Pioneer factors and ATP-dependent chromatin remodeling factors interact dynamically: A new perspective: Multiple transcription factors can effect chromatin pioneer functions through dynamic interactions with ATP-dependent chromatin remodeling factors

BioEssays

Volumn 38, Issue 11, 2016, Pages 1150-1157

  Swinstead, Erin E ^a   Paakinaho, Ville ^a   Presman, Diego M ^a   Hager, Gordon L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

chromatin binding; dynamic assisted loading; estrogen receptor; FoxA1; glucocorticoid receptor; pioneer factors; residence time

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; STEROID RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; CELL MATURATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; HUMAN; NONHUMAN; PROTEIN FUNCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; ENHANCER REGION; METABOLISM; PROMOTER REGION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENHANCER ELEMENTS, GENETIC; HUMANS; MODELS, GENETIC; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS;

EID: 84992446138     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201600137     Document Type: Article

References (90)

1. Kornberg RD. 1974. Chromatin structure: a repeating unit of histones and DNA. Science 184: 868–71.
2. van Holde KE. 1988. Chromatin. Heidelberg: Springer-Verlag.
3. Voss TC, Hager GL. 2014. Dynamic regulation of transcriptional states by chromatin and transcription factors. Nat Rev Genet 15: 69–81.
4. Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25: 2227–41.
5. Bossard P, Zaret KS. 1998. GATA transcription factors as potentiators of gut endoderm differentiation. Development 125: 4909–17.
6. Gualdi R, Bossard P, Zheng M, Hamada Y, et al. 1996. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev 10: 1670–82.
7. Cirillo LA, McPherson CE, Bossard P, Stevens K, et al. 1998. Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. EMBO J 17: 244–54.
8. Cirillo LA, Zaret KS. 1999. An early developmental transcription factor complex that is more stable on nucleosome core particles than on free DNA. Mol Cell 4: 961–9.
9. Cirillo LA, Lin FR, Cuesta I, Friedman D, et al. 2002. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9: 279–89.
10. Morisaki T, Muller WG, Golob N, Mazza D, et al. 2014. Single-molecule analysis of transcription factor binding at transcription sites in live cells. Nat Commun 5: 4456.
11. Swinstead Erin E, Miranda Tina B, Paakinaho V, Baek S, et al. 2016. Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions. Cell 165: 593–605.
12. Sugo N, Morimatsu M, Arai Y, Kousoku Y, et al. 2015. Single-molecule imaging reveals dynamics of CREB transcription factor bound to its target sequence. Sci Rep 5: 10662.
13. Liu Z, Legant WR, Chen BC, Li L, et al. 2014. 3D imaging of Sox2 enhancer clusters in embryonic stem cells. Elife 3: e04236.
14. Chen J, Zhang Z, Li L, Chen BC, et al. 2014. Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156: 1274–85.
15. Ballare C, Castellano G, Gaveglia L, Althammer S, et al. 2012. Nucleosome-driven transcription factor binding and gene regulation. Mol Cell 49: 67–79.
16. Li G, Margueron R, Hu G, Stokes D, et al. 2010. Highly compacted chromatin formed in vitro reflects the dynamics of transcription activation in vivo. Mol Cell 38: 41–53.
17. Carroll JS, Liu XS, Brodsky AS, Li W, et al. 2005. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122: 33–43.
18. Laganiere J, Deblois G, Lefebvre C, Bataille AR, et al. 2005. Location analysis of estrogen receptor alpha target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc Natl Acad Sci USA 102: 11651–6.
19. Carroll JS, Meyer CA, Song J, Li W, et al. 2006. Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289–97.
20. Lupien M, Eeckhoute J, Meyer CA, Wang Q, et al. 2008. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132: 958–70.
21. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, et al. 2010. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet 43: 27–33.
22. Rigaud G, Roux J, Pictet R, Grange T. 1991. In vivo footprinting of rat TAT gene: dynamic interplay between the glucocorticoid receptor and a liver-specific factor. Cell 67: 977–86.
23. Kong SL, Li G, Loh SL, Sung WK, et al. 2011. Cellular reprogramming by the conjoint action of ERalpha, FOXA1, and GATA3 to a ligand-inducible growth state. Mol Syst Biol 7: 526.
24. Caizzi L, Ferrero G, Cutrupi S, Cordero F, et al. 2014. Genome-wide activity of unliganded estrogen receptor-alpha in breast cancer cells. Proc Natl Acad Sci USA 111: 4892–7.
25. Eisen JA, Sweder KS, Hanawalt PC. 1995. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res 23: 2715–23.
26. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273–304.
27. Smith CL, Peterson CL. 2005. ATP-dependent chromatin remodeling. Curr Top Dev Biol 65: 115–48.
28. Fairman-Williams ME, Guenther UP, Jankowsky E. 2010. SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 20: 313–24.
29. Phelan ML, Sif S, Narlikar GJ, Kingston RE. 1999. Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol Cell 3: 247–53.
30. Wang W, Cote J, Xue Y, Zhou S, et al. 1996. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J 15: 5370–82.
31. Wang W, Xue Y, Zhou S, Kuo A, et al. 1996. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev 10: 2117–30.
32. Eberharter A, Becker PB. 2004. ATP-dependent nucleosome remodelling: factors and functions. J Cell Sci 117: 3707–11.
33. Fyodorov DV, Kadonaga JT. 2002. Dynamics of ATP-dependent chromatin assembly by ACF. Nature 418: 897–900.
34. Goldmark JP, Fazzio TG, Estep PW, Church GM, et al. 2000. The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103: 423–33.
35. Langst G, Becker PB. 2001. Nucleosome mobilization and positioning by ISWI-containing chromatin-remodeling factors. J Cell Sci 114: 2561–8.
36. Marfella CG, Imbalzano AN. 2007. The Chd family of chromatin remodelers. Mutat Res 618: 30–40.
37. Hall JA, Georgel PT. 2007. CHD proteins: a diverse family with strong ties. Biochem Cell Biol 85: 463–76.
38. Woodage T, Basrai MA, Baxevanis AD, Hieter P, et al. 1997. Characterization of the CHD family of proteins. Proc Natl Acad Sci USA 94: 11472–7.
39. Stokes DG, Perry RP. 1995. DNA-binding and chromatin localization properties of CHD1. Mol Cell Biol 15: 2745–53.
40. Bao Y, Shen X. 2007. INO80 subfamily of chromatin remodeling complexes. Mutat Res 618: 18–29.
41. Ho L, Crabtree GR. 2010. Chromatin remodelling during development. Nature 463: 474–84.
42. Narlikar GJ, Sundaramoorthy R, Owen-Hughes T. 2013. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154: 490–503.
43. Morris SA, Baek S, Sung MH, John S, et al. 2014. Overlapping chromatin remodeling systems collaborate genome-wide at dynamic chromatin transitions. Nat Struct Mol Biol 21: 73–81.
44. Erdel F, Schubert T, Marth C, Langst G, et al. 2010. Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc Natl Acad Sci USA 107: 19873–8.
45. de Dieuleveult M, Yen K, Hmitou I, Depaux A, et al. 2016. Genome-wide nucleosome specificity and function of chromatin remodellers in ES cells. Nature 530: 113–6.
46. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663–76.
47. Kidder BL, Palmer S, Knott JG. 2009. SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells 27: 317–28.
48. Singhal N, Graumann J, Wu G, Arauzo-Bravo MJ, et al. 2010. Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141: 943–55.
49. Krishnakumar R, Chen AF, Pantovich MG, Danial M, et al. 2016. FOXD3 regulates pluripotent stem cell potential by simultaneously initiating and repressing enhancer activity. Cell Stem Cell 18: 104–17.
50. Wang L, Du Y, Ward JM, Shimbo T, et al. 2014. INO80 facilitates pluripotency gene activation in embryonic stem cell self-renewal, reprogramming, and blastocyst development. Cell Stem Cell 14: 575–91.
51. Fryer CJ, Nordeen SK, Archer TK. 1998. Antiprogestins mediate differential effects on glucocorticoid receptor remodeling of chromatin structure. J Biol Chem 273: 1175–83.
52. Fryer CJ, Archer TK. 1998. Chromatin remodeling by the glucocorticoid receptor requires the BRG1 complex. Nature 393: 88–91.
53. Ichinose H, Garnier JM, Chambon P, Losson R. 1997. Ligand-dependent interaction between the estrogen receptor and the human homologues of SWI2/SNF2. Gene 188: 95–100.
54. Trotter KW, Archer TK. 2004. Reconstitution of glucocorticoid receptor-dependent transcription in vivo. Mol Cell Biol 24: 3347–58.
55. Vicent GP, Zaurin R, Ballare C, Nacht AS, et al. 2009. Erk signaling and chromatin remodeling in MMTV promoter activation by progestins. Nucl Recept Signal 7: e008.
56. Perlmann T, Wrange O. 1988. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J 7: 3073–9.
57. Pina B, Bruggemeier U, Beato M. 1990. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell 60: 719–31.
58. Venditti P, Di Croce L, Kauer M, Blank T, et al. 1998. Assembly of MMTV promoter minichromosomes with positioned nucleosomes precludes NF1 access but not restriction enzyme cleavage. Nucleic Acids Res 26: 3657–66.
59. Aoyagi S, Trotter KW, Archer TK. 2005. ATP-dependent chromatin remodeling complexes and their role in nuclear receptor-dependent transcription in vivo. Vitam Horm 70: 281–307.
60. Belandia B, Orford RL, Hurst HC, Parker MG. 2002. Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J 21: 4094–103.
