The let-7/LIN-41 pathway regulates reprogramming to human induced pluripotent stem cells by controlling expression of prodifferentiation genes

Cell Stem Cell

Volumn 14, Issue 1, 2014, Pages 40-52

  Worringer, Kathleen A ^a,b   Rand, Tim A ^a,b   Hayashi, Yohei ^a,b   Sami, Salma ^a,b   Takahashi, Kazutoshi ^c   Tanabe, Koji ^c   Narita, Megumi ^c   Srivastava, Deepak ^a,b,d   Yamanaka, Shinya ^a,b,c,d  

^a GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^b Roddenberry Center for Stem Cell Biology and Medicine at Gladstone   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; KRUPPEL LIKE FACTOR 4; LIN 41 PROTEIN; MICRORNA; MICRORNA LET 7; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE TARGETING; HUMAN; HUMAN CELL; LINEAR ENERGY TRANSFER; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; ONCOGENE C MYC; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EARLY GROWTH RESPONSE PROTEIN 1; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICRORNAS; NUCLEAR REPROGRAMMING; OCTAMER TRANSCRIPTION FACTOR-3; PROTO-ONCOGENE PROTEINS C-MYC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SOXB1 TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84891742725     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.11.001     Document Type: Article

References (70)

1. A. Banito, and J. Gil Induced pluripotent stem cells and senescence: learning the biology to improve the technology EMBO Rep. 11 2010 353 359
2. B. Boyerinas, S.M. Park, A. Hau, A.E. Murmann, and M.E. Peter The role of let-7 in cell differentiation and cancer Endocr. Relat. Cancer 17 2010 F19 F36
3. X.M. Cao, R.A. Koski, A. Gashler, M. McKiernan, C.F. Morris, R. Gaffney, R.V. Hay, and V.P. Sukhatme Identification and characterization of the Egr-1 gene product, a DNA-binding zinc finger protein induced by differentiation and growth signals Mol. Cell. Biol. 10 1990 1931 1939
4. J.H. Carter, J.M. Lefebvre, D.L. Wiest, and W.G. Tourtellotte Redundant role for early growth response transcriptional regulators in thymocyte differentiation and survival J. Immunol. 178 2007 6796 6805
5. H.M. Chang, N.J. Martinez, J.E. Thornton, J.P. Hagan, K.D. Nguyen, and R.I. Gregory Trim71 cooperates with microRNAs to repress Cdkn1a expression and promote embryonic stem cell proliferation Nat. Com. 3 2012 923
6. J. Chen, F. Lai, and L. Niswander The ubiquitin ligase mLin41 temporally promotes neural progenitor cell maintenance through FGF signaling Genes Dev. 26 2012 803 815
7. J. Chen, H. Liu, J. Liu, J. Qi, B. Wei, J. Yang, H. Liang, Y. Chen, J. Chen, and Y. Wu et al. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs Nat. Genet. 45 2013 34 42
8. S. Collins, L.A. Wolfraim, C.G. Drake, M.R. Horton, and J.D. Powell Cutting Edge: TCR-induced NAB2 enhances T cell function by coactivating IL-2 transcription J. Immunol. 177 2006 8301 8305
9. R.J. Deshaies, and C.A. Joazeiro RING domain E3 ubiquitin ligases Annu. Rev. Biochem. 78 2009 399 434
10. A. Dinkel, K. Warnatz, B. Ledermann, A. Rolink, P.F. Zipfel, K. Bürki, and H. Eibel The transcription factor early growth response 1 (Egr-1) advances differentiation of pre-B and immature B cells J. Exp. Med. 188 1998 2215 2224
11. Q. Dong, P. Meng, T. Wang, W. Qin, W. Qin, F. Wang, J. Yuan, Z. Chen, A. Yang, and H. Wang MicroRNA let-7a inhibits proliferation of human prostate cancer cells in vitro and in vivo by targeting E2F2 and CCND2 PLoS ONE 5 2010 e10147
12. I. Dubchak, M. Munoz, A. Poliakov, N. Salomonis, S. Minovitsky, R. Bodmer, and A.C. Zambon Whole-Genome rVISTA: a tool to determine enrichment of transcription factor binding sites in gene promoters from transcriptomic data Bioinformatics 29 2013 2059 2061
