MicroRNA-based discovery of barriers to dedifferentiation of fibroblasts to pluripotent stem cells

Nature Structural and Molecular Biology

Volumn 20, Issue 10, 2013, Pages 1227-1237

  Judson, Robert L ^a   Greve, Tobias S ^a   Parchem, Ronald J ^a   Blelloch, Robert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 4; MESSENGER RNA; MICRORNA; MICRORNA 181; MICRORNA 294; MICRORNA 302; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DEDIFFERENTIATION; COLONY FORMATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FIBROBLAST; GENE EXPRESSION; GENETIC SCREENING; KINETICS; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL;

ANIMALS; CELL DIFFERENTIATION; FIBROBLASTS; MICE; MICRORNAS; PLURIPOTENT STEM CELLS;

EID: 84885423826     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2665     Document Type: Article

References (60)

1. Fabian, M.R. & Sonenberg, N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 19, 586-593 (2012).
2. Bartel, D.P. Review MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
3. Baek, D. et al. The impact of microRNAs on protein output. Nature 455, 64-71 (2008).
4. Selbach, M. et al. Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63 (2008).
5. Guo, H., Ingolia, N.T., Weissman, J.S. & Bartel, D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840 (2010).
6. Lim, L.P. et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769-773 (2005). (Pubitemid 40292988)
7. Leung, A.K. et al. Genome-wide identifcation of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nat. Struct. Mol. Biol. 18, 237-244 (2011).
8. Subramanyam, D. & Blelloch, R. From microRNAs to targets: pathway discovery in cell fate transitions. Curr. Opin. Genet. Dev. 21, 498-503 (2011).
9. Christodoulou, F. et al. Ancient animal microRNAs and the evolution of tissue identity. Nature 463, 1084-1088 (2010).
10. Farh, K.K. et al. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310, 1817-1821 (2005). (Pubitemid 41814382)
11. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fbroblast cultures by defned factors. Cell 126, 663-676 (2006). (Pubitemid 44233629)
12. Samavarchi-Tehrani, P. et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 7, 64-77 (2010).
13. Buganim, Y. et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209-1222 (2012).
14. Polo, J.M. et al. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 151, 1617-1632 (2012).
15. Judson, R.L., Babiarz, J.E., Venere, M. & Blelloch, R. Embryonic stem cell-specifc microRNAs promote induced pluripotency. Nat. Biotechnol. 27, 459-461 (2009).
16. Subramanyam, D. et al. Multiple targets of miR-302 and miR-372 promote reprogramming of human fbroblasts to induced pluripotent stem cells. Nat. Biotechnol. 29, 443-448 (2011).
17. Liao, B. et al. MicroRNA cluster 302-367 enhances somatic cell reprogramming by accelerating a mesenchymal-to-epithelial transition. J. Biol. Chem. 286, 17359-17364 (2011).
18. Anokye-Danso, F. et al. Highly effcient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8, 376-388 (2011).
19. Miyoshi, N. et al. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8, 633-638 (2011).
20. Banito, A. et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev. 23, 2134-2139 (2009).
21. Hu, S. et al. MicroRNA-302 increases reprogramming effciency via repression of NR2F2. Stem Cells 31, 259-268 (2013).
22. Li, Z., Yang, C., Nakashima, K. & Rana, T.M. Small RNA-mediated regulation of iPS cell generation. EMBO J. 30, 823-834 (2011).
23. Lin, S.-L. et al. Regulation of somatic cell reprogramming through inducible mir-302 expression. Nucleic Acids Res. 39, 1054-1065 (2011).
24. Wernig, M., Meissner, A., Cassady, J.P. & Jaenisch, R. c-Myc is dispensable for direct reprogramming of mouse fbroblasts. Cell Stem Cell 2, 10-12 (2008).
25. Nakagawa, M. et al. Generation of induced pluripotent stem cells without Myc from mouse and human fbroblasts. Nat. Biotechnol. 26, 101-106 (2008).
26. Blelloch, R., Venere, M., Yen, J. & Ramalho-Santos, M. Generation of induced pluripotent stem cells in the absence of drug selection. Cell Stem Cell 1, 245-247 (2007). (Pubitemid 47355331)
27. Zhang, X.D. et al. The use of strictly standardized mean difference for hit selection in primary RNA interference high-throughput screening experiments. J. Biomol. Screen. 12, 497-509 (2007). (Pubitemid 46871831)
