An RNA toolbox for cancer immunotherapy

Pastor, Fernando; Berraondo, Pedro; Etxeberria, Iñaki; Frederick, Josh; Sahin, Ugur; Gilboa, Eli; Melero, Ignacio

doi:10.1038/nrd.2018.132

Cited by 230Immunotherapy and Immune ResponsesCancer Immunotherapy and BiomarkersRNA Interference and Gene Delivery

An RNA toolbox for cancer immunotherapy

Pastor, Fernando, Berraondo, Pedro, Etxeberria, Iñaki, Frederick, Josh, Sahin, Ugur, Gilboa, Eli, Melero, Ignacio·2018·Nature Reviews Drug Discovery

DOI 10.1038/nrd.2018.132

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Abstract

Cancer immunotherapy has revolutionized oncology practice. However, current protein and cell therapy tools used in cancer immunotherapy are far from perfect, and there is room for improvement regarding their efficacy and safety. RNA-based structures have diverse functions, ranging from gene expression and gene regulation to pro-inflammatory effects and the ability to specifically bind different molecules. These functions make them versatile tools that may advance cancer vaccines and immunomodulation, surpassing existing approaches. These technologies should not be considered as competitors of current immunotherapies but as partners in synergistic combinations and as a clear opportunity to reach more efficient and personalized results. RNA and RNA derivatives can be exploited therapeutically as a platform to encode protein sequences, provide innate pro-inflammatory signals to the immune system (such as those denoting viral infection), control the expression of other RNAs (including key immunosuppressive factors) post-transcriptionally and conform structural scaffoldings binding proteins that control immune cells by modifying their function. Nascent RNA immunotherapeutics include RNA vaccines encoding cancer neoantigens, mRNAs encoding immunomodulatory factors, viral RNA analogues, interference RNAs and protein-binding RNA aptamers. These approaches are already in early clinical development with promising safety and efficacy results.

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RNA vaccines have exhibited encouraging results in both infection therapy and cancer immunotherapy.
“RNA vaccines, for example, have exhibited encouraging results in both infection therapy and cancer immunotherapy.[6, 7, 11–15]”
From RNA delivery biomaterials for the treatment of genetic and rare diseases (2019) · cites this paper as [7]

