The Histone H2B Monoubiquitination Regulatory Pathway Is Required for Differentiation of Multipotent Stem Cells

Molecular Cell

Volumn 46, Issue 5, 2012, Pages 705-713

  Karpiuk, Oleksandra ^a   Najafova, Zeynab ^a,b   Kramer, Frank ^a   Hennion, Magali ^a   Galonska, Christina ^a   König, Annekatrin ^c   Snaidero, Nicolas ^d   Vogel, Tanja ^e   Shchebet, Andrei ^a   Begus Nahrmann, Yvonne ^a   Kassem, Moustapha ^f,g   Simons, Mikael ^a,d   Shcherbata, Halyna ^c   Beissbarth, Tim ^a   Johnsen, Steven A ^a,b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^e UNIVERSITY OF FREIBURG   (Germany)

^f UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^g KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CYCLIN DEPENDENT KINASE 9; HISTONE H2B; PROTEIN RNF40; PROTEIN WAC; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CHROMOSOME BIVALENT; CONTROLLED STUDY; HISTONE MODIFICATION; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; NUCLEAR REPROGRAMMING; REGULATORY MECHANISM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL DIFFERENTIATION; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYCLIN-DEPENDENT KINASE 9; HISTONES; HUMANS; MESENCHYMAL STEM CELLS; MULTIPOTENT STEM CELLS; PROTEIN PROCESSING, POST-TRANSLATIONAL; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84861994785     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.05.022     Document Type: Article

References (36)

