Imaging facility LIOPA, Plateformes d’Imageries du Vivant PIV, Université de Paris and CNRS UMS3612 Inserm US25; CNRS -GDR2037 Agents d’Imagerie Moléculaire; France Life Imaging ANR-11-INBS-0006.
Author contributions
HDD designed the study and performed the in vitro and in vivo experiments with the help of JS. HD synthesized the cationic lipids and prepared the figure. CM designed the plasmids. SB and SHBA helped with the immune factors to be measured and cytometry or cell experiments. BL designed the ultrasound experiments. BL, BTD, DS, VE, SHBA, and CM corrected the manuscript. NM designed the study and wrote the manuscript. All authors contributed to manuscript revision, read and approved the submitted version.
Conflicts of interest
The authors declare that they have no conflicts of interest.
Ethical approval
Animal experiments were conducted according to European and national guidelines and were approved by the institutional ethics committee APAFIS#7610.
Consent to participate
Not applicable.
Consent to publication
Not applicable.
Availability of data and materials
Not applicable.
Funding
This project has received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 665850. The funders had no role in the study design, in the collection, analysis, and interpretation of the data, in the writing of the report, or in the decision to submit the paper for publication.
Wirth T, Parker N, Ylä-Herttuala S.History of gene therapy. Gene. 2013;525:162–9. [DOI] [PubMed]
Ginn SL, Amaya AK, Alexander IE, Edelstein M, Abedi MR.Gene therapy clinical trials worldwide to 2017: an update. J Gene Med. 2018;20:e3015. Erratum in: J Gene Med. 2019;21:e3124. [DOI] [PubMed]
Tüting T, Storkus WJ, Lotze MT.Gene-based strategies for the immunotherapy of cancer. J Mol Med (Berl). 1997;75:478–91. [DOI] [PubMed]
Xu M, Mizoguchi I, Morishima N, Chiba Y, Mizuguchi J, Yoshimoto T.Regulation of antitumor immune responses by the IL-12 family cytokines, IL-12, IL-23, and IL-27. Clin Dev Immunol. 2010;2010:832454. [DOI] [PubMed] [PMC]
Ahmed Ali HA, Di J, Mei W, Zhang YC, Li Y, Du ZW, et al. Antitumor activity of lentivirus-mediated interleukin-12 gene modified dendritic cells in human lung cancer in vitro. Asian Pac J Cancer Prev. 2014;15:611–6. [DOI] [PubMed]
Li CY, Huang Q, Kung HF.Cytokine and immuno-gene therapy for solid tumors. Cell Mol Immunol. 2005;2:81–91. [PubMed]
Daud AI, DeConti RC, Andrews S, Urbas P, Riker AI, Sondak VK, et al. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol. 2008;26:5896–903. [DOI] [PubMed] [PMC]
Suzuki R, Namai E, Oda Y, Nishiie N, Otake S, Koshima R, et al. Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. J Control Release. 2010;142:245–50. [DOI] [PubMed]
Rodrigo-Garzón M, Berraondo P, Ochoa L, Zulueta JJ, González-Aseguinolaza G.Antitumoral efficacy of DNA nanoparticles in murine models of lung cancer and pulmonary metastasis. Cancer Gene Ther. 2010;17:20–7. [DOI] [PubMed]
Hernandez-Alcoceba R, Poutou J, Ballesteros-Briones MC, Smerdou C.Gene therapy approaches against cancer using in vivo and ex vivo gene transfer of interleukin-12. Immunotherapy. 2016;8:179–98. [DOI] [PubMed]
Lv H, Zhang S, Wang B, Cui S, Yan J.Toxicity of cationic lipids and cationic polymers in gene delivery. J Control Release. 2006;114:100–9. [DOI] [PubMed]
Lonez C, Vandenbranden M, Ruysschaert JM.Cationic lipids activate intracellular signaling pathways. Adv Drug Deliv Rev. 2012;64:1749–58. [DOI] [PubMed]
Tranchant I, Thompson B, Nicolazzi C, Mignet N, Scherman D.Physicochemical optimisation of plasmid delivery by cationic lipids. J Gene Med. 2004;6:S24–35. [DOI] [PubMed]
Lonez C, Bessodes M, Scherman D, Vandenbranden M, Escriou V, Ruysschaert JM.Cationic lipid nanocarriers activate Toll-like receptor 2 and NLRP3 inflammasome pathways. Nanomedicine. 2014;10:775–82. [DOI] [PubMed]
Pizzuto M, Bigey P, Lachagès AM, Hoffmann C, Ruysschaert JM, Escriou V, et al. Cationic lipids as one-component vaccine adjuvants: a promising alternative to alum. J Control Release. 2018;287:67–77. [DOI] [PubMed]
Do HD, Couillaud BM, Doan BT, Corvis Y, Mignet N.Advances on non-invasive physically triggered nucleic acid delivery from nanocarriers. Adv Drug Deliv Rev. 2019;138:3–17. [DOI] [PubMed]
