Large-scale generation of functional mRNA-encapsulating exosomes via cellular nanoporation
Open accessAbstract
Exosomes are attractive as nucleic-acid carriers because of their favourable pharmacokinetic and immunological properties and their ability to penetrate physiological barriers that are impermeable to synthetic drug-delivery vehicles. However, inserting exogenous nucleic acids, especially large messenger RNAs, into cell-secreted exosomes leads to low yields. Here we report a cellular-nanoporation method for the production of large quantities of exosomes containing therapeutic mRNAs and targeting peptides. We transfected various source cells with plasmid DNAs and stimulated the cells with a focal and transient electrical stimulus that promotes the release of exosomes carrying transcribed mRNAs and targeting peptides. Compared with bulk electroporation and other exosome-production strategies, cellular nanoporation produced up to 50-fold more exosomes and a more than 10 3-fold increase in exosomal mRNA transcripts, even from cells with low basal levels of exosome secretion. In orthotopic phosphatase and tensin homologue (PTEN)-deficient glioma mouse models, mRNA-containing exosomes restored tumour-suppressor function, enhanced inhibition of tumour growth and increased survival. Cellular nanoporation may enable the use of exosomes as a universal nucleic-acid carrier for applications requiring transcriptional manipulation.
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PTEN is commonly mutated in wide ranges of GBM, which may be a candidate for therapeutic intervention.
“A tumour suppressor gene, like phosphatase and tensin homologue (PTEN), is commonly mutated in wide ranges of GBM, which may be a great candidate for therapeutic intervention27,54.”
From Blood–brain-barrier-crossing lipid nanoparticles for mRNA delivery to the central nervous system (2025) · cites this paper as [27]
The Results section ('Functional and pharmacokinetic evaluation of CNP generated exosomes'; page not specified) calls PTEN a commonly mutated tumour suppressor gene and tests it as a therapeutic target in two PTEN-deficient glioma models. The in vivo Results report inhibited tumour growth after PTEN-restoring treatment. The copy does not establish how widely PTEN is mutated specifically across GBM. (LLM, conf=0.83)
Experimental — accuracy not yet measuredCNP technology increases exosome yield and mRNA amount within exosomes.
“The CNP technology increases the exosome yield and the mRNA amount within the exosomes [110].”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
CNP increased mRNA loading in exosomes by 100-fold compared to conventional electroporation methods.
“In addition, this strategy increased mRNA loading in exosomes by 100-fold compared to conventional electroporation methods.”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
CNP-treated exosomes from cells of the same origin have an increased mRNA encapsulation efficiency of 3-4 folds compared to exosomes produced endogenously without external stimuli.
“Compared to exosomes produced endogenously without involving external stimuli, CNP-treated exosomes from cells of the same origin have an increased mRNA encapsulation efficiency of 3–4 folds.”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
By modifying exosome CD47 with CREKA and CDX peptides, targeting ability was improved.
“By modifying the exosome CD47 with these peptides, the targeting ability was improved.”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
Chemical modification of exosomes was carried out to target GL261 gliomas and U87 glioblastomas.
“Chemical modification of exosomes was carried out to target GL261 gliomas and U87 glioblastomas.”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
When PTEN mRNA was modified with CDX peptide, resulting exosomes exhibited a twofold increase in accumulation in mouse U87 gliomas, leading to prolonged survival.
“Moreover, when PTEN mRNA was additionally modified with the CDX peptide, the resulting exosomes exhibited a twofold increase in accumulation in mouse U87 gliomas, leading to prolonged survival.”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
Modification of PTEN mRNA with CREKA peptide resulted in a 1.5-fold increase in accumulation in mouse U87 gliomas and improved survival.
“Similarly, modification of PTEN mRNA with CREKA peptide resulted in a 1.5-fold increase in accumulation in mouse U87 gliomas and improved survival [110].”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
Yang et al. modified CD47-derived exosomes by incorporating a glioma targeting peptide at N terminus, allowing selective uptake of PTEN cargo by glioma cells and effectively inhibiting tumor cell proliferation.
“Yang et al. modified CD47-derived exosomes by incorporating a glioma targeting peptide at the N terminus. This modification allowed for selective uptake of tumor suppression gene, phosphatase and tensin homolog (PTEN) cargo by glioma cells. As a result, the proliferation of tumor cells was effectively inhibited [110].”
From Exosome for mRNA delivery: Strategies and therapeutic applications (2024) · cites this paper as [110]
Mouse embryonic fibroblast-derived exosomes were able to deliver PTEN mRNA to inhibit mouse glioma growth.
“In Yang et al. research, mouse embryonic fibroblast-derived exosomes were able to deliver PTEN (phosphatase and homologous tensin) mRNA to inhibit mouse glioma growth [49].”
From The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System (2022) · cites this paper as [49]
Naturally derived membrane lipids can also be applied for mRNA delivery.
“Naturally derived membrane lipids (for example, exosomes and cell membranes) can also be applied for mRNA delivery116,249,250.”
From Lipid nanoparticles for mRNA delivery (2021) · cites this paper as [249]
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- Authors
- Yang, Z., Shi, J., Xie, J., Wang, Y., Sun, J., Liu, T., Zhao, Y., Zhao, X., Wang, X., Ma, Y., Malkoc, V., Chiang, C., Deng, W., Chen, Y., Fu, Y., Kwak, K. J., Fan, Y., Kang, C., Yin, C., Rhee, J., Bertani, P., Otero, J., Lu, W., Yun, K., Lee, A. S., Jiang, W., Teng, L., Kim, B. Y. S., & Lee, L. J.
- Affiliations
- The Ohio State University (US)
- Jilin University (CN)
- The University of Texas Southwestern Medical Center (US)
- Jinan University (CN)
- Mayo Clinic (US)
- Peking University (CN)
- Institute for Stem Cell Biology and Regenerative Medicine (US)
- Houston Methodist Research Institute (US)
- Shenzhen Bay Laboratory (CN)
- Corresponding author
- Teng, Lesheng
- Kim, Betty Y. S.
- Lee, L. James
- ORCID
- Venue
- Nature Biomedical Engineering
- Published
- 2019-12-16
- Volume
- 4
- Issue
- 1
- Pages
- 69-83
- ISSN
- 2157-846X (ISSN-L)
- PMC
- PMC7080209
- OpenAlex
- W2995128645
- Cited by
- 744
- References
- 49
- Citations by year
- 2026: 81 · 2025: 125 · 2024: 135 · 2023: 128 · 2022: 117 · 2021: 101 · 2020: 56
- FWCI
- 22.67
- Type
- journal article
- Language
- en
- Update notices
- correction (2021-06-15)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature Biomedical Engineering (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Cancer Institute (K08CA241070)
- U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (1R01NS104315)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Keywords
- exosomes, mRNA delivery, electroporation, exosome production, targeting peptides, tumor suppression, nucleic acid carriers, exosome secretion, brain tumors
- MeSH terms
- Animals, Brain Neoplasms, Cells, Cultured, Disease Models, Animal, Glioma, Humans, Mice, Inbred C57BL, RNA, Messenger, Signal Transduction, Drug Delivery Systems, Electroporation, MicroRNAs, Nanotechnology, Exosomes, HEK293 Cells
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