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Articles

In situ thermal ablation augments antitumor efficacy of adoptive T cell therapy

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Pages 22-36 | Received 03 May 2019, Accepted 05 Aug 2019, Published online: 03 Dec 2019

References

  • Kochenderfer JN, Wilson WH, Janik JE, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood. 2010;116:4099–4102.
  • Maus MV, Fraietta JA, Levine BL, et al. Adoptive immunotherapy for cancer or viruses. Annu Rev Immunol. 2014;32:189–225.
  • 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.
  • 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.
  • 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.
  • Morgan RA, Dudley ME, Wunderlich JR, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science. 2006;314:126–129.
  • Rapoport AP, Stadtmauer EA, Binder-Scholl GK, et al. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat Med. 2015;21:914–921.
  • Robbins PF, Morgan RA, Feldman SA, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. JCO. 2011;29:917–924.
  • Robbins PF, Kassim SH, Tran TL, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res. 2015;21:1019–1027.
  • Rosenberg SA, Yang JC, Sherry RM, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res. 2011;17:4550–4557.
  • 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.
  • Fisher DT, Chen Q, Skitzki JJ, et al. IL-6 trans-signaling licenses mouse and human tumor microvascular gateways for trafficking of cytotoxic T cells. J Clin Invest. 2011;121:3846–3859.
  • Joyce JA, Fearon DT. T cell exclusion, immune privilege, and the tumor microenvironment. Science. 2015;348:74–80.
  • Pockaj BA, Sherry RM, Wei JP, et al. Localization of 111indium-labeled tumor infiltrating lymphocytes to tumor in patients receiving adoptive immunotherapy. Augmentation with cyclophosphamide and correlation with response. Cancer. 1994;73:1731–1737.
  • Chen Q, Fisher DT, Clancy KA, et al. Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism. Nat Immunol. 2006;7:1299–1308.
  • Chung AS, Lee J, Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat Rev Cancer. 2010;10:505–514.
  • Slaney CY, Kershaw MH, Darcy PK. Trafficking of T Cells into Tumors. Cancer Res. 2014;74:7168–7174.
  • Mikucki ME, Fisher DT, Matsuzaki J, et al. Non-redundant requirement for CXCR3 signalling during tumoricidal T-cell trafficking across tumour vascular checkpoints. Nat Commun. 2015;6:7458.
  • Gattinoni L, Klebanoff CA, Palmer DC, et al. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest. 2005;115:1616–1626.
  • Gattinoni L, Zhong XS, Palmer DC, et al. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat Med. 2009;15:808–813.
  • Spitzer MH, Carmi Y, Reticker-Flynn NE, et al. Systemic immunity is required for effective cancer immunotherapy. Cell. 2017;168:487–502.e15.
  • Wong SL, Mangu PB, Choti MA, et al. American Society of Clinical Oncology 2009 clinical evidence review on radiofrequency ablation of hepatic metastases from colorectal cancer. JCO. 2010;28:493–508.
  • Ginzburg S, Tomaszewski JJ, Kutikov A. Focal ablation therapy for renal cancer in the era of active surveillance and minimally invasive partial nephrectomy. Nat Rev Urol. 2017;14:669–682.
  • Chu KF, Dupuy DE. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer. 2014;14:199–208.
  • den Brok MH, Sutmuller RP, van der Voort R, et al. In situ tumor ablation creates an antigen source for the generation of antitumor immunity. Cancer Res. 2004;64:4024–4029.
  • Wissniowski TT, Hansler J, Neureiter D, et al. Activation of tumor-specific T lymphocytes by radio-frequency ablation of the VX2 hepatoma in rabbits. Cancer research. 2003;63:6496–6500.
  • Zerbini A, Pilli M, Penna A, et al. Radiofrequency thermal ablation of hepatocellular carcinoma liver nodules can activate and enhance tumor-specific T-cell responses. Cancer Res. 2006;66:1139–1146.
  • Ali MY, Grimm CF, Ritter M, et al. Activation of dendritic cells by local ablation of hepatocellular carcinoma. J Hepatol. 2005;43:817–822.
  • Schueller G, Kettenbach J, Sedivy R, et al. Heat shock protein expression induced by percutaneous radiofrequency ablation of hepatocellular carcinoma in vivo. Int J Oncol. 2004;24:609–613.
  • Napoletano C, Taurino F, Biffoni M, et al. RFA strongly modulates the immune system and anti-tumor immune responses in metastatic liver patients. Int J Oncol. 2008;32:481–490.
