Nucleosome binding by the pioneer transcription factor OCT4.
Amino Acid Sequence
Base Sequence
Binding Sites
Cell-Free System
Cloning, Molecular
Cryoelectron Microscopy
DNA
/ chemistry
Enhancer Elements, Genetic
Escherichia coli
/ genetics
Gene Expression
Genetic Vectors
/ chemistry
Heterochromatin
/ chemistry
Histones
/ chemistry
Humans
Nucleic Acid Conformation
Nucleosomes
/ chemistry
Octamer Transcription Factor-3
/ chemistry
Protein Binding
Protein Conformation
Protein Isoforms
/ chemistry
RNA-Binding Proteins
/ chemistry
Recombinant Fusion Proteins
/ chemistry
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
16 07 2020
16 07 2020
Historique:
received:
06
03
2020
accepted:
24
06
2020
entrez:
18
7
2020
pubmed:
18
7
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Transcription factor binding to genomic DNA is generally prevented by nucleosome formation, in which the DNA is tightly wrapped around the histone octamer. In contrast, pioneer transcription factors efficiently bind their target DNA sequences within the nucleosome. OCT4 has been identified as a pioneer transcription factor required for stem cell pluripotency. To study the nucleosome binding by OCT4, we prepared human OCT4 as a recombinant protein, and biochemically analyzed its interactions with the nucleosome containing a natural OCT4 target, the LIN28B distal enhancer DNA sequence, which contains three potential OCT4 target sequences. By a combination of chemical mapping and cryo-electron microscopy single-particle analysis, we mapped the positions of the three target sequences within the nucleosome. A mutational analysis revealed that OCT4 preferentially binds its target DNA sequence located near the entry/exit site of the nucleosome. Crosslinking mass spectrometry consistently showed that OCT4 binds the nucleosome in the proximity of the histone H3 N-terminal region, which is close to the entry/exit site of the nucleosome. We also found that the linker histone H1 competes with OCT4 for the nucleosome binding. These findings provide important information for understanding the molecular mechanism by which OCT4 binds its target DNA in chromatin.
Identifiants
pubmed: 32678275
doi: 10.1038/s41598-020-68850-1
pii: 10.1038/s41598-020-68850-1
pmc: PMC7367260
doi:
Substances chimiques
Heterochromatin
0
Histones
0
LIN28B protein, human
0
Nucleosomes
0
Octamer Transcription Factor-3
0
POU5F1 protein, human
0
Protein Isoforms
0
RNA-Binding Proteins
0
Recombinant Fusion Proteins
0
DNA
9007-49-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11832Références
Lambert, S. A. et al. The human transcription factors. Cell 172, 650–665 (2018).
pubmed: 29425488
Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251–260 (1997).
pubmed: 9305837
Koyama, M. & Kurumizaka, H. Structural diversity of the nucleosome. J. Biochem. 163, 85–95 (2018).
pubmed: 29161414
Iwafuchi-Doi, M. & Zaret, K. S. Pioneer transcription factors in cell reprogramming. Genes Dev. 28, 2679–2692 (2014).
pubmed: 25512556
pmcid: 4265672
Zaret, K. S. & Mango, S. E. Pioneer transcription factors, chromatin dynamics, and cell fate control. Curr. Opin. Genet. Dev. 37, 76–81 (2016).
pubmed: 26826681
pmcid: 4914445
Makowski, M. M., Gaullier, G. & Luger, K. Picking a nucleosome lock: sequence- and structure-specific recognition of the nucleosome. J. Biosci. 45, 13. https://doi.org/10.1007/s12038-019-9970-7 (2020).
doi: 10.1007/s12038-019-9970-7
pubmed: 31965991
Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676 (2006).
pubmed: 16904174
Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861–872 (2007).