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Aptamer-targeted Antigen Delivery
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A TIM-3 Oligonucleotide Aptamer Enhances T Cell Functions and Potentiates Tumor Immunity in Mice
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Targeting inhibition of Foxp3 by a CD28 2′-Fluro oligonucleotide aptamer conjugated to P60-peptide enhances active cancer immunotherapy
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Aptamer-Targeted Attenuation of IL-2 Signaling in CD8 + T Cells Enhances Antitumor Immunity
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Identification of TIM3 2′-fluoro oligonucleotide aptamer by HT-SELEX for cancer immunotherapy
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Anchoring interferon alpha to apolipoprotein A-I reduces hematological toxicity while enhancing immunostimulatory properties
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siRNA and Cancer Immunotherapy
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“In comparison to other functional biomolecules such as plasmid DNA (pDNA) and recombinant proteins, mRNA exhibits several therapeutic benefits, thereby rendering it highly desirable for the development of a new generation of cancer immunotherapy drugs (Pastor et al., 2018).”
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Trial watch: TLR3 agonists in cancer therapy
Le Naour, J., Galluzzi, L., Zitvogel, L., Kroemer, G., & Vacchelli, E. (2020) · OncoImmunology · doi:10.1080/2162402x.2020.1771143 · Cited by 239 · see citing works
Rapid Surface Display of mRNA Antigens by Bacteria‐Derived Outer Membrane Vesicles for a Personalized Tumor Vaccine
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Circular RNA cancer vaccines drive immunity in hard-to-treat malignancies
Li, H., Peng, K., Yang, K., Ma, W., Qi, S., Yu, X., He, J., Lin, X., & Yu, G. (2022) · Theranostics · doi:10.7150/thno.77350 · Cited by 245 · see citing works
“Among all kinds of clinically tested cancer immune therapies, cancer vaccine is the one that shows the most promising application potentials [12-17].”
Background
Recent Advances of SHP2 Inhibitors in Cancer Therapy: Current Development and Clinical Application
Yuan, X., Bu, H., Zhou, J., Yang, C., & Zhang, H. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.0c00249 · Cited by 224 · see citing works
mRNA Delivery for Therapeutic Anti-HER2 Antibody Expression In Vivo
Rybakova, Y., Kowalski, P. S., Huang, Y., Gonzalez, J. T., Heartlein, M. W., DeRosa, F., Delcassian, D., & Anderson, D. G. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.05.012 · Cited by 218 · see citing works
Targeting mRNA processing as an anticancer strategy
Desterro, J. M. P., Bak‐Gordon, P., & Carmo‐Fonseca, M. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0042-3 · Cited by 180 · see citing works
Theranostic Nanoparticles for RNA-Based Cancer Treatment
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mRNA cancer vaccines: Advances, trends and challenges
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“The ability of triplet mRNAs encoding IL-23, IL-36, and OX40L to improve the survival rate of MC38-S tumor-bearing mice was signiﬁcantly stronger than that of the corresponding protein treatments 78 .”
Cellular RNA surveillance in health and disease
Wolin, S. L., & Maquat, L. E. (2019) · Science · doi:10.1126/science.aax2957 · Cited by 157 · see citing works
Long Noncoding RNA and Epithelial Mesenchymal Transition in Cancer
Gugnoni, M., & Ciarrocchi, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20081924 · Cited by 151 · see citing works
Polysaccharide-based nanomedicines for cancer immunotherapy: A review
Zeng, Y., Xiang, Y., Sheng, R., Tomás, H., Rodrigues, J., Gu, Z., Zhang, H., Gong, Q., & Luo, K. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.03.008 · Cited by 145 · see citing works
Intratumor Adoptive Transfer of IL-12 mRNA Transiently Engineered Antitumor CD8+ T Cells
Etxeberría, I., Bolaños, E., Quetglas, J. I., Gros, A., Villanueva, A., Palomero, J., Sánchez-Paulete, A. R., Piulats, J. M., Matías‐Guiu, X., Olivera, I., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.10.006 · Cited by 145 · see citing works
Aptamers, the Nucleic Acid Antibodies, in Cancer Therapy
Fu, Z., & Xiang, J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082793 · Cited by 144 · see citing works
Recent progress of aptamer‒drug conjugates in cancer therapy
He, J., Duan, Q., Ran, C., Fu, T., Liu, Y., & Tan, W. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2023.01.017 · Cited by 139 · see citing works
High-throughput barcoding of nanoparticles identifies cationic, degradable lipid-like materials for mRNA delivery to the lungs in female preclinical models
Xue, L., Hamilton, A. G., Zhao, G., Xiao, Z., El-Mayta, R. D., Han, X., Gong, N., Xiong, X., Xu, J., Figueroa‐Espada, C. G., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45422-9 · Cited by 142 · see citing works
Cross-priming in cancer immunology and immunotherapy
Luri‐Rey, C., Teijeira, Á., Wculek, S. K., de Andrea, C. E., Herrero, C., López‐Janeiro, Á., Rodriguez-Ruiz, M. E., Heras‐Murillo, I., Aggelakopoulou, M., Berraondo, P., et al. (2025) · Nature reviews. Cancer · doi:10.1038/s41568-024-00785-5 · Cited by 143 · see citing works