  • Fietta AM, Morosini M, Passadore I, et al. Systemic inflammatory response and downmodulation of peripheral CD25 + Foxp3+ T-regulatory cells in patients undergoing radiofrequency thermal ablation for lung cancer. Human immunology. 2009;70:477–486.
  • Ito F, Ku AW, Bucsek MJ, et al. Immune adjuvant activity of pre-resectional radiofrequency ablation protects against local and systemic recurrence in aggressive murine colorectal cancer. PLOS One. 2015;10:e0143370.
  • Dromi SA, Walsh MP, Herby S, et al. Radiofrequency ablation induces antigen-presenting cell infiltration and amplification of weak tumor-induced immunity. Radiology. 2009;251:58–66.
  • den Brok MH, Sutmuller RP, Nierkens S, et al. Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induces anti-tumour immunity. Br J Cancer. 2006;95:896–905.
  • Shi L, Chen L, Wu C, et al. PD-1 blockade boosts radiofrequency ablation-elicited adaptive immune responses against tumor. Clin Cancer Res. 2016;22:1173–1184.
  • den Brok MH, Sutmuller RP, Nierkens S, et al. Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. Cancer Res. 2006;66:7285–7292.
  • Nierkens S, den Brok MH, Ruers TJ, et al. Radiofrequency ablation in cancer therapy: tuning into in situ tumor vaccines. Volume 5. In: Keisari Y, editor. Tumor ablation. Springer; 2013. p. 39–60.
  • Gameiro SR, Higgins JP, Dreher MR, et al. Combination therapy with local radiofrequency ablation and systemic vaccine enhances antitumor immunity and mediates local and distal tumor regression. PLOS One. 2013;8:e70417.
  • Johnson EE, Yamane BH, Buhtoiarov IN, et al. Radiofrequency ablation combined with KS-IL2 immunocytokine (EMD 273066) results in an enhanced antitumor effect against murine colon adenocarcinoma. Clin Cancer Res. 2009;15:4875–4884.
  • Thakur A, Littrup P, Paul EN, et al. Induction of specific cellular and humoral responses against renal cell carcinoma after combination therapy with cryoablation and granulocyte-macrophage colony stimulating factor: a pilot study. J Immunother. 2011;34:457–467.
  • Liu Q, Zhai B, Yang W, et al. Abrogation of local cancer recurrence after radiofrequency ablation by dendritic cell-based hyperthermic tumor vaccine. Mol Ther. 2009;17:2049–2057.
  • Waitz R, Solomon SB, Petre EN, et al. Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy. Cancer Res. 2012;72:430–439.
  • Saji H, Kato H, Song W, et al. Therapeutic vaccination against murine colon carcinoma by radiofrequency ablation in combination with intratumoral naive dendritic cell injection. Cancer Res. 2007;67:1852–1852.
  • Ku AW, Muhitch JB, Powers CA, et al. Tumor-induced MDSC act via remote control to inhibit L-selectin-dependent adaptive immunity in lymph nodes. eLife. 2016;5:e17375.
  • Chen Q, Appenheimer MM, Muhitch JB, et al. Thermal facilitation of lymphocyte trafficking involves temporal induction of intravascular ICAM-1. Microcirculation. 2009;16:143–158.
  • Weninger W, Crowley MA, Manjunath N, et al. Migratory properties of naive, effector, and memory CD8(+) T cells. J Exp Med. 2001;194:953–966.
  • Chen Q, Fisher DT, Kucinska SA, et al. Dynamic control of lymphocyte trafficking by fever-range thermal stress. Cancer Immunol Immunother. 2006;55:299–311.
  • Evans SS, Wang WC, Bain MD, et al. Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood. 2001;97:2727–2733.
  • Abramoff MD, Magelhaes PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004;11:36–42.
  • von Andrian UH. Intravital microscopy of the peripheral lymph node microcirculation in mice. Microcirculation. 1996;3:287–300.
  • Mandl JN, Liou R, Klauschen F, et al. Quantification of lymph node transit times reveals differences in antigen surveillance strategies of naive CD4+ and CD8+ T cells. Proc Natl Acad Sci USA. 2012;109:18036–18041.
  • Carriere V, Colisson R, Jiguet-Jiglaire C, et al. Cancer cells regulate lymphocyte recruitment and leukocyte-endothelium interactions in the tumor-draining lymph node. Cancer Res. 2005;65:11639–11648.
  • Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science. 1996;272:60–66.
  • von Andrian UH, Mempel TR. Homing and cellular traffic in lymph nodes. Nat Rev Immunol. 2003;3:867–878.
  • Miyasaka M, Tanaka T. Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nat Rev Immunol. 2004;4:360–370.
  • Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol. 2007;25:619–647.
  • Shamri R, Grabovsky V, Gauguet JM, et al. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol. 2005;6:497–506.
