Efficient Reprogramming of Human Fibroblasts and Blood-Derived Endothelial Progenitor Cells Using Nonmodified RNA for Reprogramming and Immune Evasion

Poleganov, Marco Alexander; Eminli, Sarah; Beissert, Tim; Herz, Stephanie; Moon, Jung-Il; Goldmann, Johanna; Beyer, Arianne; Heck, Rosario; Burkhart, Isabell; Barea Roldan, Diana; Türeci, Özlem; Yi, Kevin; Hamilton, Brad; Sahin, Ugur

doi:10.1089/hum.2015.045

Cited by 77

The DOI matches its Crossref record; 9 of the 9 references it cites were found in a registry or an index.

Efficient Reprogramming of Human Fibroblasts and Blood-Derived Endothelial Progenitor Cells Using Nonmodified RNA for Reprogramming and Immune Evasion

Poleganov, Marco Alexander, Eminli, Sarah, Beissert, Tim, Herz, Stephanie, Moon, Jung-Il, Goldmann, Johanna, Beyer, Arianne, Heck, Rosario, Burkhart, Isabell, Barea Roldan, Diana, Türeci, Özlem, Yi, Kevin, Hamilton, Brad, Sahin, Ugur·2015·Human Gene Therapy

DOI 10.1089/hum.2015.045

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Abstract

mRNA reprogramming results in the generation of genetically stable induced pluripotent stem (iPS) cells while avoiding the risks of genomic integration. Previously published mRNA reprogramming protocols have proven to be inconsistent and time-consuming and mainly restricted to fibroblasts, thereby demonstrating the need for a simple but reproducible protocol applicable to various cell types. So far there have been no published reports using mRNA to reprogram any cell type derived from human blood. Nonmodified synthetic mRNAs are immunogenic and activate cellular defense mechanisms, which can lead to cell death and inhibit mRNA translation upon repetitive transfection. Hence, to overcome RNA-related toxicity we combined nonmodified reprogramming mRNAs (OCT4, SOX2, KLF4, cMYC, NANOG, and LIN28 [OSKMNL]) with immune evasion mRNAs (E3, K3, and B18R [EKB]) from vaccinia virus. Additionally, we included mature, double-stranded microRNAs (miRNAs) from the 302/367 cluster, which are known to enhance the reprogramming process, to develop a robust reprogramming protocol for the generation of stable iPS cell lines from both human fibroblasts and human blood-outgrowth endothelial progenitor cells (EPCs). Our novel combination of RNAs enables the cell to tolerate repetitive transfections for the generation of stable iPS cell colonies from human fibroblasts within 11 days while requiring only four transfections. Moreover, our method resulted in the first known mRNA-vectored reprogramming of human blood-derived EPCs within 10 days while requiring only eight daily transfections.

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Cellular reprogramming of human fibroblasts to iPSCs with mRNA-encoded transcription factors is considered to benefit from prolonged mRNA stability.
“Second, we studied the efficiency and robustness of cellular reprogramming of human fibroblasts to iPSCs with mRNA-encoded transcription factors, which is considered to benefit from prolonged mRNA stability.17,51”
From Improving mRNA-Based Therapeutic Gene Delivery by Expression-Augmenting 3′ UTRs Identified by Cellular Library Screening (2019) · cites this paper as [17]

Suppression of RNA Recognition by Toll-like Receptors: The Impact of Nucleoside Modification and the Evolutionary Origin of RNA
Karikó, K., Buckstein, M., Ni, H., & Weissman, D. (2005) · Immunity · doi:10.1016/j.immuni.2005.06.008 · Cited by 2,728
Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA
Warren, L., Manos, P. D., Ahfeldt, T., Loh, Y.-H., Li, H., Lau, F., Ebina, W., Mandal, P. K., Smith, Z. D., Meissner, A., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.012 · Cited by 2,662
Interferon-inducible antiviral effectors
Sadler, A. J., & Williams, B. R. G. (2008) · Nature Reviews Immunology · doi:10.1038/nri2314 · Cited by 2,160
The tumorigenicity of human embryonic and induced pluripotent stem cells
Ben-David, U., & Benvenisty, N. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3034 · Cited by 889
Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells
Holtkamp, S., Kreiter, S., Selmi, A., Simon, P., Koslowski, M., Huber, C., Türeci, O., & Sahin, U. (2006) · Blood · doi:10.1182/blood-2006-04-015024 · Cited by 625
Deterministic direct reprogramming of somatic cells to pluripotency
Rais, Y., Zviran, A., Geula, S., Gafni, O., Chomsky, E., Viukov, S., Mansour, A. A., Caspi, I., Krupalnik, V., Zerbib, M., et al. (2013) · Nature · doi:10.1038/nature12587 · Cited by 522
Efficient generation of human iPSCs by a synthetic self-replicative RNA
Yoshioka, N., Gros, E., Li, H.-R., Kumar, S., Deacon, D. C., Maron, C., Muotri, A. R., Chi, N. C., Fu, X.-D., Yu, B. D., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.06.001 · Cited by 312
Feeder-Free Derivation of Human Induced Pluripotent Stem Cells with Messenger RNA
Warren, L., Ni, Y., Wang, J., & Guo, X. (2012) · Scientific Reports · doi:10.1038/srep00657 · Cited by 154
Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts
Tsubooka, N., Ichisaka, T., Okita, K., Takahashi, K., Nakagawa, M., & Yamanaka, S. (2009) · Genes to Cells · doi:10.1111/j.1365-2443.2009.01301.x · Cited by 154

