Pioneer Transcription Factors Initiating Gene Network Changes

Literature Cited

1. 1. 

   Adachi K, Kopp W, Wu G, Heising S, Greber B et al. 2018. Esrrb unlocks silenced enhancers for reprogramming to naive pluripotency. Cell Stem Cell 23:266–75.e6
   [Google Scholar]
2. 2. 

   Adams EJ, Karthaus WR, Hoover E, Liu D, Gruet A et al. 2019. FOXA1 mutations alter pioneering activity, differentiation and prostate cancer phenotypes. Nature 571:408–12
   [Google Scholar]
3. 3. 

   Ballare C, Castellano G, Gaveglia L, Althammer S, Gonzalez-Vallinas J et al. 2013. Nucleosome-driven transcription factor binding and gene regulation. Mol. Cell 49:67–79
   [Google Scholar]
4. 4. 

   Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC et al. 2006. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311:856–61
   [Google Scholar]
5. 5. 

   Barozzi I, Simonatto M, Bonifacio S, Yang L, Rohs R et al. 2014. Coregulation of transcription factor binding and nucleosome occupancy through DNA features of mammalian enhancers. Mol. Cell 54:844–57
   [Google Scholar]
6. 6. 

   Becker M, Baumann C, John S, Walker DA, Vigneron M et al. 2002. Dynamic behavior of transcription factors on a natural promoter in living cells. EMBO Rep 3:1188–94
   [Google Scholar]
7. 7. 

   Belikov S, Berg OG, Wrange O 2016. Quantification of transcription factor-DNA binding affinity in a living cell. Nucleic Acids Res 44:3045–58
   [Google Scholar]
8. 8. 

   Berkes CA, Bergstrom DA, Penn BH, Seaver KJ, Knoepfler PS, Tapscott SJ 2004. Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential. Mol. Cell 14:465–77
   [Google Scholar]
9. 9. 

   Bevington SL, Cauchy P, Piper J, Bertrand E, Lalli N et al. 2016. Inducible chromatin priming is associated with the establishment of immunological memory in T cells. EMBO J 35:515–35
   [Google Scholar]
10. 10. 

    Boettiger AN, Bintu B, Moffitt JR, Wang S, Beliveau BJ et al. 2016. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 529:418–22
    [Google Scholar]
11. 11. 

    Bossard P, Zaret KS. 1998. GATA transcription factors as potentiators of gut endoderm differentiation. Development 125:4909–17
    [Google Scholar]
12. 12. 

    Bossard P, Zaret KS. 2000. Repressive and restrictive mesodermal interactions with gut endoderm: possible relation to Meckel's Diverticulum. Development 127:4915–23
    [Google Scholar]
13. 13. 

    Budry L, Balsalobre A, Gauthier Y, Khetchoumian K, L'Honore A et al. 2012. The selector gene Pax7 dictates alternate pituitary cell fates through its pioneer action on chromatin remodeling. Genes Dev 26:2299–310
    [Google Scholar]
14. 14. 

    Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10:1213–18
    [Google Scholar]
15. 15. 

    Cascio S, Zaret KS. 1991. Hepatocyte differentiation initiates during endodermal-mesenchymal interactions prior to liver formation. Development 113:217–25
    [Google Scholar]
16. 16. 

    Cernilogar FM, Hasenöder S, Wang Z, Scheibner K, Burtscher I et al. 2019. Pre-marked chromatin and transcription factor co-binding shape the pioneering activity of Foxa2. Nucleic Acids Res 47:9069–86
    [Google Scholar]
17. 17. 

    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. 276:44385–89
    [Google Scholar]
18. 18. 

    Chen J, Zhang Z, Li L, Chen BC, Revyakin A et al. 2014. Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156:1274–85
    [Google Scholar]
19. 19. 

    Chronis C, Fiziev P, Papp B, Butz S, Bonora G et al. 2017. Cooperative binding of transcription factors orchestrates reprogramming. Cell 168:442–59.e20
    [Google Scholar]
20. 20. 

    Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS 2002. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9:279–89
    [Google Scholar]
21. 21. 

    Cirillo LA, McPherson CE, Bossard P, Stevens K, Cherian S et al. 1998. Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. EMBO J 17:244–54
    [Google Scholar]
22. 22. 