13. S.A. Edwards, T. Darland, R. Sosnowski, M. Samuels, and E.D. Adamson The transcription factor, Egr-1, is rapidly modulated in response to retinoic acid in P19 embryonal carcinoma cells Dev. Biol. 148 1991 165 173
14. G. Fragola, P.L. Germain, P. Laise, A. Cuomo, A. Blasimme, F. Gross, E. Signaroldi, G. Bucci, C. Sommer, and G. Pruneri et al. Cell reprogramming requires silencing of a core subset of polycomb targets PLoS Genet. 9 2013 e1003292
15. A. Gashler, and V.P. Sukhatme Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors Prog. Nucleic Acid Res. Mol. Biol. 50 1995 191 224
16. A. Gaspar-Maia, Z.A. Qadeer, D. Hasson, K. Ratnakumar, N.A. Leu, G. Leroy, S. Liu, C. Costanzi, D. Valle-Garcia, and C. Schaniel et al. MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency Nat. Com. 4 2013 1565
17. J. Hanna, K. Saha, B. Pando, J. van Zon, C.J. Lengner, M.P. Creyghton, A. van Oudenaarden, and R. Jaenisch Direct cell reprogramming is a stochastic process amenable to acceleration Nature 462 2009 595 601
18. D.T. Harris, and H.R. Horvitz MAB-10/NAB acts with LIN-29/EGR to regulate terminal differentiation and the transition from larva to adult in C. elegans Development 138 2011 4051 4062
19. S.E. Hunter, E.F. Finnegan, D.G. Zisoulis, M.T. Lovci, K.V. Melnik-Martinez, G.W. Yeo, and A.E. Pasquinelli Functional genomic analysis of the let-7 regulatory network in Caenorhabditis elegans PLoS Genet. 9 2013 e1003353
20. S.M. Johnson, H. Grosshans, J. Shingara, M. Byrom, R. Jarvis, A. Cheng, E. Labourier, K.L. Reinert, D. Brown, and F.J. Slack RAS is regulated by the let-7 microRNA family Cell 120 2005 635 647
21. C.D. Johnson, A. Esquela-Kerscher, G. Stefani, M. Byrom, K. Kelnar, D. Ovcharenko, M. Wilson, X. Wang, J. Shelton, and J. Shingara et al. The let-7 microRNA represses cell proliferation pathways in human cells Cancer Res. 67 2007 7713 7722
22. H.H. Kim, Y. Kuwano, S. Srikantan, E.K. Lee, J.L. Martindale, and M. Gorospe HuR recruits let-7/RISC to repress c-Myc expression Genes Dev. 23 2009 1743 1748
23. K. Krishnaraju, H.Q. Nguyen, D.A. Liebermann, and B. Hoffman The zinc finger transcription factor Egr-1 potentiates macrophage differentiation of hematopoietic cells Mol. Cell. Biol. 15 1995 5499 5507
24. M.S. Kumar, J. Lu, K.L. Mercer, T.R. Golub, and T. Jacks Impaired microRNA processing enhances cellular transformation and tumorigenesis Nat. Genet. 39 2007 673 677
25. J. Kumbrink, K.H. Kirsch, and J.P. Johnson EGR1, EGR2, and EGR3 activate the expression of their coregulator NAB2 establishing a negative feedback loop in cells of neuroectodermal and epithelial origin J. Cell. Biochem. 111 2010 207 217
26. J. Lanoix, A. Mullick, Y. He, R. Bravo, and D. Skup Wild-type egr1/Krox24 promotes and dominant-negative mutants inhibit, pluripotent differentiation of p19 embryonal carcinoma cells Oncogene 17 1998 2495 2504
27. P. Laslo, C.J. Spooner, A. Warmflash, D.W. Lancki, H.J. Lee, R. Sciammas, B.N. Gantner, A.R. Dinner, and H. Singh Multilineage transcriptional priming and determination of alternate hematopoietic cell fates Cell 126 2006 755 766
28. N. Le, R. Nagarajan, J.Y. Wang, J. Svaren, C. LaPash, T. Araki, R.E. Schmidt, and J. Milbrandt Nab proteins are essential for peripheral nervous system myelination Nat. Neurosci. 8 2005 932 940
29. Y.S. Lee, and A. Dutta The tumor suppressor microRNA let-7 represses the HMGA2 oncogene Genes Dev. 21 2007 1025 1030
30. A. Legesse-Miller, O. Elemento, S.J. Pfau, J.J. Forman, S. Tavazoie, and H.A. Coller let-7 Overexpression leads to an increased fraction of cells in G2/M, direct down-regulation of Cdc34, and stabilization of Wee1 kinase in primary fibroblasts J. Biol. Chem. 284 2009 6605 6609
