Inhalable extracellular vesicle delivery of IL-12 mRNA to treat lung cancer and promote systemic immunity - Nature Nanotechnology

Inhalable extracellular vesicle delivery of IL-12 mRNA to treat lung cancer and promote systemic immunity – Nature Nanotechnology

Source Node: 3056222
  • Wolchok, J. D. et al. Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N. Engl. J. Med. 377, 1345–1356 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Ito, A., Kondo, S., Tada, K. & Kitano, S. Clinical development of immune checkpoint inhibitors. BioMed. Res. Int. 2015, 605478 (2015).

    Article 

    Google Scholar
     

  • Anderson, K. G., Stromnes, I. M. & Greenberg, P. D. Obstacles posed by the tumor microenvironment to T cell activity: a case for synergistic therapies. Cancer Cell 31, 311–325 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Shi, Y. et al. Next-generation immunotherapies to improve anticancer immunity. Front. Pharmacol. 11, 566401 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Mirlekar, B. & Pylayeva-Gupta, Y. IL-12 family cytokines in cancer and immunotherapy. Cancers (Basel). 13, 167 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Del Vecchio, M. et al. Interleukin-12: biological properties and clinical application. Clin. Cancer Res. 13, 4677–4685 (2007).

    Article 

    Google Scholar
     

  • Trinchieri, G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3, 133–146 (2003).

    Article 
    CAS 

    Google Scholar
     

  • Nguyen, K. G. et al. Localized interleukin-12 for cancer immunotherapy. Front Immunol. 11, 575597 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Moynihan, K. D. et al. Eradication of large established tumors in mice by combination immunotherapy that engages innate and adaptive immune responses. Nat. Med. 22, 1402–1410 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Mace, T. A. et al. IL-6 and PD-L1 antibody blockade combination therapy reduces tumour progression in murine models of pancreatic cancer. Gut 67, 320–332 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Agarwal, Y. et al. Intratumourally injected alum-tethered cytokines elicit potent and safer local and systemic anticancer immunity. Nat. Biomed. Eng. 6, 129–143 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Jorgovanovic, D., Song, M., Wang, L. & Zhang, Y. Roles of IFN-γ in tumor progression and regression: a review. Biomark. Res. 8, 49 (2020).

    Article 

    Google Scholar
     

  • Hotz, C. et al. Local delivery of mRNA-encoded cytokines promotes antitumor immunity and tumor eradication across multiple preclinical tumor models. Sci. Transl. Med. 13, eabc7804 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Li, Y. et al. Multifunctional oncolytic nanoparticles deliver self-replicating IL-12 RNA to eliminate established tumors and prime systemic immunity. Nat. Cancer 1, 882–893 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Liu, J. Q. et al. Intratumoral delivery of IL-12 and IL-27 mRNA using lipid nanoparticles for cancer immunotherapy. J. Control. Release 345, 306–313 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Liu, M. A. A comparison of plasmid DNA and mRNA as vaccine technologies. Vaccines 7, 37 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Sangro, B. et al. Phase I trial of intratumoral injection of an adenovirus encoding interleukin-12 for advanced digestive tumors. J. Clin. Oncol. 22, 1389–1397 (2004).

    Article 
    CAS 

    Google Scholar
     

  • Qiu, N. et al. Tumor-associated macrophage and tumor-cell dually transfecting polyplexes for efficient interleukin-12 cancer gene therapy. Adv. Mater. 33, e2006189 (2021).

    Article 

    Google Scholar
     

  • Hewitt, S. L. et al. Intratumoral IL12 mRNA therapy promotes TH1 transformation of the tumor microenvironment. Clin. Cancer Res. 26, 6284–6298 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Aslan, C. et al. Exosomes for mRNA delivery: a novel biotherapeutic strategy with hurdles and hope. BMC Biotechnol. 21, 20 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Popowski, K. D. et al. Inhalable dry powder mRNA vaccines based on extracellular vesicles. Matter 5, 2960–2974 (2022).

    Article 
    CAS 

    Google Scholar
     

  • O’Brien, K., Breyne, K., Ughetto, S., Laurent, L. C. & Breakefield, X. O. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat. Rev. Mol. Cell Biol. 21, 585–606 (2020).

    Article 

    Google Scholar
     

  • Zickler, A. M. & El Andaloussi, S. Functional extracellular vesicles aplenty. Nat. Biomed. Eng. 4, 9–11 (2020).

    Article 

    Google Scholar
     

  • Cheng, K. & Kalluri, R. Guidelines for clinical translation and commercialization of extracellular vesicles and exosomes based therapeutics. Extracell. Vesicle 2, 100029 (2023).

    Article 

    Google Scholar
     

  • Dinh, P. C. et al. Inhalation of lung spheroid cell secretome and exosomes promotes lung repair in pulmonary fibrosis. Nat. Commun. 11, 1064 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Wang, Z. et al. Exosomes decorated with a recombinant SARS-CoV-2 receptor-binding domain as an inhalable COVID-19 vaccine. Nat. Biomed. Eng. 6, 791–805 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Li, Z. et al. Cell-mimicking nanodecoys neutralize SARS-CoV-2 and mitigate lung injury in a non-human primate model of COVID-19. Nat. Nanotechnol. 16, 942–951 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Douguet, L. et al. A small-molecule P2RX7 activator promotes anti-tumor immune responses and sensitizes lung tumor to immunotherapy. Nat. Commun. 12, 653 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Casanova-Acebes, M. et al. Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells. Nature 595, 578–584 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Zhu, X. et al. Comprehensive toxicity and immunogenicity studies reveal minimal effects in mice following sustained dosing of extracellular vesicles derived from HEK293T cells. J. Extracell. Vesicles 6, 1324730 (2017).

