Abstract
Author SummaryCells respond to changes in nutrients or signaling molecules by altering the expression of genes. The rate at which genes are turned on is not uniform; some genes are induced rapidly and others are induced slowly. In brewer's yeast, previous experience can enhance the rate at which genes are turned on again, a phenomenon called “transcriptional memory.” After repression, such genes physically interact with the nuclear pore complex, leading to altered chromatin structure and binding of a poised RNA polymerase II. Human genes that are induced by interferon gamma show a similar behavior. In both cases, the phenomenon persists through several cell divisions, suggesting that it is epigenetically inherited. Here, we find that yeast and human cells utilize a similar molecular mechanism to prime genes for reactivation. In both species, the nuclear pore protein Nup100/Nup98 binds to the promoters of genes that exhibit transcriptional memory. This leads to an altered chromatin state in the promoter and binding of RNA polymerase II, poising genes for future expression. We conclude that both unicellular and multicellular organisms use nuclear pore proteins in a novel way to alter transcription based on previous experiences.
Highlights
The nuclear pore complex (NPC) is a conserved macromolecular structure that mediates the essential transport of molecules between the nucleus and the cytoplasm [1]
In brewer’s yeast, previous experience can enhance the rate at which genes are turned on again, a phenomenon called ‘‘transcriptional memory.’’ After repression, such genes physically interact with the nuclear pore complex, leading to altered chromatin structure and binding of a poised RNA polymerase II
The nuclear pore protein Nup100/Nup98 binds to the promoters of genes that exhibit transcriptional memory
Summary
The nuclear pore complex (NPC) is a conserved macromolecular structure that mediates the essential transport of molecules between the nucleus and the cytoplasm [1]. Proteins that make up the basketlike structure on the nucleoplasmic face of the NPC and the fibrils on the cytoplasmic face of the NPC play key roles in regulating nuclear transport and mRNP remodeling [4,7]. Nuclear pore proteins physically interact with chromatin to regulate transcription of certain genes. Interaction with the NPC has been proposed to promote stronger transcription [9,12,13,14,15,16], to mediate epigenetic regulation [17,18,19], to promote chromatin boundary activity [20,21], and to provide negative feedback in signaling pathways [22]. The exact biochemical nature of these roles, their generality, and their conservation is unclear
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