Histone deacetylase inhibition accelerates the early events of stem cell differentiation: Transcriptomic and epigenetic analysis

Genome Biology

Volumn 9, Issue 4, 2008, Pages

  Karantzali, Efthimia ^a,b   Schulz, Herbert ^c   Hummel, Oliver ^c   Hubner, Norbert ^c   Hatzopoulos, A K ^d,e   Kretsovali, Androniki ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; EMBRYONIC ECTODERM DEVELOPMENT PROTEIN; FIBROBLAST GROWTH FACTOR 4; GENE PRODUCT; HISTONE ACETYLTRANSFERASE PCAF; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; KRUPPEL LIKE FACTOR 4; LYSINE; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN CBX5; PROTEIN ERAS; PROTEIN FOS; PROTEIN GDF3; PROTEIN GLI2; PROTEIN LEFTY2; PROTEIN SALL1; PROTEIN SALL4; PROTEIN TCL1; PROTEIN UTX; PROTEIN ZIC3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXD3; TRANSCRIPTION FACTOR HOXA1; TRANSCRIPTION FACTOR HOXB13; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRICHOSTATIN A; HISTONE; HYDROXAMIC ACID;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA MICROARRAY; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PROTEIN METHYLATION; TRANSCRIPTION REGULATION; ACETYLATION; ANIMAL; CYTOLOGY; DRUG EFFECT; GENETIC EPIGENESIS; METABOLISM;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONES; HYDROXAMIC ACIDS; MICE;

EID: 47149108349     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2008-9-4-r65     Document Type: Article

References (46)

