Nucleic acid-based drugs for patients with solid tumours – Nature Reviews Clinical Oncology

  • Siegel, R. L., Miller, K. D., Wagle, N. S. & Jemal, A. Cancer statistics, 2023. CA Cancer J. Clin. 73, 17–48 (2023).

    Article 
    PubMed 

    Google Scholar
     

  • National Cancer Institute. SEER Training modules: Cancer classification. NIH training.seer.cancer.gov/disease/categories/classification.html (2023).

  • Sung, H. et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71, 209–249 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Hager, S., Fittler, F. J., Wagner, E. & Bros, M. Nucleic acid-based approaches for tumor therapy. Cells 9, 2061 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kulkarni, J. A. et al. The current landscape of nucleic acid therapeutics. Nat. Nanotechnol. 16, 630–643 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Paunovska, K., Loughrey, D. & Dahlman, J. E. Drug delivery systems for RNA therapeutics. Nat. Rev. Genet. 23, 265–280 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hou, X., Zaks, T., Langer, R. & Dong, Y. Lipid nanoparticles for mRNA delivery. Nat. Rev. Mater. 6, 1078–1094 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Loughrey, D. & Dahlman, J. E. Non-liver mRNA delivery. Acc. Chem. Res. 55, 13–23 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu, Q., Qian, W., Sun, X. & Jiang, S. Small-molecule inhibitors, immune checkpoint inhibitors, and more: FDA-approved novel therapeutic drugs for solid tumors from 1991 to 2021. J. Hematol. Oncol. 15, 143 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kahvejian, A., Quackenbush, J. & Thompson, J. F. What would you do if you could sequence everything? Nat. Biotechnol. 26, 1125–1133 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Qi, F., Qian, S., Zhang, S. & Zhang, Z. Single cell RNA sequencing of 13 human tissues identify cell types and receptors of human coronaviruses. Biochem. Biophys. Res. Commun. 526, 135–140 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Van de Sande, B. et al. Applications of single-cell RNA sequencing in drug discovery and development. Nat. Rev. Drug Discov. 22, 496–520 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paunovska, K., Loughrey, D., Sago, C. D., Langer, R. & Dahlman, J. E. Using large datasets to understand nanotechnology. Adv. Mater. 31, e1902798 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Radmand, A. et al. The transcriptional response to lung-targeting lipid nanoparticles in vivo. Nano Lett. 23, 993–1002 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao, Z., Anselmo, A. C. & Mitragotri, S. Viral vector-based gene therapies in the clinic. Bioeng. Transl. Med. 7, e10258 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Curreri, A., Sankholkar, D., Mitragotri, S. & Zhao, Z. RNA therapeutics in the clinic. Bioeng. Transl. Med. 8, e10374 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Baden, L. R. et al. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N. Engl. J. Med. 384, 403–416 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Polack, F. P. et al. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N. Engl. J. Med. 383, 2603–2615 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dooling, K. et al. The Advisory Committee on Immunization Practices’ updated interim recommendation for allocation of COVID-19 vaccine – United States, December 2020. MMWR Morb. Mortal. Wkly. Rep. 69, 1657–1660 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Adams, D. et al. Patisiran, an RNAi therapeutic, for hereditary transthyretin amyloidosis. N. Engl. J. Med. 379, 11–21 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Balwani, M. et al. Phase 3 trial of RNAi therapeutic givosiran for acute intermittent porphyria. N. Engl. J. Med. 382, 2289–2301 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lorentzen, C. L., Haanen, J. B., Met, Ö. & Svane, I. M. Clinical advances and ongoing trials on mRNA vaccines for cancer treatment. Lancet Oncol. 23, e450–e458 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mullard, A. 2020 FDA drug approvals. Nat. Rev. Drug. Discov. 20, 85–90 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mullard, A. Cancer drug approvals and setbacks in 2021. Nat. Cancer 2, 1246–1247 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Huayamares, S. G., Lokugamage, M. P., Da Silva Sanchez, A. J. & Dahlman, J. E. A systematic analysis of biotech startups that went public in the first half of 2021. Curr. Res. Biotechnol. 4, 392–401 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Barbier, A. J., Jiang, A. Y., Zhang, P., Wooster, R. & Anderson, D. G. The clinical progress of mRNA vaccines and immunotherapies. Nat. Biotechnol. 40, 840–854 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Food and Drug Administration. Cellular & gene therapy guidances. FDA https://www.fda.gov/vaccines-blood-biologics/biologics-guidances/cellular-gene-therapy-guidances (2024).

  • Gene therapy needs a long-term approach. Nat. Med. 27, 563 (2021).

  • Food and Drug Administration. Establishment of the Office of Therapeutic Products. FDA https://www.fda.gov/vaccines-blood-biologics/cellular-gene-therapy-products/establishment-office-therapeutic-products (2023).

  • Wang, L. L. et al. Cell therapies in the clinic. Bioeng. Transl. Med. 6, e10214 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bashor, C. J., Hilton, I. B., Bandukwala, H., Smith, D. M. & Veiseh, O. Engineering the next generation of cell-based therapeutics. Nat. Rev. Drug. Discov. 21, 655–675 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cappell, K. M. & Kochenderfer, J. N. Long-term outcomes following CAR T cell therapy: what we know so far. Nat. Rev. Clin. Oncol. 20, 359–675 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, W. W. et al. The first approved gene therapy product for cancer Ad-p53 (Gendicine): 12 years in the clinic. Hum. Gene Ther. 29, 160–179 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Daley, J. Gene therapy arrives. Nature 576, S12–S13 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Cattaneo, R., Miest, T., Shashkova, E. V. & Barry, M. A. Reprogrammed viruses as cancer therapeutics: targeted, armed and shielded. Nat. Rev. Microbiol. 6, 529–540 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gordon, E. M. & Hall, F. L. Noteworthy clinical case studies in cancer gene therapy: tumor-targeted Rexin-G advances as an efficacious anti-cancer agent. Int. J. Oncol. 36, 1341–1353 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rehman, H., Silk, A. W., Kane, M. P. & Kaufman, H. L. Into the clinic: talimogene laherparepvec (T-VEC), a first-in-class intratumoral oncolytic viral therapy. J. Immunother. Cancer 4, 53 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Maruyama, Y. et al. Regulatory issues: PMDA – review of Sakigake designation products: oncolytic virus therapy with delytact injection (Teserpaturev) for malignant glioma. Oncologist 28, 664–670 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Food and Drug Administration. Highlights of prescribing information: ADSTILADRIN® (nadofaragene firadenovec-vncg). FDA www.fda.gov/media/164029/download (2022).