    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 4:961–69
    [Google Scholar]
23. 23. 

    Cortini R, Filion GJ. 2018. Theoretical principles of transcription factor traffic on folded chromatin. Nat. Commun. 9:1740
    [Google Scholar]
24. 24. 

    Crocker J, Abe N, Rinaldi L, McGregor AP, Frankel N et al. 2015. Low affinity binding site clusters confer hox specificity and regulatory robustness. Cell 160:191–203
    [Google Scholar]
25. 25. 

    Cui F, Zhurkin VB. 2014. Rotational positioning of nucleosomes facilitates selective binding of p53 to response elements associated with cell cycle arrest. Nucleic Acids Res 42:836–47
    [Google Scholar]
26. 26. 

    Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111:185–96
    [Google Scholar]
27. 27. 

    Dann GP, Liszczak GP, Bagert JD, Muller MM, Nguyen UTT et al. 2017. ISWI chromatin remodellers sense nucleosome modifications to determine substrate preference. Nature 548:607–11
    [Google Scholar]
28. 28. 

    Denny SK, Yang D, Chuang CH, Brady JJ, Lim JS et al. 2016. Nfib promotes metastasis through a widespread increase in chromatin accessibility. Cell 166:328–42
    [Google Scholar]
29. 29. 

    Dodonova SO, Zhu F, Dienemann C, Taipale J, Cramer P 2020. Nucleosome-bound SOX2 and SOX11 structures elucidate pioneer factor function. Nature 580:669–72
    [Google Scholar]
30. 30. 

    Donaghey J, Thakurela S, Charlton J, Chen JS, Smith ZD et al. 2018. Genetic determinants and epigenetic effects of pioneer-factor occupancy. Nat. Genet. 50:250–58
    [Google Scholar]
31. 31. 

    Donovan BT, Chen H, Jipa C, Bai L, Poirier MG 2019. Dissociation rate compensation mechanism for budding yeast pioneer transcription factors. eLife 8:e43008
    [Google Scholar]
32. 32. 

    Dorigo B, Schalch T, Bystricky K, Richmond TJ 2003. Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J. Mol. Biol. 327:85–96
    [Google Scholar]
33. 33. 

    Echigoya K, Koyama M, Negishi L, Takizawa Y, Mizukami Y et al. 2020. Nucleosome binding by the pioneer transcription factor OCT4. Sci. Rep. 10:11832
    [Google Scholar]
34. 34. 

    Fan JY, Rangasamy D, Luger K, Tremethick DJ 2004. H2A.Z alters the nucleosome surface to promote HP1α-mediated chromatin fiber folding. Mol. Cell 16:655–61
    [Google Scholar]
35. 35. 

    Farley EK, Olson KM, Zhang W, Brandt AJ, Rokhsar DS, Levine MS 2015. Suboptimization of developmental enhancers. Science 350:325–28
    [Google Scholar]
36. 36. 

    Fernandez Garcia M, Moore CD, Schulz KN, Alberto O, Donague G et al. 2019. Structural features of transcription factors associating with nucleosome binding. Mol. Cell 75:921–32.e6
    [Google Scholar]
37. 37. 

    Fiedler M, Graeb M, Mieszczanek J, Rutherford TJ, Johnson CM, Bienz M 2015. An ancient Pygo-dependent Wnt enhanceosome integrated by Chip/LDB-SSDP. eLife 4:e09073
    [Google Scholar]
38. 38. 

    Fuglerud BM, Ledsaak M, Rogne M, Eskeland R, Gabrielsen OS 2018. The pioneer factor activity of c-Myb involves recruitment of p300 and induction of histone acetylation followed by acetylation-induced chromatin dissociation. Epigenet. Chromatin 11:35
    [Google Scholar]
39. 39. 

    Fukaya T, Lim B, Levine M 2016. Enhancer control of transcriptional bursting. Cell 166:358–68
    [Google Scholar]
40. 40. 

    Fyodorov DV, Zhou BR, Skoultchi AI, Bai Y 2018. Emerging roles of linker histones in regulating chromatin structure and function. Nat. Rev. Mol. Cell Biol. 19:192–206
    [Google Scholar]
41. 41. 