Soufi, A., Donahue, G. & Zaret, K. S. Facilitators and impediments of the pluripotency reprogramming factors’ initial engagement with the genome. Cell 151, 994–1004 (2012).
pubmed: 23159369
pmcid: 3508134
Soufi, A. et al. Pioneer transcription factors target partial DNA motifs on nucleosomes to initiate reprogramming. Cell 161, 555–568 (2015).
pubmed: 25892221
pmcid: 4409934
Schöler, H. R., Hatzopoulos, A. K., Balling, R., Suzuki, N. & Gruss, P. A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. EMBO J. 8, 2543–2550 (1989).
pubmed: 2573523
pmcid: 401252
Rosner, M. H. et al. A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345, 686–692 (1990).
pubmed: 1972777
Verrijzer, C. P. et al. The DNA binding specificity of the bipartite POU domain and its subdomains. EMBO J. 11, 4993–5003 (1992).
pubmed: 1361172
pmcid: 556977
Reményi, A. et al. Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev. 17, 2048–2059 (2003).
pubmed: 12923055
pmcid: 196258
Esch, D. et al. A unique Oct4 interface is crucial for reprogramming to pluripotency. Nat. Cell Biol. 15, 295–301 (2013).
pubmed: 23376973
Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917–1920 (2007).
Hanna, J. et al. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462, 595–601 (2009).
pubmed: 19898493
pmcid: 2789972
Tsialikas, J. & Romer-Seibert, J. LIN28: roles and regulation in development and beyond. Development 142, 2397–2404 (2015).
pubmed: 26199409
pmcid: 26199409
Brogaard, K. R., Xi, L., Wang, J. P. & Widom, J. A chemical approach to mapping nucleosomes at base pair resolution in yeast. Methods Enzymol. 513, 315–334 (2012).
pubmed: 22929776
pmcid: 5101424
Flaus, A., Luger, K., Tan, S. & Richmond, T. J. Mapping nucleosome position at single base-pair resolution by using site-directed hydroxyl radicals. Proc. Natl. Acad. Sci. U S A 93, 1370–1375 (1996).
pubmed: 8643638
pmcid: 39944
Reményi, A., Pohl, E., Schöler, H. R. & Wilmanns, M. Crystallization of redox-insensitive Oct1 POU domain with different DNA-response elements. Acta Crystallogr. D Biol. Crystallogr. 57, 1634–1638 (2001).
pubmed: 11679729
Smith, A. E. F. & Ford, K. G. Use of altered-specificity binding Oct-4 suggests an absence of pluripotent cell-specific cofactor usage. Nucleic Acids Res. 33, 6011–6023 (2005).
pubmed: 16243786
pmcid: 1266064
Zhou, B. R. et al. Structural insights into the histone H1-nucleosome complex. Proc. Natl. Acad. Sci. U S A. 110, 19390–19395 (2013).
pubmed: 24218562
pmcid: 3845106
Zhou, B. R. et al. Structural mechanisms of nucleosome recognition by linker histones. Mol. Cell 59, 628–638 (2015).
pubmed: 26212454
pmcid: 4546531
Bednar, J. et al. Structure and dynamics of a 197 bp nucleosome in complex with linker histone H1. Mol. Cell 66, 384–397 (2017).
pubmed: 28475873
pmcid: 5508712
Garcia-Saez, I. et al. Structure of an H1-bound 6-nucleosome array reveals an untwisted two-start chromatin fiber conformation. Mol. Cell 72, 902–915 (2018).
pubmed: 30392928
Song, F. et al. Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science 344, 376–380 (2014).
pubmed: 24763583
Meshorer, E. et al. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10, 105–116 (2006).
pubmed: 16399082
pmcid: 1868458
Gaspar-Maia, A., Alajem, A., Meshorer, E. & Ramalho-Santos, M. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 12, 36–47 (2014).
