SET7/9 methylation of the pluripotency factor LIN28A is a nucleolar localization mechanism that blocks let-7 biogenesis in human ESCs

Cell Stem Cell

Volumn 15, Issue 6, 2014, Pages 735-749

  Kim, Seung Kyoon ^a   Lee, Hosuk ^a   Han, Kyumin ^a   Kim, Sang Cheol ^b   Choi, Yoonjung ^a   Park, Sang Wook ^a   Bak, Geunu ^a   Lee, Younghoon ^a   Choi, Jung Kyoon ^a   Kim, Tae Kyung ^c   Han, Yong Mahn ^a   Lee, Daeyoup ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Samsung Medical Center   (South Korea)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LET 7 PROTEIN; LIN28A PROTEIN; LYSINE; MICRORNA; MYC PROTEIN; PROTEIN; SET7 PROTEIN; SET9 PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HISTONE LYSINE METHYLTRANSFERASE; LIN28B PROTEIN, HUMAN; MIRNLET7 MICRORNA, HUMAN; RNA BINDING PROTEIN; SETD8 PROTEIN, HUMAN; ZCCHC11 PROTEIN, HUMAN;

ARTICLE; BIOGENESIS; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN STABILITY; TRANSCRIPTION REGULATION; CELL LINE; CELL LINEAGE; GENETICS; METABOLISM; METHYLATION; ONCOGENE MYC; PHYSIOLOGY; PLURIPOTENT STEM CELL; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT;

CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CELL NUCLEOLUS; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GENES, MYC; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; METHYLATION; MICRORNAS; PLURIPOTENT STEM CELLS; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RNA-BINDING PROTEINS;

EID: 84919426973     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.10.016     Document Type: Article

References (53)