    Gao R, Liang X, Cheedipudi S, Cordero J, Jiang X et al. 2019. Pioneering function of Isl1 in the epigenetic control of cardiomyocyte cell fate. Cell Res 29:486–501
    [Google Scholar]
42. 42. 

    Gehrke AR, Neverett E, Luo YJ, Brandt A, Ricci L et al. 2019. Acoel genome reveals the regulatory landscape of whole-body regeneration. Science 363:eaau6173
    [Google Scholar]
43. 43. 

    Glont SE, Chernukhin I, Carroll JS 2019. Comprehensive genomic analysis reveals that the pioneering function of FOXA1 is independent of hormonal signaling. Cell Rep 26:2558–65.e3
    [Google Scholar]
44. 44. 

    Gualdi R, Bossard P, Zheng M, Hamada Y, Coleman JR, Zaret KS 1996. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev 10:1670–82
    [Google Scholar]
45. 45. 

    Hager GL, McNally JG, Misteli T 2009. Transcription dynamics. Mol. Cell 35:741–53
    [Google Scholar]
46. 46. 

    Hill DA, Imbalzano AN. 2000. Human SWI/SNF nucleosome remodeling activity is partially inhibited by linker histone H1. Biochemistry 39:11649–56
    [Google Scholar]
47. 47. 

    Hipp L, Beer J, Kuchler O, Reisser M, Sinske D et al. 2019. Single-molecule imaging of the transcription factor SRF reveals prolonged chromatin-binding kinetics upon cell stimulation. PNAS 116:880–89
    [Google Scholar]
48. 48. 

    Hoffman JA, Trotter KW, Ward JM, Archer TK 2018. BRG1 governs glucocorticoid receptor interactions with chromatin and pioneer factors across the genome. eLife 7:e35073
    [Google Scholar]
49. 49. 

    Holtzinger A, Evans T. 2005. Gata4 regulates the formation of multiple organs. Development 132:4005–14
    [Google Scholar]
50. 50. 

    Horn PJ, Carruthers LM, Logie C, Hill DA, Solomon MJ et al. 2002. Phosphorylation of linker histones regulates ATP-dependent chromatin remodeling enzymes. Nat. Struct. Biol. 9:263–67
    [Google Scholar]
51. 51. 

    Hsu HT, Chen HM, Yang Z, Wang J, Lee NK et al. 2015. Recruitment of RNA polymerase II by the pioneer transcription factor PHA-4. Science 348:1372–76
    [Google Scholar]
52. 52. 

    Huertas J, MacCarthy CM, Scholer HR, Cojocaru V 2020. Nucleosomal DNA dynamics mediate Oct4 pioneer factor binding. Biophys. J. 118:2280–96
    [Google Scholar]
53. 53. 

    Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS 2011. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 43:27–33
    [Google Scholar]
54. 54. 

    Iwafuchi M, Cuesta I, Donahue G, Takenaka N, Osipovich AB et al. 2020. Gene network transitions in embryos depend upon interactions between a pioneer transcription factor and core histones. Nat. Genet. 52:418–27
    [Google Scholar]
55. 55. 

    Iwafuchi-Doi M, Donahue G, Kakumanu A, Watts JA, Mahony S et al. 2016. The pioneer transcription factor FoxA maintains an accessible nucleosome configuration at enhancers for tissue-specific gene activation. Mol. Cell 62:79–91
    [Google Scholar]
56. 56. 

    Iwafuchi-Doi M, Zaret KS. 2016. Cell fate control by pioneer transcription factors. Development 143:1833–37
    [Google Scholar]
57. 57. 

    Izeddin I, Recamier V, Bosanac L, Cisse II, Boudarene L et al. 2014. Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus. eLife 3:e02230
    [Google Scholar]
58. 58. 

    Jacobs J, Atkins M, Davie K, Imrichova H, Romanelli L et al. 2018. The transcription factor Grainy head primes epithelial enhancers for spatiotemporal activation by displacing nucleosomes. Nat. Genet. 50:1011–20
    [Google Scholar]
59. 59. 

    Johnson JL, Georgakilas G, Petrovic J, Kurachi M, Cai S et al. 2018. Lineage-determining transcription factor TCF-1 initiates the epigenetic identity of T cells. Immunity 48:243–57.e10
    [Google Scholar]
60. 60. 

