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Recently, researchers have uncovered the presence of many long noncoding RNAs (lncRNAs) in embryonic stem cells and believe they are important regulators of the differentiation process. However, there are only a few examples explicitly linking lncRNA activity to transcriptional regulation. Here, we used transcript counting and spatial localization to characterize a lncRNA (dubbed  linc-HOXA1 ) located ∼50 kb from the  Hoxa  gene cluster in mouse embryonic stem cells. Single-cell transcript counting revealed that  linc-HOXA1  and  Hoxa1  RNA are highly variable at the single-cell level and that whenever  linc-HOXA1  RNA abundance was high,  Hoxa1  mRNA abundance was low and vice versa. Knockdown analysis revealed that depletion of  linc-HOXA1  RNA at its site of transcription increased transcription of the  Hoxa1  gene  cis  to the chromosome and that exposure of cells to retinoic acid can disrupt this interaction. We further showed that  linc-HOXA1  RNA represses  Hoxa1  by recruiting the protein PURB as a transcriptional cofactor. Our results highlight the power of transcript visualization to characterize lncRNA function and also suggest that PURB can facilitate lncRNA-mediated transcriptional regulation.

linc-HOXA1 is a noncoding RNA that represses Hoxa1 transcription in cis