  • Sibbald, B. Death but one unintended consequence of gene-therapy trial. CMAJ 164, 1612 (2001).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hacein-Bey-Abina, S. et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118, 3132–3142 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hacein-Bey-Abina, S. et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415–419 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Maetzig, T., Galla, M., Baum, C. & Schambach, A. Gammaretroviral vectors: biology, technology and application. Viruses 3, 677–713 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hayward, A. Origin of the retroviruses: when, where, and how? Curr. Opin. Virol. 25, 23–27 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yi, Y., Noh, M. J. & Lee, K. H. Current advances in retroviral gene therapy. Curr. Gene Ther. 11, 218–228 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Morse, M. A. et al. Tumor protein p53 mutation in archived tumor samples from a 12-year survivor of stage 4 pancreatic ductal adenocarcinoma may predict long-term survival with DeltaRex-G: a case report and literature review. Mol. Clin. Oncol. 15, 186 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pellinen, R. et al. Cancer cells as targets for lentivirus-mediated gene transfer and gene therapy. Int. J. Oncol. 25, 1753–1762 (2004).

    CAS 
    PubMed 

    Google Scholar
     

  • Yi, Y., Hahm, S. H. & Lee, K. H. Retroviral gene therapy: safety issues and possible solutions. Curr. Gene Ther. 5, 25–35 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Benihoud, K., Yeh, P. & Perricaudet, M. Adenovirus vectors for gene delivery. Curr. Opin. Biotechnol. 10, 440–447 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Crystal, R. G. Adenovirus: the first effective in vivo gene delivery vector. Hum. Gene Ther. 25, 3–11 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lynch, J. P. 3rd & Kajon, A. E. Adenovirus: epidemiology, global spread of novel serotypes, and advances in treatment and prevention. Semin. Respir. Crit. Care Med. 37, 586–602 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sakhuja, K. et al. Optimization of the generation and propagation of gutless adenoviral vectors. Hum. Gene Ther. 14, 243–254 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, C. & Samulski, R. J. Engineering adeno-associated virus vectors for gene therapy. Nat. Rev. Genet. 21, 255–272 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hudry, E. & Vandenberghe, L. H. Therapeutic AAV gene transfer to the nervous system: a clinical reality. Neuron 101, 839–862 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Goswami, R. et al. Gene therapy leaves a vicious cycle. Front. Oncol. 9, 297 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ail, D., Malki, H., Zin, E. A. & Dalkara, D. Adeno-associated virus (AAV)-based gene therapies for retinal diseases: where are we? Appl. Clin. Genet. 16, 111–130 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kuzmin, D. A. et al. The clinical landscape for AAV gene therapies. Nat. Rev. Drug. Discov. 20, 173–174 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Frampton, A. R. Jr., Goins, W. F., Nakano, K., Burton, E. A. & Glorioso, J. C. HSV trafficking and development of gene therapy vectors with applications in the nervous system. Gene Ther. 12, 891–901 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Miyagawa, Y. et al. Herpes simplex viral-vector design for efficient transduction of nonneuronal cells without cytotoxicity. Proc. Natl Acad. Sci. USA 112, E1632–E1641 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Manservigi, R., Argnani, R. & Marconi, P. HSV recombinant vectors for gene therapy. Open. Virol. J. 4, 123–156 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kremer, L. P. M. et al. High throughput screening of novel AAV capsids identifies variants for transduction of adult NSCs within the subventricular zone. Mol. Ther. Methods Clin. Dev. 23, 33–50 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Westhaus, A. et al. High-throughput in vitro, ex vivo, and in vivo screen of adeno-associated virus vectors based on physical and functional transduction. Hum. Gene Ther. 31, 575–589 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jang, M. J. et al. Spatial transcriptomics for profiling the tropism of viral vectors in tissues. Nat. Biotechnol. 41, 1272–1286 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lawler, S. E., Speranza, M.-C., Cho, C.-F. & Chiocca, E. A. Oncolytic viruses in cancer treatment: a review. JAMA Oncol. 3, 841–849 (2017).

    Article 
    PubMed 

    Google Scholar
     

  • Shalhout, S. Z., Miller, D. M., Emerick, K. S. & Kaufman, H. L. Therapy with oncolytic viruses: progress and challenges. Nat. Rev. Clin. Oncol. 20, 160–177 (2023).

    Article 
    PubMed 

    Google Scholar
     

  • Andtbacka, R. H. I. et al. Final analyses of OPTiM: a randomized phase III trial of talimogene laherparepvec versus granulocyte-macrophage colony-stimulating factor in unresectable stage III-IV melanoma. J. Immunother. Cancer 7, 145 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Food and Drug Administration. Highlights of prescribing information: IMLYGIC® (talimogene laherparepvec). FDA. www.fda.gov/media/94129/download (2015).