    Johnson TA, Chereji RV, Stavreva DA, Morris SA, Hager GL, Clark DJ 2018. Conventional and pioneer modes of glucocorticoid receptor interaction with enhancer chromatin in vivo. Nucleic Acids Res 46:203–14
    [Google Scholar]
61. 61. 

    Jozwik KM, Carroll JS. 2012. Pioneer factors in hormone-dependent cancers. Nat. Rev. Cancer 12:381–85
    [Google Scholar]
62. 62. 

    Karpova TS, Chen TY, Sprague BL, McNally JG 2004. Dynamic interactions of a transcription factor with DNA are accelerated by a chromatin remodeller. EMBO Rep 5:1064–70
    [Google Scholar]
63. 63. 

    Koerber RT, Rhee HS, Jiang C, Pugh BF 2009. Interaction of transcriptional regulators with specific nucleosomes across the Saccharomyces genome. Mol. Cell 35:889–902
    [Google Scholar]
64. 64. 

    Kornberg RD, Lorch Y. 1999. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285–94
    [Google Scholar]
65. 65. 

    Krishnakumar R, Chen AF, Pantovich MG, Danial M, Parchem RJ et al. 2016. FOXD3 regulates pluripotent stem cell potential by simultaneously initiating and repressing enhancer activity. Cell Stem Cell 18:104–17
    [Google Scholar]
66. 66. 

    Kundaje A, Meuleman W, Ernst J, Bilenky M, Meuleman W et al.(Roadmap Epigenomics Consort.) 2015. Integrative analysis of 111 reference human epigenomes. Nature 518:317–30
    [Google Scholar]
67. 67. 

    Laptenko O, Beckerman R, Freulich E, Prives C 2011. p53 binding to nucleosomes within the p21 promoter in vivo leads to nucleosome loss and transcriptional activation. PNAS 108:10385–90
    [Google Scholar]
68. 68. 

    Lee CS, Friedman JR, Fulmer JT, Kaestner KH 2005. The initiation of liver development is dependent on Foxa transcription factors. Nature 435:944–47
    [Google Scholar]
69. 69. 

    Leemans C, van der Zwalm MCH, Brueckner L, Comoglio F, van Schaik T et al. 2019. Promoter-intrinsic and local chromatin features determine gene repression in LADs. Cell 177:852–64.e14
    [Google Scholar]
70. 70. 

    Lerner J, Gomez-Garcia PA, McCarthy RL, Liu Z, Lakadamyali M, Zaret KS 2020. Two-parameter mobility assessments discriminate diverse regulatory factor behaviors in chromatin. Mol. Cell 79:677–88.e6
    [Google Scholar]
71. 71. 

    Li G, Reinberg D. 2011. Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev. 21:175–86
    [Google Scholar]
72. 72. 

    Li G, Widom J. 2004. Nucleosomes facilitate their own invasion. Nat. Struct. Mol. Biol. 11:763–69
    [Google Scholar]
73. 73. 

    Li R, Cauchy P, Ramamoorthy S, Boller S, Chavez L, Grosschedl R 2018. Dynamic EBF1 occupancy directs sequential epigenetic and transcriptional events in B-cell programming. Genes Dev 32:96–111
    [Google Scholar]
74. 74. 

    Li S, Zheng EB, Zhao L, Liu S 2019. Nonreciprocal and conditional cooperativity directs the pioneer activity of pluripotency transcription factors. Cell Rep 28:2689–703.e4
    [Google Scholar]
75. 75. 

    Li Z, Gadue P, Chen K, Jiao Y, Tuteja G et al. 2012. Foxa2 and H2A.Z mediate nucleosome depletion during embryonic stem cell differentiation. Cell 151:1608–16
    [Google Scholar]
76. 76. 

    Lidor Nili E, Field Y, Lubling Y, Widom J, Oren M, Segal E 2010. p53 binds preferentially to genomic regions with high DNA-encoded nucleosome occupancy. Genome Res 20:1361–68
    [Google Scholar]
77. 77. 

