Decreased Expression of Specific Genes in Yeast Cells Lacking Histone H1

Hellauer, Karen; Sirard, Edith; Turcotte, Bernard

doi:10.1074/jbc.m011196200

Cited by 90 publications

(71 citation statements)

References 39 publications

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“…It was previously reported that Hho1p was not a general transcriptional repressor in exponentially cycling yeast cells (7). However, the reduced binding of Hho1p to chromatin during active growth reported here may have limited the regulatory effect of the linker histone in exponential phase.…”

Section: Histone Hho1p Is Not a General Transcriptional Repressor In contrasting

confidence: 40%

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The Saccharomyces cerevisiae linker histone Hho1p is essential for chromatin compaction in stationary phase and is displaced by transcription

Schäfer

McEvoy

Patterton

2008

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

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The importance of core histones in the regulation of DNA function by chromatin is clear. However, little is known about the role of the linker histone. We investigated the role of H1 in Saccharomyces cerevisiae during extensive transcriptional reprogramming in stationary phase. Although the levels of linker histone Hho1p remained constant during growth to semiquiescence, there was a genome-wide increase in binding to chromatin. Hho1p was essential for compaction of chromatin in stationary phase, but not for general transcriptional repression. A clear, genome-wide anticorrelation was seen between the level of bound Hho1p and gene expression. Surprisingly, the rank order of gene activity was maintained even in the absence of Hho1p. Based on these findings, we suggest that linker histone Hho1p has a limited role in transcriptional regulation and that the dynamically exchanging linker histone may be evicted from chromatin by transcriptional activity.H1 ͉ nucleosome ͉ yeast T he DNA in eukaryotes is packaged into chromatin, which is formed by arrays of a nucleoprotein complex, the nucleosome. The nucleosome is composed of Ϸ168 bp of DNA spooled as two negative superhelical coils onto a central octamer composed of two copies of each of the H2A-H2B and H3-H4 heterodimeric pairs. The repeating association of DNA with the histone octamer in chromatin renders the structure sensitive to the properties of the core histones, which are tailored by reversible chemical modifications, and by isotype permutations in octamer composition. A fifth histone, linker histone H1, binds to the outside of the nucleosome, contacting the nucleosomal DNA at positions close to the center and the ends of the superhelical gyres (1). Although this central binding of the linker histone to the nucleosome suggests an important role in the regulation of DNA function, many lower eukaryotes remain viable in the absence of a linker histone (2, 3). The continuous dynamic exchange of this histone has cast doubt on the canonical organization of the nucleosome, where the linker histone is accepted as a static structural feature (4).The involvement of H1 in the condensation of the chromatin fiber is well established. H1 was shown to be required for the salt-dependent compaction of a nucleosome array into a regular 30-nm chromatin fiber in vitro (5). This compaction of chromatin, which appears to also involve the N-terminal tail of histone H4 (6), was proposed to be due to the steady-state level of the dynamically exchanging H1 molecule.Given the connection between H1 binding and chromatin compaction, which limits unimpeded access to the DNA molecule, H1 was expected to influence global DNA function, and, in particular, gene expression, in a simple, direct manner. Surprisingly, absence of Hho1p in yeast did not result in an increase in basal transcription, as was expected for a global transcriptional repressor (3). Microarray analysis of transcription in a yeast strain in which the HHO1 gene was deleted, revealed that Ͻ1% of genes were affected by a factor of...

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Section: Histone Hho1p Is Not a General Transcriptional Repressor In contrasting

confidence: 40%

“…This suggests that the generally accepted transcriptional regulatory function of H1 may be more subtle in vivo. However, the absence of H1 binding data in these previous studies (7,8) did not allow the investigators to directly relate the association of H1 to gene activity at the level of individual genes.…”

Section: Discussionmentioning

confidence: 98%

The Saccharomyces cerevisiae linker histone Hho1p is essential for chromatin compaction in stationary phase and is displaced by transcription

Schäfer

McEvoy

Patterton

2008

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

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“…Recent attempts to study the functions of linker histones in vivo have used gene inactivation approaches. Elimination of the linker histone-like protein Hho1p in Saccharomyces cerevisiae did not cause any major phenotypic effects, nor were any perturbations in chromosome structure apparent (Ushinsky et al 1997;Patterton et al 1998;Hellauer et al 2001;Downs et al 2003). This finding may be explained by the much lower abundance of Hho1p in yeast (1:37 core particles).…”

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confidence: 40%

Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure

Lu¹,

Wontakal²,

Emelyanov³

et al. 2009

Genes Dev.