1. Boiani M Scholer HR Regulatory networks in embryo-derived pluripotent stem cells. Nat Rev Mol Cell Biol 2005, 6:872-884. 10.1038/nrm1744 16227977
2. Niwa H How is pluripotency determined and maintained? Development 2007, 134:635-646. 10.1242/dev.02787 17215298
3. Niwa H Burdon T Chambers I Smith A Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 1998, 12:2048-2060. 316954 9649508 10.1101/gad.12.13.2048
4. Ying QL Nichols J Chambers I Smith A BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 2003, 115:281-292. 10.1016/ S0092-8674(03)00847-X 14636556
5. Sato N Meijer L Skaltsounis L Greengard P Brivanlou AH Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004, 10:55-63. 10.1038/nm979 14702635
6. Boyer LA Lee TI Cole MF Johnstone SE Levine SS Zucker JP Guenther MG Kumar RM Murray HL Jenner RG Gifford DK Melton DA Jaenisch R Young RA Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956. 10.1016/j.cell.2005.08.020 16153702
7. Loh YH Wu Q Chew JL Vega VB Zhang W Chen X Bourque G George J Leong B Liu J Wong KY Sung KW Lee CW Zhao XD Chiu KP Lipovich L Kuznetsov VA Robson P Stanton LW Wei CL Ruan Y Lim B Ng HH The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006, 38:431-440. 10.1038/ng1760 16518401
8. Takahashi K Yamanaka S Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676. 10.1016/j.cell.2006.07.024 16904174
9. Zhang J Tam WL Tong GQ Wu Q Chan HY Soh BS Lou Y Yang J Ma Y Chai L Ng HH Lufkin T Robson P Lim B Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat Cell Biol 2006, 8:1114-1123. 10.1038/ncb1481 16980957
10. Ivanova N Dobrin R Lu R Kotenko I Levorse J DeCoste C Schafer X Lun Y Lemischka IR Dissecting self-renewal in stem cells with RNA interference. Nature 2006, 442:533-538. 10.1038/nature04915 16767105
11. Wang J Rao S Chu J Shen X Levasseur DN Theunissen TW Orkin SH A protein interaction network for pluripotency of embryonic stem cells. Nature 2006, 444:364-368. 10.1038/nature05284 17093407
12. Fischle W Wang Y Allis CD Histone and chromatin cross-talk. Curr Opin Cell Biol 2003, 15:172-183. 10.1016/S0955-0674(03)00013-9 12648673
13. Margueron R Trojer P Reinberg D The key to development: Interpreting the histone code? Curr Opin Genet Dev 2005, 15:163-176. 10.1016/ j.gde.2005.01.005 15797199
14. Kouzarides T Chromatin modifications and their function. Cell 2007, 128:693-705. 10.1016/j.cell.2007.02.005 17320507
15. Meshorer E Yellajoshula D George E Scambler PJ Brown DT Misteli T Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 2006, 10:105-116. 1868458 16399082 10.1016/ j.devcel.2005.10.017
16. Mikkelsen TS Ku M Jaffe DB Issac B Lieberman E Giannoukos G Alvarez P Brockman W Kim TK Koche RP Lee W Mendenhall E O'Donovan A Presser A Russ C Xie X Meissner A Wernig M Jaenisch R Nusbaum C Lander ES Bernstein BE Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560. 10.1038/nature06008 17603471
17. Pan J Tian S Nie J Yang C Ruotti V Wei H Jonsdottir G Stewart R Thomson J Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 2007, 1:299-312. 10.1016/ j.stem.2007.08.003 18371364
18. Lee TI Jenner RG Boyer LA Guenther MG Levine SS Kumar RM Chevalier B Johnstone SE Cole MF Isono K Koseki H Fuchikami T Abe K Murray HL Zucker JP Yuan B Bell GW Herbolsheimer E Hannett NM Sun K Odom DT Otte AP Volkert TL Bartel DP Melton DA Gifford DK Jaenisch R Young RA Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125:301-313. 10.1016/j.cell.2006.02.043 16630818
19. Boyer LA Plath K Zeitlinger J Brambrink T Medeiros LA Lee TI Levine SS Wernig M Tajonar A Ray MK Bell GW Otte AP Vidal M Gifford DK Young RA Jaenisch R Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441:349-353. 10.1038/nature04733 16625203
20. Bernstein BE Mikkelsen TS Xie X Kamal M Huebert DJ Cuff J Fry B Meissner A Wernig M Plath K Jaenisch R Wagschal A Feil R Schreiber SL Lander ES A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125:315-326. 10.1016/j.cell.2006.02.041 16630819
21. Azuara V Perry P Sauer S Spivakov M Jørgensen HF John RM Gouti M Casanova M Warnes G Merkenschlager M Fisher AG Chromatin signatures of pluripotent cell lines. Nat Cell Biol 2006, 8:532-538. 10.1038/ncb1403 16570078
22. Zhao XD Han X Chew JL Liu J Chiu KP Choo A Orlov YL Sung WK Shahab A Kuznetsov VA Bourque G Oh S Ruan Y Ng HH Wei CL Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 2007, 1:286-298. 10.1016/j.stem.2007.08.004 18371363
