IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0046867.html
   My bibliography  Save this article

Stage and Gene Specific Signatures Defined by Histones H3K4me2 and H3K27me3 Accompany Mammalian Retina Maturation In Vivo

Author

Listed:
  • Evgenya Y Popova
  • Xuming Xu
  • Andrew T DeWan
  • Anna C Salzberg
  • Arthur Berg
  • Josephine Hoh
  • Samuel S Zhang
  • Colin J Barnstable

Abstract

The epigenetic contribution to neurogenesis is largely unknown. There is, however, growing evidence that posttranslational modification of histones is a dynamic process that shows many correlations with gene expression. Here we have followed the genome-wide distribution of two important histone H3 modifications, H3K4me2 and H3K27me3 during late mouse retina development. The retina provides an ideal model for these studies because of its well-characterized structure and development and also the extensive studies of the retinal transcriptome and its development. We found that a group of genes expressed only in mature rod photoreceptors have a unique signature consisting of de-novo accumulation of H3K4me2, both at the transcription start site (TSS) and over the whole gene, that correlates with the increase in transcription, but no accumulation of H3K27me3 at any stage. By in silico analysis of this unique signature we have identified a larger group of genes that may be selectively expressed in mature rod photoreceptors. We also found that the distribution of H3K4me2 and H3K27me3 on the genes widely expressed is not always associated with their transcriptional levels. Different histone signatures for retinal genes with the same gene expression pattern suggest the diversities of epigenetic regulation. Genes without H3K4me2 and H3K27me3 accumulation at any stage represent a large group of transcripts never expressed in retina. The epigenetic signatures defined by H3K4me2 and H3K27me3 can distinguish cell-type specific genes from widespread transcripts and may be reflective of cell specificity during retina maturation. In addition to the developmental patterns seen in wild type retina, the dramatic changes of histone modification in the retinas of mutant animals lacking rod photoreceptors provide a tool to study the epigenetic changes in other cell types and thus describe a broad range of epigenetic events in a solid tissue in vivo.

