Irreversible electroporation ablation overcomes tumor-associated immunosuppression to improve the efficacy of DC vaccination in a mice model of pancreatic cancer

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69:7–9. doi:10.3322/caac.21551.
   PubMed Web of Science ®Google Scholar
• Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin. 2009;59:225–249. doi:10.3322/caac.20006.
   PubMed Web of Science ®Google Scholar
• Palucka K, Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity. 2013;39:38–48. doi:10.1016/j.immuni.2013.07.004.
   PubMed Web of Science ®Google Scholar
• Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer. 2012;12:265–277. doi:10.1038/nrc3258.
   PubMed Web of Science ®Google Scholar
• Davalos RV, Mir LM, Rubinsky B. Tissue ablation with irreversible electroporation. Ann Biomed Eng. 2005;33:223. doi:10.1007/s10439-005-8981-8.
   PubMed Web of Science ®Google Scholar
• Martin RCG, McFarland K, Ellis S, Velanovich V. Irreversible electroporation in locally advanced pancreatic cancer: potential improved overall survival. Ann Surg Oncol. 2013;20:443–449. doi:10.1245/s10434-012-2736-1.
   PubMed Web of Science ®Google Scholar
• Vroomen L, Scheffer HJ, Melenhorst M, Jong MC, Bergh JE, Kuijk CV, Delft FV, Kazemier G and Meijerink MR. MR and CT imaging characteristics and ablation zone volumetry of locally advanced pancreatic cancer treated with irreversible electroporation. Eur Radiol. 2017;27:2521–2531. doi:10.1007/s00330-016-4581-2.
   PubMed Web of Science ®Google Scholar
• Narayanan G, Hosein PJ, Arora G,  Barbery KJ, Froud T, Livingstone AS, Franceschi D, Lima CMR and  Yrizarry J. Percutaneous irreversible electroporation for downstaging and control of unresectable pancreatic adenocarcinoma. J Vasc Interv Radiol. 2012;23:1613–1621. doi:10.1016/j.jvir.2012.09.012.
   PubMed Web of Science ®Google Scholar
• Kwon D, McFarland K, Velanovich V, Martin RC 2nd. Borderline and locally advanced pancreatic adenocarcinoma margin accentuation with intraoperative irreversible electroporation. Surgery. 2014;156:910–920. doi:10.1016/j.surg.2014.06.058.
   PubMed Web of Science ®Google Scholar
• Mansson C, Brahmstaedt R, Nilsson A, Nygren P, Karlson BM. Percutaneous irreversible electroporation for treatment of locally advanced pancreatic cancer following chemotherapy or radiochemotherapy. Eur J Surg Oncol. 2016;42:1401–1406. doi:10.1016/j.ejso.2016.01.024.
   PubMed Web of Science ®Google Scholar
• Schaft N, Dorrie J, Muller I,  Beck V, Baumann S, Schunder T, Kämpgen E and Schuler G. A new way to generate cytolytic tumor-specific T cells: electroporation of RNA coding for a T cell receptor into T lymphocytes. Cancer Immunol Immunother. 2006;55:1132–1141. doi:10.1007/s00262-005-0098-2.
   PubMed Web of Science ®Google Scholar
• White SB, Zhang Z, Chen J, Gogineni VR, Larson AC. Early immunologic response of irreversible electroporation versus cryoablation in a rodent model of pancreatic cancer. J Vasc Interv Radiol. 2018;29:1764–1769. doi:10.1016/j.jvir.2018.07.009.
   PubMed Web of Science ®Google Scholar
• Figini M, Wang X, Lyu T, Su Z, Wang B, Sun C, Shangguan J, Pan L, Zhou K, Ma Q, et al. Diffusion MRI biomarkers predict the outcome of irreversible electroporation in a pancreatic tumor mouse model. Am J Cancer Res. 2018;8:1615–1623.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Li W, Procissi D, Tyler P, Omary RA, Larson AC. Rapid dramatic alterations to the tumor microstructure in pancreatic cancer following irreversible electroporation ablation. Nanomed (Lond). 2014;9:1181–1192. doi:10.2217/nnm.13.72.
