Extra-coding RNAs regulate neuronal DNA methylation dynamics

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, Humaira Gowher, J. David Sweatt () and Jeremy J. Day ()
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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

Nature Communications, 2016, vol. 7, issue 1, 1-14

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms12091

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