Alternative splicing of MBD2 supports self-renewal in human pluripotent stem cells

Cell Stem Cell

Volumn 15, Issue 1, 2014, Pages 92-101

  Lu, Yu ^a,b,c   Loh, Yuin Han ^b,d,e   Li, Hu ^f,g,h   Cesana, Marcella ^b,d   Ficarro, Scott B ^a,b   Parikh, Jignesh R ^a,i   Salomonis, Nathan ^j   Toh, Cheng Xu Delon ^e   Andreadis, Stelios T ^k   Luckey, C John ^c   Collins, James J ^f,g   Daley, George Q ^b,d   Marto, Jarrod A ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^f Boston University   (United States)

^g HARVARD UNIVERSITY   (United States)

^h MAYO GRADUATE SCHOOL   (United States)

ⁱ BOSTON UNIVERSITY   (United States)

^j GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^k the State University of New York   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

METHYL CPG BINDING PROTEIN 2; MICRORNA; MICRORNA 301; MICRORNA 302; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HISTONE DEACETYLASE; HOMEODOMAIN PROTEIN; ISOPROTEIN; MIRN301 MICRORNA, HUMAN; MIRN302 MICRORNA, HUMAN; NANOG PROTEIN, HUMAN; NUCLEAR PROTEIN; POU5F1 PROTEIN, HUMAN; PROTEIN BINDING; RIBONUCLEOPROTEIN; SRSF2 PROTEIN, HUMAN; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; METHYL CPG BINDING PROTEIN 2A; METHYL CPG BINDING PROTEIN 2C; MI 2 PROTEIN; MTA2 PROTEIN; PROTEIN; PROTEOME; RETINOBLASTOMA BINDING PROTEIN 7; SFRS2 PROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL DIFFERENTIATION; CELL REGENERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; FIBROBLAST; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEOMICS; CELL CULTURE; CELL SURVIVAL; FEEDBACK SYSTEM; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PHYSIOLOGY; 3' UNTRANSLATED REGION; BINDING SITE; CELL FATE; CELL FUNCTION; CELL RENEWAL; CELL SPECIFICITY; CELL STRUCTURE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FUNCTIONAL GENOMICS; GENE CONTROL; GENE FUNCTION; GENE INTERACTION; GENE MUTATION; GENE ONTOLOGY; GENE TARGETING; GENETIC TRANSCRIPTION; NUCLEOTIDE SEQUENCE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CELLULAR REPROGRAMMING; DNA-BINDING PROTEINS; FEEDBACK, PHYSIOLOGICAL; FIBROBLASTS; GENE EXPRESSION PROFILING; HOMEODOMAIN PROTEINS; HUMANS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICRORNAS; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3; PLURIPOTENT STEM CELLS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEOMICS; RIBONUCLEOPROTEINS;

EID: 84904044398     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.04.002     Document Type: Article

References (46)

