IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29360-y.html
   My bibliography  Save this article

DNA sequence-dependent formation of heterochromatin nanodomains

Author

Listed:
  • Graeme J. Thorn

    (University of Essex
    Queen Mary University of London)

  • Christopher T. Clarkson

    (University of Essex
    University College London)

  • Anne Rademacher

    (German Cancer Research Center (DKFZ) & Bioquant)

  • Hulkar Mamayusupova

    (University of Essex)

  • Gunnar Schotta

    (Ludwig-Maximilians-University (LMU) Munich)

  • Karsten Rippe

    (German Cancer Research Center (DKFZ) & Bioquant)

  • Vladimir B. Teif

    (University of Essex)

Abstract

The mammalian epigenome contains thousands of heterochromatin nanodomains (HNDs) marked by di- and trimethylation of histone H3 at lysine 9 (H3K9me2/3), which have a typical size of 3–10 nucleosomes. However, what governs HND location and extension is only partly understood. Here, we address this issue by introducing the chromatin hierarchical lattice framework (ChromHL) that predicts chromatin state patterns with single-nucleotide resolution. ChromHL is applied to analyse four HND types in mouse embryonic stem cells that are defined by histone methylases SUV39H1/2 or GLP, transcription factor ADNP or chromatin remodeller ATRX. We find that HND patterns can be computed from PAX3/9, ADNP and LINE1 sequence motifs as nucleation sites and boundaries that are determined by DNA sequence (e.g. CTCF binding sites), cooperative interactions between nucleosomes as well as nucleosome-HP1 interactions. Thus, ChromHL rationalizes how patterns of H3K9me2/3 are established and changed via the activity of protein factors in processes like cell differentiation.

