Notch inhibition allows oncogene-independent generation of iPS cells

Nature Chemical Biology

Volumn 10, Issue 8, 2014, Pages 632-639

  Ichida, Justin K ^a,b,i   Julia, T C W ^a,b,c   Williams, Luis A ^a,b   Carter, Ava C ^a,b   Shi, Yingxiao ⁱ   Moura, Marcelo T ^a,b   Ziller, Michael ^a,d   Singh, Sean ^a,b   Amabile, Giovanni ^e   Bock, Christoph ^a,d   Umezawa, Akihiro ^f   Rubin, Lee L ^a   Bradner, James E ^g,h   Akutsu, Hidenori ^f   Meissner, Alexander ^a,d   Eggan, Kevin ^a,b,c  

^a Harvard University   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c HARVARD UNIVERSITY   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e HARVARD STEM CELL INSTITUTE   (United States)

^f NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^g DANA FARBER CANCER INSTITUTE   (United States)

^h HARVARD MEDICAL SCHOOL   (United States)

ⁱ UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA SECRETASE; HISTONE H2AX; KRUPPEL LIKE FACTOR 4; METHYLTRANSFERASE INHIBITOR; NOTCH RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN P21; PROTEIN P53; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLASTOCYST; CELL COMMUNICATION; CELL RENEWAL; CONTROLLED STUDY; COPY NUMBER VARIATION; DOUBLE STRANDED DNA BREAK; EMBRYO; EMBRYONIC STEM CELL; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; KERATINOCYTE; KRUPPEL LIKE FACTOR 4 GENE; NICK END LABELING; NONHUMAN; NUCLEAR REPROGRAMMING; OCTAMER TRANSCRIPTION FACTOR 4 GENE; ONCOGENE; ONCOGENE C MYC; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SOMATIC CELL; TERATOMA; TRANSCRIPTION FACTOR SOX2 GENE; ULTRAVIOLET IRRADIATION;

IPS;

ANIMALS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DIPEPTIDES; DNA-BINDING PROTEINS; GENES, MYC; GENES, P53; HUMANS; KERATINOCYTES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; METHYLTRANSFERASES; MICE; ONCOGENES; PLURIPOTENT STEM CELLS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84904749034     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1552     Document Type: Article

References (45)

