Nucleosome distortion as a possible mechanism of transcription activation domain function

Epigenetics and Chromatin

Volumn 9, Issue 1, 2016, Pages

  Erkina, Tamara Y ^a   Erkine, Alexandre M ^a  

^a BUTLER UNIVERSITY   (United States)

Author keywords

Chromatin; Chromatin remodeling; Intrinsically disordered region; Transcription regulation; Transcriptional activation domain

Indexed keywords

TRANSCRIPTION FACTOR;

AMINO ACID COMPOSITION; CELL INTERACTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE ACTIVATION; HUMAN; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; RNA SEQUENCE; SEQUENCE ANALYSIS; TRANSCRIPTION ACTIVATION DOMAIN; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

EID: 84988402913     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/s13072-016-0092-2     Document Type: Review

References (112)

1. Ptashne M, Gann A. Transcriptional activation by recruitment. Nature. 1997;386(6625):569-77.
2. Keung AJ, Bashor CJ, Kiriakov S, Collins JJ, Khalil AS. Using targeted chromatin regulators to engineer combinatorial and spatial transcriptional regulation. Cell. 2014;158(1):110-20.
3. Hahn S, Young ET. Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics. 2011;189(3):705-36.
4. Mapp AK, Ansari AZ, Ptashne M, Dervan PB. Activation of gene expression by small molecule transcription factors. Proc Natl Acad Sci USA. 2000;97(8):3930-5.
5. Garvie CW, Wolberger C. Recognition of specific DNA sequences. Mol Cell. 2001;8(5):937-46.
6. Luscombe NM, Austin SE, Berman HM, Thornton JM. An overview of the structures of protein-DNA complexes. Genome Biol. 2000; 1(1):REVIEWS001.
7. Hossain MA, Barrow JJ, Shen Y, Haq MI, Bungert J. Artificial zinc finger DNA binding domains: versatile tools for genome engineering and modulation of gene expression. J Cell Biochem. 2015;116(11):2435-44.
8. Mapp AK, Ansari AZ. A TAD further: exogenous control of gene activation. ACS Chem Biol. 2007;2(1):62-75.
9. Rodriguez-Martinez JA, Peterson-Kaufman KJ, Ansari AZ. Small-molecule regulators that mimic transcription factors. Biochim Biophys Acta. 2010;1799(10-12):768-74.
10. Eguchi A, Lee GO, Wan F, Erwin GS, Ansari AZ. Controlling gene networks and cell fate with precision-targeted DNA-binding proteins and small-molecule-based genome readers. Biochem J. 2014;462(3):397-413.
11. Ansari AZ, Mapp AK. Modular design of artificial transcription factors. Curr Opin Chem Biol. 2002;6(6):765-72.
12. Dervan PB. Molecular recognition of DNA by small molecules. Bioorg Med Chem. 2001;9(9):2215-35.
13. Minter AR, Brennan BB, Mapp AK. A small molecule transcriptional activation domain. J Am Chem Soc. 2004;126(34):10504-5.
14. Rowe SP, Casey RJ, Brennan BB, Buhrlage SJ, Mapp AK. Transcriptional up-regulation in cells mediated by a small molecule. J Am Chem Soc. 2007;129(35):10654-5.
15. Warfield L, Tuttle LM, Pacheco D, Klevit RE, Hahn S. A sequence-specific transcription activator motif and powerful synthetic variants that bind Mediator using a fuzzy protein interface. Proc Natl Acad Sci USA. 2014;111(34):E3506-13.
16. Bhaumik SR, Green MR. SAGA is an essential in vivo target of the yeast acidic activator Gal4p. Genes Dev. 2001;15(15):1935-45.
17. Titz B, Thomas S, Rajagopala SV, Chiba T, Ito T, Uetz P. Transcriptional activators in yeast. Nucleic Acids Res. 2006;34(3):955-67.
18. Beerli RR, Segal DJ, Dreier B, Barbas CF 3rd. Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc Natl Acad Sci USA. 1998;95(25):14628-33.
19. Escher D, Bodmer-Glavas M, Barberis A, Schaffner W. Conservation of glutamine-rich transactivation function between yeast and humans. Mol Cell Biol. 2000;20(8):2774-82.
20. Yanagisawa S. The transcriptional activation domain of the plant-specific Dof1 factor functions in plant, animal, and yeast cells. Plant Cell Physiol. 2001;42(8):813-22.
