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The interaction landscape between transcription factors and the nucleosome

Author

Listed:
  • Fangjie Zhu

    (University of Cambridge)

  • Lucas Farnung

    (Max Planck Institute for Biophysical Chemistry, Department of Molecular Biology)

  • Eevi Kaasinen

    (Karolinska Institutet)

  • Biswajyoti Sahu

    (University of Helsinki)

  • Yimeng Yin

    (Karolinska Institutet)

  • Bei Wei

    (Karolinska Institutet)

  • Svetlana O. Dodonova

    (Max Planck Institute for Biophysical Chemistry, Department of Molecular Biology)

  • Kazuhiro R. Nitta

    (Karolinska Institutet)

  • Ekaterina Morgunova

    (Karolinska Institutet)

  • Minna Taipale

    (University of Cambridge
    Karolinska Institutet)

  • Patrick Cramer

    (Max Planck Institute for Biophysical Chemistry, Department of Molecular Biology
    Karolinska Institutet)

  • Jussi Taipale

    (University of Cambridge
    Karolinska Institutet
    University of Helsinki)

Abstract

Nucleosomes cover most of the genome and are thought to be displaced by transcription factors in regions that direct gene expression. However, the modes of interaction between transcription factors and nucleosomal DNA remain largely unknown. Here we systematically explore interactions between the nucleosome and 220 transcription factors representing diverse structural families. Consistent with earlier observations, we find that the majority of the studied transcription factors have less access to nucleosomal DNA than to free DNA. The motifs recovered from transcription factors bound to nucleosomal and free DNA are generally similar. However, steric hindrance and scaffolding by the nucleosome result in specific positioning and orientation of the motifs. Many transcription factors preferentially bind close to the end of nucleosomal DNA, or to periodic positions on the solvent-exposed side of the DNA. In addition, several transcription factors usually bind to nucleosomal DNA in a particular orientation. Some transcription factors specifically interact with DNA located at the dyad position at which only one DNA gyre is wound, whereas other transcription factors prefer sites spanning two DNA gyres and bind specifically to each of them. Our work reveals notable differences in the binding of transcription factors to free and nucleosomal DNA, and uncovers a diverse interaction landscape between transcription factors and the nucleosome.

Suggested Citation

  • Fangjie Zhu & Lucas Farnung & Eevi Kaasinen & Biswajyoti Sahu & Yimeng Yin & Bei Wei & Svetlana O. Dodonova & Kazuhiro R. Nitta & Ekaterina Morgunova & Minna Taipale & Patrick Cramer & Jussi Taipale, 2018. "The interaction landscape between transcription factors and the nucleosome," Nature, Nature, vol. 562(7725), pages 76-81, October.
  • Handle: RePEc:nat:nature:v:562:y:2018:i:7725:d:10.1038_s41586-018-0549-5
    DOI: 10.1038/s41586-018-0549-5
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    Citations

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    Cited by:

    1. Pengcheng Zhang & Haochen Wang & Hanwen Xu & Lei Wei & Liyang Liu & Zhirui Hu & Xiaowo Wang, 2023. "Deep flanking sequence engineering for efficient promoter design using DeepSEED," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Vivekanandan Ramalingam & Xinyang Yu & Brian D. Slaughter & Jay R. Unruh & Kaelan J. Brennan & Anastasiia Onyshchenko & Jeffrey J. Lange & Malini Natarajan & Michael Buck & Julia Zeitlinger, 2023. "Lola-I is a promoter pioneer factor that establishes de novo Pol II pausing during development," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Michaël Noë & Dimitrios Mathios & Akshaya V. Annapragada & Shashikant Koul & Zacharia H. Foda & Jamie E. Medina & Stephen Cristiano & Christopher Cherry & Daniel C. Bruhm & Noushin Niknafs & Vilmos Ad, 2024. "DNA methylation and gene expression as determinants of genome-wide cell-free DNA fragmentation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Marios G. Koliopoulos & Reyhan Muhammad & Theodoros I. Roumeliotis & Fabienne Beuron & Jyoti S. Choudhary & Claudio Alfieri, 2022. "Structure of a nucleosome-bound MuvB transcription factor complex reveals DNA remodelling," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Anna Berenson & Ryan Lane & Luis F. Soto-Ugaldi & Mahir Patel & Cosmin Ciausu & Zhaorong Li & Yilin Chen & Sakshi Shah & Clarissa Santoso & Xing Liu & Kerstin Spirohn & Tong Hao & David E. Hill & Marc, 2023. "Paired yeast one-hybrid assays to detect DNA-binding cooperativity and antagonism across transcription factors," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Amir Shahein & Maria López-Malo & Ivan Istomin & Evan J. Olson & Shiyu Cheng & Sebastian J. Maerkl, 2022. "Systematic analysis of low-affinity transcription factor binding site clusters in vitro and in vivo establishes their functional relevance," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    7. Anushweta Asthana & Parameshwaran Ramanan & Alexander Hirschi & Keelan Z. Guiley & Tilini U. Wijeratne & Robert Shelansky & Michael J. Doody & Haritha Narasimhan & Hinrich Boeger & Sarvind Tripathi & , 2022. "The MuvB complex binds and stabilizes nucleosomes downstream of the transcription start site of cell-cycle dependent genes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Tianbao Li & Qi Liu & Zhong Chen & Kun Fang & Furong Huang & Xueqi Fu & Qianben Wang & Victor X. Jin, 2022. "Dynamic nucleosome landscape elicits a noncanonical GATA2 pioneer model," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    9. Pakavarin Louphrasitthiphol & Alessia Loffreda & Vivian Pogenberg & Sarah Picaud & Alexander Schepsky & Hans Friedrichsen & Zhiqiang Zeng & Anahita Lashgari & Benjamin Thomas & E. Elizabeth Patton & M, 2023. "Acetylation reprograms MITF target selectivity and residence time," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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