“The specific targeting of lipid nanoparticles carrying mRNA encoding tumour antigens towards DCs also represents a cutting-edge approach in cancer immunotherapy 298 .”
Cancer Vaccines: Adjuvant Potency, Importance of Age, Lifestyle, and Treatments
Cuzzubbo, S., Mangsbo, S. M., Nagarajan, D., Habra, K., Pockley, A. G., & McArdle, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.615240 · Cited by 130 · see citing works
Aptamers: Cutting edge of cancer therapies
Shigdar, S. L., Schrand, B., Giangrande, P. H., & de Franciscis, V. (2021) · Molecular Therapy · doi:10.1016/j.ymthe.2021.06.010 · Cited by 128 · see citing works
Adaptive design of mRNA-loaded extracellular vesicles for targeted immunotherapy of cancer
Dong, S., Liu, X., Bi, Y., Wang, Y., Antony, A., Lee, D., Huntoon, K. M., Jeong, S. D., Ma, Y., Li, X., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42365-5 · Cited by 127 · see citing works
Dendritic Cell Vaccines: A Shift from Conventional Approach to New Generations
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Combinatorial design of siloxane-incorporated lipid nanoparticles augments intracellular processing for tissue-specific mRNA therapeutic delivery
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“1b, Supplementary Schemes 1–5 and Supplementary Figs.”
Messenger RNA therapy for rare genetic metabolic diseases
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From structural design to delivery: mRNA therapeutics for cancer immunotherapy
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Engineering Prodrug Nanomedicine for Cancer Immunotherapy
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mRNA delivery systems for cancer immunotherapy: Lipid nanoparticles and beyond
Sentí, M. E., del Valle, L. G., & Schiffelers, R. M. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115190 · Cited by 116 · see citing works
Improved Nucleic Acid Therapy with Advanced Nanoscale Biotechnology
Weng, Y., Huang, Q., Li, C., Yang, Y., Wang, X., Yu, J., Huang, Y., & Liang, X. (2019) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.12.004 · Cited by 107 · see citing works
“Improve Stability and Avoid Degradation Nucleases are vital for organisms to avoid virus invasion andmissense RNA/DNA accumulation.(53) However, they are also responsible for the poor stability of NAs.”
Background
Trial Watch: experimental TLR7/TLR8 agonists for oncological indications
Frega, G., Wu, Q., Le Naour, J., Vacchelli, E., Galluzzi, L., Kroemer, G., & Kepp, O. (2020) · OncoImmunology · doi:10.1080/2162402x.2020.1796002 · Cited by 108 · see citing works
Novel strategies exploiting interleukin-12 in cancer immunotherapy.
Cirella, A., Luri-Rey, C., Trani, C. D. D., Teijeira, Á., Olivera, I., Bolaños, E., Castañón, E., Palencia, B., Brocco, D., Fernández-Sendin, M., et al. (2022) · Pharmacology and Therapeutics · doi:10.1016/j.pharmthera.2022.108189 · Cited by 89 · see citing works
Lipid Nanoparticles for Delivery of Therapeutic RNA Oligonucleotides
Moss, K. H., Popova, P. G., Hadrup, S. R., Astakhova, K., & Taskova, M. (2019) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.8b01290 · Cited by 99 · see citing works
RNA-based therapies: A cog in the wheel of lung cancer defense
Κhan, P., Siddiqui, J. A., Lakshmanan, I., Ganti, A. K., Salgia, R., Jain, M., Batra, S. K., & Nasser, M. W. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01338-2 · Cited by 100 · see citing works
Cell-Selective Messenger RNA Delivery and CRISPR/Cas9 Genome Editing by Modulating the Interface of Phenylboronic Acid-Derived Lipid Nanoparticles and Cellular Surface Sialic Acid
Tang, Q., Liu, J., Jiang, Y. Y., Zhang, M., Mao, L., & Wang, M. (2019) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b17749 · Cited by 98 · see citing works
Nanoparticle entry into cells; the cell biology weak link
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A New Era for Rare Genetic Diseases: Messenger RNA Therapy
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RNA-mediated immunotherapy regulating tumor immune microenvironment: next wave of cancer therapeutics
Pandey, P. R., Young, K. H., Kumar, D., & Jain, N. K. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01528-6 · Cited by 87 · see citing works
Advancing cancer immunotherapy through siRNA-based gene silencing for immune checkpoint blockade
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Aptamer-based rapid diagnosis for point-of-care application
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LncRNAs as Chromatin Regulators in Cancer: From Molecular Function to Clinical Potential
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RNA delivery biomaterials for the treatment of genetic and rare diseases
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Potentialities and Challenges of mRNA Vaccine in Cancer Immunotherapy
Duan, L.-J., Wang, Q., Zhang, C., Yang, D.-X., & Zhang, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.923647 · Cited by 79 · see citing works
“Among these, mRNA-based cancer vaccines demonstrate exceptional advantages in comparison with the other types of vaccines (4).”
Background
