Polycomb Regulates Mesoderm Cell Fate-Specification in Embryonic Stem Cells through Activation and Repression Mechanisms

Cell Stem Cell

Volumn 17, Issue 3, 2015, Pages 300-315

  Morey, Lluis ^a,b,f   Santanach, Alexandra ^a,b   Blanco, Enrique ^a,b   Aloia, Luigi ^a,b   Nora, Elphège P ^c,d   Bruneau, Benoit G ^c,d   Di croce, Luciano ^a,b,e  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; MEL18 PROTEIN; NUCLEIC ACID BINDING PROTEIN; POLYCOMB GROUP PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BMI1 PROTEIN; PCGF6 PROTEIN, MOUSE; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENE ACTIVATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE REPRESSION; GENE TARGETING; HEART; MESODERM; MESODERMAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CARTILAGE; CYTOLOGY; DEFICIENCY; EMBRYOID BODY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENOME; METABOLISM; MOUSE; MOUSE EMBRYONIC STEM CELL; PROTEIN STABILITY;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CARTILAGE; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYOID BODIES; GENE EXPRESSION REGULATION; GENOME; MESODERM; MICE; MOUSE EMBRYONIC STEM CELLS; MYOCARDIUM; MYOCYTES, CARDIAC; POLYCOMB REPRESSIVE COMPLEX 1; POLYCOMB-GROUP PROTEINS; PROTEIN BINDING; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84941000940     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.08.009     Document Type: Article

References (45)