131

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We generated mutant alleles of Drosophila melanogaster in which expression of the linker histone H1 can be down-regulated over a wide range by RNAi. When the H1 protein level is reduced to ;20% of the level in wildtype larvae, lethality occurs in the late larval -pupal stages of development. Here we show that H1 has an important function in gene regulation within or near heterochromatin. It is a strong dominant suppressor of position effect variegation (PEV). Similar to other suppressors of PEV, H1 is simultaneously involved in both the repression of euchromatic genes brought to the vicinity of pericentric heterochromatin and the activation of heterochromatic genes that depend on their pericentric localization for maximal transcriptional activity. Studies of H1-depleted salivary gland polytene chromosomes show that H1 participates in several fundamental aspects of chromosome structure and function. First, H1 is required for heterochromatin structural integrity and the deposition or maintenance of major pericentric heterochromatin-associated histone marks, including H3K9Me 2 and H4K20Me 2 . Second, H1 also plays an unexpected role in the alignment of endoreplicated sister chromatids. Finally, H1 is essential for organization of pericentric regions of all polytene chromosomes into a single chromocenter. Thus, linker histone H1 is essential in Drosophila and plays a fundamental role in the architecture and activity of chromosomes in vivo.[Keywords: Linker histone H1; heterochromatin; histone methylation; polytene chromosomes; chromocenter; position effect variegation] Supplemental material is available at http://www.genesdev.org. The genomes of eukaryotes are packaged into a highly compact nucleoprotein complex called chromatin. The histones constitute a family of proteins that are intimately involved in organizing chromatin structure. There are five major classes of histones: the core histones H2A, H2B, H3, and H4, and the linker histones usually referred to as H1. The nucleosome core particle is the highly conserved repetitive unit of chromatin organization. It consists of an octamer of the four core histones around which ;145 base pairs (bp) of DNA are wrapped and protected from nuclease digestion (Van Holde 1988;Wolffe 1998). The linker histone H1 binds to core particles and protects an additional ;20 bp of DNA (linker DNA). In metazoans, the abundance of linker histones, although variable during development, approaches that of core histones (Woodcock et al. 2006), suggesting that they play an important role in establishing and maintaining the structure of the chromatin fiber.Much of our knowledge about the roles of linker histones comes from in vitro studies. These studies indicate that two principal functions of linker histones are to stabilize the DNA entering and exiting the core particle and to facilitate the folding of nucleosome arrays into more compact structures (Ramakrishnan 1997;Wolffe 1997). H1 also affects nucleosome core particle spacing and mobility. In vitro studies also suggest that H1 acts pri...

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“…Several knockout studies across a wide range of organisms revealed that H1 has multiple functions, including participation in the regulation of most nuclear processes (Izzo et al 2008;Happel and Doenecke 2009), mediated at least in some cases by specific H1-protein interactions (McBryant et al 2010). H1 depletion leads to perturbation in the expression of only a subset of genes, with both up-regulation and down-regulation (Shen and Gorovsky 1996;Hellauer et al 2001;Fan et al 2005). This suggests that in vivo, rather than being simply a global repressor, H1 can act as a fine tuner of gene expression.…”

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confidence: 99%

A dual role of linker histone H1.4 Lys 34 acetylation in transcriptional activation

Kamieniarz¹,

Izzo²,

Dundr³

et al. 2012

Genes Dev.

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The linker histone H1 is a key player in chromatin organization, yet our understanding of the regulation of H1 functions by post-translational modifications is very limited. We provide here the first functional characterization of H1 acetylation. We show that H1.4K34 acetylation (H1.4K34ac) is mediated by GCN5 and is preferentially enriched at promoters of active genes, where it stimulates transcription by increasing H1 mobility and recruiting a general transcription factor. H1.4K34ac is dynamic during spermatogenesis and marks undifferentiated cells such as induced pluripotent stem (iPS) cells and testicular germ cell tumors. We propose a model for H1.4K34ac as a novel regulator of chromatin function with a dual role in transcriptional activation.

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Decreased Expression of Specific Genes in Yeast Cells Lacking Histone H1

Cited by 90 publications

References 39 publications

The Saccharomyces cerevisiae linker histone Hho1p is essential for chromatin compaction in stationary phase and is displaced by transcription

The Saccharomyces cerevisiae linker histone Hho1p is essential for chromatin compaction in stationary phase and is displaced by transcription

Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure

A dual role of linker histone H1.4 Lys 34 acetylation in transcriptional activation

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