    Article 

    Google Scholar
     

  • Mizrak, A. et al. Genetically engineered microvesicles carrying suicide mRNA/protein inhibit schwannoma tumor growth. Mol. Ther. 21, 101–108 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Kojima, R. et al. Designer exosomes produced by implanted cells intracerebrally deliver therapeutic cargo for Parkinson’s disease treatment. Nat. Commun. 9, 1305 (2018).

    Article 

    Google Scholar
     

  • Usman, W. M. et al. Efficient RNA drug delivery using red blood cell extracellular vesicles. Nat. Commun. 9, 2359 (2018).

    Article 

    Google Scholar
     

  • Lieschke, G. J., Rao, P. K., Gately, M. K. & Mulligan, R. C. Bioactive murine and human interleukin-12 fusion proteins which retain antitumor activity in vivo. Nat. Biotechnol. 15, 35–40 (1997).

    Article 
    CAS 

    Google Scholar
     

  • Tsai, S. J. et al. Exosome-mediated mRNA delivery in vivo is safe and can be used to induce SARS-CoV-2 immunity. J. Biol. Chem. 297, 101266 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Li, B. et al. Combinatorial design of nanoparticles for pulmonary mRNA delivery and genome editing. Nat. Biotechnol. 41, 1410–1415 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Gao, S., Wang, L., Liu, W., Wu, Y. & Yuan, Z. The synergistic effect of homocysteine and lipopolysaccharide on the differentiation and conversion of raw264.7 macrophages. J. Inflamm. 11, 13 (2014).

    Article 

    Google Scholar
     

  • Mei, X. et al. An inhaled bioadhesive hydrogel to shield non-human primates from SARS-CoV-2 infection. Nat. Mater. 22, 903–912 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Olivo Pimentel, V. et al. Releasing the brakes of tumor immunity with anti-PD-L1 and pushing its accelerator with L19-IL2 cures poorly immunogenic tumors when combined with radiotherapy. J. Immunother. Cancer 9, e001764 (2021).

    Article 

    Google Scholar
     

  • Leonard, J. P. et al. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-gamma production. Blood 90, 2541–2548 (1997).

    CAS 

    Google Scholar
     

  • Chiocca, E. A. et al. Regulatable interleukin-12 gene therapy in patients with recurrent high-grade glioma: results of a phase 1 trial. Sci. Transl. Med. 11, eaaw5680 (2019).

    Article 

    Google Scholar
     

  • Liu, Y. et al. Armored inducible expression of IL-12 enhances antitumor activity of glypican-3-targeted chimeric antigen receptor-engineered T cells in hepatocellular carcinoma. J. Immunol. 203, 198–207 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Zhu, M. L., Nagavalli, A. & Su, M. A. Aire deficiency promotes TRP-1-specific immune rejection of melanoma. Cancer Res. 73, 2104–2116 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Lizotte, P. H. et al. In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer. Nat. Nanotechnol. 11, 295–303 (2015).

    Article 

    Google Scholar
     

  • Gollob, J. A. et al. Phase I trial of twice-weekly intravenous interleukin 12 in patients with metastatic renal cell cancer or malignant melanoma: ability to maintain IFN-gamma induction is associated with clinical response. Clin. Cancer Res. 6, 1678–1692 (2000).

    CAS 

    Google Scholar
     

  • Smyth, M. J., Taniguchi, M. & Street, S. E. The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J. Immunol. 165, 2665–2670 (2000).

    Article 
    CAS 

    Google Scholar
     

  • Xue, D. et al. A tumor-specific pro-IL-12 activates preexisting cytotoxic T cells to control established tumors. Sci. Immunol. 7, eabi6899 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Karin, N. Chemokines in the landscape of cancer immunotherapy: how they and their receptors can be used to turn cold tumors into hot ones? Cancers 13, 6317 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Jones, D. S. 2nd et al. Cell surface-tethered IL-12 repolarizes the tumor immune microenvironment to enhance the efficacy of adoptive T cell therapy. Sci. Adv. 8, eabi8075 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Rubinstein, M. P. et al. Ex vivo interleukin-12-priming during CD8(+) T cell activation dramatically improves adoptive T cell transfer antitumor efficacy in a lymphodepleted host. J. Am. Coll. Surg. 214, 700–707 (2012).

    Article 

    Google Scholar
     

  • Müller, J. M. et al. In vivo induction of interferon gamma expression in grey horses with metastatic melanoma resulting from direct injection of plasmid DNA coding for equine interleukin 12. Schweiz Arch. Tierheilkd. 153, 509–513 (2011).

    Article 

    Google Scholar
     

  • Goldszmid, R. S. et al. NK cell-derived interferon-γ orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 36, 1047–1059 (2012).

    Article 
    CAS 

    Google Scholar
     

  • Kerkar, S. P. et al. Collapse of the tumor stroma is triggered by IL-12 induction of Fas. Mol. Ther. 21, 1369–1377 (2013).

    Article 
    CAS 

    Google Scholar
     

  • Geall, A. J. et al. Nonviral delivery of self-amplifying RNA vaccines. Proc. Natl Acad. Sci. USA 109, 14604–14609 (2012).

    Article 
    CAS 

    Google Scholar
     

  • Time Stamp:

    More from Nature Nanotechnology