28. Pfaff, N. et al. miRNA screening reveals a new miRNA family stimulating iPS cell generation via regulation of Meox2. EMBO Rep. 12, 1153-1159 (2011).
29. Houbaviy, H.B., Murray, M.F. & Sharp, P.A. Embryonic stem cell-specifc MicroRNAs. Dev. Cell 5, 351-358 (2003).
30. Marson, A. et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134, 521-533 (2008).
31. Chen, J. et al. Synergetic cooperation of microRNAs with transcription factors in iPS cell generation. PLoS ONE 7, e40849 (2012).
32. Melton, C., Judson, R.L. & Blelloch, R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463, 621-626 (2010).
33. O'loghlen, A. et al. MicroRNA Regulation of Cbx7 Mediates a Switch of Polycomb Orthologs during ESC Differentiation. Cell. Stem Cell 10, 33-46 (2012).
34. Shi, R. & Chiang, V. Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39, 519-525 (2005).
35. Dunning, M.J., Smith, M.L., Ritchie, M.E. & Tavaré, S. beadarray: R classes and methods for Illumina bead-based data. Bioinformatics 23, 2183-2184 (2007). (Pubitemid 47394121)
36. Smyth, G.K. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 397-420 (2005).
37. Poliseno, L. et al. Identifcation of the miR-106b~25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci. Signal. 3, ra29 (2010).
38. Cichocki, F. et al. Cutting edge: microRNA-181 promotes human NK cell development by regulating Notch signaling. J. Immunol. 187, 6171-6175 (2011).
39. Ji, J. et al. Identifcation of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology 50, 472-480 (2009).
40. Wang, Y. et al. Transforming growth factor-β regulates the sphere-initiating stem cell-like feature in breast cancer through miRNA-181 and ATM. Oncogene 30, 1470-1478 (2011).
41. Wang, B. et al. TGFbeta-mediated upregulation of hepatic miR-181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene 29, 1787-1797 (2010).
42. Grimson, A. et al. MicroRNA targeting specifcity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105 (2007). (Pubitemid 46991392)
43. Mikkelsen, T. et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 454, 49-55 (2008). (Pubitemid 351931978)
44. Wang, Y. et al. Embryonic stem cell-specifc microRNAs regulate the G1-S transition and promote rapid proliferation. Nat. Genet. 40, 1478-1483 (2008).
45. Marson, A. et al. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 3, 132-135 (2008).
46. Maherali, N. & Hochedlinger, K. Tgfbeta signal inhibition cooperates in the induction of iPSCs and replaces Sox2 and cMyc. Curr. Biol. 19, 1718-1723 (2009).
47. Ichida, J.K. et al. A small-molecule inhibitor of Tgf-beta; signaling replaces Sox2 in reprogramming by inducing Nanog. Stem Cells 5, 491-503 (2009).
48. Redmer, T. et al. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Rep. 12, 720-726 (2011).
49. Veeman, M.T., Slusarski, D.C., Kaykas, A., Louie, S.H. & Moon, R.T. Zebrafsh Prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13, 680-685 (2003). (Pubitemid 36453318)
50. Kohn, A.D. et al. Construction and characterization of a conditionally active version of the serine/threonine kinase Akt. J. Biol. Chem. 273, 11937-11943 (1998). (Pubitemid 28272103)
51. Yu, Y. et al. Stimulation of somatic cell reprogramming by Eras-Akt-Foxo1 signaling axis. Stem Cells doi:10.1002/stem.1447 (14 June 2013).
52. Liao, J. et al. Inhibition of PTEN tumor suppressor promotes the generation of induced pluripotent stem cells. Mol. Ther. 21, 1242-1250 (2013).
53. Menendez, S., Camus, S. & Belmonte, J.C.I. p53: Guardian of reprogramming. Cell Cycle 9, 3887-3891 (2010).
54. Vazquez-Martin, A. et al. Activation of AMP-activated protein kinase (AMPK) provides a metabolic barrier to reprogramming somatic cells into stem cells. Cell Cycle 11, 974-989 (2012).
55. Jin, L. et al. Ubiquitin-dependent regulation of COPII coat size and function. Nature 482, 495-500 (2012).
56. Jayawardena, T.M. et al. MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fbroblasts to cardiomyocytes. Circ. Res. 110, 1465-1473 (2012).
57. Yoo, A.S. et al. MicroRNA-mediated conversion of human fbroblasts to neurons. Nature 476, 228-231 (2011).
58. Nam, Y. et al. Reprogramming of human fbroblasts toward a cardiac fate. Proc. Natl. Acad. Sci. USA 110, 5588-5593 (2013).
59. Park, C.Y., Choi, Y.S. & McManus, M.T. Analysis of microRNA knockouts in mice. Hum. Mol. Genet. 19, R169-R175 (2010).
60. Ebert, M.S. & Sharp, P.A. Roles for MicroRNAs in conferring robustness to biological processes. Cell 149, 515-524 (2012).