   PubMed Web of Science ®Google Scholar
• Bipat S, Phoa SSKS, Delden OMV,   Bossuyt PMM, Gouma DJ, Laméris JS and Stoker J. Ultrasonography, computed tomography and magnetic resonance imaging for diagnosis and determining resectability of pancreatic adenocarcinoma. J Comput Assist Tomogr. 2005;29:438–445. doi:10.1097/01.rct.0000164513.23407.b3.
   PubMed Web of Science ®Google Scholar
• Chandarana H, Babb J, Macari M. Signal characteristic and enhancement patterns of pancreatic adenocarcinoma: evaluation with dynamic gadolinium enhanced MRI. Clin Radiol. 2007;62:876–883. doi:10.1016/j.crad.2007.03.005.
   PubMed Web of Science ®Google Scholar
• Butts K, Daniel BL, Chen L,  Bouley DM, Wansapura J, Maier SE, Dumoulin C and  Watkins R. Diffusion-weighted MRI after cryosurgery of the canine prostate. Magnetic resonance imaging. J Magn Reson Imaging. 2003;17:131–135.
   PubMed Web of Science ®Google Scholar
• Ansari D, Kristoffersson S, Andersson R, Bergenfeldt M. The role of irreversible electroporation (IRE) for locally advanced pancreatic cancer: a systematic review of safety and efficacy. Scand J Gastroenterol. 2017;52:1165–1171. doi:10.1080/00365521.2017.1346705.
   PubMed Web of Science ®Google Scholar
• Tasu JP, Vesselle G, Herpe G, Richer JP, Boucecbi S,  Vélasco S, Debeane B, Carretier M and Tougeron D. Irreversible electroporation for locally advanced pancreatic cancer: where do we stand in 2017? Pancreas. 2017;46:283–287. doi:10.1097/mpa.0000000000000793.
   PubMed Web of Science ®Google Scholar
• Huang KW, Yang PC, Pua U, Kim MD, Li SP, Qiu YD, Song TQ and Liang PC. The efficacy of combination of induction chemotherapy and irreversible electroporation ablation for patients with locally advanced pancreatic adenocarcinoma. J Surg Oncol. 2018;118:31–36. doi:10.1002/jso.25110.
   PubMed Web of Science ®Google Scholar
• Okada T, Linguraru MG, Hori M, Summers RM, Tomiyama N, Sato Y. Abdominal multi-organ segmentation from CT images using conditional shape-location and unsupervised intensity priors. Med Image Anal. 2015;26:1–18. doi:10.1016/j.media.2015.06.009.
   PubMed Web of Science ®Google Scholar
• Al-Sakere B, Bernat C, Andre F, Connault E, Opolon P, Davalos RV and Mir LM. A study of the immunological response to tumor ablation with irreversible electroporation. Technol Cancer Res Treat. 2007;6:301–306. doi:10.1177/153303460700600406.
   PubMed Web of Science ®Google Scholar
• Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer. 2012;12:860–875. doi:10.1038/nrc3380.
   PubMed Web of Science ®Google Scholar
• Zhao J, Wen X, Tian L, et al. Irreversible electroporation reverses resistance to immune checkpoint blockade in pancreatic cancer. Nat Commun. 2019;10:899. doi:10.1038/s41467-019-08782-1.
   PubMed Web of Science ®Google Scholar
• Bulvik BE, Rozenblum N, Gourevich S, Ahmed M, Andriyanov AV, Galun E and Goldberg SN. Irreversible electroporation versus radiofrequency ablation: A comparison of local and systemic effects in a small-animal model. Radiology. 2016;280:413–424. doi:10.1148/radiol.2015151166.
