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Extra-coding RNAs regulate neuronal DNA methylation dynamics

Author

Listed:
  • Katherine E. Savell

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Nancy V. N. Gallus

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Rhiana C. Simon

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Jordan A. Brown

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Jasmin S. Revanna

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Mary Katherine Osborn

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Esther Y. Song

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • John J. O’Malley

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Christian T. Stackhouse

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Allison Norvil

    (Purdue University)

  • Humaira Gowher

    (Purdue University)

  • J. David Sweatt

    (McKnight Brain Institute, University of Alabama at Birmingham)

  • Jeremy J. Day

    (McKnight Brain Institute, University of Alabama at Birmingham)

Abstract

Epigenetic mechanisms such as DNA methylation are essential regulators of the function and information storage capacity of neurons. DNA methylation is highly dynamic in the developing and adult brain, and is actively regulated by neuronal activity and behavioural experiences. However, it is presently unclear how methylation status at individual genes is targeted for modification. Here, we report that extra-coding RNAs (ecRNAs) interact with DNA methyltransferases and regulate neuronal DNA methylation. Expression of ecRNA species is associated with gene promoter hypomethylation, is altered by neuronal activity, and is overrepresented at genes involved in neuronal function. Knockdown of the Fos ecRNA locus results in gene hypermethylation and mRNA silencing, and hippocampal expression of Fos ecRNA is required for long-term fear memory formation in rats. These results suggest that ecRNAs are fundamental regulators of DNA methylation patterns in neuronal systems, and reveal a promising avenue for therapeutic targeting in neuropsychiatric disease states.

Suggested Citation

  • Katherine E. Savell & Nancy V. N. Gallus & Rhiana C. Simon & Jordan A. Brown & Jasmin S. Revanna & Mary Katherine Osborn & Esther Y. Song & John J. O’Malley & Christian T. Stackhouse & Allison Norvil , 2016. "Extra-coding RNAs regulate neuronal DNA methylation dynamics," Nature Communications, Nature, vol. 7(1), pages 1-14, November.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12091
    DOI: 10.1038/ncomms12091
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    Cited by:

    1. Carla L. Esposito & Ida Autiero & Annamaria Sandomenico & H. Li & Mahmoud A. Bassal & Maria L. Ibba & Dongfang Wang & Lucrezia Rinaldi & Simone Ummarino & Giulia Gaggi & Marta Borchiellini & Piotr Swi, 2023. "Targeted systematic evolution of an RNA platform neutralizing DNMT1 function and controlling DNA methylation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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