    Liu H, Dong P, Ioannou MS, Li L, Shea J et al. 2018. Visualizing long-term single-molecule dynamics in vivo by stochastic protein labeling. PNAS 115:343–48
    [Google Scholar]
78. 78. 

    Liu Z, Kraus WL. 2017. Catalytic-independent functions of PARP-1 determine Sox2 pioneer activity at intractable genomic loci. Mol. Cell 65:589–603.e9
    [Google Scholar]
79. 79. 

    Liu Z, Tjian R. 2018. Visualizing transcription factor dynamics in living cells. J. Cell Biol. 217:1181–91
    [Google Scholar]
80. 80. 

    Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251–55
    [Google Scholar]
81. 81. 

    Ma PC, Rould MA, Weintraub H, Pabo CO 1994. Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 77:451–59
    [Google Scholar]
82. 82. 

    Mahony S, Edwards MD, Mazzoni EO, Sherwood RI, Kakumanu A et al. 2014. An integrated model of multiple-condition ChIP-seq data reveals predeterminants of Cdx2 binding. PLOS Comput. Biol. 10:e1003501
    [Google Scholar]
83. 83. 

    Mivelaz M, Cao A-M, Kubik S, Zencir S, Hovius R et al. 2020. Chromatin fiber invasion and nucleosome displacement by the Rap1 transcription factor. Mol. Cell 77:488–500.e9
    [Google Scholar]
84. 84. 

    Mayran A, Drouin J. 2018. Pioneer transcription factors shape the epigenetic landscape. J. Biol. Chem. 293:13795–804
    [Google Scholar]
85. 85. 

    Mayran A, Khetchoumian K, Hariri F, Pastinen T, Gauthier Y et al. 2018. Pioneer factor Pax7 deploys a stable enhancer repertoire for specification of cell fate. Nat. Genet. 50:259–69
    [Google Scholar]
86. 86. 

    Mazza D, Abernathy A, Golob N, Morisaki T, McNally JG 2012. A benchmark for chromatin binding measurements in live cells. Nucleic Acids Res 40:e119
    [Google Scholar]
87. 87. 

    McDaniel SL, Gibson TJ, Schulz KN, Fernandez Garcia M, Nevil M et al. 2019. Continued activity of the pioneer factor Zelda is required to drive zygotic genome activation. Mol. Cell 74:185–95.e4
    [Google Scholar]
88. 88. 

    McPherson CE, Shim EY, Friedman DS, Zaret KS 1993. An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell 75:387–98
    [Google Scholar]
89. 89. 

    Meers MP, Janssens DH, Henikoff S 2019. Pioneer factor-nucleosome binding events during differentiation are motif encoded. Mol. Cell 75:562–75.e5
    [Google Scholar]
90. 90. 

    Menet JS, Pescatore S, Rosbash M 2014. CLOCK:BMAL1 is a pioneer-like transcription factor. Genes Dev 28:8–13
    [Google Scholar]
91. 91. 

    Michael AK, Grand RS, Isbel L, Cavadini S, Kozicka Z et al. 2020. Mechanisms of OCT4-SOX2 motif readout on nucleosomes. Science 368:64981460–65
    [Google Scholar]
92. 92. 

    Mieczkowski J, Cook A, Bowman SK, Mueller B, Alver BH et al. 2016. MNase titration reveals differences between nucleosome occupancy and chromatin accessibility. Nat. Commun. 7:11485
    [Google Scholar]
93. 93. 

    Minderjahn J, Schmidt A, Fuchs A, Schill R, Raithel J et al. 2020. Mechanisms governing the pioneering and redistribution capabilities of the non-classical pioneer PU.1. Nat. Commun. 11:402
    [Google Scholar]
94. 94. 

    Morris SA. 2016. Direct lineage reprogramming via pioneer factors; a detour through developmental gene regulatory networks. Development 143:2696–705
    [Google Scholar]
95. 95. 

    Mueller F, Wach P, McNally JG 2008. Evidence for a common mode of transcription factor interaction with chromatin as revealed by improved quantitative fluorescence recovery after photobleaching. Biophys. J. 94:3323–39
    [Google Scholar]
96. 96. 

    Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A et al. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197–208
    [Google Scholar]
97. 97. 