1. Azuara V., Perry P., Sauer S., Spivakov M., Jorgensen H.F., John R.M., Gouti M., Casanova M., Warnes G., Merkenschlager M., Fisher A.G. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 2006, 8:532-538.
2. Batchelder C., Dunn M.A., Choy B., Suh Y., Cassie C., Shim E.Y., Shin T.H., Mello C., Seydoux G., Blackwell T.K. Transcriptional repression by the Caenorhabditis elegans germ-line protein PIE-1. Genes Dev. 1999, 13:202-212.
3. Bernstein B.E., Mikkelsen T.S., Xie X., Kamal M., Huebert D.J., Cuff J., Fry B., Meissner A., Wernig M., Plath K., et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125:315-326.
4. Bernstein B.E., Stamatoyannopoulos J.A., Costello J.F., Ren B., Milosavljevic A., Meissner A., Kellis M., Marra M.A., Beaudet A.L., Ecker J.R., et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat. Biotechnol. 2010, 28:1045-1048.
5. Buszczak M., Paterno S., Spradling A.C. Drosophila stem cells share a common requirement for the histone H2B ubiquitin protease scrawny. Science 2009, 323:248-251.
6. Collas P. Programming differentiation potential in mesenchymal stem cells. Epigenetics 2010, 5:476-482.
7. Fisher C.L., Fisher A.G. Chromatin states in pluripotent, differentiated, and reprogrammed cells. Curr. Opin. Genet. Dev. 2011, 21:140-146.
8. Gaspar-Maia A., Alajem A., Polesso F., Sridharan R., Mason M.J., Heidersbach A., Ramalho-Santos J., McManus M.T., Plath K., Meshorer E., Ramalho-Santos M. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 2009, 460:863-868.
9. Gomes N.P., Bjerke G., Llorente B., Szostek S.A., Emerson B.M., Espinosa J.M. Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev. 2006, 20:601-612.
10. Guenther M.G., Levine S.S., Boyer L.A., Jaenisch R., Young R.A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130:77-88.
11. Hanyu-Nakamura K., Sonobe-Nojima H., Tanigawa A., Lasko P., Nakamura A. Drosophila Pgc protein inhibits P-TEFb recruitment to chromatin in primordial germ cells. Nature 2008, 451:730-733.
12. Harris S.A., Enger R.J., Riggs B.L., Spelsberg T.C. Development and characterization of a conditionally immortalized human fetal osteoblastic cell line. J. Bone Miner. Res. 1995, 10:178-186.
13. Iankova I., Petersen R.K., Annicotte J.S., Chavey C., Hansen J.B., Kratchmarova I., Sarruf D., Benkirane M., Kristiansen K., Fajas L. Peroxisome proliferator-activated receptor gamma recruits the positive transcription elongation factor b complex to activate transcription and promote adipogenesis. Mol. Endocrinol. 2006, 20:1494-1505.
14. Johnsen S.A. The enigmatic role of H2Bub1 in cancer. FEBS Lett. 2012, 586:1592-1601.
15. Kaichi S., Takaya T., Morimoto T., Sunagawa Y., Kawamura T., Ono K., Shimatsu A., Baba S., Heike T., Nakahata T., Hasegawa K. Cyclin-dependent kinase 9 forms a complex with GATA4 and is involved in the differentiation of mouse ES cells into cardiomyocytes. J. Cell. Physiol. 2011, 226:248-254.
16. Kelley D.E., Stokes D.G., Perry R.P. CHD1 interacts with SSRP1 and depends on both its chromodomain and its ATPase/helicase-like domain for proper association with chromatin. Chromosoma 1999, 108:10-25.
17. Kim J., Guermah M., McGinty R.K., Lee J.S., Tang Z., Milne T.A., Shilatifard A., Muir T.W., Roeder R.G. RAD6-mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 2009, 137:459-471.
18. Lee J.S., Garrett A.S., Yen K., Takahashi Y.H., Hu D., Jackson J., Seidel C., Pugh B.F., Shilatifard A. Codependency of H2B monoubiquitination and nucleosome reassembly on Chd1. Genes Dev. 2012, 26:914-919.
19. Meissner A. Epigenetic modifications in pluripotent and differentiated cells. Nat. Biotechnol. 2010, 28:1079-1088.
20. Minsky N., Shema E., Field Y., Schuster M., Segal E., Oren M. Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat. Cell Biol. 2008, 10:483-488.
21. Noer A., Lindeman L.C., Collas P. Histone H3 modifications associated with differentiation and long-term culture of mesenchymal adipose stem cells. Stem Cells Dev. 2009, 18:725-736.
22. Park G., Gong Z., Chen J., Kim J.E. Characterization of the DOT1L network: implications of diverse roles for DOT1L. Protein J. 2010, 29:213-223.
23. Pavri R., Zhu B., Li G., Trojer P., Mandal S., Shilatifard A., Reinberg D. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 2006, 125:703-717.
24. Pirngruber J., Shchebet A., Johnsen S.A. Insights into the function of the human P-TEFb component CDK9 in the regulation of chromatin modifications and co-transcriptional mRNA processing. Cell Cycle 2009, 8:3636-3642.
25. Pirngruber J., Shchebet A., Schreiber L., Shema E., Minsky N., Chapman R.D., Eick D., Aylon Y., Oren M., Johnsen S.A. CDK9 directs H2B monoubiquitination and controls replication-dependent histone mRNA 3' end processing. EMBO Rep. 2009, 10:894-900.
26. Prenzel T., Begus-Nahrmann Y., Kramer F., Hennion M., Hsu C., Gorsler T., Hintermair C., Eick D., Kremmer E., Simons M., et al. Estrogen-dependent gene transcription in human breast cancer cells relies upon proteasome-dependent monoubiquitination of histone H2B. Cancer Res. 2011, 71:5739-5753.
27. Shchebet A., Karpiuk O., Kremmer E., Eick D., Johnsen S.A. Phosphorylation of cyclin-dependent kinase-9 controls ubiquitin-conjugating enzyme-2A function. Cell Cycle 2012, 11:1-6.
28. Shema E., Tirosh I., Aylon Y., Huang J., Ye C., Moskovits N., Raver-Shapira N., Minsky N., Pirngruber J., Tarcic G., et al. The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev. 2008, 22:2664-2676.
29. Simone C., Stiegler P., Bagella L., Pucci B., Bellan C., De Falco G., De Luca A., Guanti G., Puri P.L., Giordano A. Activation of MyoD-dependent transcription by cdk9/cyclin T2. Oncogene 2002, 21:4137-4148.
30. Simonsen J.L., Rosada C., Serakinci N., Justesen J., Stenderup K., Rattan S.I., Jensen T.G., Kassem M. Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat. Biotechnol. 2002, 20:592-596.
31. Sims R.J., Millhouse S., Chen C.F., Lewis B.A., Erdjument-Bromage H., Tempst P., Manley J.L., Reinberg D. Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol. Cell 2007, 28:665-676.
32. Vethantham V., Yang Y., Bowman C., Asp P., Lee J.H., Skalnik D.G., Dynlacht B.D. Dynamic loss of H2B ubiquitylation without corresponding changes in H3K4 tri-methylation during myogenic differentiation. Mol. Cell Biol. 2012, 32:1044-1055.
33. Yu W., Wang Y., Shaw C.A., Qin X.F., Rice A.P. Induction of the HIV-1 Tat co-factor cyclin T1 during monocyte differentiation is required for the regulated expression of a large portion of cellular mRNAs. Retrovirology 2006, 3:32. 10.1186/1742-4690-3-32.
34. Zhang F., Yu X. WAC, a functional partner of RNF20/40, regulates histone H2B ubiquitination and gene transcription. Mol. Cell 2011, 41:384-397.
35. Zhang F., Barboric M., Blackwell T.K., Peterlin B.M. A model of repression: CTD analogs and PIE-1 inhibit transcriptional elongation by P-TEFb. Genes Dev. 2003, 17:748-758.
36. Zhu B., Zheng Y., Pham A.D., Mandal S.S., Erdjument-Bromage H., Tempst P., Reinberg D. Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol. Cell 2005, 20:601-611.