23. Barski A Cuddapah S Cui K Roh TY Schones DE Wang Z Wei G Chepelev I Zhao K High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837. 10.1016/j.cell.2007.05.009 17512414
24. Spivakov M Fisher AG Epigenetic signatures of stem-cell identity. Nat Rev Genet 2007, 8:263-271. 10.1038/nrg2046 17363975
25. Bernstein BE Meissner A Lander ES The mammalian epigenome. Cell 2007, 128:669-681. 10.1016/j.cell.2007.01.033 17320505
26. Surani MA Hayashi K Hajkova P Genetic and epigenetic regulators of pluripotency. Cell 2007, 128:747-762. 10.1016/j.cell.2007.02.010 17320511
27. Torres-Padilla ME Parfitt DE Kouzarides T Zernicka-Goetz M Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007, 445:214-218. 10.1038/nature05458 17215844
28. Wu Q Chen X Zhang J Loh YH Low TY Zhang W Zhang W Sze SK Lim B Ng HH Sall4 interacts with Nanog and co-occupies Nanog genomic sites in embryonic stem cells. J Biol Chem 2006, 281:24090-24094. 10.1074/ jbc.C600122200 16840789
29. Kuroda T Tada M Kubota H Kimura H Hatano SY Suemori H Nakatsuji N Tada T Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 2005, 25:2475-2485. 1061601 15743839 10.1128/MCB.25.6.2475-2485.2005
30. Rodda DJ Chew JL Lim LH Loh YH Wang B Ng HH Robson P Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005, 280:24731-24737. 10.1074/jbc.M502573200 15860457
31. Dennis G Jr Sherman BT Hosack DA Yang J Gao W Lane HC Lempicki RA DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003, 4:P3. 10.1186/gb-2003-4-5-p3 12734009
32. Lee ER Murdoch FE Fritsch MK High histone acetylation and decreased polycomb repressive complex 2 member levels regulate gene specific transcriptional changes during early embryonic stem cell differentiation induced by retinoic acid. Stem Cells 2007, 25:2191-2199. 10.1634/ stemcells.2007-0203 17525233
33. Taddei A Roche D Bickmore WA Almouzni G The effects of histone deacetylase inhibitors on heterochromatin: Implications for anticancer therapy? EMBO Rep 2005, 6:520-524. 1369099 15940285 10.1038/ sj.embor.7400441
34. Gregory RI O'Neill LP Randall TE Fournier C Khosla S Turner BM Feil R Inhibition of histone deacetylases alters allelic chromatin conformation at the imprinted U2af1-rs1 locus in mouse embryonic stem cells. J Biol Chem 2002, 277:11728-11734. 10.1074/jbc.M105775200 11821379
35. Lee JH Hart SR Skalnik DG Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 2004, 38:32-38. 10.1002/ gene.10250 14755802
36. Kawamura T Ono K Morimoto T Wada H Hirai M Hidaka K Morisaki T Heike T Nakahata T Kita T Hasegawa K Acetylation of GATA-4 is involved in the differentiation of embryonic stem cells into cardiac myocytes. J Biol Chem 2005, 280:19682-19688. 10.1074/jbc.M412428200 15764815
37. Balasubramaniyan V Boddeke E Bakels R Kust B Kooistra S Veneman A Copray S Effects of histone deacetylation inhibition on neuronal differentiation of embryonic mouse neural stem cells. Neuroscience 2006, 143:939-951. 10.1016/j.neuroscience.2006.08.082 17084985
38. McCool KW Xu X Singer DB Murdoch FE Fritsch MK The role of histone acetylation in regulating early gene expression patterns during early embryonic stem cell differentiation. J Biol Chem 2007, 282:6696-6706. 10.1074/jbc.M609519200 17204470
39. Zupkovitz G Tischler J Posch M Sadzak I Ramsauer K Egger G Grausenburger R Schweifer N Chiocca S Decker T Seiser C Negative and positive regulation of gene expression by mouse histone deacetylase 1. Mol Cell Biol 2006, 26:7913-7928. 1636735 16940178 10.1128/MCB.01220-06
40. Schuettengruber B Chourrout D Vervoort M Leblanc B Cavalli G Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745. 10.1016/j.cell.2007.02.009 17320510
41. Christensen J Agger K Cloos PA Pasini D Rose S Sennels L Rappsilber J Hansen KH Salcini AE Helin K RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 2007, 128:1063-1076. 10.1016/j.cell.2007.02.003 17320161
42. Agger K Cloos PA Christensen J Pasini D Rose S Rappsilber J Issaeva I Canaani E Salcini AE Helin K UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007, 449:731-734. 10.1038/nature06145 17713478
43. Swigut T Wysocka J H3K27 demethylases, at long last. Cell 2007, 131:29-32. 10.1016/j.cell.2007.09.026 17923085
44. Irizarry RA Bolstad BM Collin F Cope LM Hobbs B Speed TP Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003, 31:15. 10.1093/nar/gng015
45. Benjamini Y Hochberg Y Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 1995, 57:289-300.
46. Eisen MB Spellman PT Brown PO Botstein D Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95:14863-14868. 24541 9843981 10.1073/pnas.95.25.14863