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

Human Gene Therapy

Volumn 26, Issue 11, 2015, Pages 751-766

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

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b BIONTECH AG   (Germany)

^c Stemgent   (United States)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

^e WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; DESMIN; DOUBLE STRANDED RNA; KRUPPEL LIKE FACTOR 4; LIN28 PROTEIN; MESSENGER RNA; MICRORNA; MYC PROTEIN; NESTIN; NONMODIFIED MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; VIRUS MESSENGER RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DNA FINGERPRINTING; ENDOTHELIAL PROGENITOR CELL; FIBROBLAST; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNE EVASION; IMMUNOCYTOCHEMISTRY; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTRACELLULAR SPACE; KARYOTYPING; MOUSE; NEWBORN; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; RNA TRANSLATION; TERATOMA; UPREGULATION; VACCINIA VIRUS; CELL REPROGRAMMING TECHNIQUE; CYTOLOGY; GENETICS; IMMUNOLOGY; INDUCED PLURIPOTENT STEM CELL; METABOLISM;

CELLULAR REPROGRAMMING TECHNIQUES; ENDOTHELIAL PROGENITOR CELLS; FIBROBLASTS; HUMANS; IMMUNE EVASION; INDUCED PLURIPOTENT STEM CELLS; MICRORNAS; RNA, MESSENGER; TRANSFECTION; VACCINIA VIRUS;

EID: 84946919738     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2015.045     Document Type: Article

References (68)

1. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
2. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126: 663-676.
3. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
4. Brambrink T, Foreman R, Welstead GG, et al. Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2008;2:151-159.
5. Ramos-Mejia V, Montes R, Bueno C, et al. Residual expression of the reprogramming factors prevents differentiation of iPSC generated from human fibroblasts and cord blood CD34+ progenitors. PLoS ONE 2012;7:e35824.
6. Ben-David U, Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat Rev Cancer 2011;11:268-277.
7. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007;448:313-317.
8. Fusaki N, Ban H, Nishiyama A, et al. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci 2009;85:348-362.
9. Stadtfeld M, Nagaya M, Utikal J, et al. Induced pluripotent stem cells generated without viral integration. Science 2008;322:945-949.
10. Yu J, Hu K, Smuga-Otto K, et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009;324:797-801.
11. Anokye-Danso F, Trivedi CM, Juhr D, et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011;8:376-388.
12. Miyoshi N, Ishii H, Nagano H, et al. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 2011;8: 633-638.
13. Kim D, Kim CH, Moon JI, et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009;4:472-476.
14. Zhou H, Wu S, Joo JY, et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009;4:381-384.
15. Yoshioka N, Gros E, Li HR, et al. Efficient generation of human iPSCs by a synthetic selfreplicative RNA. Cell Stem Cell 2013;13:246-254.
16. Durruthy-Durruthy J, Briggs SF, Awe J, et al. Rapid and efficient conversion of integration-free human induced pluripotent stem cells to GMP-grade culture conditions. PLoS ONE 2014;9:e94231.
17. Warren L, Manos PD, Ahfeldt T, et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010;7:618-630.
18. Warren L, Ni Y, Wang J, et al. Feeder-free derivation of human induced pluripotent stem cells with messenger RNA. Sci Rep 2012;2:657.
19. Choi SM, Liu H, Chaudhari P, et al. Reprogramming of EBV-immortalized B-lymphocyte cell lines into induced pluripotent stem cells. Blood 2011;118: 1801-1805.
20. Loh YH, Agarwal S, Park IH, et al. Generation of induced pluripotent stem cells from human blood. Blood 2009;113:5476-5479.
21. Okita K, Yamakawa T, Matsumura Y, et al. An efficient nonviral method to generate integrationfree human-induced pluripotent stem cells from cord blood and peripheral blood cells. Stem Cells 2013;31:458-466.
22. Rajesh D, Dickerson SJ, Yu J, et al. Human lymphoblastoid B-cell lines reprogrammed to EBV-free induced pluripotent stem cells. Blood 2011;118: 1797-1800.
23. Staerk J, DawlatyMM, Gao Q, et al. Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 2010;7:20-24.
24. Chang WY, Lavoie JR, Kwon SY, et al. Feederindependent derivation of induced-pluripotent stem cells from peripheral blood endothelial progenitor cells. Stem Cell Res 2013;10:195-202.
25. Geti I, Ormiston ML, Rouhani F, et al. A practical and efficient cellular substrate for the generation of induced pluripotent stem cells from adults: Blood-derived endothelial progenitor cells. Stem Cells Transl Med 2012;1:855-865.
26. Martin-Ramirez J, Hofman M, van den Biggelaar M, et al. Establishment of outgrowth endothelial cells from peripheral blood. Nat Protoc 2012;7:1709-1715.
27. Lin RZ, Dreyzin A, Aamodt K, et al. Functional endothelial progenitor cells from cryopreserved umbilical cord blood. Cell Transplant 2011;20:515-522.
28. Borden EC, Sen GC, Uze G, et al. Interferons at age 50: Past, current and future impact on biomedicine. Nat Rev Drug Discov 2007;6:975-990.
29. Nallagatla SR, Toroney R, Bevilacqua PC. Regulation of innate immunity through RNA structure and the protein kinase PKR. Curr Opin Struct Biol 2011;21:119-127.
30. Wilkins C, Gale M, Jr. Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 2010;22:41-47.
31. Der SD, Zhou A, Williams BR, et al. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 1998;95:15623-15628.
32. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol 2008;8:559-568.
33. Garcia MA, Gil J, Ventoso I, et al. Impact of protein kinase PKR in cell biology: From antiviral to antiproliferative action. Microbiol Mol Biol Rev 2006;70:1032-1060.
34. Mandal PK, Rossi DJ. Reprogramming human fibroblasts to pluripotency using modified mRNA. Nat Protoc 2013;8:568-582.
35. Lee J, Sayed N, Hunter A, et al. Activation of innate immunity is required for efficient nuclear reprogramming. Cell 2012;151:547-558.
36. Angel M, Yanik MF. Innate immune suppression enables frequent transfection with RNA encoding reprogramming proteins. PLoS ONE 2010;5:e11756.
37. Arnold A, Naaldijk YM, Fabian C, et al. Reprogramming of human Huntington fibroblasts using mRNA. ISRN Cell Biol 2012;2012:12.
