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Comparative RNA editing in autistic and neurotypical cerebella

Molecular Psychiatry volume 18, pages 1041–1048 (2013)Cite this article

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Abstract

Adenosine-to-inosine (A-to-I) RNA editing is a neurodevelopmentally regulated epigenetic modification shown to modulate complex behavior in animals. Little is known about human A-to-I editing, but it is thought to constitute one of many molecular mechanisms connecting environmental stimuli and behavioral outputs. Thus, comprehensive exploration of A-to-I RNA editing in human brains may shed light on gene–environment interactions underlying complex behavior in health and disease. Synaptic function is a main target of A-to-I editing, which can selectively recode key amino acids in synaptic genes, directly altering synaptic strength and duration in response to environmental signals. Here, we performed a high-resolution survey of synaptic A-to-I RNA editing in a human population, and examined how it varies in autism, a neurodevelopmental disorder in which synaptic abnormalities are a common finding. Using ultra-deep (>1000 × ) sequencing, we quantified the levels of A-to-I editing of 10 synaptic genes in postmortem cerebella from 14 neurotypical and 11 autistic individuals. A high dynamic range of editing levels was detected across individuals and editing sites, from 99.6% to below detection limits. In most sites, the extreme ends of the population editing distributions were individuals with autism. Editing was correlated with isoform usage, clusters of correlated sites were identified, and differential editing patterns examined. Finally, a dysfunctional form of the editing enzyme adenosine deaminase acting on RNA B1 was found more commonly in postmortem cerebella from individuals with autism. These results provide a population-level, high-resolution view of A-to-I RNA editing in human cerebella and suggest that A-to-I editing of synaptic genes may be informative for assessing the epigenetic risk for autism.

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Acknowledgements

We thank Oliver St Lawrence, Jamie Jett, Benjamin Boese and Tim Harkins at 454, our wonderful lab mates, Professor David Bartel, Thutrang Nguyen, Eran Mick and Elena Helman for their tremendous help. Human tissue was obtained from the National Institute of Child Health and Human Development Brain and Tissue Bank for Developmental Disorders at the University of Maryland, Baltimore, MD, USA contract HHSN275200900011C, re. no. N01-HD-9-0011, and from The Harvard Brain Tissue Resource Center, through the Autism Tissue Program. The Harvard Brain Tissue Resource Center is supported by grant MH068855. The Molecular Genetics Core Facility at Children’s Hospital Boston Intellectual and Developmental Disabilities Research Center (IDDRC) is supported by grant NIH-P30-HD18655. This study was generously supported by the Nancy Lurie Marks Family Foundation, The Roche Applied Science Sequencing Grant Program, Autism Speaks, Simons Foundation and the NIH Grant 1R01MH085143-01.

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Authors and Affiliations

  1. Harvard-MIT Division of Health Sciences and Technology, Cambridge, MA, USA

    A Eran, E N Brown & I S Kohane

  2. Program in Genomics, Boston Children’s Hospital, Boston, MA, USA

    A Eran, K Vatalaro, J McCarthy, F Rahimov, C Collins, K Markianos & L M Kunkel

  3. Department of Genetics, Stanford University, Stanford, CA, USA

    J B Li

  4. Department of Genetics, Harvard Medical School, Boston, MA, USA

    F Rahimov, C Collins & L M Kunkel

  5. Department of Pediatrics, Harvard Medical School, Boston, MA, USA

    K Markianos, D M Margulies, I S Kohane & L M Kunkel

  6. Correlagen Diagnostics, Waltham, MA, USA

    D M Margulies

  7. Center for Biomedical Informatics, Harvard Medical School, Boston, MA, USA

    D M Margulies & I S Kohane

  8. Department of Anesthesia and Critical Care, Neuroscience Statistics Research Laboratory, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

    E N Brown

  9. Department of Brain and Cognitive Sciences, MIT, Cambridge, MA, USA

    E N Brown

  10. Broad Institute of Harvard and MIT, Cambridge, MA, USA

    S E Calvo

  11. The Manton Center for Orphan Disease Research, Boston, MA, USA

    L M Kunkel

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Eran, A., Li, J., Vatalaro, K. et al. Comparative RNA editing in autistic and neurotypical cerebella. Mol Psychiatry 18, 1041–1048 (2013). https://doi.org/10.1038/mp.2012.118

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