Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae

Xie, Junhua; Pierce, Michael; Gailus‐Durner, Valérie; Wagner, Marisa; Winter, Edward; Vershon, Andrew K.

doi:10.1093/emboj/18.22.6448

Cited by 192 publications

(306 citation statements)

References 27 publications

(58 reference statements)

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“…These proteins are involved in specific functions and in some cases seem to partially overlap with Sir2 silencing from a genetic point of view. Hst1 is involved in the specific repression of mid-sporulation genes, expressed during the middle period of the sequential program of sporulation (Xie et al, 1999). Hst1 is the most closely related by sequence to Sir2 and its overexpression can suppress some of the silencing defects produced by mutation of SIR2 (Xie et al, 1999).…”

Section: Class III Functionsmentioning

confidence: 99%

“…Hst1 is involved in the specific repression of mid-sporulation genes, expressed during the middle period of the sequential program of sporulation (Xie et al, 1999). Hst1 is the most closely related by sequence to Sir2 and its overexpression can suppress some of the silencing defects produced by mutation of SIR2 (Xie et al, 1999). Hst2 is localized in the cytoplasm (Perrod et al, 2001), although an interesting recent report shows it is actively exported from the nucleus, suggesting it may have a nuclear role (Wilson et al, 2006).…”

Section: Class III Functionsmentioning

confidence: 99%

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NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs

2007

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Histone deacetylases (HDACs) catalyse the removal of acetyl groups from the N-terminal tails of histones. All known HDACs can be categorized into one of four classes (I-IV). The class III HDAC or silencing information regulator 2 (Sir2) family exhibits characteristics consistent with a distinctive role in regulation of chromatin structure. Accumulating data suggest that these deacetylases acquired new roles as genomic complexity increased, including deacetylation of non-histone proteins and functional diversification in mammals. However, the intrinsic regulation of chromatin structure in species as diverse as yeast and humans, underscores the pressure to conserve core functions of class III HDACs, which are also known as Sirtuins. One of the key factors that might have contributed to this preservation is the intimate relationship between some members of this group of proteins (SirT1, SirT2 and SirT3) and deacetylation of a specific residue in histone H4, lysine 16 (H4K16). Evidence accumulated over the years has uncovered a unique role for H4K16 in chromatin structure throughout eukaryotes. Here, we review the recent findings about the functional relationship between H4K16 and the Sir2 class of deacetylases and how that relationship might impact aging and diseases including cancer and diabetes.

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Section: Class III Functionsmentioning

confidence: 99%

Section: Class III Functionsmentioning

confidence: 99%

NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs

2007

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“…Some MSGs, however, including NDT80 itself, have a second layer of control to ensure they are not expressed inappropriately. Genes in this subset of MSGs have MSEs that are recognized by Ndt80 during meiosis, but are also bound by the transcriptional repressor Sum1 during mitosis and early meiosis (18,19,33). Sum1 is transiently destabilized during meiosis, and Sum1 repression is removed during late prophase (13).…”

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confidence: 99%

Arg-Pro-X-Ser/Thr Is a Consensus Phosphoacceptor Sequence for the Meiosis-Specific Ime2 Protein Kinase in Saccharomyces cerevisiae