38. Drews K, Tavernier G, Demeester J, et al. The cytotoxic and immunogenic hurdles associated with non-viral mRNA-mediated reprogramming of human fibroblasts. Biomaterials 2012;33:4059-4068.
39. Plews JR, Li J, Jones M, et al. Activation of pluripotency genes in human fibroblast cells by a novel mRNA based approach. PLoS ONE 2010;5:e14397.
40. Tavernier G, Wolfrum K, Demeester J, et al. Activation of pluripotency-Associated genes in mouse embryonic fibroblasts by non-viral transfection with in vitro-derived mRNAs encoding Oct4, Sox2, Klf4 and cMyc. Biomaterials 2012;33:412-417.
41. Yakubov E, Rechavi G, Rozenblatt S, et al. Reprogramming of human fibroblasts to pluripotent stem cells using mRNA of four transcription factors. Biochem Biophys Res Commun 2010;394:189-193.
42. Davies MV, Elroy-Stein O, Jagus R, et al. The vaccinia virus K3L gene product potentiates translation by inhibiting double-stranded-RNA-Activated protein kinase and phosphorylation of the alpha subunit of eukaryotic initiation factor 2. J Virol 1992;66: 1943-1950.
43. Perdiguero B, Esteban M. The interferon system and vaccinia virus evasion mechanisms. J Interferon Cytokine Res 2009;29:581-598.
44. Romano PR, Zhang F, Tan SL, et al. Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: Role of complex formation and the E3 N-Terminal domain. Mol Cell Biol 1998;18:7304-7316.
45. Symons JA, Alcami A, Smith GL. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 1995;81:551-560.
46. Holtkamp S, Kreiter S, Selmi A, et al.Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood 2006;108:4009-4017.
47. Kreiter S, Konrad T, SesterM, et al. Simultaneous ex vivo quantification of antigen-specific CD4+ and CD8+ T cell responses using in vitro transcribed RNA. Cancer Immunol Immunother 2007;56:1577-1587.
48. Grudzien E, Stepinski J, Jankowska-Anyszka M, et al. Novel cap analogs for in vitro synthesis of mRNAs with high translational efficiency. RNA 2004;10:1479-1487.
49. Kowalska J, Lewdorowicz M, Zuberek J, et al. Synthesis and characterization of mRNA cap analogs containing phosphorothioate substitutions that bind tightly to eIF4E and are resistant to the decapping pyrophosphatase DcpS RNA 2008;14: 1119-1131.
50. Koste L, Beissert T, Hoff H, et al. T-cell receptor transfer into human T cells with ecotropic retroviral vectors. Gene Ther 2014;21:533-538.
51. Chen J, Wang G, Lu C, et al. Synergetic cooperation of microRNAs with transcription factors in iPS cell generation. PLoS ONE 2012;7:e40849.
52. Carey BW, Markoulaki S, Hanna JH, et al. Reprogramming factor stoichiometry influences the epigenetic state and biological properties of induced pluripotent stem cells. Cell Stem Cell 2011;9: 588-598.
53. Petrova A, Celli A, Jacquet L, et al. 3D in vitro model of a functional epidermal permeability barrier from human embryonic stem cells and induced pluripotent stem cells. Stem Cell Rep 2014;2:675-689.
54. Wang G, McCain ML, Yang L, et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat Med 2014;20:616-623.
55. Heng BC, Heinimann K, Miny P, et al. mRNA transfection-based, feeder-free, induced pluripotent stem cells derived from adipose tissue of a 50-year-old patient. Metab Eng 2013;18:9-24.
56. Kariko K, Buckstein M, Ni H, et al. Suppression of RNA recognition by Toll-like receptors: The impact of nucleoside modification and the evolutionary origin of RNA. Immunity 2005;23:165-175.
57. Judson RL, Babiarz JE, Venere M, et al. Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 2009;27:459-461.
58. Subramanyam D, Lamouille S, Judson RL, et al. Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat Biotechnol 2011;29: 443-448.
59. Yang CS, Li Z, Rana TM. microRNAs modulate iPS cell generation. RNA 2011;17:1451-1460.
60. Hanna J, Saha K, Pando B, et al. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 2009;462:595-601.
61. Ruiz S, Panopoulos AD, Herrerias A, et al. A high proliferation rate is required for cell reprogramming and maintenance of human embryonic stem cell identity. Curr Biol 2011;21:45-52.
62. Piaggio G, Rosti V, Corselli M, et al. Endothelial colonyforming cells from patients with chronic myeloproliferative disorders lack the disease-specific molecular clonality marker. Blood 2009;114:3127-3130.
63. Yoder MC, Mead LE, Prater D, et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007;109:1801-1809.
64. Han J, Yuan P, Yang H, et al. Tbx3 improves the germ-line competency of induced pluripotent stem cells. Nature 2010;463:1096-1100.
65. Maekawa M, Yamaguchi K, Nakamura T, et al. Direct reprogramming of somatic cells is promoted by maternal transcription factor Glis1. Nature 2011;474:225-229.
66. Tsubooka N, Ichisaka T, Okita K, et al. Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts. Genes Cells 2009;14:683-694.
67. Zhao Y, Yin X, Qin H, et al. Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell 2008;3:475-479.
68. Rais Y, Zviran A, Geula S, et al. Deterministic direct reprogramming of somatic cells to pluripotency. Nature 2013;502:65-70.