1. V. Ambros, and H.R. Horvitz Heterochronic mutants of the nematode Caenorhabditis elegans Science 226 1984 409 416
2. E. Balzer, and E.G. Moss Localization of the developmental timing regulator Lin28 to mRNP complexes, P-bodies and stress granules RNA Biol. 4 2007 16 25
3. M. Benhamed, U. Herbig, T. Ye, A. Dejean, and O. Bischof Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells Nat. Cell Biol. 14 2012 266 275
4. L.A. Boyer, T.I. Lee, M.F. Cole, S.E. Johnstone, S.S. Levine, J.P. Zucker, M.G. Guenther, R.M. Kumar, H.L. Murray, and R.G. Jenner Core transcriptional regulatory circuitry in human embryonic stem cells Cell 122 2005 947 956
5. H.-M. Chang, R. Triboulet, J.E. Thornton, and R.I. Gregory A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway Nature 497 2013 244 248
6. L.-L. Chen, and G.G. Carmichael Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA Mol. Cell 35 2009 467 478
7. X. Chen, H. Xu, P. Yuan, F. Fang, M. Huss, V.B. Vega, E. Wong, Y.L. Orlov, W. Zhang, and J. Jiang Integration of external signaling pathways with the core transcriptional network in embryonic stem cells Cell 133 2008 1106 1117
8. S. Chuikov, J.K. Kurash, J.R. Wilson, B. Xiao, N. Justin, G.S. Ivanov, K. McKinney, P. Tempst, C. Prives, and S.J. Gamblin Regulation of p53 activity through lysine methylation Nature 432 2004 353 360
9. J.-F. Couture, E. Collazo, G. Hauk, and R.C. Trievel Structural basis for the methylation site specificity of SET7/9 Nat. Struct. Mol. Biol. 13 2006 140 146
10. A. Desjardins, J. Bouvette, and P. Legault Stepwise assembly of multiple Lin28 proteins on the terminal loop of let-7 miRNA precursors Nucleic Acids Res. 42 2014 4615 4628
11. P.-O. Estève, H.G. Chin, J. Benner, G.R. Feehery, M. Samaranayake, G.A. Horwitz, S.E. Jacobsen, and S. Pradhan Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells Proc. Natl. Acad. Sci. U S A 106 2009 5076 5081
12. P.M. Evans, W. Zhang, X. Chen, J. Yang, K.K. Bhakat, and C. Liu Kruppel-like factor 4 is acetylated by p300 and regulates gene transcription via modulation of histone acetylation J. Biol. Chem. 282 2007 33994 34002
13. L. Fang, L. Zhang, W. Wei, X. Jin, P. Wang, Y. Tong, J. Li, J.X. Du, and J. Wong A Methylation-phosphorylation switch determines Sox2 stability and function in ESC maintenance or differentiation Mol Cell 55 2014 537 551
14. R.N. Freiman, and R. Tjian Regulating the regulators: lysine modifications make their mark Cell 112 2003 11 17
15. W. Gu, and R.G. Roeder Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain Cell 90 1997 595 606
16. Y. Guo, Y. Chen, H. Ito, A. Watanabe, X. Ge, T. Kodama, and H. Aburatani Identification and characterization of lin-28 homolog B (LIN28B) in human hepatocellular carcinoma Gene 384 2006 51 61
17. J.P. Hagan, E. Piskounova, and R.I. Gregory Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells Nat. Struct. Mol. Biol. 16 2009 1021 1025
18. I. Heo, C. Joo, J. Cho, M. Ha, J. Han, and V.N. Kim Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA Mol. Cell 32 2008 276 284
19. I. Heo, C. Joo, Y.-K. Kim, M. Ha, M.-J. Yoon, J. Cho, K.-H. Yeom, J. Han, and V.N. Kim TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation Cell 138 2009 696 708
20. I. Heo, M. Ha, J. Lim, M.-J. Yoon, J.-E. Park, S.C. Kwon, H. Chang, and V.N. Kim Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs Cell 151 2012 521 532
21. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080
22. H. Ji, G. Wu, X. Zhan, A. Nolan, C. Koh, A. De Marzo, H.M. Doan, J. Fan, C. Cheadle, and M. Fallahi Cell-type independent MYC target genes reveal a primordial signature involved in biomass accumulation PLoS ONE 6 2011 e26057
23. V.N. Kim MicroRNA biogenesis: coordinated cropping and dicing Nat. Rev. Mol. Cell Biol. 6 2005 376 385
24. S.-K. Kim, I. Jung, H. Lee, K. Kang, M. Kim, K. Jeong, C.S. Kwon, Y.-M. Han, Y.S. Kim, D. Kim, and D. Lee Human histone H3K79 methyltransferase DOT1L protein [corrected] binds actively transcribing RNA polymerase II to regulate gene expression J. Biol. Chem. 287 2012 39698 39709
25. H. Kontaki, and I. Talianidis Lysine methylation regulates E2F1-induced cell death Mol. Cell 39 2010 152 160
26. A. Kouskouti, E. Scheer, A. Staub, L. Tora, and I. Talianidis Gene-specific modulation of TAF10 function by SET9-mediated methylation Mol. Cell 14 2004 175 182
27. B.A. Malynn, I.M. de Alboran, R.C. O'Hagan, R. Bronson, L. Davidson, R.A. DePinho, and F.W. Alt N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation Genes Dev. 14 2000 1390 1399