21. Piskacek S, Gregor M, Nemethova M, Grabner M, Kovarik P, Piskacek M. Nine-amino-acid transactivation domain: establishment and prediction utilities. Genomics. 2007;89(6):756-68.
22. Ma J, Przibilla E, Hu J, Bogorad L, Ptashne M. Yeast activators stimulate plant gene expression. Nature. 1988;334(6183):631-3.
23. Liu J, Perumal NB, Oldfield CJ, Su EW, Uversky VN, Dunker AK. Intrinsic disorder in transcription factors. Biochemistry. 2006;45(22):6873-88.
24. Minezaki Y, Homma K, Kinjo AR, Nishikawa K. Human transcription factors contain a high fraction of intrinsically disordered regions essential for transcriptional regulation. J Mol Biol. 2006;359(4):1137-49.
25. Mitchell PJ, Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989;245(4916):371-8.
26. Ma J, Ptashne M. A new class of yeast transcriptional activators. Cell. 1987;51(1):113-9.
27. Lu X, Ansari AZ, Ptashne M. An artificial transcriptional activating region with unusual properties. Proc Natl Acad Sci USA. 2000;97(5):1988-92.
28. Regier JL, Shen F, Triezenberg SJ. Pattern of aromatic and hydrophobic amino acids critical for one of two subdomains of the VP16 transcriptional activator. Proc Natl Acad Sci USA. 1993;90(3):883-7.
29. Cress WD, Triezenberg SJ. Critical structural elements of the VP16 transcriptional activation domain. Science. 1991;251(4989):87-90.
30. Drysdale CM, Duenas E, Jackson BM, Reusser U, Braus GH, Hinnebusch AG. The transcriptional activator GCN4 contains multiple activation domains that are critically dependent on hydrophobic amino acids. Mol Cell Biol. 1995;15(3):1220-33.
31. Erkine AM, Gross DS. Dynamic chromatin alterations triggered by natural and synthetic activation domains. J Biol Chem. 2003;278(10):7755-64.
32. Abedi M, Caponigro G, Shen J, Hansen S, Sandrock T, Kamb A. Transcriptional transactivation by selected short random peptides attached to lexA-GFP fusion proteins. BMC Mol Biol. 2001;2:10.
33. Gerber HP, Seipel K, Georgiev O, Hofferer M, Hug M, Rusconi S, Schaffner W. Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science. 1994;263(5148):808-11.
34. Blair WS, Bogerd HP, Madore SJ, Cullen BR. Mutational analysis of the transcription activation domain of RelA: identification of a highly synergistic minimal acidic activation module. Mol Cell Biol. 1994;14(11):7226-34.
35. Wu Y, Reece RJ, Ptashne M. Quantitation of putative activator-target affinities predicts transcriptional activating potentials. EMBO J. 1996;15(15):3951-63.
36. Buhrlage SJ, Bates CA, Rowe SP, Minter AR, Brennan BB, Majmudar CY, Wemmer DE, Al-Hashimi H, Mapp AK. Amphipathic small molecules mimic the binding mode and function of endogenous transcription factors. ACS Chem Biol. 2009;4(5):335-44.
37. Saha S, Ansari AZ, Jarrell KA, Ptashne M, Jarell KA. RNA sequences that work as transcriptional activating regions. Nucleic Acids Res. 2003;31(5):1565-70.
38. Nyanguile O, Uesugi M, Austin DJ, Verdine GL. A nonnatural transcriptional coactivator. Proc Natl Acad Sci USA. 1997;94(25):13402-6.
39. Tompa P. Intrinsically disordered proteins: a 10-year recap. Trends Biochem Sci. 2012;37(12):509-16.
40. Oldfield CJ, Dunker AK. Intrinsically disordered proteins and intrinsically disordered protein regions. Annu Rev Biochem. 2014;83:553-84.
41. Uversky VN. The multifaceted roles of intrinsic disorder in protein complexes. FEBS Lett. 2015;589(19 PartA):2498-506.
42. Giniger E, Ptashne M. Transcription in yeast activated by a putative amphipathic alpha helix linked to a DNA binding unit. Nature. 1987;330(6149):670-2.
43. Kussie PH, Gorina S, Marechal V, Elenbaas B, Moreau J, Levine AJ, Pavletich NP. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science. 1996;274(5289):948-53.
44. Radhakrishnan I, Perez-Alvarado GC, Parker D, Dyson HJ, Montminy MR, Wright PE. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions. Cell. 1997;91(6):741-52.
45. Jonker HR, Wechselberger RW, Boelens R, Folkers GE, Kaptein R. Structural properties of the promiscuous VP16 activation domain. Biochemistry. 2005;44(3):827-39.
