Smads orchestrate specific histone modifications and chromatin remodeling to activate transcription

EMBO Journal

Volumn 25, Issue 19, 2006, Pages 4490-4502

  Ross, Sarah ^a   Cheung, Edwin ^b,c   Petrakis, Thodoris G ^a   Howell, Michael ^a   Kraus, W Lee ^b   Hill, Caroline S ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b Department of Obstetrics Gynecology   (United States)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

Brg1; Chromatin; Smad; TGF ; Transcription

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE H3; LYSINE; NAKED DNA; PROTEIN P300; PROTEIN SWI; SMAD PROTEIN; SMAD2 PROTEIN; SMAD4 PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; TRANSCRIPTION INITIATION;

ACETYLATION; ANIMALS; CELLS, CULTURED; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; HELA CELLS; HISTONES; HUMANS; MICE; MODELS, GENETIC; NIH 3T3 CELLS; NUCLEAR PROTEINS; P300-CBP TRANSCRIPTION FACTORS; PHOSPHORYLATION; PROTEIN BINDING; SMAD2 PROTEIN; SMAD4 PROTEIN; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 33749344476     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601332     Document Type: Article

References (45)

1. Alberts AS, Geneste O, Treisman R (1998) Activation of SRF-regulated chromosomal templates by Rho-family GTPases requires a signal that also induces H4 hyperacetylation. Cell 92: 475-487
2. Cereghini S, Yaniv M (1984) Assembly of transfected DNA into chromatin: structural changes in the origin-promoter-enhancer region upon replication. EMBO J 3: 1243-1253
3. Chacko BM, Qin BY, Tiwari A, Shi G, Lam S, Hayward LJ, De Caestecker M, Lin K (2004) Structural basis of heteromeric smad protein assembly in TGF-b signaling. Mol Cell 15: 813-823
4. Cheung E, Schwabish MA, Kraus WL (2003) Chromatin exposes intrinsic differences in the transcriptional activities of estrogen receptors α and β. EMBO J 22: 600-611
5. Conaway RC, Sato S, Tomomori-Sato C, Yao T, Conaway JW (2005) The mammalian Mediator complex and its role in transcriptional regulation. Trends Biochem Sci 30: 250-255
6. Cote J, Utley RT, Workman JL (1995) Basic analysis of transcription factor binding to nucleosomes. Methods Mol Genet 6: 108-128
7. Daujat S, Bauer UM, Shah V, Turner B, Berger S, Kouzarides T (2002) Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr Biol 12: 2090-2097
8. de Caestecker MP, Yahata T, Wang D, Parks WT, Huang S, Hill CS, Shioda T, Roberts AB, Lechleider RJ (2000) The Smad4 activation domain (SAD) is a proline-rich, p300-dependent transcriptional activation domain. J Biol Chem 275: 2115-2122
9. de la Cruz X, Lois S, Sanchez-Molina S, Martinez-Balbas MA (2005) Do protein motifs read the histone code? Bioessays 27: 164-175
10. Feng XH, Zhang Y, Wu RY, Derynck R (1998) The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for Smad3 in TGF-β-induced transcriptional activation. Genes Dev 12: 2153-2163
11. Hata A, Lo RS, Wotton D, Lagna G, Massagué J (1997) Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 388: 82-87
12. He W, Dorn DC, Erdjument-Bromage H, Tempst P, Moore MA, Massague J (2006) Hematopoiesis controlled by distinct TIF1γ and Smad4 branches of the TGFb pathway. Cell 125: 929-941
13. Howell M, Inman GJ, Hill CS (2002) A novel Xenopus Smad-interacting forkhead transcription factor (XFast-3) cooperates with XFast-1 in regulating gastrulation movements. Development 129: 2823-2834
14. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, Laping NJ, Hill CS (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 62: 65-74
15. Jones KA, Kadonaga JT, Rosenfeld PJ, Kelly TJ, Tjian R (1987) A cellular DNA-binding protein that activates eukaryotic transcription and DNA replication. Cell 48: 79-89
16. Kato Y, Habas R, Katsuyama Y, Naar AM, He X (2002) A component of the ARC/Mediator complex required for TGF β/Nodal signalling. Nature 418: 641-646
17. Kraus WL, Kadonaga JT (1998) p300 and estrogen receptor cooperatively activate transcription via differential enhancement of initiation and reinitiation. Genes Dev 12: 331-342
18. Lau OD, Kundu TK, Soccio RE, Ait-Si-Ali S, Khalil EM, Vassilev A, Wolffe AP, Nakatani Y, Roeder RG, Cole PA (2000) HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol Cell 5: 589-595