Suggested Citation

  • Evgenya Y Popova & Xuming Xu & Andrew T DeWan & Anna C Salzberg & Arthur Berg & Josephine Hoh & Samuel S Zhang & Colin J Barnstable, 2012. "Stage and Gene Specific Signatures Defined by Histones H3K4me2 and H3K27me3 Accompany Mammalian Retina Maturation In Vivo," PLOS ONE, Public Library of Science, vol. 7(10), pages 1-14, October.
    • Handle: RePEc:plo:pone00:0046867
    DOI: 10.1371/journal.pone.0046867
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0046867
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0046867&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0046867?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. Tarjei S. Mikkelsen & Manching Ku & David B. Jaffe & Biju Issac & Erez Lieberman & Georgia Giannoukos & Pablo Alvarez & William Brockman & Tae-Kyung Kim & Richard P. Koche & William Lee & Eric Mendenh, 2007. "Genome-wide maps of chromatin state in pluripotent and lineage-committed cells," Nature, Nature, vol. 448(7153), pages 553-560, August.
    2. Alvaro Rada-Iglesias & Ruchi Bajpai & Tomek Swigut & Samantha A. Brugmann & Ryan A. Flynn & Joanna Wysocka, 2011. "A unique chromatin signature uncovers early developmental enhancers in humans," Nature, Nature, vol. 470(7333), pages 279-283, February.
    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. Liang-Yu Fu & Tao Zhu & Xinkai Zhou & Ranran Yu & Zhaohui He & Peijing Zhang & Zhigui Wu & Ming Chen & Kerstin Kaufmann & Dijun Chen, 2022. "ChIP-Hub provides an integrative platform for exploring plant regulome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Tomoya Sakamoto & Kirill Batmanov & Shibiao Wan & Yuanjun Guo & Ling Lai & Rick B. Vega & Daniel P. Kelly, 2022. "The nuclear receptor ERR cooperates with the cardiogenic factor GATA4 to orchestrate cardiomyocyte maturation," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    3. Gaylor Boulay & Liliane C. Broye & Rui Dong & Sowmya Iyer & Rajendran Sanalkumar & Yu-Hang Xing & Rémi Buisson & Shruthi Rengarajan & Beverly Naigles & Benoît Duc & Angela Volorio & Mary E. Awad & Raf, 2024. "EWS-WT1 fusion isoforms establish oncogenic programs and therapeutic vulnerabilities in desmoplastic small round cell tumors," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Daniel Sánchez-Taltavull & Parameswaran Ramachandran & Nelson Lau & Theodore J Perkins, 2016. "Bayesian Correlation Analysis for Sequence Count Data," PLOS ONE, Public Library of Science, vol. 11(10), pages 1-24, October.
    5. Yayoi Natsume-Kitatani & Hiroshi Mamitsuka, 2016. "Classification of Promoters Based on the Combination of Core Promoter Elements Exhibits Different Histone Modification Patterns," PLOS ONE, Public Library of Science, vol. 11(3), pages 1-18, March.
    6. Jessica L Larson & Guo-Cheng Yuan, 2012. "Chromatin States Accurately Classify Cell Differentiation Stages," PLOS ONE, Public Library of Science, vol. 7(2), pages 1-9, February.
    7. Masaki Kikuchi & Satoshi Morita & Masatoshi Wakamori & Shin Sato & Tomomi Uchikubo-Kamo & Takehiro Suzuki & Naoshi Dohmae & Mikako Shirouzu & Takashi Umehara, 2023. "Epigenetic mechanisms to propagate histone acetylation by p300/CBP," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Linghua Zhou & Yong Shen & Libo Jiang & Danni Yin & Jingxin Guo & Hui Zheng & Hao Sun & Rongling Wu & Yunqian Guo, 2015. "Systems Mapping for Hematopoietic Progenitor Cell Heterogeneity," PLOS ONE, Public Library of Science, vol. 10(5), pages 1-18, May.
    9. Victor Lopez Soriano & Alfredo Dueñas Rey & Rajarshi Mukherjee & Frauke Coppieters & Miriam Bauwens & Andy Willaert & Elfride De Baere, 2024. "Multi-omics analysis in human retina uncovers ultraconserved cis-regulatory elements at rare eye disease loci," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Samuel Abassah-Oppong & Matteo Zoia & Brandon J. Mannion & Raquel Rouco & Virginie Tissières & Cailyn H. Spurrell & Virginia Roland & Fabrice Darbellay & Anja Itum & Julie Gamart & Tabitha A. Festa-Da, 2024. "A gene desert required for regulatory control of pleiotropic Shox2 expression and embryonic survival," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    11. 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.
    12. Kosei Nagata & Hironori Hojo & Song Ho Chang & Hiroyuki Okada & Fumiko Yano & Ryota Chijimatsu & Yasunori Omata & Daisuke Mori & Yuma Makii & Manabu Kawata & Taizo Kaneko & Yasuhide Iwanaga & Hideki N, 2022. "Runx2 and Runx3 differentially regulate articular chondrocytes during surgically induced osteoarthritis development," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    13. Raquel Rouco & Olimpia Bompadre & Antonella Rauseo & Olivier Fazio & Rodrigue Peraldi & Fabrizio Thorel & Guillaume Andrey, 2021. "Cell-specific alterations in Pitx1 regulatory landscape activation caused by the loss of a single enhancer," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    14. Lasse K. Markussen & Elizabeth A. Rondini & Olivia Sveidahl Johansen & Jesper G. S. Madsen & Elahu G. Sustarsic & Ann-Britt Marcher & Jacob B. Hansen & Zachary Gerhart-Hines & James G. Granneman & Sus, 2022. "Lipolysis regulates major transcriptional programs in brown adipocytes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Liu Wang & Jie Wu & Madeline Sramek & S. M. Bukola Obayomi & Peidong Gao & Yan Li & Aleksey V. Matveyenko & Zong Wei, 2024. "Heterogeneous enhancer states orchestrate β cell responses to metabolic stress," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    16. Mohammad Jaber & Ahmed Radwan & Netanel Loyfer & Mufeed Abdeen & Shulamit Sebban & Areej Khatib & Hazar Yassen & Thorsten Kolb & Marc Zapatka & Kirill Makedonski & Aurelie Ernst & Tommy Kaplan & Yosef, 2022. "Comparative parallel multi-omics analysis during the induction of pluripotent and trophectoderm states," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    17. Dongjun Chung & Dan Park & Kevin Myers & Jeffrey Grass & Patricia Kiley & Robert Landick & Sündüz Keleş, 2013. "dPeak: High Resolution Identification of Transcription Factor Binding Sites from PET and SET ChIP-Seq Data," PLOS Computational Biology, Public Library of Science, vol. 9(10), pages 1-13, October.
    18. Federica Baccini & Monica Bianchini & Filippo Geraci, 2022. "Graph-Based Integration of Histone Modification Profiles," Mathematics, MDPI, vol. 10(11), pages 1-15, May.
    19. Marco Luciani & Chiara Garsia & Stefano Beretta & Ingrid Cifola & Clelia Peano & Ivan Merelli & Luca Petiti & Annarita Miccio & Vasco Meneghini & Angela Gritti, 2024. "Human iPSC-derived neural stem cells displaying radial glia signature exhibit long-term safety in mice," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    20. 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.

    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:plo:pone00:0046867. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.