46. Uesugi M, Nyanguile O, Lu H, Levine AJ, Verdine GL. Induced alpha helix in the VP16 activation domain upon binding to a human TAF. Science. 1997;277(5330):1310-3.
47. Lee CW, Martinez-Yamout MA, Dyson HJ, Wright PE. Structure of the p53 transactivation domain in complex with the nuclear receptor coactivator binding domain of CREB binding protein. Biochemistry. 2010;49(46):9964-71.
48. Brent R, Ptashne M. A eukaryotic transcriptional activator bearing the DNA specificity of a prokaryotic repressor. Cell. 1985;43(3 Pt 2):729-36.
49. Horikoshi M, Hai T, Lin YS, Green MR, Roeder RG. Transcription factor ATF interacts with the TATA factor to facilitate establishment of a preinitiation complex. Cell. 1988;54(7):1033-42.
50. Stringer KF, Ingles CJ, Greenblatt J. Direct and selective binding of an acidic transcriptional activation domain to the TATA-box factor TFIID. Nature. 1990;345(6278):783-6.
51. Hermann S, Berndt KD, Wright AP. How transcriptional activators bind target proteins. J Biol Chem. 2001;276(43):40127-32.
52. Capella M, Re DA, Arce AL, Chan RL. Plant homeodomain-leucine zipper I transcription factors exhibit different functional AHA motifs that selectively interact with TBP or/and TFIIB. Plant Cell Rep. 2014;33(6):955-67.
53. Khan SH, Ling J, Kumar R. TBP binding-induced folding of the glucocorticoid receptor AF1 domain facilitates its interaction with steroid receptor coactivator-1. PLoS ONE. 2011;6(7):e21939.
54. Lin YS, Ha I, Maldonado E, Reinberg D, Green MR. Binding of general transcription factor TFIIB to an acidic activating region. Nature. 1991;353(6344):569-71.
55. Choy B, Green MR. Eukaryotic activators function during multiple steps of preinitiation complex assembly. Nature. 1993;366(6455):531-6.
56. Xiao H, Pearson A, Coulombe B, Truant R, Zhang S, Regier JL, Triezenberg SJ, Reinberg D, Flores O, Ingles CJ, et al. Binding of basal transcription factor TFIIH to the acidic activation domains of VP16 and p53. Mol Cell Biol. 1994;14(10):7013-24.
57. Chabot PR, Raiola L, Lussier-Price M, Morse T, Arseneault G, Archambault J, Omichinski JG. Structural and functional characterization of a complex between the acidic transactivation domain of EBNA2 and the Tfb1/p62 subunit of TFIIH. PLoS Pathog. 2014;10(3):e1004042.
58. Stargell LA, Struhl K. The TBP-TFIIA interaction in the response to acidic activators in vivo. Science. 1995;269(5220):75-8.
59. Ozer J, Bolden AH, Lieberman PM. Transcription factor IIA mutations show activator-specific defects and reveal a IIA function distinct from stimulation of TBP-DNA binding. J Biol Chem. 1996;271(19):11182-90.
60. Tan Q, Linask KL, Ebright RH, Woychik NA. Activation mutants in yeast RNA polymerase II subunit RPB3 provide evidence for a structurally conserved surface required for activation in eukaryotes and bacteria. Genes Dev. 2000;14(3):339-48.
61. Goodrich JA, Tjian R. TBP-TAF complexes: selectivity factors for eukaryotic transcription. Curr Opin Cell Biol. 1994;6(3):403-9.
62. Walker SS, Reese JC, Apone LM, Green MR. Transcription activation in cells lacking TAFIIS. Nature. 1996;383(6596):185-8.
63. Moqtaderi Z, Bai Y, Poon D, Weil PA, Struhl K. TBP-associated factors are not generally required for transcriptional activation in yeast. Nature. 1996;383(6596):188-91.
64. Kim YJ, Bjorklund S, Li Y, Sayre MH, Kornberg RD. A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell. 1994;77(4):599-608.
65. Koleske AJ, Young RA. An RNA polymerase II holoenzyme responsive to activators. Nature. 1994;368(6470):466-9.
66. Aguilar X, Blomberg J, Brannstrom K, Olofsson A, Schleucher J, Bjorklund S. Interaction studies of the human and Arabidopsis thaliana Med25-ACID proteins with the herpes simplex virus VP16- and plant-specific Dreb2a transcription factors. PLoS ONE. 2014;9(5):e98575.
