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A CpG island (CGI) lies at the 5′ end of the  Airn  macro non-protein-coding (nc) RNA that represses the flanking  Igf2r  promoter  in cis  on paternally inherited chromosomes. In addition to being modified on maternally inherited chromosomes by a DNA methylation imprint, the  Airn  CGI shows two unusual organization features: its position immediately downstream of the  Airn  promoter and transcription start site and a series of tandem direct repeats (TDRs) occupying its second half. The physical separation of the  Airn  promoter from the CGI provides a model to investigate if the CGI plays distinct transcriptional and epigenetic roles. We used homologous recombination to generate embryonic stem cells carrying deletions at the endogenous locus of the entire CGI or just the TDRs. The deleted  Airn  alleles were analyzed by using an ES cell imprinting model that recapitulates the onset of  Igf2r  imprinted expression in embryonic development or by using knock-out mice. The results show that the CGI is required for efficient  Airn  initiation and to maintain the unmethylated state of the  Airn  promoter, which are both necessary for  Igf2r  repression on the paternal chromosome. The TDRs occupying the second half of the CGI play a minor role in  Airn  transcriptional elongation or processivity, but are essential for methylation on the maternal  Airn  promoter that is necessary for  Igf2r  to be expressed from this chromosome. Together the data indicate the existence of a class of regulatory CGIs in the mammalian genome that act downstream of the promoter and transcription start.

A Downstream CpG Island Controls Transcript Initiation and Elongation and the Methylation State of the Imprinted Airn Macro ncRNA Promoter