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Research works printed but not linked: 59

10.1016/j.cell.2007.11.019 · DOI · Paper page
10.1016/j.cell.2006.07.024 · DOI · Paper page
10.1126/science.1151526 · DOI · Paper page
10.1016/j.stem.2008.01.004 · DOI
10.1371/journal.pone.0035824 · DOI
10.1038/nature05934 · DOI
10.2183/pjab.85.348 · DOI · Paper page
10.1126/science.1162494 · DOI · Paper page
10.1126/science.1172482 · DOI · Paper page
10.1016/j.stem.2011.03.001 · DOI
10.1016/j.stem.2011.05.001 · DOI
10.1016/j.stem.2009.05.005 · DOI · Paper page
10.1016/j.stem.2009.04.005 · DOI · Paper page
10.1371/journal.pone.0094231 · DOI
10.1182/blood-2011-03-340620 · DOI
10.1182/blood-2009-02-204800 · DOI · Paper page
10.1002/stem.1293 · DOI
10.1182/blood-2011-01-332064 · DOI
10.1016/j.stem.2010.06.002 · DOI
10.1016/j.scr.2012.11.006 · DOI
10.5966/sctm.2012-0093 · DOI
10.1038/nprot.2012.093 · DOI
10.3727/096368910X532729 · DOI
10.1038/nrd2422 · DOI · Paper page
10.1016/j.sbi.2010.11.003 · DOI
10.1016/j.coi.2009.12.003 · DOI
10.1073/pnas.95.26.15623 · DOI
10.1128/MMBR.00027-06 · DOI · Paper page
10.1038/nprot.2013.019 · DOI
10.1016/j.cell.2012.09.034 · DOI
10.1371/journal.pone.0011756 · DOI
10.5402/2012/124878 · DOI
10.1016/j.biomaterials.2012.02.025 · DOI
10.1371/journal.pone.0014397 · DOI
10.1016/j.biomaterials.2011.09.062 · DOI
10.1016/j.bbrc.2010.02.150 · DOI
10.1128/jvi.66.4.1943-1950.1992 · DOI
10.1089/jir.2009.0073 · DOI
10.1128/MCB.18.12.7304 · DOI
10.1016/0092-8674(95)90076-4 · DOI
10.1007/s00262-007-0302-7 · DOI
10.1261/rna.7380904 · DOI
10.1261/rna.990208 · DOI
10.1038/gt.2014.25 · DOI
10.1371/journal.pone.0040849 · DOI
10.1016/j.stem.2011.11.003 · DOI
10.1016/j.stemcr.2014.03.009 · DOI
10.1038/nm.3545 · DOI · Paper page
10.1016/j.ymben.2013.02.004 · DOI
10.1038/nbt.1535 · DOI
10.1038/nbt.1862 · DOI
10.1261/rna.2664111 · DOI
10.1038/nature08592 · DOI · Paper page
10.1016/j.cub.2010.11.049 · DOI
10.1182/blood-2008-12-190991 · DOI
10.1182/blood-2006-08-043471 · DOI
10.1038/nature08735 · DOI · Paper page
10.1038/nature10106 · DOI
10.1016/j.stem.2008.10.002 · DOI · Paper page

Sorted by citations

Improving mRNA-Based Therapeutic Gene Delivery by Expression-Augmenting 3′ UTRs Identified by Cellular Library Screening
Orlandini von Niessen, A. G., Poleganov, M. A., Rechner, C., Plaschke, A., Kranz, L. M., Fesser, S., Diken, M., Löwer, M., Vallazza, B., Beissert, T., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2018.12.011 · Cited by 365
Self-citation
Strategies for controlling the innate immune activity of conventional and self-amplifying mRNA therapeutics: Getting the message across
Minnaert, A.-K., Vanluchene, H., Verbeke, R., Lentacker, I., De Smedt, S. C., Raemdonck, K., Sanders, N. N., & Remaut, K. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113900 · Cited by 157
Nanomedicine-Based Approaches for mRNA Delivery
Uchida, S., Perche, F., Pichon, C., & Cabral, H. (2020) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.0c00618 · Cited by 139
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Meng, C., Chen, Z., Li, G., Welte, T., & Shen, H. (2021) · Advanced Therapeutics · doi:10.1002/adtp.202000099 · Cited by 130
Viral and Synthetic RNA Vector Technologies and Applications
Schott, J. W., Morgan, M., Galla, M., & Schambach, A. (2016) · Molecular Therapy · doi:10.1038/mt.2016.143 · Cited by 76

Authors: Poleganov, M. A., Eminli, S., Beissert, T., Herz, S., Moon, J.-I., Goldmann, J., Beyer, A., Heck, R., Burkhart, I., Barea Roldan, D., Türeci, Ö., Yi, K., Hamilton, B., & Sahin, U.
Affiliations: Johannes Gutenberg University Mainz
Stemgent, Cambridge, Massachusetts.
Whitehead Institute for Biomedical Research
Venue: Human Gene Therapy
Publisher: SAGE Publications
Published: 2015-08-27
Volume: 26
Issue: 11
Pages: 751-766
ISSN: 1043-0342
1557-7422
DOI: 10.1089/hum.2015.045
Cited by: 77
References: 9
Language: en
Licence: journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)

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Efficient Reprogramming of Human Fibroblasts and Blood-Derived Endothelial Progenitor Cells Using Nonmodified RNA for Reprogramming and Immune Evasion

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