67. Biddick R, Young ET. Yeast mediator and its role in transcriptional regulation. CR Biol. 2005;328(9):773-82.
68. Koh SS, Ansari AZ, Ptashne M, Young RA. An activator target in the RNA polymerase II holoenzyme. Mol Cell. 1998;1(6):895-904.
69. Myers LC, Gustafsson CM, Hayashibara KC, Brown PO, Kornberg RD. Mediator protein mutations that selectively abolish activated transcription. Proc Natl Acad Sci USA. 1999;96(1):67-72.
70. Jeong CJ, Yang SH, Xie Y, Zhang L, Johnston SA, Kodadek T. Evidence that Gal11 protein is a target of the Gal4 activation domain in the mediator. Biochemistry. 2001;40(31):9421-7.
71. Ansari AZ, Koh SS, Zaman Z, Bongards C, Lehming N, Young RA, Ptashne M. Transcriptional activating regions target a cyclin-dependent kinase. Proc Natl Acad Sci USA. 2002;99(23):14706-9.
72. Qiu H, Hu C, Yoon S, Natarajan K, Swanson MJ, Hinnebusch AG. An array of coactivators is required for optimal recruitment of TATA binding protein and RNA polymerase II by promoter-bound Gcn4p. Mol Cell Biol. 2004;24(10):4104-17.
73. Rachez C, Lemon BD, Suldan Z, Bromleigh V, Gamble M, Naar AM, Erdjument-Bromage H, Tempst P, Freedman LP. Ligand-dependent transcription activation by nuclear receptors requires the DRIP complex. Nature. 1999;398(6730):824-8.
74. Malik S, Roeder RG. Transcriptional regulation through Mediator-like coactivators in yeast and metazoan cells. Trends Biochem Sci. 2000;25(6):277-83.
75. Malik S, Roeder RG. Dynamic regulation of pol II transcription by the mammalian Mediator complex. Trends Biochem Sci. 2005;30(5):256-63.
76. Ito M, Yuan CX, Okano HJ, Darnell RB, Roeder RG. Involvement of the TRAP220 component of the TRAP/SMCC coactivator complex in embryonic development and thyroid hormone action. Mol Cell. 2000;5(4):683-93.
77. Reeves WM, Hahn S. Activator-independent functions of the yeast mediator sin4 complex in preinitiation complex formation and transcription reinitiation. Mol Cell Biol. 2003;23(1):349-58.
78. Svaren J, Schmitz J, Horz W. The transactivation domain of Pho4 is required for nucleosome disruption at the PHO5 promoter. EMBO J. 1994;13(20):4856-62.
79. Stafford GA, Morse RH. Chromatin remodeling by transcriptional activation domains in a yeast episome. J Biol Chem. 1997;272(17):11526-34.
80. Moreira JM, Holmberg S. Nucleosome structure of the yeast CHA1 promoter: analysis of activation-dependent chromatin remodeling of an RNA-polymerase-II-transcribed gene in TBP and RNA pol II mutants defective in vivo in response to acidic activators. EMBO J. 1998;17(20):6028-38.
81. Di Mauro E, Kendrew SG, Caserta M. Two distinct nucleosome alterations characterize chromatin remodeling at the Saccharomyces cerevisiae ADH2 promoter. J Biol Chem. 2000;275(11):7612-8.
82. Sullivan EK, Weirich CS, Guyon JR, Sif S, Kingston RE. Transcriptional activation domains of human heat shock factor 1 recruit human SWI/SNF. Mol Cell Biol. 2001;21(17):5826-37.
83. Workman JL, Kingston RE. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem. 1998;67:545-79.
84. Fry CJ, Peterson CL. Chromatin remodeling enzymes: who's on first? Curr Biol. 2001;11(5):R185-97.
85. Hassan AH, Neely KE, Vignali M, Reese JC, Workman JL. Promoter targeting of chromatin-modifying complexes. Front Biosci. 2001;6:D1054-64.
86. Knutson BA, Hahn S. Domains of Tra1 important for activator recruitment and transcription coactivator functions of SAGA and NuA4 complexes. Mol Cell Biol. 2011;31(4):818-31.
87. Brown CE, Howe L, Sousa K, Alley SC, Carrozza MJ, Tan S, Workman JL. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit. Science. 2001;292(5525):2333-7.
88. Bhaumik SR, Raha T, Aiello DP, Green MR. In vivo target of a transcriptional activator revealed by fluorescence resonance energy transfer. Genes Dev. 2004;18(3):333-43.
89. Majmudar CY, Labut AE, Mapp AK. Tra1 as a screening target for transcriptional activation domain discovery. Bioorg Med Chem Lett. 2009;19(14):3733-5.