31. V. Lejard, F. Blais, M.J. Guerquin, A. Bonnet, M.A. Bonnin, E. Havis, M. Malbouyres, C.B. Bidaud, G. Maro, and P. Gilardi-Hebenstreit et al. EGR1 and EGR2 involvement in vertebrate tendon differentiation J. Biol. Chem. 286 2011 5855 5867
32. Y.C. Lin, L.C. Hsieh, M.W. Kuo, J. Yu, H.H. Kuo, W.L. Lo, R.J. Lin, A.L. Yu, and W.H. Li Human TRIM71 and its nematode homologue are targets of let-7 microRNA and its zebrafish orthologue is essential for development Mol. Biol. Evol. 24 2007 2525 2534
33. M. Luo, T. Ling, W. Xie, H. Sun, Y. Zhou, Q. Zhu, M. Shen, L. Zong, G. Lyu, and Y. Zhao et al. NuRD blocks reprogramming of mouse somatic cells into pluripotent stem cells Stem Cells 31 2013 1278 1286
34. M. Maekawa, and S. Yamanaka Glis1, a unique pro-reprogramming factor, may facilitate clinical applications of iPSC technology Cell Cycle 10 2011 3613 3614
35. N. Maherali, R. Sridharan, W. Xie, J. Utikal, S. Eminli, K. Arnold, M. Stadtfeld, R. Yachechko, J. Tchieu, and R. Jaenisch et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution Cell Stem Cell 1 2007 55 70
36. B.R. Maller Schulman, X. Liang, C. Stahlhut, C. DelConte, G. Stefani, and F.J. Slack The let-7 microRNA target gene, Mlin41/Trim71 is required for mouse embryonic survival and neural tube closure Cell Cycle 7 2008 3935 3942
37. F. Mayr, and U. Heinemann Mechanisms of Lin28-mediated miRNA and mRNA regulation - a structural and functional perspective Int. J. Mol. Sci. 14 2013 16532 16553
38. C. Mayr, M.T. Hemann, and D.P. Bartel Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation Science 315 2007 1576 1579
39. A. Meissner, M. Wernig, and R. Jaenisch Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells Nat. Biotechnol. 25 2007 1177 1181
40. C. Melton, R.L. Judson, and R. Blelloch Opposing microRNA families regulate self-renewal in mouse embryonic stem cells Nature 463 2010 621 626
41. M. Nakagawa, M. Koyanagi, K. Tanabe, K. Takahashi, T. Ichisaka, T. Aoi, K. Okita, Y. Mochiduki, N. Takizawa, and S. Yamanaka Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts Nat. Biotechnol. 26 2008 101 106
42. M.A. Newman, J.M. Thomson, and S.M. Hammond Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing RNA 14 2008 1539 1549
43. H.Q. Nguyen, B. Hoffman-Liebermann, and D.A. Liebermann The zinc finger transcription factor Egr-1 is essential for and restricts differentiation along the macrophage lineage Cell 72 1993 197 209
44. F. O'Farrell, S.S. Esfahani, Y. Engstrom, and P. Kylsten Regulation of the Drosophila lin-41 homologue dappled by let-7 reveals conservation of a regulatory mechanism within the LIN-41 subclade Dev. Dynam 237 2008 196 208
45. K. Okita, T. Ichisaka, and S. Yamanaka Generation of germline-competent induced pluripotent stem cells Nature 448 2007 313 317
46. I.H. Park, R. Zhao, J.A. West, A. Yabuuchi, H. Huo, T.A. Ince, P.H. Lerou, M.W. Lensch, and G.Q. Daley Reprogramming of human somatic cells to pluripotency with defined factors Nature 451 2008 141 146
47. V. Pasque, A. Radzisheuskaya, A. Gillich, R.P. Halley-Stott, M. Panamarova, M. Zernicka-Goetz, M.A. Surani, and J.C. Silva Histone variant macroH2A marks embryonic differentiation in vivo and acts as an epigenetic barrier to induced pluripotency J. Cell Sci. 125 2012 6094 6104
48. A. Plechanovová, E.G. Jaffray, M.H. Tatham, J.H. Naismith, and R.T. Hay Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis Nature 489 2012 115 120
49. Y. Rais, A. Zviran, S. Geula, O. Gafni, E. Chomsky, S. Viukov, A.A. Mansour, I. Caspi, V. Krupalnik, and M. Zerbib et al. Deterministic direct reprogramming of somatic cells to pluripotency Nature 502 2013 65 70
50. B.J. Reinhart, F.J. Slack, M. Basson, A.E. Pasquinelli, J.C. Bettinger, A.E. Rougvie, H.R. Horvitz, and G. Ruvkun The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans Nature 403 2000 901 906