et al. 2006

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Ime2 is a meiosis-specific protein kinase in Saccharomyces cerevisiae that is functionally related to cyclin-dependent kinase. Although Ime2 regulates multiple steps in meiosis, only a few of its substrates have been identified. Here we show that Ime2 phosphorylates Sum1, a repressor of meiotic gene transcription, on Thr-306. Ime2 protein kinase assays on Sum1 mutants and synthetic peptides define a consensus motif Arg-Pro-X-Ser/Thr that is required for efficient phosphorylation by Ime2. The carboxyl residue adjacent to the phosphoacceptor (+1 position) also influences the efficiency of Ime2 phosphorylation with alanine being a preferred residue. This information has predictive value in identifying new potential Ime2 targets as shown by the ability of Ime2 to phosphorylate Sgs1 and Gip1 in vitro, and could be important in differentiating mitotic and meiotic regulatory pathways. Keywordsyeast; meiosis; protein kinase; Ime2; Sum1; consensus phosphorylation site Meiosis is a specialized form of cell division that produces the haploid cells required for sexual reproduction. It is characterized by DNA replication, high levels of genetic recombination, and two sequential rounds of chromosome segregation. These processes require the choreographed expression of meiosis-specific genes in a transcriptional cascade (11,31). In the budding yeast Saccharomyces cerevisiae, meiosis is induced by nutrient depletion and is coupled to spore formation. Starvation for key nutrients induces expression of the early gene transcriptional activator Ime1 (12). One of the genes activated by Ime1 encodes Ime2, a serine/threonine kinase that is functionally related to the Cdc28 cyclin-dependent kinase (CDK) and which shows similarity to the CMGC-group of protein kinases (10). Ime2 is required for critical events in meiosis, including the replication of DNA, the regulation of meiotic gene expression, and the meiotic divisions. † This work was supported by grants from the National Institutes of Health to Andrew Vershon (GM 58762) and Edward Winter GM (GM061817).*>To whom correspondence should be addressed: 233 South 10th St., Philadelphia, PA 19107. Phone:(215) 923-9162. E-mail: edward.winter@jefferson.edu.. Π These authors contributed equally to this work. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptThe role that Ime2 plays in regulating meiotic S phase is related to that of Cdc28 in triggering Sphase in mitosis. In both mitosis and meiosis the G 1 -S transition is prohibited by the Clb5,6/ Cdc28 inhibitor Sic1 (24). Entry into S phase is delayed until Sic1 is phosphorylated, a reaction catalyzed in mitosis by Cdc28 in complex with the G 1 -phase cyclins Cln1 and Cln2 (15,30). In meiosis, Ime2 is required for Sic1 degradation and DNA replication (7). Others have recently demonstrated that Ime2 directly phosphorylates multiple sites in Sic1 in vitro. This is insufficient to trigger meiotic Sic1 destruction, however, suggesting that Ime2 does not simply replace the function of Cln1,2-/Cdc28 in meiosis to ...

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“…The Ume6͞Ime1 complex also indirectly controls the transition from early to middle gene expression through its participation in the induction of Ndt80, a transcription factor that activates middle genes once recombination is completed (monitored by the pachytene checkpoint system; refs. [25][26][27][28]. The observation from recent microarray analysis that URS1 occurs in the promoters of some of these genes (12,13) suggests that Ume6 may also more directly regulate a subset of middle͞late expression.…”

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confidence: 99%

The Ume6 regulon coordinates metabolic and meiotic gene expression in yeast

Williams

Primig

Washburn

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

111

121

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The Ume6 transcription factor in yeast is known to both repress and activate expression of diverse genes during growth and meiotic development. To obtain a more complete profile of the functions regulated by this protein, microarray analysis was used to examine transcription in wild-type and ume6⌬ diploids during vegetative growth in glucose and acetate. Two different genetic backgrounds (W303 and SK1) were examined to identify a core set of strain-independent Ume6-regulated genes. Among genes whose expression is controlled by Ume6 in both backgrounds, 82 contain homologies to the Ume6-binding site (URS1) and are expected to be directly regulated by Ume6. The vast majority of those whose functions are known participate in carbon͞nitrogen metabolism and͞or meiosis. Approximately half of the Ume6 direct targets are induced during meiosis, with most falling into the early meiotic expression class (cluster 4), and a smaller subset in the middle and later classes (clusters 5-7). Based on these data, we propose that Ume6 serves a unique role in diploid cells, coupling metabolic responses to nutritional cues with the initiation and progression of meiosis. Finally, expression patterns in the two genetic backgrounds suggest that SK1 is better adapted to respiration and W303 to fermentation, which may in part account for the more efficient and synchronous sporulation of SK1.

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Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae

Cited by 192 publications

References 27 publications

NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs

NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs

Arg-Pro-X-Ser/Thr Is a Consensus Phosphoacceptor Sequence for the Meiosis-Specific Ime2 Protein Kinase in Saccharomyces cerevisiae

The Ume6 regulon coordinates metabolic and meiotic gene expression in yeast

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