Identification of a large protein network involved in epigenetic transmission in replicating DNA of embryonic stem cells

Nucleic Acids Research

Volumn 42, Issue 11, 2014, Pages 6972-6986

  Aranda, Sergi ^a,b   Rutishauser, Dorothea ^a   Ernfors, Patrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOPROTEIN; ENZYME; HETEROCHROMATIN PROTEIN 1; HISTONE DEACETYLASE 1; HISTONE H3; NUCLEOSOMAL REMODELLING AND DEACETYLASE PROTEIN; UHRF1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DEACETYLATION; DNA ISOLATION; DNA PROTEIN COMPLEX; DNA REPLICATION; DNA REPLICATION ORIGIN; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; HISTONE ACETYLATION; HISTONE METHYLATION; MISMATCH REPAIR; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STRUCTURAL PROTEOMICS;

ANIMALS; CELLS, CULTURED; DNA; DNA MISMATCH REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; HETEROCHROMATIN; HISTONE DEACETYLASE 1; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS;

EID: 84903192816     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku374     Document Type: Article

References (58)

1. Young, R.A. (2011) Control of the embryonic stem cell state. Cell, 144, 940-954.
2. Tsubouchi, T. and Fisher, A.G. (2013) Reprogramming and the pluripotent stem cell cycle. Curr. Top. Dev. Biol., 104, 223-241.
3. Orkin, S.H. and Hochedlinger, K. (2011) Chromatin connections to pluripotency and cellular reprogramming. Cell, 145, 835-850.
4. Hu, G. and Wade, P.A. (2012) NuRD and pluripotency: A complex balancing act. Cell Stem Cell, 10, 497-503.
5. Ku, M., Koche, R.P., Rheinbay, E., Mendenhall, E.M., Endoh, M., Mikkelsen, T.S., Presser, A., Nusbaum, C., Xie, X., Chi, A.S. et al. (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet., 4, e1000242.
6. Ho, L., Jothi, R., Ronan, J.L., Cui, K., Zhao, K. and Crabtree, G.R. (2009) An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc. Natl. Acad. Sci. U.S.A., 106, 5187-5191.
7. Reynolds, N., Latos, P., Hynes-Allen, A., Loos, R., Leaford, D., O'Shaughnessy, A., Mosaku, O., Signolet, J., Brennecke, P., Kalkan, T. et al. (2012) NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment. Cell Stem Cell, 10, 583-594.
8. Savatier, P., Huang, S., Szekely, L., Wiman, K.G. and Samarut, J. (1994) Contrasting patterns of retinoblastoma protein expression in mouse embryonic stem cells and embryonic fibroblasts. Oncogene, 9, 809-818.
9. Sirbu, B.M., Couch, F.B., Feigerle, J.T., Bhaskara, S., Hiebert, S.W. and Cortez, D. (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev., 25, 1320-1327.
10. Lopez-Contreras, A.J., Ruppen, I., Nieto-Soler, M., Murga, M., Rodriguez-Acebes, S., Remeseiro, S., Rodrigo-Perez, S., Rojas, A.M., Mendez, J., Munoz, J. et al. (2013) A proteomic characterization of factors enriched at nascent DNA molecules. Cell Rep., 3, 1105-1116.
11. Sirbu, B.M., McDonald, W.H., Dungrawala, H., Badu-Nkansah, A., Kavanaugh, G.M., Chen, Y., Tabb, D.L. and Cortez, D. (2013) Identification of proteins at active, stalled, and collapsed replication forks using isolation of proteins on nascent DNA (iPOND) coupled with mass spectrometry. J. Biol. Chem., 288, 31458-31467.
12. Cervantes, R.B., Stringer, J.R., Shao, C., Tischfield, J.A. and Stambrook, P.J. (2002) Embryonic stem cells and somatic cells differ in mutation frequency and type. Proc. Natl. Acad. Sci. U.S.A., 99, 3586-3590.
13. Fan, J., Robert, C., Jang, Y.Y., Liu, H., Sharkis, S., Baylin, S.B. and Rassool, F.V. (2011) Human induced pluripotent cells resemble embryonic stem cells demonstrating enhanced levels of DNA repair and efficacy of nonhomologous end-joining. Mutat. Res., 713, 8-17.
14. Hong, Y., Cervantes, R.B., Tichy, E., Tischfield, J.A. and Stambrook, P.J. (2007) Protecting genomic integrity in somatic cells and embryonic stem cells. Mutat. Res., 614, 48-55.
15. Andang, M., Moliner, A., Doege, C.A., Ibanez, C.F. and Ernfors, P. (2008) Optimized mouse ES cell culture system by suspension growth in a fully defined medium. Nat. Protoc., 3, 1013-1017.