    Nozaki T, Imai R, Tanbo M, Nagashima R, Tamura S et al. 2017. Dynamic organization of chromatin domains revealed by super-resolution live-cell imaging. Mol. Cell 67:282–93.e7
    [Google Scholar]
98. 98. 

    Oldfield AJ, Yang P, Conway AE, Cinghu S, Freudenberg JM et al. 2014. Histone-fold domain protein NF-Y promotes chromatin accessibility for cell type-specific master transcription factors. Mol. Cell 55:708–22
    [Google Scholar]
99. 99. 

    Ou HD, Phan S, Deerinck TJ, Thor A, Ellisman MH, O'Shea CC 2017. ChromEMT: visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science 357:eaag0025
    [Google Scholar]
100. 100. 

     Paakinaho V, Presman DM, Ball DA, Johnson TA, Schiltz RL et al. 2017. Single-molecule analysis of steroid receptor and cofactor action in living cells. Nat. Commun. 8:15896
     [Google Scholar]
101. 101. 

     Parolia A, Cieslik M, Chu SC, Xiao L, Ouchi T et al. 2019. Distinct structural classes of activating FOXA1 alterations in advanced prostate cancer. Nature 571:413–18
     [Google Scholar]
102. 102. 

     Pepenella S, Murphy KJ, Hayes JJ 2014. Intra- and inter-nucleosome interactions of the core histone tail domains in higher-order chromatin structure. Chromosoma 123:3–13
     [Google Scholar]
103. 103. 

     Perlmann T, Wrange O. 1988. Specific glucocorticoid receptor binding to DNA reconstituted in nucleosome. EMBO J 7:3073–79
     [Google Scholar]
104. 104. 

     Pfeifer GP, Steigerwald SD, Mueller PR, Wold B, Riggs AD 1989. Genomic sequencing and methylation analysis by ligation medicated PCR. Science 246:810–13 Erratum. 1990. Science 248:802
     [Google Scholar]
105. 105. 

     Phair RD, Scaffidi P, Elbi C, Vecerova J, Dey A et al. 2004. Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol. 24:6393–402
     [Google Scholar]
106. 106. 

     Pihlajamaa P, Sahu B, Lyly L, Aittomaki V, Hautaniemi S, Janne OA 2014. Tissue-specific pioneer factors associate with androgen receptor cistromes and transcription programs. EMBO J 33:312–26
     [Google Scholar]
107. 107. 

     Plys AJ, Davis CP, Kim J, Rizki G, Keenen MM et al. 2019. Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2. Genes Dev 33:799–813
     [Google Scholar]
108. 108. 

     Polach KJ, Widom J. 1995. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254:130–49
     [Google Scholar]
109. 109. 

     Polach KJ, Widom J. 1996. A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J. Mol. Biol. 258:800–12
     [Google Scholar]
110. 110. 

     Poleshko A, Smith CL, Nguyen SC, Sivaramakrishnan P, Wong KG et al. 2019. H3K9me2 orchestrates inheritance of spatial positioning of peripheral heterochromatin through mitosis. eLife 8:e49278
     [Google Scholar]
111. 111. 

     Raccaud M, Friman ET, Alber AB, Agarwal H, Deluz C et al. 2019. Mitotic chromosome binding predicts transcription factor properties in interphase. Nat. Commun. 10:487
     [Google Scholar]
112. 112. 

     Ramachandran A, Omar M, Cheslock P, Schnitzler GR 2003. Linker histone H1 modulates nucleosome remodeling by human SWI/SNF. J. Biol. Chem. 278:48590–601
     [Google Scholar]
113. 113. 

     Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW et al. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593–99
     [Google Scholar]
114. 114. 

     Remenyi A, Lins K, Nissen LJ, Reinbold R, Scholer HR, Wilmanns M 2003. Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev 17:2048–59
     [Google Scholar]
115. 115. 

     Ricci MA, Manzo C, Garcia-Parajo MF, Lakadamyali M, Cosma MP. 2015. Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160:1145–58
116. 116. 

     Roe JS, Hwang CI, Somerville TDD, Milazzo JP, Lee EJ et al. 2017. Enhancer reprogramming promotes pancreatic cancer metastasis. Cell 170:875–88.e20
     [Google Scholar]
117. 117. 

