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Insulators can block the action of enhancers on promoters and the spreading of repressive chromatin, as well as facilitating specific enhancer-promoter interactions. However, recent studies have called into question whether the activities ascribed to insulators in model transgene assays actually reflect their functions in the genome. The Drosophila  even skipped  ( eve ) gene is a Polycomb (Pc) domain with a Pc-group response element (PRE) at one end, flanked by an insulator, an arrangement also seen in other genes. Here, we show that this insulator has three major functions. It blocks the spreading of the  eve  Pc domain, preventing repression of the adjacent gene,  TER94 . It prevents activation of  TER94  by  eve  regulatory DNA. It also facilitates normal  eve  expression. When Homie is deleted in the context of a large transgene that mimics both  eve  and  TER94  regulation,  TER94  is repressed. This repression depends on the  eve  PRE. Ubiquitous  TER94  expression is “replaced” by expression in an  eve  pattern when Homie is deleted, and this effect is reversed when the PRE is also removed. Repression of  TER94  is attributable to spreading of the  eve  Pc domain into the  TER94  locus, accompanied by an increase in histone H3 trimethylation at lysine 27. Other PREs can functionally replace the  eve  PRE, and other insulators can block PRE-dependent repression in this context. The full activity of the  eve  promoter is also dependent on Homie, and other insulators can promote normal  eve  enhancer-promoter communication. Our data suggest that this is not due to preventing promoter competition, but is likely the result of the insulator organizing a chromosomal conformation favorable to normal enhancer-promoter interactions. Thus, insulator activities in a native context include enhancer blocking and enhancer-promoter facilitation, as well as preventing the spread of repressive chromatin.

The Drosophila eve Insulator Homie Promotes eve Expression and Protects the Adjacent Gene from Repression by Polycomb Spreading