Evolution of imprinting via lineage-specific insertion of retroviral promoters

Aaron B. Bogutz, Julie Brind’Amour, Hisato Kobayashi, Kristoffer N. Jensen, Kazuhiko Nakabayashi, Hiroo Imai, Matthew C. Lorincz () and Louis Lefebvre ()
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Aaron B. Bogutz: University of British Columbia
Julie Brind’Amour: University of British Columbia
Hisato Kobayashi: Nara Medical University
Kristoffer N. Jensen: University of British Columbia
Kazuhiko Nakabayashi: Division of Developmental Genomics, Research Institute, National Center for Child Health and Development
Hiroo Imai: Kyoto University
Matthew C. Lorincz: University of British Columbia
Louis Lefebvre: University of British Columbia

Nature Communications, 2019, vol. 10, issue 1, 1-14

Abstract: Abstract Imprinted genes are expressed from a single parental allele, with the other allele often silenced by DNA methylation (DNAme) established in the germline. While species-specific imprinted orthologues have been documented, the molecular mechanisms underlying the evolutionary switch from biallelic to imprinted expression are unknown. During mouse oogenesis, gametic differentially methylated regions (gDMRs) acquire DNAme in a transcription-guided manner. Here we show that oocyte transcription initiating in lineage-specific endogenous retroviruses (ERVs) is likely responsible for DNAme establishment at 4/6 mouse-specific and 17/110 human-specific imprinted gDMRs. The latter are divided into Catarrhini- or Hominoidea-specific gDMRs embedded within transcripts initiating in ERVs specific to these primate lineages. Strikingly, imprinting of the maternally methylated genes Impact and Slc38a4 was lost in the offspring of female mice harboring deletions of the relevant murine-specific ERVs upstream of these genes. Our work reveals an evolutionary mechanism whereby maternally silenced genes arise from biallelically expressed progenitors.

Date: 2019
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DOI: 10.1038/s41467-019-13662-9

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