  • Chesney, J. A. et al. Randomized, double-blind, placebo-controlled, global phase III trial of talimogene laherparepvec combined with pembrolizumab for advanced melanoma. J. Clin. Oncol. 41, 528–540 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ferrucci, P. F., Pala, L., Conforti, F. & Cocorocchio, E. Talimogene laherparepvec (T-VEC): an intralesional cancer immunotherapy for advanced melanoma. Cancers 13, 1386 (2021).

    Article 

    Google Scholar
     

  • Georgina, L. et al. 429 long-term analysis of MASTERKEY-265 phase 1b trial of talimogene laherparepvec (T-VEC) plus pembrolizumab in patients with unresectable stage IIIB-IVM1c melanoma. J. Immunother. Cancer 8, A261 (2020).


    Google Scholar
     

  • Sobol, R. E. et al. Analysis of adenoviral p53 gene therapy clinical trials in recurrent head and neck squamous cell carcinoma. Front. Oncol. 11, 645745 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yao, M. et al. Prognostic comparison between cTACE and H101-TACE in unresectable hepatocellular carcinoma (HCC): a propensity-score matching analysis. Appl. Bionics Biomech. 2022, 9084852 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • GeoVax. Gedeptin Technology Overview. GeoVax www.geovax.com/our-technology/gedeptin-technology-overview (2024).

  • Rosenthal, E. L. et al. Phase I dose-escalating trial of Escherichia coli purine nucleoside phosphorylase and fludarabine gene therapy for advanced solid tumors. Ann. Oncol. 26, 1481–1487 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xie, Y. et al. Alpha-herpesvirus thymidine kinase genes mediate viral virulence and are potential therapeutic targets. Front. Microbiol. 10, 941 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deswal, P. Hookipa debuts phase I/II data. ClinicalTrials Arena www.clinicaltrialsarena.com/news/hookipa-debuts-phase-1-2-data/?cf-view (2023).

  • Palmer, C. D. et al. Individualized, heterologous chimpanzee adenovirus and self-amplifying mRNA neoantigen vaccine for advanced metastatic solid tumors: phase 1 trial interim results. Nat. Med. 28, 1619–1629 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shigdar, S., Schrand, B., Giangrande, P. H. & de Franciscis, V. Aptamers: cutting edge of cancer therapies. Mol. Ther. 29, 2396–2411 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Agnello, L. et al. Aptamer-based strategies to boost immunotherapy in TNBC. Cancers 15, 2010 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sorscher, E. J., Hong, J. S., Allan, P. W., Waud, W. R. & Parker, W. B. In vivo antitumor activity of intratumoral fludarabine phosphate in refractory tumors expressing E. coli purine nucleoside phosphorylase. Cancer Chemother. Pharmacol. 70, 321–329 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nakamura, T. et al. The effect of size and charge of lipid nanoparticles prepared by microfluidic mixing on their lymph node transitivity and distribution. Mol. Pharm. 17, 944–953 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dilliard, S. A., Cheng, Q. & Siegwart, D. J. On the mechanism of tissue-specific mRNA delivery by selective organ targeting nanoparticles. Proc. Natl Acad. Sci. USA 118, e2109256118 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hobbs, S. K. et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl Acad. Sci. USA 95, 4607–4612 (1998).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dvorak, H. F., Nagy, J. A., Dvorak, J. T. & Dvorak, A. M. Identification and characterization of the blood vessels of solid tumors that are leaky to circulating macromolecules. Am. J. Pathol. 133, 95–109 (1988).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Iyer, A. K., Khaled, G., Fang, J. & Maeda, H. Exploiting the enhanced permeability and retention effect for tumor targeting. Drug. Discov. Today 11, 812–818 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhen, Z. et al. Tumor vasculature targeted photodynamic therapy for enhanced delivery of nanoparticles. ACS Nano 8, 6004–6013 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lazarovits, J., Chen, Y. Y., Sykes, E. A. & Chan, W. C. Nanoparticle-blood interactions: the implications on solid tumour targeting. Chem. Commun. 51, 2756–2767 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Chan, W. C. W. Principles of nanoparticle delivery to solid tumors. BME Front. 4, 0016 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ruoslahti, E., Bhatia, S. N. & Sailor, M. J. Targeting of drugs and nanoparticles to tumors. J. Cell Biol. 188, 759–768 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Matsumura, Y. & Maeda, H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 46, 6387–6392 (1986).

    CAS 
    PubMed 

    Google Scholar
     

  • Huayamares, S. G. et al. High-throughput screens identify a lipid nanoparticle that preferentially delivers mRNA to human tumors in vivo. J. Control. Rel. 357, 394–403 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Kon, E., Ad-El, N., Hazan-Halevy, I., Stotsky-Oterin, L. & Peer, D. Targeting cancer with mRNA–lipid nanoparticles: key considerations and future prospects. Nat. Rev. Clin. Oncol. 20, 739–754 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lammers, T., Kiessling, F., Hennink, W. E. & Storm, G. Drug targeting to tumors: principles, pitfalls and (pre-)clinical progress. J. Control. Rel. 161, 175–187 (2012).

    Article 
    CAS 

    Google Scholar
     

  • Schlich, M. et al. Cytosolic delivery of nucleic acids: the case of ionizable lipid nanoparticles. Bioeng. Transl. Med. 6, e10213 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gilleron, J. et al. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nat. Biotechnol. 31, 638–646 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sheth, V., Wang, L., Bhattacharya, R., Mukherjee, P. & Wilhelm, S. Strategies for delivering nanoparticles across tumor blood vessels. Adv. Funct. Mater. 31, 2007363 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sabnis, S. et al. A novel amino lipid series for mRNA delivery: improved endosomal escape and sustained pharmacology and safety in non-human primates. Mol. Ther. 26, 1509–1519 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guimaraes, P. P. G. et al. Ionizable lipid nanoparticles encapsulating barcoded mRNA for accelerated in vivo delivery screening. J. Control. Rel. 316, 404–417 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Hatit, M. Z. C. et al. Species-dependent in vivo mRNA delivery and cellular responses to nanoparticles. Nat. Nanotechnol. 17, 310–318 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Santinha, A. J. et al. Transcriptional linkage analysis with in vivo AAV-Perturb-seq. Nature 622, 367–375 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huayamares, S. G. et al. Nanoparticle delivery of a prodrug-activating bacterial enzyme leads to anti-tumor responses. Nat Commun. (in the press, 2024).

