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The human  DHRS4  gene cluster consists of  DHRS4  and two immediately downstream homologous genes,  DHRS4L2  and  DHRS4L1 , generated by evolutionarily gene-duplication events. We previously demonstrated that a head-to-head natural antisense transcript (NAT) of  DHRS4 , denoted  DHRS4-AS1 , regulates all three genes of the  DHRS4  gene cluster. However, it is puzzling that  DHRS4L2  and  DHRS4L1  did not evolve their own specific NATs to regulate themselves, as it seems both have retained sequences highly homologous to  DHRS4-AS1 . In a search of the  DHRS4-AS1  region for nearby enhancers, we identified an enhancer located 13.8 kb downstream of the  DHRS4-AS1  transcriptional start site. We further showed, by using a chromosome conformation capture (3C) assay, that this enhancer is capable of physically interacting with the  DHRS4-AS1  promoter through chromosomal looping. The enhancer produced an eRNA, termed AS1eRNA, that enhanced  DHRS4-AS1  transcription by mediating the spatial interactions of the enhancer and  DHRS4-AS1  promoter in cooperation with RNA polymerase II and p300/CBP. Moreover, the distributions of activating acetyl-H3 and H3K4me3 modifications were found to be greater at the  DHRS4-AS1  promoter than at the homologous duplicated regions. We propose that AS1eRNA-driven DNA looping and activating histone modifications promote the expression of  DHRS4-AS1  to economically control the  DHRS4  gene cluster.

Enhancer RNA-driven looping enhances the transcription of the long noncoding RNA DHRS4-AS1, a controller of the DHRS4 gene cluster