  • Sharma MD, Hou DY, Baban B, et al. Reprogrammed foxp3(+) regulatory T cells provide essential help to support cross-presentation and CD8(+) T cell priming in naive mice. Immunity. 2010;33:942–954.
  • Yang WL, Nair DG, Makizumi R, et al. Heat shock protein 70 is induced in mouse human colon tumor xenografts after sublethal radiofrequency ablation. Ann Surg Oncol. 2004;11:399–406.
  • Rai R, Richardson C, Flecknell P, et al. Study of apoptosis and heat shock protein (HSP) expression in hepatocytes following radiofrequency ablation (RFA). J Surg Res. 2005;129:147–151.
  • Zerbini A, Pilli M, Fagnoni F, et al. Increased immunostimulatory activity conferred to antigen-presenting cells by exposure to antigen extract from hepatocellular carcinoma after radiofrequency thermal ablation. J Immunother. 2008;31:271–282.
  • Blachere NE, Li Z, Chandawarkar RY, et al. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J Exp Med. 1997;186:1315–1322.
  • Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004;427:154–159.
  • Druzd D, Matveeva O, Ince L, et al. Lymphocyte circadian clocks control lymph node trafficking and adaptive immune responses. Immunity. 2017;46:120–132.
  • Cyster JG, Schwab SR. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol. 2012;30:69–94.
  • Evans SS, Bain MD, Wang WC. Fever-range hyperthermia stimulates alpha4beta7 integrin-dependent lymphocyte-endothelial adhesion. Int J Hyperthermia. 2000;16:45–59.
  • Evans SS, Repasky EA, Fisher DT. Fever and the thermal regulation of immunity: the immune system feels the heat. Nat Rev Immunol. 2015;15:335–349.
  • Rozenblum N, Zeira E, Bulvik B, et al. Radiofrequency ablation: inflammatory changes in the periablative zone can induce global organ effects, including liver regeneration. Radiology. 2015;276:416–425.
  • Nomoto Y, Yamamoto M, Fukushima T, et al. Expression of nuclear factor kappa B and tumor necrosis factor alpha in the mouse brain after experimental thermal ablation injury. Neurosurgery. 2001;48:158–166.
  • Ahmed M, Kumar G, Navarro G, et al. Systemic siRNA nanoparticle-based drugs combined with radiofrequency ablation for cancer therapy. PLOS One. 2015;10:e0128910.
  • Collins T, Read MA, Neish AS, et al. Transcriptional regulation of endothelial cell adhesion molecules: NF-kappa B and cytokine-inducible enhancers. FASEBJ. 1995;9:899–909.
  • Ledebur HC, Parks TP. Transcriptional regulation of the intercellular adhesion molecule-1 gene by inflammatory cytokines in human endothelial cells. Essential roles of a variant NF-kappa B site and p65 homodimers. J Biol Chem. 1995;270:933–943.
  • Schell SR, Wessels FJ, Abouhamze A, et al. Pro- and antiinflammatory cytokine production after radiofrequency ablation of unresectable hepatic tumors. J Am Coll Surg. 2002;195:774–781.
  • Schneider T, Sevko A, Heussel CP, et al. Serum inflammatory factors and circulating immunosuppressive cells are predictive markers for efficacy of radiofrequency ablation in non-small-cell lung cancer. Clin Exp Immunol. 2015;180:467–474.
  • Gu T, Ge Y, Song Y, et al. Hepatic radiofrequency ablation causes an increase of circulating histones in patients with hepatocellular carcinoma. Scand J Clin Lab Invest. 2015;75:621–627.
  • Ypsilantis P, Lambropoulou M, Evagellou A, et al. Immune and inflammatory responses of the intestinal mucosa following extended liver radiofrequency ablation. Gastroenterol Res Pract. 2017;2017:3450635.
  • Robbins PF, Dudley ME, Wunderlich J, et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol. 2004;173:7125–7130.
  • D'Angelo SP, Melchiori L, Merchant MS, et al. Antitumor activity associated with prolonged persistence of adoptively transferred NY-ESO-1 (c259) T cells in synovial sarcoma. Cancer Discov. 2018;8:944–957.
  • Huang J, Khong HT, Dudley ME, et al. Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J Immunother. 2005;28:258–267.
  • Brentjens RJ, Riviere I, Park JH, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118:4817–4828.
  • Zhou J, Dudley ME, Rosenberg SA, et al. Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in a melanoma patient receiving adoptive cell transfer therapy. J Immunother. 2005;28:53–62.
  • Park JR, Digiusto DL, Slovak M, et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther. 2007;15:825–833.