  • Noble, R. et al. Spatial structure governs the mode of tumour evolution. Nat. Ecol. Evol. 6, 207–217 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Lomakin, A. et al. Spatial genomics maps the structure, nature and evolution of cancer clones. Nature 611, 594–602 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ota, Y. et al. A practical spatial analysis method for elucidating the biological mechanisms of cancers with abdominal dissemination in vivo. Sci. Rep. 12, 20303 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hsieh, W.-C. et al. Spatial multi-omics analyses of the tumor immune microenvironment. J. Biomed. Sci. 29, 96 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kranz, L. M. et al. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature 534, 396–401 (2016).

    Article 
    PubMed 

    Google Scholar
     

  • Beck, J. D. et al. mRNA therapeutics in cancer immunotherapy. Mol. Cancer 20, 69 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mullard, A. COVID-19 vaccine success enables a bolder vision for mRNA cancer vaccines, says BioNTech CEO. Nat. Rev. Drug Discov. 20, 500–501 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, J. et al. Targeting CLDN18.2 in cancers of the gastrointestinal tract: new drugs and new indications. Front. Oncol. 13, 1132319 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mackensen, A. et al. CLDN6-specific CAR-T cells plus amplifying RNA vaccine in relapsed or refractory solid tumors: the phase 1 BNT211-01 trial. Nat. Med. 29, 2844–2853 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Qu, H., Jin, Q. & Quan, C. CLDN6: from traditional barrier function to emerging roles in cancers. Int. J. Mol. Sci. 22, 13416 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Doherty, K. CLDN6 CAR T-cell therapy shows encouraging efficacy in relapsed/refractory advanced solid tumours. OncLive www.onclive.com/view/cldn6-car-t-cell-therapy-shows-encouraging-efficacy-in-relapsed-refractory-advanced-solid-tumors (2022).

  • Qian Wei, Z.-Y. F., Zhang, Z.-M. & Zhang, T.-F. Therapeutic tumor vaccines – a rising star to benefit cancer patients. Artif. Intell. Cancer 2, 25–41 (2021).

    Article 

    Google Scholar
     

  • BioNTech. BioNTech expands clinical oncolocgy portfolio with first patient dosed in phase 2 trial of mRNA-based individualized immunotherapy BNT122 in colorectal cancer patients. BioNTech investors.biontech.de/news-releases/news-release-details/biontech-expands-clinical-oncology-portfolio-first-patient-dosed (2021).

  • Lopez, J. S. et al. A phase Ib study to evaluate RO7198457, an individualized neoantigen specific immunotherapy (iNeST), in combination with atezolizumab in patients with locally advanced or metastatic solid tumors [abstract]. Cancer Res. 80 (Suppl. 16), CT301 (2020).

    Article 

    Google Scholar
     

  • Rojas, L. A. et al. Personalized RNA neoantigen vaccines stimulate T cells in pancreatic cancer. Nature 618, 144–150 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dolgin, E. Personalized cancer vaccines pass first major clinical test. Nat. Rev. Drug Discov. 22, 607–609 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, S. et al. Payload distribution and capacity of mRNA lipid nanoparticles. Nat. Commun. 13, 5561 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Burris, H. A. et al. A phase I multicenter study to assess the safety, tolerability, and immunogenicity of mRNA-4157 alone in patients with resected solid tumors and in combination with pembrolizumab in patients with unresectable solid tumors [abstract]. J. Clin. Oncol. 37 (Suppl. 15), 2523 (2019).

    Article 

    Google Scholar
     

  • Bauman, J. et al. Safety, tolerability, and immunogenicity of mRNA-4157 in combination with pembrolizumab in subjects with unresectable solid tumors (KEYNOTE-603): an update [abstract 798]. J. Immunother. Cancer 8 (Suppl. 3), A477 (2020).


    Google Scholar
     

  • Moderna. Moderna and Merck announce mRNA-4157/V940, an investigational personalized mRNA cancer vaccine, in combination with KEYTRUDA(R) (pembrolizumab), met primary efficacy endpoint in phase 2b KEYNOTE-942 trial. moderna investors.modernatx.com/news/news-details/2022/Moderna-and-Merck-Announce-mRNA-4157V940-an-Investigational-Personalized-mRNA-Cancer-Vaccine-in-Combination-with-KEYTRUDAR-pembrolizumab-Met-Primary-Efficacy-Endpoint-in-Phase-2b-KEYNOTE-942-Trial/default.aspx (2022).

  • Khattak, A. et al. A personalized cancer vaccine, mRNA-4157, combined with pembrolizumab versus pembrolizumab in patients with resected high-risk melanoma: efficacy and safety results from the randomized, open-label Phase 2 mRNA-4157-P201/Keynote-942 trial [abstract]. Cancer Res. 83 (Suppl. 8), CT001–CT001 (2023).

    Article 

    Google Scholar
     

  • Ryan, C. FDA grants breakthrough therapy designation to mRNA-4157/V940 plus pembrolizumab in high-risk melanoma. OncLive www.onclive.com/view/fda-grants-breakthrough-therapy-designation-to-mrna-4157-v940-plus-pembrolizumab-in-high-risk-melanoma (2023).

  • Patel, M. et al. Phase 1 study of mRNA-2752, a lipid nanoparticle encapsulating mRNAs encoding human OX40L/IL-23/IL-36γ, for intratumoral (ITu) injection +/- durvalumab in advanced solid tumors and lymphoma [abstract 539]. J. Immunother. Cancer 9 (Suppl. 2), A569 (2021).