Suggested Citation

  • Graeme J. Thorn & Christopher T. Clarkson & Anne Rademacher & Hulkar Mamayusupova & Gunnar Schotta & Karsten Rippe & Vladimir B. Teif, 2022. "DNA sequence-dependent formation of heterochromatin nanodomains," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29360-y
    DOI: 10.1038/s41467-022-29360-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29360-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-29360-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Andrew Angel & Jie Song & Caroline Dean & Martin Howard, 2011. "A Polycomb-based switch underlying quantitative epigenetic memory," Nature, Nature, vol. 476(7358), pages 105-108, August.
    2. Yin Shen & Feng Yue & David F. McCleary & Zhen Ye & Lee Edsall & Samantha Kuan & Ulrich Wagner & Jesse Dixon & Leonard Lee & Victor V. Lobanenkov & Bing Ren, 2012. "A map of the cis-regulatory sequences in the mouse genome," Nature, Nature, vol. 488(7409), pages 116-120, August.
    3. Yu-Ching Teng & Aishwarya Sundaresan & Ryan O’Hara & Vincent U. Gant & Minhua Li & Sara Martire & Jane N. Warshaw & Amrita Basu & Laura A. Banaszynski, 2021. "ATRX promotes heterochromatin formation to protect cells from G-quadruplex DNA-mediated stress," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    4. Michaela J. Obersriebnig & Emil M. H. Pallesen & Kim Sneppen & Ala Trusina & Geneviève Thon, 2016. "Nucleation and spreading of a heterochromatic domain in fission yeast," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    5. Michael B. Stadler & Rabih Murr & Lukas Burger & Robert Ivanek & Florian Lienert & Anne Schöler & Erik van Nimwegen & Christiane Wirbelauer & Edward J. Oakeley & Dimos Gaidatzis & Vijay K. Tiwari & Di, 2011. "DNA-binding factors shape the mouse methylome at distal regulatory regions," Nature, Nature, vol. 480(7378), pages 490-495, December.
    6. Veronika Ostapcuk & Fabio Mohn & Sarah H. Carl & Anja Basters & Daniel Hess & Vytautas Iesmantavicius & Lisa Lampersberger & Matyas Flemr & Aparna Pandey & Nicolas H. Thomä & Joerg Betschinger & Marc , 2018. "Activity-dependent neuroprotective protein recruits HP1 and CHD4 to control lineage-specifying genes," Nature, Nature, vol. 557(7707), pages 739-743, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xuelong Yao & Zongyang Lu & Zhanying Feng & Lei Gao & Xin Zhou & Min Li & Suijuan Zhong & Qian Wu & Zhenbo Liu & Haofeng Zhang & Zeyuan Liu & Lizhi Yi & Tao Zhou & Xudong Zhao & Jun Zhang & Yong Wang , 2022. "Comparison of chromatin accessibility landscapes during early development of prefrontal cortex between rhesus macaque and human," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Wei Vivian Li & Yiling Chen & Jingyi Jessica Li, 2017. "TROM: A Testing-Based Method for Finding Transcriptomic Similarity of Biological Samples," Statistics in Biosciences, Springer;International Chinese Statistical Association, vol. 9(1), pages 105-136, June.
    3. Amir D. Hay & Noah J. Kessler & Daniel Gebert & Nozomi Takahashi & Hugo Tavares & Felipe K. Teixeira & Anne C. Ferguson-Smith, 2023. "Epigenetic inheritance is unfaithful at intermediately methylated CpG sites," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    4. Marko Dunjić & Felix Jonas & Gilad Yaakov & Roye More & Yoav Mayshar & Yoach Rais & Ayelet-Hashahar Orenbuch & Saifeng Cheng & Naama Barkai & Yonatan Stelzer, 2023. "Histone exchange sensors reveal variant specific dynamics in mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Guillaume Harmange & Raúl A. Reyes Hueros & Dylan L. Schaff & Benjamin Emert & Michael Saint-Antoine & Laura C. Kim & Zijian Niu & Shivani Nellore & Mitchell E. Fane & Gretchen M. Alicea & Ashani T. W, 2023. "Disrupting cellular memory to overcome drug resistance," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Ravneet Jaura & Ssu-Yu Yeh & Kaitlin N. Montanera & Alyssa Ialongo & Zobia Anwar & Yiming Lu & Kavindu Puwakdandawa & Ho Sung Rhee, 2022. "Extended intergenic DNA contributes to neuron-specific expression of neighboring genes in the mammalian nervous system," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Beatriz del Blanco & Sergio Niñerola & Ana M. Martín-González & Juan Paraíso-Luna & Minji Kim & Rafael Muñoz-Viana & Carina Racovac & Jose V. Sanchez-Mut & Yijun Ruan & Ángel Barco, 2024. "Kdm1a safeguards the topological boundaries of PRC2-repressed genes and prevents aging-related euchromatinization in neurons," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    8. Yanting Luo & Jianlin He & Xiguang Xu & Ming-an Sun & Xiaowei Wu & Xuemei Lu & Hehuang Xie, 2018. "Integrative single-cell omics analyses reveal epigenetic heterogeneity in mouse embryonic stem cells," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-21, March.
    9. Renata Bordeira-Carriço & Joana Teixeira & Marta Duque & Mafalda Galhardo & Diogo Ribeiro & Rafael D. Acemel & Panos. N. Firbas & Juan J. Tena & Ana Eufrásio & Joana Marques & Fábio J. Ferreira & Telm, 2022. "Multidimensional chromatin profiling of zebrafish pancreas to uncover and investigate disease-relevant enhancers," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Nina Schmolka & Ino D. Karemaker & Richard Cardoso da Silva & Davide C. Recchia & Vincent Spegg & Jahnavi Bhaskaran & Michael Teske & Nathalie P. Wagenaar & Matthias Altmeyer & Tuncay Baubec, 2023. "Dissecting the roles of MBD2 isoforms and domains in regulating NuRD complex function during cellular differentiation," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    11. Hanna Braun & Ziyan Xu & Fiona Chang & Nikenza Viceconte & Grishma Rane & Michal Levin & Liudmyla Lototska & Franziska Roth & Alexia Hillairet & Albert Fradera-Sola & Vartika Khanchandani & Zi Wayne S, 2023. "ZNF524 directly interacts with telomeric DNA and supports telomere integrity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Jingting Xu & Hong Hu & Yang Dai, 2016. "LMethyR-SVM: Predict Human Enhancers Using Low Methylated Regions based on Weighted Support Vector Machines," PLOS ONE, Public Library of Science, vol. 11(9), pages 1-18, September.
    13. Tomas Zelenka & Antonios Klonizakis & Despina Tsoukatou & Dionysios-Alexandros Papamatheakis & Sören Franzenburg & Petros Tzerpos & Ioannis-Rafail Tzonevrakis & George Papadogkonas & Manouela Kapsetak, 2022. "The 3D enhancer network of the developing T cell genome is shaped by SATB1," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    14. Yu Chen & Mengjiao Luo & Haixia Tu & Yaling Qi & Yueshuai Guo & Xiangzheng Zhang & Yiqiang Cui & Mengmeng Gao & Xin Zhou & Tianyu Zhu & Hui Zhu & Chenghao Situ & Yan Li & Xuejiang Guo, 2024. "STYXL1 regulates CCT complex assembly and flagellar tubulin folding in sperm formation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    15. Xuemeng Zhou & Tsz Wing Sam & Ah Young Lee & Danny Leung, 2021. "Mouse strain-specific polymorphic provirus functions as cis-regulatory element leading to epigenomic and transcriptomic variations," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    16. Victoria Honnell & Jackie L. Norrie & Anand G. Patel & Cody Ramirez & Jiakun Zhang & Yu-Hsuan Lai & Shibiao Wan & Michael A. Dyer, 2022. "Identification of a modular super-enhancer in murine retinal development," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    17. Takayoshi Matsumura & Haruhito Totani & Yoshitaka Gunji & Masahiro Fukuda & Rui Yokomori & Jianwen Deng & Malini Rethnam & Chong Yang & Tze King Tan & Tadayoshi Karasawa & Kazuomi Kario & Masafumi Tak, 2022. "A Myb enhancer-guided analysis of basophil and mast cell differentiation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    18. Linlin Zhao & Sarah Richards & Franziska Turck & Markus Kollmann, 2020. "Information integration and decision making in flowering time control," PLOS ONE, Public Library of Science, vol. 15(9), pages 1-14, September.
    19. Abrar Aljahani & Peng Hua & Magdalena A. Karpinska & Kimberly Quililan & James O. J. Davies & A. Marieke Oudelaar, 2022. "Analysis of sub-kilobase chromatin topology reveals nano-scale regulatory interactions with variable dependence on cohesin and CTCF," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    20. Yiming Lu & Wubin Qu & Guangyu Shan & Chenggang Zhang, 2015. "DELTA: A Distal Enhancer Locating Tool Based on AdaBoost Algorithm and Shape Features of Chromatin Modifications," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-20, June.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29360-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.