Saccharomyces cerevisiae Linker Histone Hho1p Functionally Interacts with Core Histone H4 and Negatively Regulates the Establishment of Transcriptionally Silent Chromatin

Yu, Qun; Kuzmiak, Holly; Zou, Yanfei; Olsen, Lars; Defossez, Pierre‐Antoine; Bi, Xin

doi:10.1074/jbc.m806274200

Cited by 26 publications

(24 citation statements)

References 51 publications

(87 reference statements)

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“…A general role for Hho1p in the formation of DNA loops and for DNA compaction during stationary phase was also reported (62,63). In contrast, Hho1p has also been demonstrated to prevent the establishment of silent chromatin, perhaps by modifying the barriers that separate transcriptionally active chromatin from heterochromatin (57,(63)(64)(65). Thus, both H1 and Hho1p have been implicated in long-range DNA looping and DNA compaction; however, the molecular mechanisms by which these proteins exert such functions are likely to differ.…”

Section: Figmentioning

confidence: 86%

Yeast HMO1: Linker Histone Reinvented

Panday

Grove

2017

Microbiol Mol Biol Rev

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SUMMARY Eukaryotic genomes are packaged in chromatin. The higher-order organization of nucleosome core particles is controlled by the association of the intervening linker DNA with either the linker histone H1 or high mobility group box (HMGB) proteins. While H1 is thought to stabilize the nucleosome by preventing DNA unwrapping, the DNA bending imposed by HMGB may propagate to the nucleosome to destabilize chromatin. For metazoan H1, chromatin compaction requires its lysine-rich C-terminal domain, a domain that is buried between globular domains in the previously characterized yeast Saccharomyces cerevisiae linker histone Hho1p. Here, we discuss the functions of S. cerevisiae HMO1, an HMGB family protein unique in containing a terminal lysine-rich domain and in stabilizing genomic DNA. On ribosomal DNA (rDNA) and genes encoding ribosomal proteins, HMO1 appears to exert its role primarily by stabilizing nucleosome-free regions or “fragile” nucleosomes. During replication, HMO1 likewise appears to ensure low nucleosome density at DNA junctions associated with the DNA damage response or the need for topoisomerases to resolve catenanes. Notably, HMO1 shares with the mammalian linker histone H1 the ability to stabilize chromatin, as evidenced by the absence of HMO1 creating a more dynamic chromatin environment that is more sensitive to nuclease digestion and in which chromatin-remodeling events associated with DNA double-strand break repair occur faster; such chromatin stabilization requires the lysine-rich extension of HMO1. Thus, HMO1 appears to have evolved a unique linker histone-like function involving the ability to stabilize both conventional nucleosome arrays as well as DNA regions characterized by low nucleosome density or the presence of noncanonical nucleosomes.

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Section: Figmentioning

confidence: 86%

Yeast HMO1: Linker Histone Reinvented

Panday

Grove

2017

Microbiol Mol Biol Rev

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“…cerevisiae also has three other types of histones, encoded by single-copy genes. Histone H1, encoded by HHO1, appears to play a limited role in chromatin structure and gene expression (Patterton et al 1998;Levy et al 2008;Schafer et al 2008;Yu et al 2009). An essential centromere-specific variant of histone H3, Cse4 (Meluh et al 1998), plays an essential role in centromere function that will be described in Biggins, planned YeastBook chapter.…”

Section: S Cerevisiae Histone Genesmentioning

confidence: 99%

Chromatin and Transcription in Yeast

2012

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Understanding the mechanisms by which chromatin structure controls eukaryotic transcription has been an intense area of investigation for the past 25 years. Many of the key discoveries that created the foundation for this field came from studies of Saccharomyces cerevisiae, including the discovery of the role of chromatin in transcriptional silencing, as well as the discovery of chromatin-remodeling factors and histone modification activities. Since that time, studies in yeast have continued to contribute in leading ways. This review article summarizes the large body of yeast studies in this field.