    Article 

    Google Scholar
     

  • Hamid, O. et al. Preliminary safety, antitumor activity and pharmacodynamics results of HIT-IT MEDI1191 (mRNA IL-12) in patients with advanced solid tumours and superficial lesions [abstract 19O]. Ann. Oncol. 32 (Suppl. 1), S9 (2021).

    Article 

    Google Scholar
     

  • Carneiro, B. A. et al. First-in-human study of MEDI1191 (mRNA encoding IL-12) plus durvalumab in patients (pts) with advanced solid tumors [abstract]. Cancer Res. 82 (Suppl. 12), CT183 (2022).

    Article 

    Google Scholar
     

  • Taylor, N. P. AstraZeneca discards Moderna-partnered solid tumor prospect, kidney disease asset in pipeline clear-out. Fierce Biotech www.fiercebiotech.com/biotech/astrazeneca-discards-moderna-partnered-solid-tumor-prospect-kidney-disease-asset-pipeline (2022).

  • Chen, H., Liu, H. & Qing, G. Targeting oncogenic Myc as a strategy for cancer treatment. Signal. Transduct. Target. Ther. 3, 5 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Biospace. Omega Therapeutics announces promising preliminary clinical data for OTX-2002 from ongoing MYCHELANGELO™ I trial. BioSpace www.biospace.com/article/releases/omega-therapeutics-announces-promising-preliminary-clinical-data-for-otx-2002-from-ongoing-mychelangelo-i-trial/ (2023).

  • Omega Therapeutics. MYCHELANGELO™ I: preliminary phase 1 clinical update. Omega Therapeutics ir.omegatherapeutics.com/static-files/19eca20b-260d-4f30-8a13-16b05a5cb26b (2023).

  • Besin, G. et al. Accelerated blood clearance of lipid nanoparticles entails a biphasic humoral response of B-1 followed by B-2 lymphocytes to distinct antigenic moieties. Immunohorizons 3, 282–293 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bavli, Y. et al. Anti-PEG antibodies before and after a first dose of Comirnaty® (mRNA-LNP-based SARS-CoV-2 vaccine). J. Control. Rel. 354, 316–322 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Sanchez, A. J. D. S. et al. Substituting poly(ethylene glycol) lipids with poly(2-ethyl-2-oxazoline) lipids improves lipid nanoparticle repeat dosing. Adv. Healthc. Mater. https://doi.org/10.1002/adhm.202304033 (2024).

    Article 
    PubMed 

    Google Scholar
     

  • Hattab, D., Gazzali, A. M. & Bakhtiar, A. Clinical advances of siRNA-based nanotherapeutics for cancer treatment. Pharmaceutics 13, 1009 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Molyneaux, M., Berman, B., Xu, J., Evans, D. M. & Lu, P. Y. Effect of TGF-B1/COX-2 small interfering RNA combination product (STP705) on cell viability and tumor growth in a human squamous carcinoma xenograft tumor model in nude mice [abstract 15580]. J. Am. Acad. Dermatol. 83 (Suppl. 6), AB156 (2020).

    Article 

    Google Scholar
     

  • Sirnaomics. Sirnaomics achieves 100% complete response in phase II clinical trial of STP705 for treatment of cutaneous basal cell carcinoma. Sirnaomics sirnaomics.com/en/news-room/press-release/20220829sirnaomics-achieves-100-complete-response-in-phase-ii-clinical-trial-of-stp705-for-treatment-of-cutaneous-basal-cell-carcinoma/ (2022).

  • Sirnaomics. Pipeline. Sirnaomics sirnaomics.com/en/science-pipeline/pipeline/ (2023).

  • Sirnaomics. Sirnaomics launches phase I clinical trial of RNAi therapeutic STP707 delivered systemically for the treatment of solid tumors. Sirnaomics sirnaomics.com/en/news-room/press-release/20220209sirnaomics-launches-phase-i-clinical-trial-of-rnai-therapeutic-stp707-delivered-systemically-for-the-treatment-of-solid-tumors-1/ (2022).

  • Zhou, J. et al. Simultaneous silencing of TGF-β1 and COX-2 reduces human skin hypertrophic scar through activation of fibroblast apoptosis. Oncotarget 8, 80651–80665 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yan, Z. et al. Human rhomboid family-1 gene silencing causes apoptosis or autophagy to epithelial cancer cells and inhibits xenograft tumor growth. Mol. Cancer Ther. 7, 1355–1364 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Leng, Q., Scaria, P., Lu, P., Woodle, M. C. & Mixson, A. J. Systemic delivery of HK Raf-1 siRNA polyplexes inhibits MDA-MB-435 xenografts. Cancer Gene Ther. 15, 485–495 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tandon, M., Vemula, S. V. & Mittal, S. K. Emerging strategies for EphA2 receptor targeting for cancer therapeutics. Expert. Opin. Ther. Targets 15, 31–51 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cina, C. et al. A novel glutathione S-transferase P (GSTP) siRNA (NDT-05-1040) for the treatment of KRAS-driven non-small cell lung cancer [abstract]. Cancer Res. 78 (Suppl. 13), 5918 (2018).

    Article 

    Google Scholar
     

  • Jiao, L. et al. Glutathione S-transferase gene polymorphisms and risk and survival of pancreatic cancer. Cancer 109, 840–848 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bio-Path Holdings. Bio-Path Holdings presents data from ongoing phase 2 study of prexigebersen at 2021 American Society of Hematology Annual Meeting. Bio-Path Holdings www.sec.gov/Archives/edgar/data/1133818/000155837021016703/bpth-20211213xex99d1.htm (2021).