28. C. Melton, R.L. Judson, and R. Blelloch Opposing microRNA families regulate self-renewal in mouse embryonic stem cells Nature 463 2010 621 626
29. M. Moretto-Zita, H. Jin, Z. Shen, T. Zhao, S.P. Briggs, and Y. Xu Phosphorylation stabilizes Nanog by promoting its interaction with Pin1 Proc. Natl. Acad. Sci. U S A 107 2010 13312 13317
30. E.G. Moss, and L. Tang Conservation of the heterochronic regulator Lin-28, its developmental expression and microRNA complementary sites Dev. Biol. 258 2003 432 442
31. Y. Nam, C. Chen, R.I. Gregory, J.J. Chou, and P. Sliz Molecular basis for interaction of let-7 microRNAs with Lin28 Cell 147 2011 1080 1091
32. 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
33. K. Nishioka, S. Chuikov, K. Sarma, H. Erdjument-Bromage, C.D. Allis, P. Tempst, and D. Reinberg Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation Genes Dev. 16 2002 479 489
34. E. Piskounova, S.R. Viswanathan, M. Janas, R.J. LaPierre, G.Q. Daley, P. Sliz, and R.I. Gregory Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28 J. Biol. Chem. 283 2008 21310 21314
35. E. Piskounova, C. Polytarchou, J.E. Thornton, R.J. LaPierre, C. Pothoulakis, J.P. Hagan, D. Iliopoulos, and R.I. Gregory Lin28A and Lin28B inhibit let-7 microRNA biogenesis by distinct mechanisms Cell 147 2011 1066 1079
36. A. Polesskaya, S. Cuvellier, I. Naguibneva, A. Duquet, E.G. Moss, and A. Harel-Bellan Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency Genes Dev. 21 2007 1125 1138
37. C. Qiu, Y. Ma, J. Wang, S. Peng, and Y. Huang Lin28-mediated post-transcriptional regulation of Oct4 expression in human embryonic stem cells Nucleic Acids Res. 38 2010 1240 1248
38. 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
39. N. Shyh-Chang, and G.Q. Daley Lin28: primal regulator of growth and metabolism in stem cells Cell Stem Cell 12 2013 395 406
40. K.N. Smith, A.M. Singh, and S. Dalton Myc represses primitive endoderm differentiation in pluripotent stem cells Cell Stem Cell 7 2010 343 354
41. B.D. Strahl, and C.D. Allis The language of covalent histone modifications Nature 403 2000 41 45
42. K. Subramanian, D. Jia, P. Kapoor-Vazirani, D.R. Powell, R.E. Collins, D. Sharma, J. Peng, X. Cheng, and P.M. Vertino Regulation of estrogen receptor α by the SET7 lysine methyltransferase Mol. Cell 30 2008 336 347
43. Y. Tao, R.L. Neppl, Z.-P. Huang, J. Chen, R.-H. Tang, R. Cao, Y. Zhang, S.-W. Jin, and D.-Z. Wang The histone methyltransferase Set7/9 promotes myoblast differentiation and myofibril assembly J. Cell Biol. 194 2011 551 565
44. B.M. Turner Cellular memory and the histone code Cell 111 2002 285 291
45. S.R. Viswanathan, G.Q. Daley, and R.I. Gregory Selective blockade of microRNA processing by Lin28 Science 320 2008 97 100
46. S.R. Viswanathan, J.T. Powers, W. Einhorn, Y. Hoshida, T.L. Ng, S. Toffanin, M. O'Sullivan, J. Lu, L.A. Phillips, and V.L. Lockhart Lin28 promotes transformation and is associated with advanced human malignancies Nat. Genet. 41 2009 843 848
47. L.X. Wang, J. Wang, T.T. Qu, Y. Zhang, and Y.F. Shen Reversible acetylation of Lin28 mediated by PCAF and SIRT1 Biochim. Biophys. Acta 1843 2014 1188 1195
48. F. Wei, H.R. Schöler, and M.L. Atchison Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation J. Biol. Chem. 282 2007 21551 21560
49. J.A. West, S.R. Viswanathan, A. Yabuuchi, K. Cunniff, A. Takeuchi, I.-H. Park, J.E. Sero, H. Zhu, A. Perez-Atayde, and A.L. Frazier A role for Lin28 in primordial germ-cell development and germ-cell malignancy Nature 460 2009 909 913
50. M.L. Wilbert, S.C. Huelga, K. Kapeli, T.J. Stark, T.Y. Liang, S.X. Chen, B.Y. Yan, J.L. Nathanson, K.R. Hutt, and M.T. Lovci LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance Mol. Cell 48 2012 195 206
51. F. Yu, H. Yao, P. Zhu, X. Zhang, Q. Pan, C. Gong, Y. Huang, X. Hu, F. Su, J. Lieberman, and E. Song let-7 regulates self renewal and tumorigenicity of breast cancer cells Cell 131 2007 1109 1123
52. 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 Induced pluripotent stem cell lines derived from human somatic cells Science 318 2007 1917 1920
53. H. Zhu, N. Shyh-Chang, A.V. Segrè, G. Shinoda, S.P. Shah, W.S. Einhorn, A. Takeuchi, J.M. Engreitz, J.P. Hagan, M.G. Kharas DIAGRAM Consortium MAGIC Investigators The Lin28/let-7 axis regulates glucose metabolism Cell 147 2011 81 94