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The Groucho co-repressor inhibits progression through the early transcription elongation checkpoint to repress gene expression

The Groucho/Transducin-Like Enhancer of split (Gro/TLE) family proteins act as corepressors for many transcription factors that act in several key pathways during development and cancer. Recent studies have shown that Gro is enriched at a subset of genes that exhibit RNA polymerase II (RNAP II) pausing in Drosophila melanogaster cells and that depletion of Gro can lead to pause release. Here we compare Gro requirement across three cell lines and find that although Gro target sites are largely cell-type specific, Gro is recruited across a similar profile of genomic features. Gro recruitment frequently overlaps that of general factors which promote RNAP II pausing but it does not preclude recruitment of factors that mediate release of paused RNAP II, indicating that Gro restricts the activity of pause release factors rather than their recruitment. Genetic interaction analyses reveal that the association of Gro with factors known to promote RNAP II pausing in Drosophila cell lines reflects a functional relationship in vivo. Knock-down of factors that promote RNAP II pausing enhance gro knock-down phenotypes during wing vein patterning. However, knocking down these factors in the eye concurrently with gro had different effects on patterning (enhancement) and growth (rescue), indicating that the molecular mechanisms underlying Gro function differ in these two processes. Our results identify a mechanism through which developmentally regulated transcription factors can establish RNAP II pausing to modulate transcription.