     Sanulli S, Trnka MJ, Dharmarajan V, Tibble RW, Pascal BD et al. 2019. HP1 reshapes nucleosome core to promote phase separation of heterochromatin. Nature 575:390–94
     [Google Scholar]
118. 118. 

     Sardina JL, Collombet S, Tian TV, Gomez A, Di Stefano B et al. 2018. Transcription factors drive Tet2-mediated enhancer demethylation to reprogram cell fate. Cell Stem Cell 23:727–41.e9
     [Google Scholar]
119. 119. 

     Schaeffner M, Mrozek-Gorska P, Buschle A, Woellmer A, Tagawa T et al. 2019. BZLF1 interacts with chromatin remodelers promoting escape from latent infections with EBV. Life Sci. Alliance 2:e201800108
     [Google Scholar]
120. 120. 

     Schep AN, Buenrostro JD, Denny SK, Schwartz K, Sherlock G, Greenleaf WJ 2015. Structured nucleosome fingerprints enable high-resolution mapping of chromatin architecture within regulatory regions. Genome Res 25:1757–70
     [Google Scholar]
121. 121. 

     Sekiya T, Muthurajan UM, Luger K, Tulin AV, Zaret KS 2009. Nucleosome-binding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes Dev 23:804–9
     [Google Scholar]
122. 122. 

     Sekiya T, Zaret KS. 2007. Repression by Groucho/TLE/Grg proteins: Genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol. Cell 28:291–303
     [Google Scholar]
123. 123. 

     Sherwood RI, Hashimoto T, O'Donnell CW, Lewis S, Barkal AA et al. 2014. Discovery of directional and nondirectional pioneer transcription factors by modeling DNase profile magnitude and shape. Nat. Biotechnol. 32:171–78
     [Google Scholar]
124. 124. 

     Shim EY, Woodcock C, Zaret KS 1998. Nucleosome positioning by the winged-helix transcription factor HNF3. Genes Dev 12:5–10
     [Google Scholar]
125. 125. 

     Skene PJ, Henikoff S. 2017. An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites. eLife 6:e21856
     [Google Scholar]
126. 126. 

     Soufi A, Donahue G, Zaret KS 2012. Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome. Cell 151:994–1004
     [Google Scholar]
127. 127. 

     Soufi A, Garcia MF, Jaroszewicz A, Osman N, Pellegrini M, Zaret KS 2015. Pioneer transcription factors target partial DNA motifs on nucleosomes to initiate reprogramming. Cell 161:555–68
     [Google Scholar]
128. 128. 

     Sprague BL, Pego RL, Stavreva DA, McNally JG 2004. Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys. J. 86:3473–95
     [Google Scholar]
129. 129. 

     Spruce C, Dlamini S, Ananda G, Bronkema N, Tian H et al. 2020. HELLS and PRDM9 form a pioneer complex to open chromatin at meiotic recombination hot spots. Genes Dev 34:398–412
     [Google Scholar]
130. 130. 

     Sridharan R, Gonzales-Cope M, Chronis C, Bonora G, McKee R et al. 2013. Proteomic and genomic approaches reveal critical functions of H3K9 methylation and heterochromatin protein-1γ in reprogramming to pluripotency. Nat. Cell Biol. 15:872–82
     [Google Scholar]
131. 131. 

     Stavreva DA, Garcia DA, Fettweis G, Gudla PR, Zaki GF et al. 2019. Transcriptional bursting and co-bursting regulation by steroid hormone release pattern and transcription factor mobility. Mol. Cell 75:1161–77.e11
     [Google Scholar]
132. 132. 

     Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH 2017. Phase separation drives heterochromatin domain formation. Nature 547:241–45
     [Google Scholar]
133. 133. 

     Sugo N, Morimatsu M, Arai Y, Kousoku Y, Ohkuni A et al. 2015. Single-molecule imaging reveals dynamics of CREB transcription factor bound to its target sequence. Sci. Rep. 5:10662
     [Google Scholar]
134. 134. 

     Sun Y, Nien CY, Chen K, Liu HY, Johnston J et al. 2015. Zelda overcomes the high intrinsic nucleosome barrier at enhancers during Drosophila zygotic genome activation. Genome Res 25:1703–14
     [Google Scholar]
135. 135. 