Spray dried lipid nanoparticle formulations enable intratracheal delivery of mRNA
Friis, K. P., Gracin, S., Oag, S., Leijon, A., Sand, E., Lindberg, B., Lázaro‐Ibáñez, E., Lindqvist, J., Whitehead, K. A., & Bak, A. (2023) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.09.031 · Cited by 76 · see citing works
Mechanisms of Leukemia Immune Evasion and Their Role in Relapse After Haploidentical Hematopoietic Cell Transplantation
Rovatti, P. E., Gambacorta, V., Lorentino, F., Ciceri, F., & Vago, L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00147 · Cited by 73 · see citing works
“Recently, novel approaches to transfer high concentration of cytokines to the tumor site and reduce their systemic effects are emerging, including gene therapy “Trojan Horse” strategies (188) and the use of lipid nanoparticles to convey to the tumor site mRNAs encoding cytokines (189).”
Background
Nanomaterials for mRNA ‐based therapeutics: Challenges and opportunities
Li, D., Liu, Q., Yang, M., Xu, H., Zhu, M., Zhang, Y., Xu, J., Tian, C., Yao, J., Wang, L., et al. (2023) · Bioengineering & Translational Medicine · doi:10.1002/btm2.10492 · Cited by 71 · see citing works
“Over the past few years, evidence has revealed that mRNA-based therapeutics have gained immense interest and are demonstrating to be viable options in a wide range of diseases, including cancer,70 infectious disease,71 and rare genetic diseases.72 mRNAs can use the human body to translate and encode therapeutic protei…”
Background
Investigation of pH-Responsiveness inside Lipid Nanoparticles for Parenteral mRNA Application Using Small-Angle X-ray Scattering
Uebbing, L., Ziller, A., Siewert, C., Schroer, M. A., Blanchet, C. E., Svergun, D. I., Ramishetti, S., Peer, D., Şahin, U., Haas, H., et al. (2020) · Langmuir · doi:10.1021/acs.langmuir.0c02446 · Cited by 69 · see citing works
Charge-altering releasable transporters enhance mRNA delivery in vitro and exhibit in vivo tropism
Li, Z., Amaya, L., Pi, R., Wang, S. K., Ranjan, A., Waymouth, R. M., Blish, C. A., Chang, H. Y., & Wender, P. A. (2023) · Nature Communications · doi:10.1038/s41467-023-42672-x · Cited by 64 · see citing works
Cancer immunomodulation using bispecific aptamers
Thomas, B. J., Porciani, D., & Burke, D. H. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.01.008 · Cited by 63 · see citing works
“Despite these promising discoveries, only two immunomodulating aptamers, NOX E36 and NOX A12 (antagonists of the chemokines CCL2 and CXCL2, respectively), have moved into the clinical pipeline for cancer treatment thus far.(29,97,98) A comprehensive list of published immunomodulating aptamers is provided in Table 4, t…”
Background
Circular RNA‐based neoantigen vaccine for hepatocellular carcinoma immunotherapy
Wang, F., Guang, C., Wang, Y., Zhuang, Q., Cai, Z., Li, Y., Gao, S., Li, F., Zhang, C., Zhao, B., et al. (2024) · MedComm · doi:10.1002/mco2.667 · Cited by 63 · see citing works
Advances in RNA-based cancer therapeutics: pre-clinical and clinical implications
Yan, Y., Liu, S., Wen, J., He, Y., Duan, C., Nabavi, N., Ashrafizadeh, M., Sethi, G., Liu, L., & Ma, R. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02463-y · Cited by 68 · see citing works
Aptamer‐functionalized quantum dots as theranostic nanotools against cancer and bacterial infections: A comprehensive overview of recent trends
Davodabadi, F., Mirinejad, S., Fathi‐karkan, S., Majidpour, M., Ajalli, N., Sheervalilou, R., Sargazi, S., Rozmus, D., Rahdar, A., & Diez-Pascual, A. M. (2023) · Biotechnology Progress · doi:10.1002/btpr.3366 · Cited by 60 · see citing works
Therapeutic mRNA delivery to leukocytes
Granot-Matok, Y., Kon, E., Dammes, N., Mechtinger, G., & Peer, D. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.05.032 · Cited by 61 · see citing works
The tiny big world of solid lipid nanoparticles and nanostructured lipid carriers: an updated review
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Authors: Pastor, F., Berraondo, P., Etxeberria, I., Frederick, J., Sahin, U., Gilboa, E., & Melero, I.
Affiliations: Centro de Investigación Médica Aplicada (ES)
Navarre Institute of Health Research (ES)
Moderna Therapeutics (United States) (US)
University of Miami (US)
Corresponding author: Melero, Ignacio
ORCID: Pastor, Fernando
Berraondo, Pedro
Gilboa, Eli
Melero, Ignacio
Venue: Nature Reviews Drug Discovery
Publisher: Springer Science and Business Media LLC
Published: 2018-09-07
Volume: 17
Issue: 10
Pages: 751-767
ISSN: 1474-1776 (ISSN-L)
1474-1784
DOI: 10.1038/nrd.2018.132
OpenAlex: W2889813782
Cited by: 229
References: 179
Citations by year: 2026: 11 · 2025: 27 · 2024: 24 · 2023: 39 · 2022: 40 · 2021: 33 · 2020: 27 · 2019: 27 · 2018: 1
FWCI: 2.25
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Reviews Drug Discovery (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
Keywords: cancer immunotherapy, RNA vaccines, neoantigens, mRNA vaccines, RNA interference, RNA aptamers, immunomodulation, innate immune activation, post-transcriptional regulation, cancer vaccines, combination immunotherapy
MeSH terms: Animals, Humans, Immunotherapy, Neoplasms, RNA, Cancer Vaccines, RNA Interference, Immunomodulation

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