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Systemic reprogramming of tumour immunity via IL-10-mRNA nanoparticles

Nature Nanotechnology volume 20, pages 1526–1538 (2025)Cite this article

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Abstract

Daily subcutaneous injections of recombinant interleukin-10 (IL-10) demonstrated encouraging but preliminary efficacy in certain tumour types during early phase clinical trials. However, these antitumour effects were not consistently replicated in larger trials, probably due to insufficient intratumoural recombinant IL-10 accumulation, which ultimately restricted clinical benefit. Here we show that intravenous injections of IL-10 messenger RNA (mRNA) nanoparticles (IL-10-mRNA@NPs) induce potent immune surveillance across diverse preclinical tumour models and mitigate systemic toxicities. In particular, IL-10-mRNA@NPs sustain in situ IL-10 production within tumours, promoting substantial infiltration and proliferation of cytotoxic T cells, activation and maturation of dendritic cells, and an augmented expression of major histocompatibility complex class I molecules in immunosuppressive orthotopic early stage hepatocellular carcinoma tumours. Moreover, in mice with orthotopic middle-to-late-stage hepatocellular carcinoma tumours, combining IL-10-mRNA@NPs with immune checkpoint blockades results in 43% of mice showing complete tumour eradication and a sixfold increase in median survival compared with mice treated with immune checkpoint blockades alone. Furthermore, this combination induces long-lasting antitumour immune memory, conferring 100% protection against tumour rechallenges. The intravenous IL-10-mRNA@NPs strategy may have potential to overcome the challenges associated with recombinant IL-10 in clinical trials across a broad spectrum of immunosuppressive tumours.

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Fig. 1: Antitumour efficacy and safety of repeated rIL-10 versus IL-10-mRNA@NPs injections.
Fig. 2: i.v. IL-10-mRNA@NPs elicit immune-driven antitumour responses in multiple tumour models.
Fig. 3: In vivo therapeutic evaluation and immunomodulatory effects of i.v. IL-10-mRNA@NPs in an orthotopic early stage metastatic HCC model.
Fig. 4: IL-10-mRNA@NPs sensitize mice with immunosuppressive orthotopic metastatic middle-to-late-stage HCC tumours to ICBs therapy, achieving tumour eradication along with increased median survival.
Fig. 5: Combination of IL-10-mRNA@NPs with ICBs therapy reshaped the TME towards a more pronounced antitumour condition for mice bearing orthotopic immunosuppressive middle-to-late-stage HCC tumours.
Fig. 6: IL-10-mRNA@NPs in combination with ICBs induced long-term immune memory effect in mice with orthotopic immunosuppressive middle-to-late-stage HCC tumours.

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All data supporting the findings of this study are presented in the Article and the Supplementary Information. Source data are provided with this paper.

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Acknowledgements

This work was supported by the American Lung Association (ALA) Cancer Discovery Award (no. LCD 1034625; W.T.), the ALA Courtney Cox Cole Lung Cancer Research Award (no. 2022A017206; W.T.), the Harvard/Brigham Health & Technology Innovation Fund (no. 2023A004452; W.T.), Nanotechnology Foundation (no. 2022A002721; W.T.), the Distinguished Chair Professorship Foundation (no. 018129; W.T.) and Department Institutional Fund (no. GR0116589; K.S.). W.T. is also a recipient of the LEO Foundation Research Grant (no. LF-OC-24-001665), the American Heart Association (AHA) Transformational Project Award (no. 23TPA1072337), the AHA’s Second Century Early Faculty Independence Award (no. 23SCEFIA1151841), the American Society of Transplantation Career Transition Grant (no. 1173492), the Novo Nordisk ValidatioNN Award (no. 2023A009607), the Harvard/Brigham the Khoury Innovation Award (no. 2020A003219), the Department Basic Scientist Grant (no. 2420 BPA075) and the Gillian Reny Stepping Strong Center for Trauma Innovation Breakthrough Innovator Award (no. 113548). We thank L. Luo from the Department of Medicine, University of California, Los Angeles and T. A. Van Schaik from the Center for Stem Cell and Translational Immunotherapy, Brigham and Women’s Hospital, Harvard Medical School, for helpful discussions.

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Authors and Affiliations

  1. Center for Nanomedicine and Department of Anesthesiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Chuang Liu, Xiangang Huang, Alexey V. Yaremenko, Xueyan Zhen, Xinru You, Yi Tang, Seyoung Koo, Wei Chen, Na Kong & Wei Tao

  2. Center for Stem Cell and Translational Immunotherapy, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Chuang Liu, Kok-Siong Chen, Filippo Rossignoli & Khalid Shah

  3. Department of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Chuang Liu, Kok-Siong Chen, Filippo Rossignoli & Khalid Shah

  4. Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Sihan Xiong

  5. Liangzhu Laboratory, Zhejiang University Medical Center, Hangzhou, China

    Na Kong

  6. College of Pharmacy, School of Medicine, Hangzhou Normal University, Hangzhou, China

    Tian Xie

  7. Harvard Stem Cell Institute, Harvard University, Cambridge, MA, USA

    Khalid Shah

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Contributions

C.L., N.K. and W.T. conceived and designed this study. C.L. performed the animal experiments and data analysis and wrote the original draft. W.T. supervised the project and edited and revised the manuscript. C.L., S.X., A.V.Y., Y.T. and X.H. synthesized the NPs. K.-S.C. performed the bulk RNA-sequencing data analysis. F.R. assisted in the flow cytometry compensation and gating strategy. C.L., X.Z., A.V.Y., S.X. and X.Y. performed the cell staining for flow cytometry. K.S. reviewed the data, edited and revised the manuscript. N.K. and T.X. discussed the results and commented on the manuscript. All authors provided feedback.

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Correspondence to Wei Tao.

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Competing interests

C.L., N.K. and W.T. are inventors on a US patent application (BWH Invention no. 2025-409) filed by the Brigham and Women’s Hospital related to the technology disclosed here. W.T. has received consultancy fees, lecture fees, been on the scientific advisory board or conducted sponsored research at Harvard Medical School/Brigham and Women’s Hospital for the following entities: Novo Nordisk A/S, Henlius USA Inc. K.S. owns equity in and is a member of the Board of Directors of AMASA Therapeutics, a startup company developing stem-cell-based therapies for cancer. K.S.’s interests were reviewed and are managed by Brigham and Women’s Hospital and Mass General Brigham in accordance with their conflict-of-interest policies. The other authors declare no competing interests.

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Liu, C., Huang, X., Chen, KS. et al. Systemic reprogramming of tumour immunity via IL-10-mRNA nanoparticles. Nat. Nanotechnol. 20, 1526–1538 (2025). https://doi.org/10.1038/s41565-025-01980-7

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