61. Lee HL, Archer TK. 1998. Prolonged glucocorticoid exposure dephosphorylates histone H1 and inactivates the MMTV promoter. EMBO J 17: 1454–66.
62. Johnson TA, Elbi C, Parekh BS, Hager GL, et al. 2008. Chromatin remodeling complexes interact dynamically with a glucocorticoid receptor regulated promoter. Mol Biol Cell 19: 3308–22.
63. Hsiao PW, Fryer CJ, Trotter KW, Wang W, et al. 2003. BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol 23: 6210–20.
64. Jeong KW, Lee YH, Stallcup MR. 2009. Recruitment of the SWI/SNF chromatin remodeling complex to steroid hormone-regulated promoters by nuclear receptor coactivator flightless-I. J Biol Chem 284: 29298–309.
65. Nie Z, Xue Y, Yang D, Zhou S, et al. 2000. A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex. Mol Cell Biol 20: 8879–88.
66. Inoue H, Furukawa T, Giannakopoulos S, Zhou S, et al. 2002. Largest subunits of the human SWI/SNF chromatin-remodeling complex promote transcriptional activation by steroid hormone receptors. J Biol Chem 277: 41674–85.
67. Nagaich AK, Walker DA, Wolford RG, Hager GL. 2004. Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. MolCell 14: 163–74.
68. Li M, Hada A, Sen P, Olufemi L, et al. 2015. Dynamic regulation of transcription factors by nucleosome remodeling. Elife 4: e06249.
69. Muchardt C, Yaniv M. 1993. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J 12: 4279–90.
70. Erdel F, Krug J, Langst G, Rippe K. 2011. Targeting chromatin remodelers: signals and search mechanisms. Biochim Biophys Acta 1809: 497–508.
71. Schnitzler G, Sif S, Kingston RE. 1998. Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell 94: 17–27.
72. Kassabov SR, Henry NM, Zofall M, Tsukiyama T, et al. 2002. High-resolution mapping of changes in histone-DNA contacts of nucleosomes remodeled by ISW2. Mol Cell Biol 22: 7524–34.
73. McKnight JN, Jenkins KR, Nodelman IM, Escobar T, et al. 2011. Extranucleosomal DNA binding directs nucleosome sliding by Chd1. Mol Cell Biol 31: 4746–59.
74. Nagaich AK, Walker DA, Wolford RG, Hager GL. 2004. Rapid periodic binding and displacement of the glucocorticoid receptor during chromatin remodeling. Mol Cell 14: 163–74.
75. Theodorou V, Stark R, Menon S, Carroll JS. 2012. GATA3 acts upstream of FOXA1 in mediating ESR1 binding by shaping enhancer accessibility. Genome Res 23: 12–22.
76. Hu G, Schones DE, Cui K, Ybarra R, et al. 2011. Regulation of nucleosome landscape and transcription factor targeting at tissue-specific enhancers by BRG1. Genome Res 21: 1650–8.
77. Sanalkumar R, Johnson KD, Gao X, Boyer ME, et al. 2014. Mechanism governing a stem cell-generating cis-regulatory element. Proc Natl Acad Sci USA 111: E1091–100.
78. Takaku M, Grimm SA, Shimbo T, Perera L, et al. 2016. GATA3-dependent cellular reprogramming requires activation-domain dependent recruitment of a chromatin remodeler. Genome Biol 17: 36.
79. Ramakrishnan V, Finch JT, Graziano V, Lee PL, et al. 1993. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature 362: 219–23.
80. Clark KL, Halay ED, Lai E, Burley SK. 1993. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364: 412–20.
81. Chaya D, Hayamizu T, Bustin M, Zaret KS. 2001. Transcription factor FoxA (HNF3) on a nucleosome at an enhancer complex in liver chromatin. J Biol Chem 276: 44385–9.
82. Sekiya T, Muthurajan UM, Luger K, Tulin AV, et al. 2009. Nucleosome-binding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes Dev 23: 804–9.
83. Mueller F, Stasevich TJ, Mazza D, McNally JG. 2013. Quantifying transcription factor kinetics: at work or at play? Crit Rev Biochem Mol Biol 48: 492–514.
84. Stasevich TJ, McNally JG. 2011. Assembly of the transcription machinery: ordered and stable, random and dynamic, or both? Chromosoma 120: 533–45.
85. Mazza D, Abernathy A, Golob N, Morisaki T, et al. 2012. A benchmark for chromatin binding measurements in live cells. Nucleic Acids Res 40: e119.
86. Speil J, Baumgart E, Siebrasse JP, Veith R, et al. 2011. Activated STAT1 transcription factors conduct distinct saltatory movements in the cell nucleus. Biophys J 101: 2592–600.
87. van Royen ME, van Cappellen WA, Geverts B, Schmidt T, et al. 2014. Androgen receptor complexes probe DNA for recognition sequences by short random interactions. J Cell Sci 127: 1406–16.
88. Izeddin I, Recamier V, Bosanac L, Cisse II, et al. 2014. Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus. Elife 3: e02230.
89. Elf J, Li GW, Xie XS. 2007. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316: 1191–4.
90. White MD, Angiolini JF, Alvarez YD, Kaur G, et al. 2016. Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165: 75–87.