19. Lee KA, Green MR (1987) A cellular transcription factor E4F1 interacts with an E1a-inducible enhancer and mediates constitutive enhancer function in vitro. EMBO J 6: 1345-1353
20. Lehmann M (2004) Anything else but GAGA: a nonhistone protein complex reshapes chromatin structure. Trends Genet 20: 15-22
21. Lemon B, Inouye C, King DS, Tjian R (2001) Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 414: 924-928
22. Levy L, Hill CS (2006) Alterations in components of the TGF-β superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev 17: 41-58
23. Lin YS, Carey MF, Ptashne M, Green MR (1988) GAL4 derivatives function alone and synergistically with mammalian activators in vitro. Cell 54: 659-664
24. Liu F, Hata A, Baker JC, Doody J, Carcamo J, Harland RM, Massague J (1996) A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381: 620-623
25. Liu F, Pouponnot C, Massague J (1997) Dual role of the Smad4/DPC4 tumor suppressor in TGFβ-inducible transcriptional complexes. Genes Dev 11: 3157-3167
26. Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ (1997) Characterization of nucleosome core particles containing histone proteins made in bacteria. J Mol Biol 272: 301-311
27. Massagué J, Seoane J, Wotton D (2005) Smad transcription factors. Genes Dev 19: 2783-2810
28. Narlikar GJ, Fan HY, Kingston RE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475-487
29. Norman C, Runswick M, Pollock R, Treisman R (1988) Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55: 989-1003
30. Pierreux CE, Nicolás FJ, Hill CS (2000) Transforming growth factor β-independent shuttling of Smad4 between the cytoplasm and nucleus. Mol Cell Biol 20: 9041-9054
31. Randall RA, Germain S, Inman GJ, Bates PA, Hill CS (2002) Different Smad2 partners bind a common hydrophobic pocket in Smad2 via a defined proline-rich motif. EMBO J 21: 145-156
32. Randall RA, Howell M, Page CS, Daly A, Bates PA, Hill CS (2004) Recognition of phosphorylated-Smad2-containing complexes by a novel Smad interaction motif. Mol Cell Biol 24: 1106-1121
33. Roberts CW, Orkin SH (2004) The SWI/SNF complex-chromatin and cancer. Nat Rev Cancer 4: 133-142
34. Roeder RG (2005) Transcriptional regulation and the role of diverse coactivators in animal cells. FEBS Lett 579: 909-915
35. Rudnicki MA, McBurney MW (1987) Cell culture methods and induction of differentiation of embryonal carcinoma cell lines. In Teratocarcinoma and Embryonic Stem Cells. A Pratical Approach, Robertson E (ed), pp 19-50. Oxford/Washington, DC: IRL Press
36. Ryu S, Zhou S, Ladurner AG, Tjian R (1999) The transcriptional cofactor complex CRSP is required for activity of the enhancer-binding protein Sp1. Nature 397: 446-450
37. Saijoh Y, Adachi H, Sakuma R, Yeo CY, Yashiro K, Watanabe M, Hashiguchi H, Mochida K, Ohishi S, Kawabata M, Miyazono K, Whitman M, Hamada H (2000) Left-right asymmetric expression of lefty2 and nodal is induced by a signaling pathway that includes the transcription factor FAST2. Mol Cell 5: 35-47
38. Schiltz RL, Mizzen CA, Vassilev A, Cook RG, Allis CD, Nakatani Y (1999) Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J Biol Chem 274: 1189-1192
39. Schmierer B, Hill CS (2005) Kinetic analysis of Smad nucleocytoplasmic shuttling reveals a mechanism for transforming growth factor β-dependent nuclear accumulation of Smads. Mol Cell Biol 25: 9845-9858
40. Steger DJ, Eberharter A, John S, Grant PA, Workman JL (1998) Purified histone acetyltransferase complexes stimulate HIV-1 transcription from preassembled nucleosomal arrays. Proc Natl Acad Sci USA 95: 12924-12929
41. Stroschein SL, Wang W, Zhou S, Zhou Q, Luo K (1999) Negative feedback regulation of TGF-β signaling by the SnoN oncoprotein. Science 286: 771-774
42. ten Dijke P, Hill CS (2004) New insights into TGF-β-Smad signalling. Trends Biochem Sci 29: 265-273
43. Vo N, Goodman RH (2001) CREB-binding protein and p300 in transcriptional regulation. J Biol Chem 276: 13505-13508
44. Wang G, Long J, Matsuura I, He D, Liu F (2005) The Smad3 linker region contains a transcriptional activation domain. Biochem J 386: 29-34
45. Wu R-Y, Zhang Y, Feng X-H, Derynck R (1997) Heteromeric and homomeric interactions correlate with signaling activity and functional cooperativity of Smad3 and Smad4/DPC4. Mol Cell Biol 17: 2521-2528