  • Anderluzzi, G. et al. The role of nanoparticle format and route of administration on self-amplifying mRNA vaccine potency. J. Control. Rel. 342, 388–399 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Pardi, N. et al. Expression kinetics of nucleoside-modified mRNA delivered in lipid nanoparticles to mice by various routes. J. Control. Rel. 217, 345–351 (2015).

    Article 
    CAS 

    Google Scholar
     

  • De Lombaerde, E., De Wever, O. & De Geest, B. G. Delivery routes matter: safety and efficacy of intratumoral immunotherapy. Biochim. Biophys. Acta Rev. Cancer 1875, 188526 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Wu, L. et al. Quantitative comparison of three widely-used pulmonary administration methods in vivo with radiolabeled inhalable nanoparticles. Eur. J. Pharm. Biopharm. 152, 108–115 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, J. Q. et al. Is AAV-delivered IL-27 a potential immunotherapeutic for cancer? Am. J. Cancer Res. 10, 3565–3574 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kedmi, R., Ben-Arie, N. & Peer, D. The systemic toxicity of positively charged lipid nanoparticles and the role of Toll-like receptor 4 in immune activation. Biomaterials 31, 6867–6875 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tousignant, J. D. et al. Comprehensive analysis of the acute toxicities induced by systemic administration of cationic lipid:plasmid DNA complexes in mice. Hum. Gene Ther. 11, 2493–2513 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

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

    Article 
    CAS 

    Google Scholar
     

  • Mitchell, M. J. et al. Engineering precision nanoparticles for drug delivery. Nat. Rev. Drug. Discov. 20, 101–124 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, H.-J. et al. Stimuli-responsive clustered nanoparticles for improved tumor penetration and therapeutic efficacy. Proc. Natl Acad. Sci. USA 113, 4164–4169 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scheetz, L. et al. Engineering patient-specific cancer immunotherapies. Nat. Biomed. Eng. 3, 768–782 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sindhwani, S. et al. The entry of nanoparticles into solid tumours. Nat. Mater. 19, 566–575 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Naumenko, V. A. et al. Extravasating neutrophils open vascular barrier and improve liposomes delivery to tumors. ACS Nano 13, 12599–12612 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lin, Z. P., Ngo, W., Mladjenovic, S. M., Wu, J. L. Y. & Chan, W. C. W. Nanoparticles bind to endothelial cells in injured blood vessels via a transient protein corona. Nano Lett. 23, 1003–1009 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sun, D., Zhou, S. & Gao, W. What went wrong with anticancer nanomedicine design and how to make it right. ACS Nano 14, 12281–12290 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wilhelm, S. et al. Analysis of nanoparticle delivery to tumours. Nat. Rev. Mater. 1, 16014 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Prabhakar, U. et al. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res. 73, 2412–2417 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Price, L. S. L., Stern, S. T., Deal, A. M., Kabanov, A. V. & Zamboni, W. C. A reanalysis of nanoparticle tumor delivery using classical pharmacokinetic metrics. Sci. Adv. 6, eaay9249 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McNeil, S. E. Evaluation of nanomedicines: stick to the basics. Nat. Rev. Mater. 1, 16073 (2016).

    Article 

    Google Scholar
     

  • Ding, H. et al. Long distance from microvessel to cancer cell predicts poor prognosis in non-small cell lung cancer patients. Front. Oncol. 11, 632352 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Miar, A. et al. Hypoxia induces transcriptional and translational downregulation of the type I IFN pathway in multiple cancer cell types. Cancer Res. 80, 5245–5256 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tang, Y., Weng, X., Liu, C., Li, X. & Chen, C. Hypoxia enhances activity and malignant behaviors of colorectal cancer cells through the STAT3/microRNA-19a/PTEN/PI3K/AKT axis. Anal. Cell Pathol. 2021, 4132488 (2021).

    Article 

    Google Scholar
     

  • Durymanov, M. O., Rosenkranz, A. A. & Sobolev, A. S. Current approaches for improving intratumoral accumulation and distribution of nanomedicines. Theranostics 5, 1007–1020 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gerweck, L. E., Kozin, S. V. & Stocks, S. J. The pH partition theory predicts the accumulation and toxicity of doxorubicin in normal and low-pH-adapted cells. Br. J. Cancer 79, 838–842 (1999).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huayamares, S. G. et al. Constructing a biomaterial to simulate extracellular drug transport in solid tumors. Macromol. Biosci. 20, 2000251 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Cheng, Q. et al. Selective organ targeting (SORT) nanoparticles for tissue-specific mRNA delivery and CRISPR-Cas gene editing. Nat. Nanotechnol. 15, 313–320 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mohanty, R. P., Liu, X. & Ghosh, D. Electrostatic driven transport enhances penetration of positively charged peptide surfaces through tumor extracellular matrix. Acta Biomater. 113, 240–251 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pressnall, M. M. et al. Glatiramer acetate enhances tumor retention and innate activation of immunostimulants. Int. J. Pharmaceutics 605, 120812 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Huang, A. et al. Human intratumoral therapy: linking drug properties and tumor transport of drugs in clinical trials. J. Control. Rel. 326, 203–221 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Pressnall, M. M., Huayamares, S. G. & Berkland, C. J. Immunostimulant complexed with polylysine limits transport and maintains immune cell activation. J. Pharm. Sci. 109, 2836–2846 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Henke, E., Nandigama, R. & Ergün, S. Extracellular matrix in the tumor microenvironment and its impact on cancer therapy. Front. Mol. Biosci. 6, 160 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hartmann, N. et al. Prevailing role of contact guidance in intrastromal T-cell trapping in human pancreatic cancer. Clin. Cancer Res. 20, 3422–3433 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gordon-Weeks, A. & Yuzhalin, A. E. Cancer extracellular matrix proteins regulate tumour immunity. Cancers 12, 3331 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tan, T. et al. Bioinspired lipoproteins-mediated photothermia remodels tumor stroma to improve cancer cell accessibility of second nanoparticles. Nat. Commun. 10, 3322 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Miao, L., Lin, C. M. & Huang, L. Stromal barriers and strategies for the delivery of nanomedicine to desmoplastic tumors. J. Control. Rel. 219, 192–204 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Hall, C., Lueshen, E., Mošat, A. & Linninger, A. A. Interspecies scaling in pharmacokinetics: a novel whole-body physiologically based modeling framework to discover drug biodistribution mechanisms in vivo. J. Pharm. Sci. 101, 1221–1241 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nair, A. B. & Jacob, S. A simple practice guide for dose conversion between animals and human. J. Basic. Clin. Pharm. 7, 27–31 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Elmeliegy, M., Udata, C., Liao, K. & Yin, D. Considerations on the calculation of the human equivalent dose from toxicology studies for biologic anticancer agents. Clin. Pharmacokinetics 60, 563–567 (2021).

