High-Efficiency Transfection of Primary Human and Mouse T Lymphocytes Using RNA Electroporation
Open accessAbstract
The use of nonviral gene transfer methods in primary lymphocytes has been hampered by low gene transfer efficiency and high transfection-related toxicity. In this report, high gene transfection efficiency with low transfection-related toxicity was achieved by electroporation using in vitro-transcribed mRNA. Using these methods, >90% transgene expression with >80% viable cells was observed in stimulated primary human and murine T lymphocytes transfected with GFP or mCD62L. Electroporation of unstimulated human PBMCs or murine splenocytes with GFP RNA yielded 95 and 56% GFP+ cells, respectively. Electroporation of mRNA for NY-ESO-1, MART-1, and p53 antigen-specific TCRs into human T lymphocytes redirected these lymphocytes to recognize melanoma cell lines in an MHC-restricted manner. The onset of gene expression was rapid (within 30 min) and durable (up to 7 days postelectroporation) using both GFP and TCR-mediated recognition of target cells. There was no adverse effect observed on the T lymphocytes subjected to RNA electroporation evaluated by cell growth rate, annexin-V staining of apoptotic cells, BrdU incorporation, tumor antigen-specific recognition or antigen-specific TCR affinity. The results of this study indicate that mRNA electroporation provides a powerful tool to introduce genes into both human and murine primary T lymphocytes.
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The improvement of RNA kinetics by these modifications may also be of interest for other cellular settings, such as T cells, B cells, and muscle cells.
“In principle, the improvement of RNA kinetics by these modifications is not restricted to DCs but is similar in K562 cells and may also be of interest for other cellular settings, such as T cells, 43 B cells, 44 and muscle cells, 45 which are attractive host cells for the expression of IVT RNA-encoded proteins.”
From Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells (2006) · cites this paper as [43]
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Zhao, H., Hemmi, H., Akira, S., Cheng, S. H., Scheule, R. K., & Yew, N. S. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2003.11.012 · Cited by 85 · see citing works
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Research works printed but not linked: 29
- [1]1. Rudoll, T. ... High-efficiency retroviral vector mediated gene transfer into human peripheral blood CD4+ T lymphocytes Gene Ther. 1996; 3:695 PubMed Google Scholar
- [2]2. Costello, E. ∙ Munoz, M. ∙ Buetti, E. ... Gene transfer into stimulated and unstimulated T lymphocytes by HIV-1-derived lentiviral vectors Gene Ther. 2000; 7:596 Crossref Scopus (76) PubMed Google Scholar
- [3]3. Ferber, D. Gene therapy: safer and virus-free? Science. 2001; 294:1638 Crossref Scopus (289) PubMed Google Scholar
- [4]4. Bell, M.P. ∙ Huntoon, C.J. ∙ Graham, D. ... The analysis of costimulatory receptor signaling cascades in normal T lymphocytes using in vitro gene transfer and reporter gene analysis Nat. Med. 2001; 7:1155 Crossref Scopus (27) PubMed Google Scholar
- [5]5. Van Tendeloo, V.F. ... High-level transgene expression in primary human T lymphocytes and adult bone marrow CD34+ cells via electroporation-mediated gene delivery Gene Ther. 2000; 7:1431 Crossref Scopus (55) PubMed Google Scholar
- [6]6. Cotten, M. ∙ Saltik, M. Intracellular delivery of lipopolysaccharide during DNA transfection activates a lipid A-dependent cell death response that can be prevented by polymyxin B Hum. Gene Ther. 1997; 8:555 Crossref Scopus (15) PubMed Google Scholar
- [7]7. Ebert, O. ... Lymphocyte apoptosis: induction by gene transfer techniques Gene Ther. 1997; 4:296 Crossref Scopus (59) PubMed Google Scholar
- [8]8. Lai, W. ∙ Chang, C.H. ∙ Farber, D.L. Gene transfection and expression in resting and activated murine CD4 T cell subsets J. Immunol. Methods. 2003; 282:93 Crossref Scopus (41) PubMed Google Scholar
- [9]9. Sullenger, B.A. ∙ Gilboa, E. Emerging clinical applications of RNA Nature. 2002; 418:252 Crossref Scopus (289) PubMed Google Scholar
- [10]10. Van Tendeloo, V.F. ... Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells Blood. 2001; 98:49 Crossref Scopus (423) PubMed Google Scholar
- [11]11. Zhao, Y. ∙ Boczkowski, E. ∙ Nair, S.K. ... Inhibition of invariant chain expression in dendritic cells presenting endogenous antigens stimulates CD4+ T-cell responses and tumor immunity Blood. 2003; 102:4137 Crossref Scopus (0) PubMed Google Scholar
- [12]12. Zhao, Y. ∙ Zheng, Z. ∙ Robbins, P. ... Primary human lymphocytes retrovirally transduced with NY-ESO-1 antigen specific TCR genes recognize and kill NY-ESO-1 positive melanoma as well as other tumors Blood. 2003; 102:2752 Crossref Scopus (35) Google Scholar