1. G. Balázsi, A. van Oudenaarden, and J.J. Collins Cellular decision making and biological noise: from microbes to mammals Cell 144 2011 910 925
2. M. Bar, S.K. Wyman, B.R. Fritz, J. Qi, K.S. Garg, R.K. Parkin, E.M. Kroh, A. Bendoraite, P.S. Mitchell, and A.M. Nelson et al. MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries Stem Cells 26 2008 2496 2505
3. T. Baubec, R. Ivánek, F. Lienert, and D. Schübeler Methylation-dependent and -independent genomic targeting principles of the MBD protein family Cell 153 2013 480 492
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 et al. Core transcriptional regulatory circuitry in human embryonic stem cells Cell 122 2005 947 956
5. U. Braunschweig, S. Gueroussov, A.M. Plocik, B.R. Graveley, and B.J. Blencowe Dynamic integration of splicing within gene regulatory pathways Cell 152 2013 1252 1269
6. L.M. Brill, W. Xiong, K.-B. Lee, S.B. Ficarro, A. Crain, Y. Xu, A. Terskikh, E.Y. Snyder, and S. Ding Phosphoproteomic analysis of human embryonic stem cells Cell Stem Cell 5 2009 204 213
7. M. Buljan, G. Chalancon, S. Eustermann, G.P. Wagner, M. Fuxreiter, A. Bateman, and M.M. Babu Tissue-specific splicing of disordered segments that embed binding motifs rewires protein interaction networks Mol. Cell 46 2012 871 883
8. P. Cahan, and G.Q. Daley Origins and implications of pluripotent stem cell variability and heterogeneity Nat. Rev. Mol. Cell Biol. 14 2013 357 368
9. N.-Y. Chia, Y.-S. Chan, B. Feng, X. Lu, Y.L. Orlov, D. Moreau, P. Kumar, L. Yang, J. Jiang, and M.-S. Lau et al. A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity Nature 468 2010 316 320
10. S. Das, S. Jena, and D.N. Levasseur Alternative splicing produces Nanog protein variants with different capacities for self-renewal and pluripotency in embryonic stem cells J. Biol. Chem. 286 2011 42690 42703
11. A. De Los Angeles, Y.-H. Loh, P.J. Tesar, and G.Q. Daley Accessing naïve human pluripotency Curr. Opin. Genet. Dev. 22 2012 272 282
12. J.D. Ellis, M. Barrios-Rodiles, R. Colak, M. Irimia, T. Kim, J.A. Calarco, X. Wang, Q. Pan, D. O'Hanlon, and P.M. Kim et al. Tissue-specific alternative splicing remodels protein-protein interaction networks Mol. Cell 46 2012 884 892
13. S.B. Ficarro, G. Adelmant, M.N. Tomar, Y. Zhang, V.J. Cheng, and J.A. Marto Magnetic bead processor for rapid evaluation and optimization of parameters for phosphopeptide enrichment Anal. Chem. 81 2009 4566 4575
14. S.B. Ficarro, Y. Zhang, M.J. Carrasco-Alfonso, B. Garg, G. Adelmant, J.T. Webber, C.J. Luckey, and J.A. Marto Online nanoflow multidimensional fractionation for high efficiency phosphopeptide analysis Mol. Cell. Proteomics 10 2011 011064
15. M. Gabut, P. Samavarchi-Tehrani, X. Wang, V. Slobodeniuc, D. O'Hanlon, H.-K. Sung, M. Alvarez, S. Talukder, Q. Pan, and E.O. Mazzoni et al. An alternative splicing switch regulates embryonic stem cell pluripotency and reprogramming Cell 147 2011 132 146
16. C.A. Gifford, M.J. Ziller, H. Gu, C. Trapnell, J. Donaghey, A. Tsankov, A.K. Shalek, D.R. Kelley, A.A. Shishkin, and R. Issner et al. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells Cell 153 2013 1149 1163
17. A. Gore, Z. Li, H.-L. Fung, J.E. Young, S. Agarwal, J. Antosiewicz-Bourget, I. Canto, A. Giorgetti, M.A. Israel, and E. Kiskinis et al. Somatic coding mutations in human induced pluripotent stem cells Nature 471 2011 63 67
18. M.G. Guenther, G.M. Frampton, F. Soldner, D. Hockemeyer, M. Mitalipova, R. Jaenisch, and R.A. Young Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells Cell Stem Cell 7 2010 249 257
19. H. Han, M. Irimia, P.J. Ross, H.-K. Sung, B. Alipanahi, L. David, A. Golipour, M. Gabut, I.P. Michael, and E.N. Nachman et al. MBNL proteins repress ES-cell-specific alternative splicing and reprogramming Nature 498 2013 241 245
20. B. Hendrich, and A. Bird Identification and characterization of a family of mammalian methyl-CpG binding proteins Mol. Cell. Biol. 18 1998 6538 6547
21. G. Hu, and P.A. Wade NuRD and pluripotency: a complex balancing act Cell Stem Cell 10 2012 497 503
22. N.T. Ingolia, L.F. Lareau, and J.S. Weissman Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes Cell 147 2011 789 802
23. J. Kim, J. Chu, X. Shen, J. Wang, and S.H. Orkin An extended transcriptional network for pluripotency of embryonic stem cells Cell 132 2008 1049 1061