51. B. Robertson, A.B. Dalby, J. Karpilow, A. Khvorova, D. Leake, and A. Vermeulen Specificity and functionality of microRNA inhibitors Silence 1 2010 10
52. A. Rybak, H. Fuchs, L. Smirnova, C. Brandt, E.E. Pohl, R. Nitsch, and F.G. Wulczyn A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment Nat. Cell Biol. 10 2008 987 993
53. A. Rybak, H. Fuchs, K. Hadian, L. Smirnova, E.A. Wulczyn, G. Michel, R. Nitsch, D. Krappmann, and F.G. Wulczyn The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2 Nat. Cell Biol. 11 2009 1411 1420
54. V.B. Sampson, N.H. Rong, J. Han, Q. Yang, V. Aris, P. Soteropoulos, N.J. Petrelli, S.P. Dunn, and L.J. Krueger MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells Cancer Res. 67 2007 9762 9770
55. B.R. Schulman, A. Esquela-Kerscher, and F.J. Slack Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis Dev. Dynam. 234 2005 1046 1054
56. B.R. Sevetson, J. Svaren, and J. Milbrandt A novel activation function for NAB proteins in EGR-dependent transcription of the luteinizing hormone beta gene J. Biol. Chem. 275 2000 9749 9757
57. F.J. Slack, M. Basson, Z. Liu, V. Ambros, H.R. Horvitz, and G. Ruvkun The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor Mol. Cell 5 2000 659 669
58. F. Spaapen, G.G. van den Akker, M.M. Caron, P. Prickaerts, C. Rofel, V.E. Dahlmans, D.A. Surtel, Y. Paulis, F. Schweizer, and T.J. Welting et al. The immediate early gene product EGR1 and polycomb group proteins interact in epigenetic programming during chondrogenesis PLoS ONE 8 2013 e58083
59. V.P. Sukhatme, X.M. Cao, L.C. Chang, C.H. Tsai-Morris, D. Stamenkovich, P.C. Ferreira, D.R. Cohen, S.A. Edwards, T.B. Shows, and T. Curran et al. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization Cell 53 1988 37 43
60. J. Svaren, B.R. Sevetson, E.D. Apel, D.B. Zimonjic, N.C. Popescu, and J. Milbrandt NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli Mol. Cell. Biol. 16 1996 3545 3553
61. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
62. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, and S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872
63. K. Tanabe, M. Nakamura, M. Narita, K. Takahashi, and S. Yamanaka Maturation, not initiation, is the major roadblock during reprogramming toward pluripotency from human fibroblasts Proc. Natl. Acad. Sci. USA 110 2013 12172 12179
64. P. Topilko, S. Schneider-Maunoury, G. Levi, A. Trembleau, D. Gourdji, M.A. Driancourt, C.V. Rao, and P. Charnay Multiple pituitary and ovarian defects in Krox-24 (NGFI-A, Egr-1)-targeted mice Mol. Endocrinol. 12 1998 107 122
65. S.R. Viswanathan, G.Q. Daley, and R.I. Gregory Selective blockade of microRNA processing by Lin28 Science 320 2008 97 100
66. M. Wernig, A. Meissner, R. Foreman, T. Brambrink, M. Ku, K. Hochedlinger, B.E. Bernstein, and R. Jaenisch In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state Nature 448 2007 318 324
67. M. Wernig, A. Meissner, J.P. Cassady, and R. Jaenisch c-Myc is dispensable for direct reprogramming of mouse fibroblasts Cell Stem Cell 2 2008 10 12
68. J. Yu, M.A. Vodyanik, K. Smuga-Otto, J. Antosiewicz-Bourget, J.L. Frane, S. Tian, J. Nie, G.A. Jonsdottir, V. Ruotti, and R. Stewart et al. Induced pluripotent stem cell lines derived from human somatic cells Science 318 2007 1917 1920
69. A.C. Zambon, S. Gaj, I. Ho, K. Hanspers, K. Vranizan, C.T. Evelo, B.R. Conklin, A.R. Pico, and N. Salomonis GO-Elite: a flexible solution for pathway and ontology over-representation Bioinformatics 28 2012 2209 2210
70. L. Zhang, J. Cho, D. Ptak, and Y.F. Leung The role of egr1 in early zebrafish retinogenesis PLoS ONE 8 2013 e56108