- [13]13. Morgan, R.A. ... High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens J. Immunol. 2003; 171:3287 Crossref Scopus (196) PubMed Google Scholar
- [14]14. Overwijk, W.W. ... Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells J. Exp. Med. 2003; 198:569 Crossref Scopus (802) PubMed Google Scholar
- [15]15. Gattinoni, L. ∙ Klebanoff, C.A. ∙ Palmer, D.C. ... Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells J. Clin. Invest. 2005; 115:1616 Crossref Scopus (805) PubMed Google Scholar
- [16]16. Theobald, M. ∙ Biggs, J. ∙ Dittmer, D. ... Targeting p53 as a general tumor antigen Proc. Natl. Acad. Sci. USA. 1995; 92:11993 Crossref Scopus (279) PubMed Google Scholar
- [17]17. Smits, E. ... RNA-based gene transfer for adult stem cells and T cells Leukemia. 2004; 18:1898 Crossref Scopus (54) PubMed Google Scholar
- [19]19. Dudley, M.E. ... Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes Science. 2002; 298:850 Crossref Scopus (2493) PubMed Google Scholar
- [20]20. Rosenberg, S.A. ∙ Dudley, M.E. Cancer regression in patients with metastatic melanoma after the transfer of autologous antitumor lymphocytes Proc. Natl. Acad. Sci. USA. 2004; 101(Suppl. 2):14639 Crossref Scopus (322) PubMed Google Scholar
- [21]21. Yee, C. ... Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells Proc. Natl. Acad. Sci. USA. 2002; 99:16168 Crossref Scopus (1033) PubMed Google Scholar
- [22]22. Liu, K. ∙ Rosenberg, S.A. Interleukin-2-independent proliferation of human melanoma-reactive T lymphocytes transduced with an exogenous IL-2 gene is stimulation dependent J. Immunother. 2003; 26:190 Crossref Scopus (33) PubMed Google Scholar
- [23]23. Tan, J.T. ... IL-7 is critical for homeostatic proliferation and survival of naive T cells Proc. Natl. Acad. Sci. USA. 2001; 98:8732 Crossref Scopus (807) PubMed Google Scholar
- [24]24. Topp, M.S. ∙ Riddell, S.R. ∙ Akatsuka, Y. ... Restoration of CD28 expression in CD28− CD8+ memory effector T cells reconstitutes antigen-induced IL-2 production J. Exp. Med. 2003; 198:947 Crossref Scopus (131) PubMed Google Scholar
- [25]25. Ochsenbein, A.F. ... CD27 expression promotes long-term survival of functional effector-memory CD8+ cytotoxic T lymphocytes in HIV-infected patients J. Exp. Med. 2004; 200:1407 Crossref Scopus (113) PubMed Google Scholar
- [26]26. Lee, S.J. ... 4-1BB and OX40 dual costimulation synergistically stimulates primary specific CD8 T cells for robust effector function J. Immunol. 2004; 173:3002 Crossref Scopus (107) PubMed Google Scholar
- [27]27. Walcheck, B. ... Neutrophil rolling altered by inhibition of L-selectin shedding in vitro Nature. 1996; 380:720 Crossref Scopus (271) PubMed Google Scholar
- [28]28. Zheng, W.P. ... Up-regulation of Hlx in immature Th cells induces IFN-gamma expression J. Immunol. 2004; 172:114 Crossref Scopus (45) PubMed Google Scholar
- [29]29. Rufer, N. ∙ Migliaccio, M. ∙ Antonchuk, J. ... Transfer of the human telomerase reverse transcriptase (TERT) gene into T lymphocytes results in extension of replicative potential Blood. 2001; 98:597 Crossref Scopus (157) PubMed Google Scholar
- [30]30. Fratantoni, J.C. ∙ Dzekunov, S. ∙ Singh, V. ... A non-viral gene delivery system designed for clinical use Cytotherapy. 2003; 5:208
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- Authors
- Zhao, Y., Zheng, Z., Cohen, C. J., Gattinoni, L., Palmer, D. C., Restifo, N. P., Rosenberg, S. A., & Morgan, R. A.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Morgan, Richard A.
- ORCID
- Venue
- Molecular Therapy
- Publisher
- Elsevier BV
- Published
- 2006-01
- Volume
- 13
- Issue
- 1
- Pages
- 151-159
- ISSN
- 1525-0016 (ISSN-L)
- PMC
- PMC1473967
- OpenAlex
- W2021032653
- Cited by
- 283
- References
- 1
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 9 · 2023: 20 · 2022: 19 · 2021: 22 · 2020: 14 · 2019: 13 · 2018: 22 · 2017: 16 · 2016: 18 · 2015: 14 · 2014: 14 · 2013: 15 · 2012: 15
- FWCI
- 5.31
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Molecular Therapy (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (Z99 CA999999)
- National Cancer Institute (Z01BC010763)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- RNA electroporation, mRNA electroporation, T cells, transfection efficiency, nonviral gene transfer, T cell receptor gene transfer, NY-ESO-1, Melan-A, p53, transfection toxicity, primary human T cells
- MeSH terms
- Animals, Antigens, Neoplasm, Cell Survival, Cells, Cultured, Humans, Membrane Proteins, Neoplasm Proteins, Receptors, Antigen, T-Cell, RNA, Messenger, Spleen, T-Lymphocytes, Transfection, Tumor Suppressor Protein p53, Apoptosis, Electroporation, L-Selectin, Cell Proliferation, Green Fluorescent Proteins, Mice, MART-1 Antigen
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