Innate immune suppression enables frequent transfection with RNA encoding reprogramming proteins

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Angel, Matthew ^a   Yanik, Mehmet Fatih ^a,b  

^a Department of Electrical Engineering and Computer Science   (United States)

^b Massachusetts Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INITIATION FACTOR 2ALPHA; KRUPPEL LIKE FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN UTF1; RNA; SMALL INTERFERING RNA; STAT2 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; KRUPPEL LIKE FACTOR; NUCLEAR PROTEIN; POU5F1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; STAT2 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR SOX; UTF1 PROTEIN, HUMAN;

ARTICLE; DESENSITIZATION; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; PROTEIN EXPRESSION; ANIMAL; CELL CULTURE; CELL LINE; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; MOUSE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

RNA VIRUSES;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; FIBROBLASTS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; INTERFERON-BETA; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SOXB1 TRANSCRIPTION FACTORS; STAT2 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; TRANSFECTION;

EID: 77955352428     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011756     Document Type: Article

References (51)

1. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
2. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317.
3. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, et al. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324.
4. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
5. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
6. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, et al. (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451: 141-146.
7. Lowry WE, Richter L, Yachechko R, Pyle AD, Tchieu J, et al. (2008) Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci U S A 105: 2883-2888.
8. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, et al. (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801.
9. Jia F, Wilson KD, Sun N, Gupta DM, Huang M, et al. A nonviral minicircle vector for deriving human iPS cells. Nat Methods 7: 197-199.
10. Zhou H, Wu S, Joo JY, Zhu S, Han DW, et al. (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4: 381-384.
11. Kim D, Kim CH, Moon JI, Chung YG, Chang MY, et al. (2009) Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4: 472-476.
12. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.
13. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 59-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
14. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M, Jr. (2008) Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454: 523-527.
15. Takahasi K, Yoneyama M, Nishihori T, Hirai R, Kumeta H, et al. (2008) Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol Cell 29: 428-440.
16. Yoneyama M, Fujita T (2008) Structural mechanism of RNA recognition by the RIG-I-like receptors. Immunity 29: 178-181.
17. Schmidt A, Schwerd T, Hamm W, Hellmuth JC, Cui S, et al. (2009) 59-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc Natl Acad Sci U S A 106: 12067-12072.
18. Schlee M, Roth A, Hornung V, Hagmann CA, Wimmenauer V, et al. (2009) Recognition of 59 triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 31: 25-34.
19. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
20. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D (2004) mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 279: 12542-12550.
21. Kariko K, Buckstein M, Ni H, Weissman D (2005) Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity 23: 165-175.
22. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
23. Das HK, Das A, Ghosh-Dastidar P, Ralston RO, Yaghmai B, et al. (1981) Protein synthesis in rabbit reticulocytes. Purification and characterization of a double-stranded RNA-dependent protein synthesis inhibitor from reticulocyte lysates. J Biol Chem 256: 6491-6495.
24. Levin DH, Petryshyn R, London IM (1981) Characterization of purified double-stranded RNA-activated eIF-2 alpha kinase from rabbit reticulocytes. J Biol Chem 256: 7638-7641.
25. Bode JG, Brenndorfer ED, Haussinger D (2007) Subversion of innate host antiviral strategies by the hepatitis C virus. Arch Biochem Biophys 462: 254-265.
26. Malone RW, Felgner PL, Verma IM (1989) Cationic liposome-mediated RNA transfection. Proc Natl Acad Sci U S A 86: 6077-6081.
27. Kozak M (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44: 283-292.
28. Russell JE, Liebhaber SA (1996) The stability of human beta-globin mRNA is dependent on structural determinants positioned within its 39 untranslated region. Blood 87: 5314-5323.
29. Yu J, Russell JE (2001) Structural and functional analysis of an mRNP complex that mediates the high stability of human beta-globin mRNA. Mol Cell Biol 21: 5879-5888.
30. Angel M (2008) Extended Transient Transfection by Repeated Delivery of In Vitro-Transcribed RNA [Master's Thesis]. CambridgeMassachusetts: Massachusetts Institute of Technology. 56 p.
31. Zhao Y, Yin X, Qin H, Zhu F, Liu H, et al. (2008) Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell 3: 475-479.
32. Xu B, Zhang K, Huang Y (2009) Lin28 modulates cell growth and associates with a subset of cell cycle regulator mRNAs in mouse embryonic stem cells. RNA 15: 357-361.
33. Viswanathan SR, Daley GQ, Gregory RI (2008) Selective blockade of microRNA processing by Lin28. Science 320: 97-100.
34. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, et al. (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10: 987-993.
35. Heo I, Joo C, Cho J, Ha M, Han J, et al. (2008) Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol Cell 32: 276-284.
36. Mayr C, Hemann MT, Bartel DP (2007) Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315: 1576-1579.
37. Lee YS, Dutta A (2007) The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 21: 1025-1030.
38. Dangi-Garimella S, Yun J, Eves EM, Newman M, Erkeland SJ, et al. (2009) Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7. EMBO J 28: 347-358.
39. Shell S, Park SM, Radjabi AR, Schickel R, Kistner EO, et al. (2007) Let-7 expression defines two differentiation stages of cancer. Proc Natl Acad Sci U S A 104: 11400-11405.
40. Li O, Vasudevan D, Davey CA, Droge P (2006) High-level expression of DNA architectural factor HMGA2 and its association with nucleosomes in human embryonic stem cells. Genesis 44: 523-529.
41. Nishino J, Kim I, Chada K, Morrison SJ (2008) Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 135: 227-239.
42. Fedele M, Visone R, De Martino I, Troncone G, Palmieri D, et al. (2006) HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 9: 459-471.
43. De Martino I, Visone R, Palmieri D, Cappabianca P, Chieffi P, et al. (2007) The Mia/Cd-rap gene expression is downregulated by the high-mobility group A proteins in mouse pituitary adenomas. Endocr Relat Cancer 14: 875-886.
44. Paterson BM, Rosenberg M (1979) Efficient translation of prokaryotic mRNAs in a eukaryotic cell-free system requires addition of a cap structure. Nature 279: 692-696.
45. Melton DA, Krieg PA, Rebagliati MR, Maniatis T, Zinn K, et al. (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res 12: 7035-7056.
46. Zabner J, Fasbender AJ, Moninger T, Poellinger KA, Welsh MJ (1995) Cellular and molecular barriers to gene transfer by a cationic lipid. J Biol Chem 270: 18997-19007.
47. Kilbourne ED, Smart KM, Pokorny BA (1961) Inhibition by cortisone of the synthesis and action of interferon. Nature 190: 650-651.
48. Symons JA, Alcami A, Smith GL (1995) Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81: 551-560.
49. Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RM (1995) Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J Biol Chem 270: 15974-15978.
50. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
51. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, et al. (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25: 681-686.