90. Barlev NA, Candau R, Wang L, Darpino P, Silverman N, Berger SL. Characterization of physical interactions of the putative transcriptional adaptor, ADA2, with acidic activation domains and TATA- binding protein. J Biol Chem. 1995;270(33):19337-44.
91. Thut CJ, Chen JL, Klemm R, Tjian R. p53 transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science. 1995;267(5194):100-4.
92. Henriksson A, Almlof T, Ford J, McEwan IJ, Gustafsson JA, Wright AP. Role of the Ada adaptor complex in gene activation by the glucocorticoid receptor. Mol Cell Biol. 1997;17(6):3065-73.
93. Neely KE, Hassan AH, Wallberg AE, Steger DJ, Cairns BR, Wright AP, Workman JL. Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays. Mol Cell. 1999;4(4):649-55.
94. Neely KE, Hassan AH, Brown CE, Howe L, Workman JL. Transcription activator interactions with multiple SWI/SNF subunits. Mol Cell Biol. 2002;22(6):1615-25.
95. Prochasson P, Neely KE, Hassan AH, Li B, Workman JL. Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activator-interaction domains. Mol Cell. 2003;12(4):983-90.
96. Kundu TK, Palhan VB, Wang Z, An W, Cole PA, Roeder RG. Activator-dependent transcription from chromatin in vitro involving targeted histone acetylation by p300. Mol Cell. 2000;6(3):551-61.
97. Lau OD, Kundu TK, Soccio RE, Ait-Si-Ali S, Khalil EM, Vassilev A, Wolffe AP, Nakatani Y, Roeder RG, Cole PA. HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol Cell. 2000;5(3):589-95.
98. Mukherjee SP, Behar M, Birnbaum HA, Hoffmann A, Wright PE, Ghosh G. Analysis of the RelA:CBP/p300 interaction reveals its involvement in NF-kappaB-driven transcription. PLoS Biol. 2013;11(9):e1001647.
99. Cosma MP, Tanaka T, Nasmyth K. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell. 1999;97(3):299-311.
100. Cosma MP, Panizza S, Nasmyth K. Cdk1 triggers association of RNA polymerase to cell cycle promoters only after recruitment of the mediator by SBF. Mol Cell. 2001;7(6):1213-20.
101. Sigler PB. Transcriptional activation. Acid blobs and negative noodles. Nature. 1988;333(6170):210-2.
102. Ansari AZ, Reece RJ, Ptashne M. A transcriptional activating region with two contrasting modes of protein interaction. Proc Natl Acad Sci USA. 1998;95(23):13543-8.
103. Ferreira ME, Hermann S, Prochasson P, Workman JL, Berndt KD, Wright AP. Mechanism of transcription factor recruitment by acidic activators. J Biol Chem. 2005;280(23):21779-84.
104. Maeda R, Suzuki H, Tanaka Y, Tamura TA. Interaction between transactivation domain of p53 and middle part of TBP-like protein (TLP) is involved in TLP-stimulated and p53-activated transcription from the p21 upstream promoter. PLoS ONE. 2014;9(3):e90190.
105. Yuan CX, Gurley WB. Potential targets for HSF1 within the preinitiation complex. Cell Stress Chaperones. 2000;5(3):229-42.
106. Wang M, Weiss M, Simonovic M, Haertinger G, Schrimpf SP, Hengartner MO, von Mering C. PaxDb, a database of protein abundance averages across all three domains of life. Mol Cell Proteomics. 2012;11(8):492-500.
107. Waters ML. Aromatic interactions in model systems. Curr Opin Chem Biol. 2002;6(6):736-41.
108. Alevizopoulos A, Dusserre Y, Tsai-Pflugfelder M, von der Weid T, Wahli W, Mermod N. A proline-rich TGF-beta-responsive transcriptional activator interacts with histone H3. Genes Dev. 1995;9(24):3051-66.
109. Ha N, Hellauer K, Turcotte B. Fusions with histone H3 result in highly specific alteration of gene expression. Nucleic Acids Res. 2000;28(4):1026-35.
110. Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell. 2002;9(2):279-89.
111. Altmann H, Wendler W, Winnacker EL. Transcriptional activation by CTF proteins is mediated by a bipartite low-proline domain. Proc Natl Acad Sci USA. 1994;91(9):3901-5.
112. Wenzelides S, Altmann H, Wendler W, Winnacker EL. CTF5 - a new transcriptional activator of the NFI/CTF family. Nucleic Acids Res. 1996;24(12):2416-21.