1. Aoi, T. et al. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 321, 699-702 (2008).
2. Nakagawa, M. et al. Generation of induced pluripotent stem cells without Myc from mouse and human fbroblasts. Nat. Biotechnol. 26, 101-106 (2008).
3. Kawamura, T. et al. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460, 1140-1144 (2009).
4. Okita, K. et al. A more efcient method to generate integration-free human iPS cells. Nat. Methods 8, 409-412 (2011).
5. Son, M.J. et al. Nicotinamide overcomes pluripotency defcits and reprogramming barriers. Stem Cells 31, 1121-1135 (2013).
6. Hong, H. et al. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460, 1132-1135 (2009).
7. Utikal, J. et al. Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 460, 1145-1148 (2009).
8. Marión, R.M. et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460, 1149-1153 (2009).
9. Li, H. et al. Te Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460, 1136-1139 (2009).
10. Li, Y. et al. Te p53-PUMA axis suppresses iPSC generation. Nat Commun. 4, 2174 (2013).
11. Lake, B.B. et al. Context-dependent enhancement of induced pluripotent stem cell reprogramming by silencing Puma. Stem Cells 30, 888-897 (2012).
12. Guo, S. et al. Nonstochastic reprogramming from a privileged somatic cell state. Cell 156, 649-662 (2014).
13. Lee, Y.L. et al. Sirtuin 1 facilitates generation of induced pluripotent stem cells from mouse embryonic fbroblasts through the miR-34a and p53 pathways. PLoS ONE 7, e45633 (2012).
14. Brosh, R. et al. p53 counteracts reprogramming by inhibiting mesenchymal-to-epithelial transition. Cell Death Difer. 20, 312-320 (2013).
15. Ye, D. et al. MiR-138 promotes induced pluripotent stem cell generation through the regulation of the p53 signaling. Stem Cells 30, 1645-1654 (2012).
16. Wang, J. et al. p53-facilitated miR-199a-3p regulates somatic cell reprogramming. Stem Cells 30, 1405-1413 (2012).
17. Zhu, S. et al. Reprogramming of human primary somatic cells by OCT4 and chemical compounds. Cell Stem Cell 7, 651-655 (2010).
18. Silva, J. et al. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 6, e253 (2008).
19. Ichida, J.K. et al. A small-molecule inhibitor of Tgf-β signaling replaces Sox2 in reprogramming by inducing Nanog. Cell Stem Cell 5, 491-503 (2009).
20. Hou, P. et al. Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341, 651-654 (2013).
21. Huangfu, D. et al. Induction of pluripotent stem cells by defned factors is greatly improved by small-molecule compounds. Nat. Biotechnol. 26, 795-797 (2008).
22. Federation, A.J., Bradner, J.E. & Meissner, A. Te use of small molecules in somatic-cell reprogramming. Trends Cell Biol. 24, 179-187 (2014).
23. Amabile, G. & Meissner, A. Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol. Med. 15, 59-68 (2009).
24. Eminli, S. et al. Diferentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat. Genet. 41, 968-976 (2009).
25. Gurdon, J.B. Te developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol. Exp. Morphol. 10, 622-640 (1962).
26. Li, J., Greco, V., Guasch, G., Fuchs, E. & Mombaerts, P. Mice cloned from skin cells. Proc. Natl. Acad. Sci. USA 104, 2738-2743 (2007).
27. Artavanis-Tsakonas, S. & Muskavitch, M.A. Notch: the past, the present, and the future. Curr. Top. Dev. Biol. 92, 1-29 (2010).
28. Bray, S.J. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689 (2006).
29. WAF1/Cip1 functions as a suppressor of malignant skin tumor formation and a determinant of keratinocyte stem-cell potential. Proc. Natl. Acad. Sci. USA 96, 9089-9094 (1999).
30. Cip1/WAF1 alters keratinocyte growth and diferentiation and promotes ras-tumor progression. Genes Dev. 10, 3065-3075 (1996).
31. Aasen, T. & Belmonte, J.C. Isolation and cultivation of human keratinocytes from skin or plucked hair for the generation of induced pluripotent stem cells. Nat. Protoc. 5, 371-382 (2010).
32. Aasen, T. et al. Efcient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat. Biotechnol. 26, 1276-1284 (2008).
33. Blanpain, C., Lowry, W.E., Pasolli, H.A. & Fuchs, E. Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev. 20, 3022-3035 (2006).
34. Bock, C. et al. Reference maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 144, 439-452 (2011).
35. Fuwa, H. et al. Divergent synthesis of multifunctional molecular probes to elucidate the enzyme specifcity of dipeptidic γ-secretase inhibitors. ACS Chem. Biol. 2, 408-418 (2007).
36. Nam, Y., Sliz, P., Song, L., Aster, J.C. & Blacklow, S.C. Structural basis for cooperativity in recruitment of MAML coactivators to Notch transcription complexes. Cell 124, 973-983 (2006).
37. Nam, Y., Weng, A.P., Aster, J.C. & Blacklow, S.C. Structural requirements for assembly of the CSL.Intracellular Notch1.Mastermind-like 1 transcriptional activation complex. J. Biol. Chem. 278, 21232-21239 (2003).
38. Lefort, K. & Dotto, G.P. Notch signaling in the integrated control of keratinocyte growth/diferentiation and tumor suppression. Semin. Cancer Biol. 14, 374-386 (2004).
39. Jones, P.H. & Watt, F.M. Separation of human epidermal stem cells from transit amplifying cells on the basis of diferences in integrin function and expression. Cell 73, 713-724 (1993).
40. Kavian, N. et al. Targeting ADAM-17/notch signaling abrogates the development of systemic sclerosis in a murine model. Arthritis Rheum. 62, 3477-3487 (2010).
41. Allen, A.S. et al. De novo mutations in epileptic encephalopathies. Nature 501, 217-221 (2013).
42. Huangfu, D. et al. Induction of pluripotent stem cells from primary human fbroblasts with only Oct4 and Sox2. Nat. Biotechnol. 26, 1269-1275 (2008).
43. Mikkelsen, T.S. et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 454, 49-55 (2008).
44. Onder, T.T. et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 483, 598-602 (2012).
45. Gore, A. et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 471, 63-67 (2011).