16. Andang, M., Hjerling-Leffler, J., Moliner, A., Lundgren, T.K., Castelo-Branco, G., Nanou, E., Pozas, E., Bryja, V., Halliez, S., Nishimaru, H. et al. (2008) Histone H2AX-dependent GABA(A) receptor regulation of stem cell proliferation. Nature, 451, 460-464.
17. Ying, Q.L. and Smith, A.G. (2003) Defined conditions for neural commitment and differentiation. Methods Enzymol., 365, 327-341.
18. Aranda, S., Alvarez, M., Turro, S., Laguna, A. and de la Luna, S. (2008) Sprouty2-mediated inhibition of fibroblast growth factor signaling is modulated by the protein kinase DYRK1A. Mol. Cell. Biol., 28, 5899-5911.
19. Lou, H., Komata, M., Katou, Y., Guan, Z., Reis, C.C., Budd, M., Shirahige, K. and Campbell, J.L. (2008) Mrc1 and DNA polymerase epsilon function together in linking DNA replication and the S phase checkpoint. Mol. Cell, 32, 106-117.
20. Gambus, A., Jones, R.C., Sanchez-Diaz, A., Kanemaki, M., van Deursen, F., Edmondson, R.D. and Labib, K. (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks.Nat. Cell Biol., 8, 358-366.
21. Cardoso, M.C., Leonhardt, H. and Nadal-Ginard, B. (1993) Reversal of terminal differentiation and control of DNA replication: Cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell, 74, 979-992.
22. Taddei, A., Roche, D., Sibarita, J.B., Turner, B.M. and Almouzni, G. (1999) Duplication and maintenance of heterochromatin domains. J. Cell Biol., 147, 1153-1166.
23. Atchison, L., Ghias, A., Wilkinson, F., Bonini, N. and Atchison, M.L. (2003) Transcription factor YY1 functions as a PcG protein in vivo. EMBO J., 22, 1347-1358.
24. Wilkinson, F.H., Park, K. and Atchison, M.L. (2006) Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proc. Natl. Acad. Sci. U.S.A., 103, 19296-19301.
25. Cohen, P.T., Philp, A. and Vazquez-Martin, C. (2005) Protein phosphatase 4-from obscurity to vital functions. FEBS Lett., 579, 3278-3286.
26. Hombauer, H., Campbell, C.S., Smith, C.E., Desai, A. and Kolodner, R.D. (2011) Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell, 147, 1040-1053.
27. Yang, X.J. and Seto, E. (2003) Collaborative spirit of histone deacetylases in regulating chromatin structure and gene expression. Curr. Opin. Genet. Dev., 13, 143-153.
28. Clapier, C.R. and Cairns, B.R. (2009) The biology of chromatin remodeling complexes. Annu. Rev. Biochem., 78, 273-304.
29. Dovey, O.M., Foster, C.T. and Cowley, S.M. (2010) Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc. Natl. Acad. Sci. U.S.A., 107, 8242-8247.
30. Guetg, C., Scheifele, F., Rosenthal, F., Hottiger, M.O. and Santoro, R. (2012) Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol. Cell, 45, 790-800.
31. Bozhenok, L., Wade, P.A. and Varga-Weisz, P. (2002) WSTF-ISWI chromatin remodeling complex targets heterochromatic replication foci. EMBO J., 21, 2231-2241.
32. Sharif, J., Muto, M., Takebayashi, S., Suetake, I., Iwamatsu, A., Endo, T.A., Shinga, J., Mizutani-Koseki, Y., Toyoda, T., Okamura, K. et al. (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature, 450, 908-912.
33. Rowbotham, S.P., Barki, L., Neves-Costa, A., Santos, F., Dean, W., Hawkes, N., Choudhary, P., Will, W.R., Webster, J., Oxley, D. et al. (2011) Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell, 42, 285-296.
34. Kim, J.K., Esteve, P.O., Jacobsen, S.E. and Pradhan, S. (2009) UHRF1 binds G9a and participates in p21 transcriptional regulation in mammalian cells. Nucleic Acids Res., 37, 493-505.
35. Alabert, C. and Groth, A. (2012) Chromatin replication and epigenome maintenance.Nat. Rev. Mol. Cell Biol., 13, 153-167.
36. Scharf, A.N., Barth, T.K. and Imhof, A. (2009) Establishment of histone modifications after chromatin assembly. Nucleic Acids Res., 37, 5032-5040.
37. Zee, B.M., Britton, L.M., Wolle, D., Haberman, D.M. and Garcia, B.A. (2012) Origins and formation of histone methylation across the human cell cycle. Mol. Cell. Biol., 32, 2503-2514.