Hildebrandt B, Wust P, Ahlers O, Dieing A, Sreenivasa G, Kerner T, et al. The cellular and molecular basis of hyperthermia. Crit Rev Oncol Hematol. 2002;43:33–56. [DOI] [PubMed]
Haen SP, Pereira PL, Salih HR, Rammensee HG, Gouttefangeas C.More than just tumor destruction: immunomodulation by thermal ablation of cancer. Clin Dev Immunol. 2011;2011:160250. [DOI] [PubMed] [PMC]
Huang S, Qu N, Men Y, Liu Z.Effects of thermal ablation on Treg/Th17 in hepatocellular carcinoma of mice. Eur J Inflamm. 2019;17:1–9. [DOI]
Fietta AM, Morosini M, Passadore I, Cascina A, Draghi P, Dore R, et al. Systemic inflammatory response and downmodulation of peripheral CD25+Foxp3+ T-regulatory cells in patients undergoing radiofrequency thermal ablation for lung cancer. Hum Immunol. 2009;70:477–86. [DOI] [PubMed]
Rangamuwa K, Leong T, Weeden C, Asselin-Labat ML, Bozinovski S, Christie M, et al. Thermal ablation in non-small cell lung cancer: a review of treatment modalities and the evidence for combination with immune checkpoint inhibitors. Transl Lung Cancer Res. 2021;10:2842–57. [DOI] [PubMed] [PMC]
Joiner JB, Pylayeva-Gupta Y, Dayton PA.Focused ultrasound for immunomodulation of the tumor microenvironment. J Immunol. 2020;205:2327–41. [DOI] [PubMed] [PMC]
Bessodes M, Mignet N.Lipids for nucleic acid delivery: synthesis and particle formation. Methods Mol Biol. 2013;948:67–84. [DOI] [PubMed]
Byk G, Dubertret C, Escriou V, Frederic M, Jaslin G, Rangara R, et al. Synthesis, activity, and structure−activity relationship studies of novel cationic lipids for DNA transfer. J Med Chem. 1998;41:229–35. [DOI] [PubMed]
Bessodes M, Dhotel H, Mignet N.Lipids for nucleic acid delivery: cationic or neutral lipoplexes, synthesis, and particle formation. Methods Mol Biol. 2019;1943:123–39. [DOI] [PubMed]
Marie C, Vandermeulen G, Quiviger M, Richard M, Préat V, Scherman D.pFARs, plasmids free of antibiotic resistance markers, display high-level transgene expression in muscle, skin and tumour cells. J Gene Med. 2010;12:323–32. [DOI] [PubMed]
Manta S, Renault G, Delalande A, Couture O, Lagoutte I, Seguin J, et al. Cationic microbubbles and antibiotic-free miniplasmid for sustained ultrasound-mediated transgene expression in liver. J Control Release. 2017;262:170–81. [DOI] [PubMed]
Seguin J, Doan BT, Latorre Ossa H, Jugé L, Gennisson JL, Tanter M, et al. Evaluation of nonradiative clinical imaging techniques for the longitudinal assessment of tumour growth in murine CT26 colon carcinoma. Int J Mol Imaging. 2013;2013:983534. [DOI] [PubMed] [PMC]
Nomura T, Yasuda K, Yamada T, Okamoto S, Mahato RI, Watanabe Y, et al. Gene expression and antitumor effects following direct interferon (IFN)-γ gene transfer with naked plasmid DNA and DC-chol liposome complexes in mice. Gene Ther. 1999;6:121–9. [DOI] [PubMed]
Coll JL, Chollet P, Brambilla E, Desplanques D, Behr JP, Favrot M.In vivo delivery to tumors of DNA complexed with linear polyethylenimine. Hum Gene Ther. 1999;10:1659–66. [DOI] [PubMed]
Mukhopadhyay A, Wright J, Shirley S, Canton DA, Burkart C, Connolly RJ, et al. Characterization of abscopal effects of intratumoral electroporation-mediated IL-12 gene therapy. Gene Ther. 2019;26:1–15. [DOI] [PubMed] [PMC]
Lopes A, Vandermeulen G, Préat V.Cancer DNA vaccines: current preclinical and clinical developments and future perspectives. J Exp Clin Cancer Res. 2019;38:146. [DOI] [PubMed] [PMC]
Razi Soofiyani S, Kazemi T, Lotfipour F, Mohammad hosseini A, Shanehbandi D, Hallaj-Nezhadi S, et al. Gene therapy with IL-12 induced enhanced anti-tumor activity in fibrosarcoma mouse model. Artif Cells Nanomed Biotechnol. 2016;44:1988–93. [DOI] [PubMed]
Magnin R, Rabusseau F, Salabartan F, Mériaux S, Aubry JF, Le Bihan D, et al. Magnetic resonance-guided motorized transcranial ultrasound system for blood-brain barrier permeabilization along arbitrary trajectories in rodents. J Ther Ultrasound. 2015;3:22. [DOI] [PubMed] [PMC]
Pasquet L, Bellard E, Chabot S, Markelc B, Rols MP, Teissie J, et al. Pre-clinical investigation of the synergy effect of interleukin-12 gene-electro-transfer during partially irreversible electropermeabilization against melanoma. J Immunother Cancer. 2019;7:161. [DOI] [PubMed] [PMC]