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“…It is required for chromatin compaction during stationary phase and for higher-order chromatin organization during vegetative growth, and it represses homologous recombination in the context of DNA double-strand breaks (8,12,46). Hho1 has also been implicated in both transcriptional repression and activation, although the effects of HHO1 deletion on genome-wide transcription are modest (22,35,51,56). Here, we investigated the role of Hho1 during the entire sporulation program, from induction through formation of mature spores and on to early germination.…”

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confidence: 99%

The Linker Histone Plays a Dual Role during Gametogenesis in Saccharomyces cerevisiae

Bryant

Govin

Zhang

et al. 2012

Molecular and Cellular Biology

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fThe differentiation of gametes involves dramatic changes to chromatin, affecting transcription, meiosis, and cell morphology. Sporulation in Saccharomyces cerevisiae shares many chromatin features with spermatogenesis, including a 10-fold compaction of the nucleus. To identify new proteins involved in spore nuclear organization, we purified chromatin from mature spores and discovered a significant enrichment of the linker histone (Hho1). The function of Hho1 has proven to be elusive during vegetative growth, but here we demonstrate its requirement for efficient sporulation and full compaction of the spore genome. Hho1 chromatin immunoprecipitation followed by sequencing (ChIP-seq) revealed increased genome-wide binding in mature spores and provides novel in vivo evidence of the linker histone binding to nucleosomal linker DNA. We also link Hho1 function to the transcription factor Ume6, the master repressor of early meiotic genes. Hho1 and Ume6 are depleted during meiosis, and analysis of published ChIP-chip data obtained during vegetative growth reveals a high binding correlation of both proteins at promoters of early meiotic genes. Moreover, Ume6 promotes binding of Hho1 to meiotic gene promoters. Thus, Hho1 may play a dual role during sporulation: Hho1 and Ume6 depletion facilitates the onset of meiosis via activation of Ume6-repressed early meiotic genes, whereas Hho1 enrichment in mature spores contributes to spore genome compaction. Gametogenesis is a complex, highly regulated differentiation program that is integral to the survival of higher eukaryotes. Mammalian spermatogenesis begins with DNA replication and recombination, ultimately generating four genetically unique haploid cells. The postmeiotic differentiation of spermatozoa involves a complete reorganization of the chromatin and a dramatic compaction of the nucleus that prepare the genome for passage to a new generation (16,30). In fact, specific combinations of histone posttranslational modifications (PTMs) are found at genes encoding important developmental regulators (5,20).Gametogenesis in Saccharomyces cerevisiae, or sporulation, shares several chromatin features with mammalian spermatogenesis, namely, drastic compaction of the nucleus and stage-specific appearance of histone PTMs such as phosphorylation of histone H3 at serine 10 (H3S10ph), H3T11ph, and H4S1ph (17, 31). Sporulation takes place in diploid yeast deprived of nitrogen and a fermentable carbon source (15,39). Under these starvation conditions, yeast cells enter a meiotic program similar to that found in mammalian spermatogenesis. During the postmeiotic phase, cell and nuclear volumes are substantially decreased, the genome is compacted, transcription is silenced, and a protective spore wall is synthesized. The resultant quiescent spore is able to survive unfavorable growth conditions of heat, dehydration, and chemical insult. When a fermentable carbon source is reintroduced, spores are induced to reenter the cell cycle through a process called germination, characterized by a spec...

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Saccharomyces cerevisiae Linker Histone Hho1p Functionally Interacts with Core Histone H4 and Negatively Regulates the Establishment of Transcriptionally Silent Chromatin

Cited by 26 publications

References 51 publications

Yeast HMO1: Linker Histone Reinvented

Yeast HMO1: Linker Histone Reinvented

Chromatin and Transcription in Yeast

The Linker Histone Plays a Dual Role during Gametogenesis in Saccharomyces cerevisiae

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