   PubMed Web of Science ®Google Scholar
• Geschwind JF, Artemov D, Abraham S, Omdal D, Huncharek MS, McGee C, Arepally A, Lambert D, Venbrux AC and Lund GB. Chemoembolization of liver tumor in a rabbit model: assessment of tumor cell death with diffusion-weighted MR imaging and histologic analysis. J Vasc Interv Radiol. 2000;11:1245–1255. doi:10.1016/s1051-0443(07)61299-8.
   PubMed Web of Science ®Google Scholar
• Butts K, Daniel BL, Chen L, Bouley DM, Wansapura J,  Maier SE, Dumoulin C and Watkins R. Diffusion-weighted MRI after cryosurgery of the canine prostate. Magnetic resonance imaging. J Magn Reson Imagin. 2003;17:131–135. doi:10.1002/jmri.10227.
   PubMed Web of Science ®Google Scholar
• Jacobs MA, Herskovits EH, Kim HS. Uterine fibroids: diffusion-weighted MR imaging for monitoring therapy with focused ultrasound surgery–preliminary study. Radiolog. 2005;236:196–203. doi:10.1148/radiol.2361040312.
   Google Scholar
• Kurosawa J, Tawada K, Mikata R, Ishihara T, Tsuyuguchi T, Saito M, Shimofusa R, Yoshitomi H, Ohtsuka M, Miyazaki M, et al. Prognostic relevance of apparent diffusion coefficient obtained by diffusion-weighted MRI in pancreatic cancer. J Magn Reson Imaging. 2015;42:1532–1537. doi:10.1002/jmri.24939.
   PubMed Web of Science ®Google Scholar
• Wang Y, Chen ZE, Nikolaidis P, McCarthy RJ, Merrick L, Sternick LA, Horowitz JM, Yaghmai V and Miller FH. Diffusion-weighted magnetic resonance imaging of pancreatic adenocarcinomas: association with histopathology and tumor grade. J Magn Reson Imaging. 2011;33:136–142. doi:10.1002/jmri.22414.
   PubMed Web of Science ®Google Scholar
• Dalah E, Erickson B, Oshima K,Schott D, Hall WA, Paulson E, Tai A, Knechtges P and Li XA. Correlation of ADC with pathological treatment response for radiation therapy of pancreatic cancer. Transl Oncol. 2018;11:391–398. doi:10.1016/j.tranon.2018.01.018.
   PubMed Web of Science ®Google Scholar
• Yang J, Hu S, Shangguan J, Eresen A, Li Y, Pan L, Ma Q, Velichko Y, Wang J, Hu C, et al. Dendritic cell immunotherapy induces anti-tumor effect in a transgenic mouse model of pancreatic ductal adenocarcinoma. Am J Cancer Res. 2019;9:2456–2468.
   PubMed Web of Science ®Google Scholar
• Pan L, Shang N, Shangguan J,  Figini M, Xing W, Wang B , Sun C, Yang J, Zhang Y, Hu S, et al. Magnetic resonance imaging monitoring therapeutic response to dendritic cell vaccine in murine orthotopic pancreatic cancer models. Am J Cancer Res. 2019;9:562–573.
   PubMed Web of Science ®Google Scholar
• Shangguan A, Shang N, Figini M, Pan L, Yang J, Ma Q, Hu S, Eresen A, Sun C, Wang B, et al. Prophylactic dendritic cell vaccination controls pancreatic cancer growth in a mouse model. Cytotherapy. 2020;22:6–15. doi:10.1016/j.jcyt.2019.12.001.
   PubMed Web of Science ®Google Scholar
• Cemazar M, Sersa G, Frey W, Miklavcic D, Teissié J. Recommendations and requirements for reporting on applications of electric pulse delivery for electroporation of biological samples. Bioelectrochemistry. 2018;122:69–76. doi:10.1016/j.bioelechem.2018.03.005.
   PubMed Web of Science ®Google Scholar