1. T. Akasaka, M. van Lohuizen, N. van der Lugt, Y. Mizutani-Koseki, M. Kanno, M. Taniguchi, M. Vidal, M. Alkema, A. Berns, and H. Koseki Mice doubly deficient for the Polycomb Group genes Mel18 and Bmi1 reveal synergy and requirement for maintenance but not initiation of Hox gene expression Development 128 2001 1587 1597
2. L. Aloia, B. Di Stefano, A. Sessa, L. Morey, A. Santanach, A. Gutierrez, L. Cozzuto, S.A. Benitah, T. Graf, V. Broccoli, and L. Di Croce Zrf1 is required to establish and maintain neural progenitor identity Genes Dev. 28 2014 182 197
3. B.A. Benayoun, E.A. Pollina, D. Ucar, S. Mahmoudi, K. Karra, E.D. Wong, K. Devarajan, A.C. Daugherty, A.B. Kundaje, E. Mancini, and et al. H3K4me3 breadth is linked to cell identity and transcriptional consistency Cell 158 2014 673 688
4. S.W. Bruggeman, M.E. Valk-Lingbeek, P.P. van der Stoop, J.J. Jacobs, K. Kieboom, E. Tanger, D. Hulsman, C. Leung, Y. Arsenijevic, S. Marino, and M. van Lohuizen Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice Genes Dev. 19 2005 1438 1443
5. B.G. Bruneau Signaling and transcriptional networks in heart development and regeneration Cold Spring Harb. Perspect. Biol. 5 2013 a008292
6. G. Buchwald, P. van der Stoop, O. Weichenrieder, A. Perrakis, M. van Lohuizen, and T.K. Sixma Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b EMBO J. 25 2006 2465 2474
7. R. Cao, L. Wang, H. Wang, L. Xia, H. Erdjument-Bromage, P. Tempst, R.S. Jones, and Y. Zhang Role of histone H3 lysine 27 methylation in Polycomb-group silencing Science 298 2002 1039 1043
8. A.M. Craft, N. Ahmed, J.S. Rockel, G.S. Baht, B.A. Alman, R.A. Kandel, A.E. Grigoriadis, and G.M. Keller Specification of chondrocytes and cartilage tissues from embryonic stem cells Development 140 2013 2597 2610
9. C. Creppe, A. Palau, R. Malinverni, V. Valero, and M. Buschbeck A Cbx8-containing polycomb complex facilitates the transition to gene activation during ES cell differentiation PLoS Genet. 10 2014 e1004851
10. R. David, V.B. Jarsch, F. Schwarz, P. Nathan, M. Gegg, H. Lickert, and W.M. Franz Induction of MesP1 by Brachyury(T) generates the common multipotent cardiovascular stem cell Cardiovasc. Res. 92 2011 115 122
11. P. Delgado-Olguín, Y. Huang, X. Li, D. Christodoulou, C.E. Seidman, J.G. Seidman, A. Tarakhovsky, and B.G. Bruneau Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis Nat. Genet. 44 2012 343 347
12. L. Di Croce, and K. Helin Transcriptional regulation by Polycomb group proteins Nat. Struct. Mol. Biol. 20 2013 1147 1155
13. N. Dimitrova, J.R. Zamudio, R.M. Jong, D. Soukup, R. Resnick, K. Sarma, A.J. Ward, A. Raj, J.T. Lee, P.A. Sharp, and T. Jacks LincRNA-p21 activates p21 in cis to promote Polycomb target gene expression and to enforce the G1/S checkpoint Mol. Cell 54 2014 777 790
14. S. Elderkin, G.N. Maertens, M. Endoh, D.L. Mallery, N. Morrice, H. Koseki, G. Peters, N. Brockdorff, and K. Hiom A phosphorylated form of Mel-18 targets the Ring1B histone H2A ubiquitin ligase to chromatin Mol. Cell 28 2007 107 120
15. M.J. Evans, and M.H. Kaufman Establishment in culture of pluripotential cells from mouse embryos Nature 292 1981 154 156
16. A.M. Farcas, N.P. Blackledge, I. Sudbery, H.K. Long, J.F. McGouran, N.R. Rose, S. Lee, D. Sims, A. Cerase, T.W. Sheahan, and et al. KDM2B links the Polycomb Repressive Complex 1 (PRC1) to recognition of CpG islands eLife 1 2012 e00205
17. A. Frangini, M. Sjöberg, M. Roman-Trufero, G. Dharmalingam, V. Haberle, T. Bartke, B. Lenhard, M. Malumbres, M. Vidal, and N. Dillon The aurora B kinase and the polycomb protein ring1B combine to regulate active promoters in quiescent lymphocytes Mol. Cell 51 2013 647 661
18. Z. Gao, J. Zhang, R. Bonasio, F. Strino, A. Sawai, F. Parisi, Y. Kluger, and D. Reinberg PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes Mol. Cell 45 2012 344 356
19. Z. Gao, P. Lee, J.M. Stafford, M. von Schimmelmann, A. Schaefer, and D. Reinberg An AUTS2-Polycomb complex activates gene expression in the CNS Nature 516 2014 349 354
20. J. He, L. Shen, M. Wan, O. Taranova, H. Wu, and Y. Zhang Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes Nat. Cell Biol. 15 2013 373 384
21. B.G. Herrmann, S. Labeit, A. Poustka, T.R. King, and H. Lehrach Cloning of the T gene required in mesoderm formation in the mouse Nature 343 1990 617 622
22. S.E. Junco, R. Wang, J.C. Gaipa, A.B. Taylor, V. Schirf, M.D. Gearhart, V.J. Bardwell, B. Demeler, P.J. Hart, and C.A. Kim Structure of the polycomb group protein PCGF1 in complex with BCOR reveals basis for binding selectivity of PCGF homologs Structure 21 2013 665 671
23. S.J. Kattman, A.D. Witty, M. Gagliardi, N.C. Dubois, M. Niapour, A. Hotta, J. Ellis, and G. Keller Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines Cell Stem Cell 8 2011 228 240
