Journal
GENETICS
Volume 206, Issue 4, Pages 1895-1907Publisher
GENETICS SOCIETY AMERICA
DOI: 10.1534/genetics.117.201632
Keywords
transcriptional memory; GAL genes; gene positioning; epigenetic; RNA polymerase II; chromatin; nuclear pore complex
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Funding
- National Institutes of Health [R01 GM-080484, R01 GM-118712]
- American Heart Association
- Cellular and Molecular Basis of Disease training grant [T32 GM-008061]
- Rappaport Fellowship for Research Excellence
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Previously expressed inducible genes can remain poised for faster reactivation for multiple cell divisions, a conserved phenomenon called epigenetic transcriptional memory. The GAL genes in Saccharomyces cerevisiae show faster reactivation for up to seven generations after being repressed. During memory, previously produced Gal1 protein enhances the rate of reactivation of GAL1, GAL10, GAL2, and GAL7. These genes also interact with the nuclear pore complex (NPC) and localize to the nuclear periphery both when active and during memory. Peripheral localization of GAL1 during memory requires the Gal1 protein, a memory-specific cis-acting element in the promoter, and the NPC protein Nup100. However, unlike other examples of transcriptional memory, the interaction with NPC is not required for faster GAL gene reactivation. Rather, downstream of Gal1, the Tup1 transcription factor and growth in glucose promote GAL transcriptional memory. Cells only show signs of memory and only benefit from memory when growing in glucose. Tup1 promotes memory-specific chromatin changes at the GAL1 promoter: incorporation of histone variant H2A. Z and dimethylation of histone H3, lysine 4. Tup1 and H2A. Z function downstream of Gal1 to promote binding of a preinitiation form of RNA Polymerase II at the GAL1 promoter, poising the gene for faster reactivation. This mechanism allows cells to integrate a previous experience (growth in galactose, reflected by Gal1 levels) with current conditions (growth in glucose, potentially through Tup1 function) to overcome repression and to poise critical GAL genes for future reactivation.
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