Christophorou, M. A. et al. Citrullination regulates pluripotency and histone H1 binding to chromatin. Nature 507, 104–108 (2014).
pubmed: 24463520
pmcid: 4843970
Dimitrov, S., Almouzni, G., Dasso, M. & Wolffe, A. P. Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. Dev. Biol. 160, 214–227 (1993).
pubmed: 8224538
Zhu, F. et al. The interaction landscape between transcription factors and the nucleosome. Nature 562, 76–81 (2018).
pubmed: 30250250
pmcid: 6173309
Michael, A. K. et al. Mechanisms of OCT4-SOX2 motif readout on nucleosomes. Science https://doi.org/10.1126/science.abb0074 (2020).
doi: 10.1126/science.abb0074
pubmed: 32327602
Li, S., Zheng, E. B., Zhao, L. & Liu, S. Nonreciprocal and conditional cooperativity directs the pioneer activity of pluripotency transcription factors. Cell Rep. 28, 2689-2703.e4 (2019).
pubmed: 31484078
pmcid: 6750763
Dodonova, S. O. et al. Nucleosome-bound SOX2 and SOX11 structures elucidate pioneer factor function. Nature 580, 669–672 (2020).
pubmed: 32350470
Cirillo, L. A. et al. Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. EMBO J. 17, 244–254 (1998).
pubmed: 9427758
pmcid: 1170375
Clark, K., Halay, E., Lai, E. & Burley, S. K. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364, 412–420 (1993).
pubmed: 8332212
Zhang, Y. et al. Histone H1 depletion impairs embryonic stem cell differentiation. PLoS Genet. 8, e1002691. https://doi.org/10.1371/journal.pgen.1002691 (2012).
doi: 10.1371/journal.pgen.1002691
pubmed: 22589736
pmcid: 3349736
Izzo, A. et al. Dynamic changes in H1 subtype composition during epigenetic reprogramming. J. Cell Biol. 216, 3017–3028 (2017).
pubmed: 28794128
pmcid: 5626532
Caron, F. & Thomas, J. O. Exchange of histone H1 between segments of chromatin. J. Mol. Biol. 146, 513–537 (1981).
pubmed: 7277492
Misteli, T., Gunjan, A., Hock, R., Bustin, M. & Brown, D. T. Dynamic binding of histone H1 to chromatin in living cells. Nature 408, 877–881 (2000).
pubmed: 11130729
Machida, S. et al. Nap1 stimulates homologous recombination by RAD51 and RAD54 in higher-ordered chromatin containing histone H1. Sci. Rep. 4, 4863. https://doi.org/10.1038/srep04863 (2015).
doi: 10.1038/srep04863
Kujirai, T. et al. Methods for preparing nucleosomes containing histone variants. Methods Mol. Biol. 1832, 3–20 (2018).
pubmed: 30073519
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466
pmcid: 5494038
Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
pubmed: 26278980
pmcid: 6760662
Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. Elife 7, e42166. https://doi.org/10.7554/eLife.42166 (2018).
doi: 10.7554/eLife.42166
pubmed: 30412051
pmcid: 30412051
Scheres, S. H. Processing of structurally heterogeneous cryo-EM data in RELION. Methods Enzymol. 579, 125–157 (2016).
pubmed: 27572726
Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63–65 (2004).
Kleywegt, G. J. et al. The uppsala electron-density server. Acta Crystallogr. D Biol. Crystallogr. 60, 2240–2249 (2004).
pubmed: 15572777
Pettersen, E. F. et al. UCSF Chimera—A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
Leitner, A., Walzthoeni, T. & Aebersold, R. Lysine-specific chemical cross-linking of protein complexes and identification of cross-linking sites using LC-MS/MS and the xQuest/xProphet software pipeline. Nat. Protoc. 9, 120–137 (2014).
pubmed: 24356771
Kobayashi, W. et al. Structural and biochemical analyses of the nuclear pore complex component ELYS identify residues responsible for nucleosome binding. Commun. Biol. 2, 163. https://doi.org/10.1038/s42003-019-0385-7 (2019).
doi: 10.1038/s42003-019-0385-7
pubmed: 31069272
pmcid: 6499780
Grimm, M., Zimniak, T., Kahraman, A. & Herzog, F. xVis: a web server for the schematic visualization and interpretation of crosslink-derived spatial restraints. Nucleic Acids Res. 43, W362–W369 (2015).
pubmed: 25956653
pmcid: 4489277
Okuda, S. et al. jPOSTrepo: an international standard data repository for proteomes. Nucleic Acids Res. 45, D1107–D1111 (2017).
pubmed: 27899654
pmcid: 27899654