The histone deacetylase (HDAC) Rpd3 antagonizes heterochromatin formation at telomeres in Saccharomyces cerevisiae
In Saccharomyces cerevisiae, spreading of the telomeric SIR heterochromatin complexes into
centromere-proximal euchromatic regions is prevented by the activity of boundary elements.
So far, these boundaries have been associated with chromatin opening activities, like histone
acetyltransferases (HATs) or histone methyltransferases. Here, we show that the opposite
enzymatic activity, the histone deacetylase (HDAC) Rpd3, was necessary to prevent the
encroachment of heterochromatin into euchromatin at telomeres in S. cerevisiae.
We found by ChIP analysis that in the absence of Rpd3, the SIR complexes were
mislocalized to more centromere-proximal regions, showing that Rpd3 was necessary to
restrict SIR complexes to the telomere. Furthermore, quantitative RT-PCR showed that SIR
proteins repressed subtelomeric genes in rpd3Δ cells, suggesting a role for Rpd3 in the
restriction of telomeric heterochromatin. When combined with the absence of the known
boundary factor, the HAT SAS-I, rpd3Δ caused inappropriate SIR spreading that was lethal to
yeast cells. Significantly, the lethality between sas2Δ rpd3Δ was suppressed by sir deletions,
suggesting parallel functions for the two enzymes in restricting SIR proteins to
heterochromatin despite their opposing enzymatic activity. In addition, Rpd3 was capable of
creating a boundary when targeted to the heterochromatic loci, indicating a boundary function
for Rpd3. Further analysis showed that Rpd3 in essence functioned by removing acetyl
groups, such that they were no longer available for NAD+-dependent deacetylation via Sir2.
This further suggested that prevention of O-acetyl-ADP-ribose (OAADPR) production during
deacetylation by Sir2 in effect prevented SIR propagation. This hypothesis was strengthened
by the notion that inhibition of OAADPR binding to Sir3 created a halt to SIR spreading. In
further experiments, we found that Rpd3 interacted in vivo with Cac1, the largest subunit of
the chromatin assembly complex CAF-I, suggesting that it deacetylated cytoplasmic histone
acetylation marks in a replication-coupled fashion. Thus, Rpd3 likely performed its function
in SIR restriction through a transient contact to chromatin, rather than being permanently
located at subtelomeric regions.
In summary, our data indicated that Rpd3 effectively removed acetyl groups in
subtelomeric regions and therefore deprived Sir2 of its ability to perform the deacetylation
reaction and in doing so to produce OAADPR. This in essence prevented SIR propagation
and created a boundary against heterochromatin spreading.
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