24. K. Kim, A. Doi, B. Wen, K. Ng, R. Zhao, P. Cahan, J. Kim, M.J. Aryee, H. Ji, and L.I.R. Ehrlich et al. Epigenetic memory in induced pluripotent stem cells Nature 467 2010 285 290
25. X. Le Guezennec, M. Vermeulen, A.B. Brinkman, W.A.M. Hoeijmakers, A. Cohen, E. Lasonder, and H.G. Stunnenberg MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties Mol. Cell. Biol. 26 2006 843 851
26. M.R. Lee, N. Prasain, H.-D. Chae, Y.-J. Kim, C. Mantel, M.C. Yoder, and H.E. Broxmeyer Epigenetic regulation of NANOG by miR-302 cluster-MBD2 completes induced pluripotent stem cell reprogramming Stem Cells 31 2013 666 681
27. S. Lin, G. Coutinho-Mansfield, D. Wang, S. Pandit, and X.-D. Fu The splicing factor SC35 has an active role in transcriptional elongation Nat. Struct. Mol. Biol. 15 2008 819 826
28. S. Loewer, M.N. Cabili, M. Guttman, Y.-H. Loh, K. Thomas, I.H. Park, M. Garber, M. Curran, T. Onder, and S. Agarwal et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells Nat. Genet. 42 2010 1113 1117
29. A. Marson, S.S. Levine, M.F. Cole, G.M. Frampton, T. Brambrink, S. Johnstone, M.G. Guenther, W.K. Johnston, M. Wernig, and J. Newman et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells Cell 134 2008 521 533
30. T.T. Onder, N. Kara, A. Cherry, A.U. Sinha, N. Zhu, K.M. Bernt, P. Cahan, B.O. Marcarci, J. Unternaehrer, and P.B. Gupta et al. Chromatin-modifying enzymes as modulators of reprogramming Nature 483 2012 598 602
31. 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
32. D.H. Phanstiel, J. Brumbaugh, C.D. Wenger, S. Tian, M.D. Probasco, D.J. Bailey, D.L. Swaney, M.A. Tervo, J.M. Bolin, and V. Ruotti et al. Proteomic and phosphoproteomic comparison of human ES and iPS cells Nat. Methods 8 2011 821 827
33. 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
34. N. Reynolds, P. Latos, A. Hynes-Allen, R. Loos, D. Leaford, A. O'Shaughnessy, O. Mosaku, J. Signolet, P. Brennecke, and T. Kalkan et al. NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment Cell Stem Cell 10 2012 583 594
35. N. Salomonis, C.R. Schlieve, L. Pereira, C. Wahlquist, A. Colas, A.C. Zambon, K. Vranizan, M.J. Spindler, A.R. Pico, and M.S. Cline et al. Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation Proc. Natl. Acad. Sci. USA 107 2010 10514 10519
36. 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
37. F. Tang, C. Barbacioru, S. Bao, C. Lee, E. Nordman, X. Wang, K. Lao, and M.A. Surani Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis Cell Stem Cell 6 2010 468 478
38. M. Vidal, M.E. Cusick, and A.-L. Barabási Interactome networks and human disease Cell 144 2011 986 998
39. E.T. Wang, R. Sandberg, S. Luo, I. Khrebtukova, L. Zhang, C. Mayr, S.F. Kingsmore, G.P. Schroth, and C.B. Burge Alternative isoform regulation in human tissue transcriptomes Nature 456 2008 470 476
40. Y. Wang, Z. Xu, J. Jiang, C. Xu, J. Kang, L. Xiao, M. Wu, J. Xiong, X. Guo, and H. Liu Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal Dev. Cell 25 2013 69 80
41. J.Q. Wu, L. Habegger, P. Noisa, A. Szekely, C. Qiu, S. Hutchison, D. Raha, M. Egholm, H. Lin, and S. Weissman et al. Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing Proc. Natl. Acad. Sci. USA 107 2010 5254 5259
42. R. Xiao, Y. Sun, J.-H. Ding, S. Lin, D.W. Rose, M.G. Rosenfeld, X.-D. Fu, and X. Li Splicing regulator SC35 is essential for genomic stability and cell proliferation during mammalian organogenesis Mol. Cell. Biol. 27 2007 5393 5402
43. W. Xie, M.D. Schultz, R. Lister, Z. Hou, N. Rajagopal, P. Ray, J.W. Whitaker, S. Tian, R.D. Hawkins, and D. Leung et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells Cell 153 2013 1134 1148
44. Y. Zhang, H.H. Ng, H. Erdjument-Bromage, P. Tempst, A. Bird, and D. Reinberg Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation Genes Dev. 13 1999 1924 1935
45. Y. Zhang, N. Fatima, and M.L. Dufau Coordinated changes in DNA methylation and histone modifications regulate silencing/derepression of luteinizing hormone receptor gene transcription Mol. Cell. Biol. 25 2005 7929 7939
46. Z. Zhou, J. Qiu, W. Liu, Y. Zhou, R.M. Plocinik, H. Li, Q. Hu, G. Ghosh, J.A. Adams, M.G. Rosenfeld, and X.D. Fu The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus Mol. Cell 47 2012 422 433