expressing the inducible caspase-9 safety transgene. Blood. 2014;123:3895–3905.
  • Zhou X, Dotti G, Krance RA, et al. Inducible caspase-9 suicide gene controls adverse effects from alloreplete T cells after haploidentical stem cell transplantation. Blood. 2015;125:4103–4113.
  • Diaconu I, Ballard B, Zhang M, et al. Inducible caspase-9 selectively modulates the toxicities of CD19-specific chimeric antigen receptor-modified T cells. Mol Ther. 2017;25:580–592.
  • Serafini M, Manganini M, Borleri G, et al. Characterization of CD20-transduced t lymphocytes as an alternative suicide gene therapy approach for the treatment of graft-versus-host disease. Human Gene Therapy. 2004;15;1:63-76.
  • Wang X, Chang WC, Wong CLW, et al. A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood. 2011;118:1255–1263.
  • Philip B, Kokalaki E, Mekkaoui L, et al. A highly compact epitope-based marker/suicide gene for easier and safer T-cell therapy. Blood. 2014;124:1277–1287.
  • Alvarez-Vallina L, Hawkins RE. Antigen-specific targeting of CD28-mediated T cell co-stimulation using chimeric single-chain antibody variable fragment-CD28 receptors. Eur J Immunol. 1996;26:2304–2309.
  • Kloss CC, Condomines M, Cartellieri M, et al. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat Biotechnol. 2013;31:71–75.
  • Lanitis E, Poussin M, Klattenhoff AW, et al. Chimeric antigen receptor T cells with dissociated signaling domains exhibit focused antitumor activity with reduced potential for toxicity in vivo. Cancer Immunol Res. 2013;1:43–53.
  • Scheuermann R, Racila E. CD19 antigen in leukemia and lymphoma diagnosis and immunotherapy. Leuk Lymphoma. 1995;18:385–397.
  • Hegde M, Corder A, Chow KK, et al. Combinational targeting offsets antigen escape and enhances effector functions of adoptively transferred T cells in glioblastoma. Mol Ther. 2013;21:2087–2101.
  • Fedorov VD, Themeli M, Sadelain M. PD-1- and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Sci Transl Med. 2013;5:215ra172.
  • Roybal KT, Rupp LJ, Morsut L, et al. Precision tumor recognition by T cells with combinatorial antigen-sensing circuits. Cell. 2016;164:770–779.
  • Roybal KT, Williams JZ, Morsut L, et al. Engineering T cells with customized therapeutic article engineering T cells with customized therapeutic response programs using synthetic notch receptors. Cell. 2016;167:419–432.
  • Wu C-Y, Roybal KT, Puchner EM, et al. Remote control of therapeutic T cells through a small molecule-gated chimeric receptor. Science. 2015;350:aab4077-1-aab4077-10.
  • Foster AE, Mahendravada A, Shinners NP, et al. Regulated expansion and survival of chimeric antigen receptor-modified T cells using small molecule-dependent inducible MyD88/CD40. Mol Ther. 2017;25:1–13.
  • Narayanan P, Lapteva N, Seethammagari M, et al. A composite MyD88/CD40 switch synergistically activates mouse and human dendritic cells for enhanced antitumor efficacy. J Clin Invest. 2011;121:1524–1534.
  • Mata M, Gerken C, Nguyen P, et al. Inducible activation of MyD88 and CD40 in CAR T-cells results in controllable and potent antitumor activity in preclinical solid tumor models. Cancer Discov. 2017;7:1306–1319.

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