    Article 

    Google Scholar
     

  • Li, Y., Wang, J., Wientjes, M. G. & Au, J. L. Delivery of nanomedicines to extracellular and intracellular compartments of a solid tumor. Adv. Drug. Deliv. Rev. 64, 29–39 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Heldin, C. H., Rubin, K., Pietras, K. & Ostman, A. High interstitial fluid pressure – an obstacle in cancer therapy. Nat. Rev. Cancer 4, 806–813 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Danhier, F. To exploit the tumor microenvironment: since the EPR effect fails in the clinic, what is the future of nanomedicine? J. Control. Rel. 244, 108–121 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Gualdrón-López, M. et al. Multiparameter flow cytometry analysis of the human spleen applied to studies of plasma-derived EVs from Plasmodium vivax patients. Front. Cell Infect. Microbiol. 11, 596104 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bjornson-Hooper, Z. B. et al. A comprehensive atlas of immunological differences between humans, mice, and non-human primates. Front. Immunol. 13, 867015 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Europeam Medicines Agency. Assessment report: Imlygic. EMA www.ema.europa.eu/en/documents/assessment-report/imlygic-epar-public-assessment-report_en.pdf (2015).

  • Europeam Medicines Agency. Annex I: Summary of product characteristics. Imlygic. EMA www.ema.europa.eu/en/documents/product-information/imlygic-epar-product-information_en.pdf (2015).

  • Barrett, J. A. et al. Regulated intratumoral expression of IL-12 using a RheoSwitch Therapeutic System(®) (RTS(®)) gene switch as gene therapy for the treatment of glioma. Cancer Gene Ther. 25, 106–116 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    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 
    PubMed 

    Google Scholar
     

  • BioNTech. US Securities and Exchange Commission. Form F-1: Registration Statement. www.sec.gov/Archives/edgar/data/1776985/000119312520022991/d838504df1.htmUS Securities and Exchange Commission (2020).

  • Madigan, V., Zhang, F. & Dahlman, J. E. Drug delivery systems for CRISPR-based genome editors. Nat. Rev. Drug Discov. 22, 875–894 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, Z. et al. Recent advances and applications of CRISPR-Cas9 in cancer immunotherapy. Mol. Cancer 22, 35 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fujii, E., Kato, A. & Suzuki, M. Patient-derived xenograft (PDX) models: characteristics and points to consider for the process of establishment. J. Toxicol. Pathol. 33, 153–160 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rab, R. et al. Evaluating antitumor activity of Escherichia coli purine nucleoside phosphorylase against head and neck patient-derived xenografts. Cancer Rep. 6, e1708 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Parker, W. B. et al. The use of Trichomonas vaginalis purine nucleoside phosphorylase to activate fludarabine in the treatment of solid tumors. Cancer Chemother. Pharmacol. 85, 573–583 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chuprin, J. et al. Humanized mouse models for immuno-oncology research. Nat. Rev. Clin. Oncol. 20, 192–206 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dray, B. K. et al. Mismatch repair gene mutations lead to Lynch syndrome colorectal cancer in rhesus macaques. Genes. Cancer 9, 142–152 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Simmons, H. A. & Mattison, J. A. The incidence of spontaneous neoplasia in two populations of captive rhesus macaques (Macaca mulatta). Antioxid. Redox Signal. 14, 221–227 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Simon, D., Bruno, G., Jehad, C., Maurizio, C. & Cline, J. M. Spontaneous, naturally occurring cancers in non-human primates as a translational model for cancer immunotherapy. J. Immunother. Cancer 11, e005514 (2023).

    Article 

    Google Scholar
     

  • Shah, S. B. et al. Combinatorial treatment rescues tumour-microenvironment-mediated attenuation of MALT1 inhibitors in B-cell lymphomas. Nat. Mater. 22, 511–523 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barbolosi, D., Ciccolini, J., Lacarelle, B., Barlési, F. & André, N. Computational oncology – mathematical modelling of drug regimens for precision medicine. Nat. Rev. Clin. Oncol. 13, 242–254 (2016).

    Article 
    PubMed 

    Google Scholar
     

  • Fotakis, G., Trajanoski, Z. & Rieder, D. Computational cancer neoantigen prediction: current status and recent advances. Immunooncol. Technol. 12, 100052 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Food and Drug Administration. Focus Area: Novel technologies to improve predictivity of non-clinical studies and replace, reduce, and refine reliance on animal testing. FDA www.fda.gov/science-research/focus-areas-regulatory-science-report/focus-area-novel-technologies-improve-predictivity-non-clinical-studies-and-replace-reduce-and (2022).

  • Cheng, F. et al. Research advances on the stability of mRNA vaccines. Viruses 15, 668 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Polaka, S. et al. in Pharmacokinetics and Toxicokinetic Considerations Vol. 2 (ed. Tekade, R. K.) 543–567 (Academic Press, 2022).