38. Xu, M., Wang, W., Chen, S. and Zhu, B. (2012) A model for mitotic inheritance of histone lysine methylation. EMBO Rep., 13, 60-67.
39. Bantscheff, M., Hopf, C., Savitski, M.M., Dittmann, A., Grandi, P., Michon, A.M., Schlegl, J., Abraham, Y., Becher, I., Bergamini, G. et al. (2011) Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat. Biotechnol., 29, 255-265.
40. Huangfu, D., Maehr, R., Guo, W., Eijkelenboom, A., Snitow, M., Chen, A.E. and Melton, D.A. (2008) Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat. Biotechnol., 26, 795-797.
41. Huangfu, D., Osafune, K., Maehr, R., Guo, W., Eijkelenboom, A., Chen, S., Muhlestein, W. and Melton, D.A. (2008) Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat. Biotechnol., 26, 1269-1275.
42. Sakaue-Sawano, A., Kurokawa, H., Morimura, T., Hanyu, A., Hama, H., Osawa, H., Kashiwagi, S., Fukami, K., Miyata, T., Miyoshi, H. et al. (2008) Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell, 132, 487-498.
43. Quesney-Huneeus, V., Wiley, M.H. and Siperstein, M.D. (1979) Essential role for mevalonate synthesis in DNA replication. Proc. Natl. Acad. Sci. U.S.A., 76, 5056-5060.
44. Lee, M.H., Cho, Y.S. and Han, Y.M. (2007) Simvastatin suppresses self-renewal of mouse embryonic stem cells by inhibiting RhoA geranylgeranylation. Stem Cells, 25, 1654-1663.
45. Berthon, J., Fujikane, R. and Forterre, P. (2009) When DNA replication and protein synthesis come together. Trends Biochem. Sci., 34, 429-434.
46. Chodavarapu, S., Felczak, M.M. and Kaguni, J.M. (2011) Two forms of ribosomal protein L2 of Escherichia coli that inhibit DnaA in DNA replication. Nucleic Acids Res., 39, 4180-4191.
47. Li, J., Tan, J., Zhuang, L., Banerjee, B., Yang, X., Chau, J.F., Lee, P.L., Hande, M.P., Li, B. and Yu, Q. (2007) Ribosomal protein S27-like, a p53-inducible modulator of cell fate in response to genotoxic stress. Cancer Res., 67, 11317-11326.
48. Martins, S., Eikvar, S., Furukawa, K. and Collas, P. (2003) HA95 and LAP2 beta mediate a novel chromatin-nuclear envelope interaction implicated in initiation of DNA replication. J. Cell. Biol., 160, 177-188.
49. Kaufman, P.D. and Rando, O.J. (2010) Chromatin as a potential carrier of heritable information. Curr. Opin. Cell Biol., 22, 284-290.
50. Morey, L., Brenner, C., Fazi, F., Villa, R., Gutierrez, A., Buschbeck, M., Nervi, C., Minucci, S., Fuks, F. and Di Croce, L. (2008) MBD3, a component of the NuRD complex, facilitates chromatin alteration and deposition of epigenetic marks. Mol. Cell. Biol., 28, 5912-5923.
51. Reynolds, N., Salmon-Divon, M., Dvinge, H., Hynes-Allen, A., Balasooriya, G., Leaford, D., Behrens, A., Bertone, P. and Hendrich, B. (2012) NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J., 31, 593-605.
52. Sims, J.K. and Wade, P.A. (2011) Mi-2/NuRD complex function is required for normal S phase progression and assembly of pericentric heterochromatin. Mol. Biol. Cell, 22, 3094-3102.
53. Cartron, P.F., Blanquart, C., Hervouet, E., Gregoire, M. and Vallette, F.M. (2013) HDAC1-mSin3a-NCOR1, Dnmt3b-HDAC1-Egr1 and Dnmt1-PCNA-UHRF1-G9a regulate the NY-ESO1 gene expression. Mol. Oncol., 7, 452-463.
54. Sarraf, S.A. and Stancheva, I. (2004) Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell, 15, 595-605.
55. Esteve, P.O., Chin, H.G., Smallwood, A., Feehery, G.R., Gangisetty, O., Karpf, A.R., Carey, M.F. and Pradhan, S. (2006) Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev., 20, 3089-3103.
56. Helleday, T., Petermann, E., Lundin, C., Hodgson, B. and Sharma, R.A. (2008) DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer, 8, 193-204.
57. Nathanson, D.A., Gini, B., Mottahedeh, J., Visnyei, K., Koga, T., Gomez, G., Eskin, A., Hwang, K., Wang, J., Masui, K. et al. (2014) Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA. Science, 343, 72-76.
58. Johnson, B.E., Mazor, T., Hong, C., Barnes, M., Aihara, K., McLean, C.Y., Fouse, S.D., Yamamoto, S., Ueda, H., Tatsuno, K. et al. (2014) Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science, 343, 189-193.