     Suter DM, Molina N, Gatfield D, Schneider K, Schibler U, Naef F 2011. Mammalian genes are transcribed with widely different bursting kinetics. Science 332:472–74
     [Google Scholar]
136. 136. 

     Swinstead EE, Miranda TB, Paakinaho V, Baek S, Goldstein I et al. 2016. Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions. Cell 165:593–605
     [Google Scholar]
137. 137. 

     Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T et al. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–72
     [Google Scholar]
138. 138. 

     Taylor IC, Workman JL, Schuetz TJ, Kingston RE 1991. Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev 5:1285–98
     [Google Scholar]
139. 139. 

     Teves SS, An L, Bhargava-Shah A, Xie L, Darzacq X, Tjian R 2018. A stable mode of bookmarking by TBP recruits RNA polymerase II to mitotic chromosomes. eLife 7:e35621
     [Google Scholar]
140. 140. 

     Valencia AM, Collings CK, Dao HT, St Pierre R, Cheng YC et al. 2019. Recurrent SMARCB1 mutations reveal a nucleosome acidic patch interaction site that potentiates mSWI/SNF complex chromatin remodeling. Cell 179:1342–56.e23
     [Google Scholar]
141. 141. 

     von Hippel PH, Berg OG 1989. Facilitated target location in biological systems. J. Biol. Chem. 264:675–78
     [Google Scholar]
142. 142. 

     Voss TC, Hager GL. 2014. Dynamic regulation of transcriptional states by chromatin and transcription factors. Nat. Rev. Genet. 15:69–81
     [Google Scholar]
143. 143. 

     Wang A, Yue F, Li Y, Xie R, Harper T et al. 2015. Epigenetic priming of enhancers predicts developmental competence of hESC-derived endodermal lineage intermediates. Cell Stem Cell 16:386–99
     [Google Scholar]
144. 144. 

     Wapinski OL, Vierbuchen T, Qu K, Lee QY, Chanda S et al. 2013. Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell 155:621–35
     [Google Scholar]
145. 145. 

     Watt AJ, Zhao R, Li J, Duncan SA 2007. Development of the mammalian liver and ventral pancreas is dependent on GATA4. BMC Dev. Biol. 7:37
     [Google Scholar]
146. 146. 

     Watts JA, Zhang C, Klein-Szanto AJ, Kormish JD, Fu J et al. 2011. Study of FoxA pioneer factor at silent genes reveals Rfx-repressed enhancer at Cdx2 and a potential indicator of esophageal adenocarcinoma development. PLOS Genet 7:e1002277
     [Google Scholar]
147. 147. 

     White MD, Angiolini JF, Alvarez YD, Kaur G, Zhao ZW et al. 2016. Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165:75–87
     [Google Scholar]
148. 148. 

     Whitton H, Singh LN, Patrick MA, Price AJ, Osorio FG et al. 2018. Changes at the nuclear lamina alter binding of pioneer factor Foxa2 in aged liver. Aging Cell 17:e12742
     [Google Scholar]
149. 149. 

     Xu J, Watts JA, Pope SD, Gadue P, Kamps M et al. 2009. Transcriptional competence and the active marking of tissue-specific enhancers by defined transcription factors in embryonic and induced pluripotent stem cells. Genes Dev 23:2824–38
     [Google Scholar]
150. 150. 

     Yan C, Chen H, Bai L 2018. Systematic study of nucleosome-displacing factors in budding yeast. Mol. Cell 71:294–305.e4
     [Google Scholar]
151. 151. 

     Yu X, Buck MJ. 2019. Defining TP53 pioneering capabilities with competitive nucleosome binding assays. Genome Res 29:107–15
     [Google Scholar]
152. 152. 

     Zhao R, Watt AJ, Li J, Luebke-Wheeler J, Morrisey EE, Duncan SA 2005. GATA6 is essential for embryonic development of the liver but dispensable for early heart formation. Mol. Cell. Biol. 25:2622–31
     [Google Scholar]
153. 153. 

     Zhu F, Farnung L, Kaasinen E, Sahu B, Yin Y et al. 2018. The interaction landscape between transcription factors and the nucleosome. Nature 562:76–81
     [Google Scholar]