24. J. Larraín, D. Bachiller, B. Lu, E. Agius, S. Piccolo, and E.M. De Robertis BMP-binding modules in chordin: a model for signalling regulation in the extracellular space Development 127 2000 821 830
25. A. Laugesen, and K. Helin Chromatin repressive complexes in stem cells, development, and cancer Cell Stem Cell 14 2014 735 751
26. Z. Li, R. Cao, M. Wang, M.P. Myers, Y. Zhang, and R.M. Xu Structure of a Bmi-1-Ring1B polycomb group ubiquitin ligase complex J. Biol. Chem. 281 2006 20643 20649
27. N.M. Luis, L. Morey, L. Di Croce, and S.A. Benitah Polycomb in stem cells: PRC1 branches out Cell Stem Cell 11 2012 16 21
28. L. Morey, and K. Helin Polycomb group protein-mediated repression of transcription Trends Biochem. Sci. 35 2010 323 332
29. L. Morey, G. Pascual, L. Cozzuto, G. Roma, A. Wutz, S.A. Benitah, and L. Di Croce Nonoverlapping functions of the Polycomb group Cbx family of proteins in embryonic stem cells Cell Stem Cell 10 2012 47 62
30. L. Morey, L. Aloia, L. Cozzuto, S.A. Benitah, and L. Di Croce RYBP and Cbx7 define specific biological functions of polycomb complexes in mouse embryonic stem cells Cell Rep. 3 2013 60 69
31. A. O'Loghlen, A.M. Muñoz-Cabello, A. Gaspar-Maia, H.A. Wu, A. Banito, N. Kunowska, T. Racek, H.N. Pemberton, P. Beolchi, F. Lavial, and et al. MicroRNA regulation of Cbx7 mediates a switch of Polycomb orthologs during ESC differentiation Cell Stem Cell 10 2012 33 46
32. H. Oguro, J. Yuan, H. Ichikawa, T. Ikawa, S. Yamazaki, H. Kawamoto, H. Nakauchi, and A. Iwama Poised lineage specification in multipotential hematopoietic stem and progenitor cells by the polycomb protein Bmi1 Cell Stem Cell 6 2010 279 286
33. J. Qin, W.A. Whyte, E. Anderssen, E. Apostolou, H.H. Chen, S. Akbarian, R.T. Bronson, K. Hochedlinger, S. Ramaswamy, R.A. Young, and H. Hock The polycomb group protein L3mbtl2 assembles an atypical PRC1-family complex that is essential in pluripotent stem cells and early development Cell Stem Cell 11 2012 319 332
34. M.C. Ramel, and C.S. Hill Spatial regulation of BMP activity FEBS Lett. 586 2012 1929 1941
35. K. Ross, A.K. Sedello, G.P. Todd, M. Paszkowski-Rogacz, A.W. Bird, L. Ding, T. Grinenko, K. Behrens, N. Hubner, M. Mann, and et al. Polycomb group ring finger 1 cooperates with Runx1 in regulating differentiation and self-renewal of hematopoietic cells Blood 119 2012 4152 4161
36. Y. Saga, S. Miyagawa-Tomita, A. Takagi, S. Kitajima, Ji. Miyazaki, and T. Inoue MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube Development 126 1999 3437 3447
37. C.A. Schaaf, Z. Misulovin, M. Gause, A. Koenig, D.W. Gohara, A. Watson, and D. Dorsett Cohesin and polycomb proteins functionally interact to control transcription at silenced and active genes PLoS Genet. 9 2013 e1003560
38. L.L. Smith, J. Yeung, B.B. Zeisig, N. Popov, I. Huijbers, J. Barnes, A.J. Wilson, E. Taskesen, R. Delwel, J. Gil, and et al. Functional crosstalk between Bmi1 and MLL/Hoxa9 axis in establishment of normal hematopoietic and leukemic stem cells Cell Stem Cell 8 2011 649 662
39. M. Suzuki, Y. Mizutani-Koseki, Y. Fujimura, H. Miyagishima, T. Kaneko, Y. Takada, T. Akasaka, H. Tanzawa, Y. Takihara, M. Nakano, and et al. Involvement of the Polycomb-group gene Ring1B in the specification of the anterior-posterior axis in mice Development 129 2002 4171 4183
40. L. Tavares, E. Dimitrova, D. Oxley, J. Webster, R. Poot, J. Demmers, K. Bezstarosti, S. Taylor, H. Ura, H. Koide, and et al. RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3 Cell 148 2012 664 678
41. J.A. Wamstad, J.M. Alexander, R.M. Truty, A. Shrikumar, F. Li, K.E. Eilertson, H. Ding, J.N. Wylie, A.R. Pico, J.A. Capra, and et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage Cell 151 2012 206 220
42. H. Wang, L. Wang, H. Erdjument-Bromage, M. Vidal, P. Tempst, R.S. Jones, and Y. Zhang Role of histone H2A ubiquitination in Polycomb silencing Nature 431 2004 873 878
43. X. Wu, J.V. Johansen, and K. Helin Fbxl10/Kdm2b recruits polycomb repressive complex 1 to CpG islands and regulates H2A ubiquitylation Mol. Cell 49 2013 1134 1146
44. D. Zdzieblo, X. Li, Q. Lin, M. Zenke, D.J. Illich, M. Becker, and A.M. Müller Pcgf6, a polycomb group protein, regulates mesodermal lineage differentiation in murine ESCs and functions in iPS reprogramming Stem Cells 32 2014 3112 3125
45. D. Zencak, M. Lingbeek, C. Kostic, M. Tekaya, E. Tanger, D. Hornfeld, M. Jaquet, F.L. Munier, D.F. Schorderet, M. van Lohuizen, and Y. Arsenijevic Bmi1 loss produces an increase in astroglial cells and a decrease in neural stem cell population and proliferation J. Neurosci. 25 2005 5774 5783