  • Hemmrich, E. & McNeil, S. Active ingredient vs excipient debate for nanomedicines. Nat. Nanotechnol. 18, 692–695 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Marden, E., Ntai, I., Bass, S. & Flühmann, B. Correction to: Reflections on FDA draft guidance for products containing nanomaterials: is the abbreviated new drug application (ANDA) a suitable pathway for nanomedicines? AAPS J. 20, 104 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Kiaie, S. H. et al. Recent advances in mRNA-LNP therapeutics: immunological and pharmacological aspects. J. Nanobiotechnol. 20, 276 (2022).

    Article 
    CAS 

    Google Scholar
     

  • Sayedahmed, E. E., Kumari, R. & Mittal, S. K. Current use of adenovirus vectors and their production methods. Methods Mol. Biol. 1937, 155–175 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kim, J. W. et al. in: Gene Therapy for Neurological Disorders: Methods and Protocols (ed. Manfredsson, F. P.) 115–130 (Springer, 2016).

  • Tombácz, I. et al. Highly efficient CD4+ T cell targeting and genetic recombination using engineered CD4+ cell-homing mRNA-LNPs. Mol. Ther. 29, 3293–3304 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rurik, J. G. et al. CAR T cells produced in vivo to treat cardiac injury. Science 375, 91–96 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Breda, L. et al. In vivo hematopoietic stem cell modification by mRNA delivery. Science 381, 436–443 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shi, D., Toyonaga, S. & Anderson, D. G. In vivo RNA delivery to hematopoietic stem and progenitor cells via targeted lipid nanoparticles. Nano Lett. 23, 2938–2944 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barbieri, I. & Kouzarides, T. Role of RNA modifications in cancer. Nat. Rev. Cancer 20, 303–322 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Qiu, L., Jing, Q., Li, Y. & Han, J. RNA modification: mechanisms and therapeutic targets. Mol. Biomed. 4, 25 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Morse, M. A. et al. Clinical trials of self-replicating RNA-based cancer vaccines. Cancer Gene Ther. 30, 803–811 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Delgado, A. & Guddati, A. K. Clinical endpoints in oncology – a primer. Am. J. Cancer Res. 11, 1121–1131 (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Food and Drug Administration. Diversity plans to improve enrollment of participants from underrepresented racial and ethnic populations in clinical trials; availability: draft guidance for industry. FDA www.fda.gov/regulatory-information/search-fda-guidance-documents/diversity-plans-improve-enrollment-participants-underrepresented-racial-and-ethnic-populations (2022).

  • Lek, A. et al. Death after high-dose rAAV9 gene therapy in a patient with Duchenne’s muscular dystrophy. N. Engl. J. Med. 389, 1203–1210 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ilham, S. et al. Cancer incidence in immunocompromised patients: a single-center cohort study. BMC Cancer 23, 33 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fourie Zirkelbach, J. et al. Improving dose-optimization processes used in oncology drug development to minimize toxicity and maximize benefit to patients. J. Clin. Oncol. 40, 3489–3500 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Shah, M., Rahman, A., Theoret, M. R. & Pazdur, R. The drug-dosing conundrum in oncology – when less is more. N. Engl. J. Med. 385, 1445–1447 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Khattak, A. et al. Distant metastasis-free survival results from the randomized, phase 2 mRNA-4157-P201/KEYNOTE-942 trial [abstract]. J. Clin. Oncol. 41 (Suppl. 17), LBA9503 (2023).

    Article 

    Google Scholar
     

  • Ruzzi, F. et al. Virus-like particle (VLP) vaccines for cancer immunotherapy. Int J. Mol. Sci. 24, 12963 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tornesello, A. L., Tagliamonte, M., Buonaguro, F. M., Tornesello, M. L. & Buonaguro, L. Virus-like particles as preventive and therapeutic cancer vaccines. Vaccines 10, 227 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, Y. et al. mRNA vaccine in cancer therapy: current advance and future outlook. Clin. Transl. Med. 13, e1384 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reichmuth, A. M., Oberli, M. A., Jaklenec, A., Langer, R. & Blankschtein, D. mRNA vaccine delivery using lipid nanoparticles. Ther. Deliv. 7, 319–334 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Perche, F. et al. Enhancement of dendritic cells transfection in vivo and of vaccination against B16F10 melanoma with mannosylated histidylated lipopolyplexes loaded with tumor antigen messenger RNA. Nanomed. Nanotechnol. Biol. Med. 7, 445–453 (2011).

    Article 
    CAS 

    Google Scholar
     

  • Raimondo, T. M., Reed, K., Shi, D., Langer, R. & Anderson, D. G. Delivering the next generation of cancer immunotherapies with RNA. Cell 186, 1535–1540 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Food and Drug Administration. Highlights of prescribing information: ONPATTRO® (patisiran). FDA www.accessdata.fda.gov/drugsatfda_docs/label/2018/210922s000lbl.pdf (2018).

  • Bratman, S. V. et al. Personalized circulating tumor DNA analysis as a predictive biomarker in solid tumor patients treated with pembrolizumab. Nat. Cancer 1, 873–881 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pessoa, L. S., Heringer, M. & Ferrer, V. P. ctDNA as a cancer biomarker: a broad overview. Crit. Rev. Oncol. Hematol. 155, 103109 (2020).

    Article 
    PubMed 

    Google Scholar
     

  • Wen, X., Pu, H., Liu, Q., Guo, Z. & Luo, D. Circulating tumor DNA – a novel biomarker of tumor progression and its favorable detection techniques. Cancers 14, 6025 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nassiri, F. et al. Oncolytic DNX-2401 virotherapy plus pembrolizumab in recurrent glioblastoma: a phase 1/2 trial. Nat. Med. 29, 1370–1378 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar