HIRA, a Conserved Histone Chaperone, Plays an Essential Role in Low-dose Stress Response via Transcriptional Stimulation in Fission Yeast

Chujo, Moeko; Tarumoto, Yusuke; Miyatake, Koichi; Nishida, Eisuke; Ishikawa, Fuyuki

doi:10.1074/jbc.m112.349944

Cited by 15 publications

(12 citation statements)

References 62 publications

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“…Considering the genome-wide effect of HIRA on transcription regulation post UVC, it is tempting to speculate that HIRA may also stimulate transcription induction of early UV-responsive genes. Lending support to this idea, the ortholog of HIRA in fission yeast is required for the induction of stress-responsive genes 90 . Future studies will address whether this function of HIRA is conserved in higher eukaryotes.…”

Section: Genome-wide Impact Of Hira On Transcription Restart Post Uvmentioning

confidence: 95%

Dissecting regulatory pathways for transcription recovery following DNA damage reveals a non-canonical function of the histone chaperone HIRA

Bouvier

Chevallier

et al. 2020

Preprint

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Transcription restart after a genotoxic challenge is a fundamental yet poorly understood process. Here, we dissect the interplay between transcription and chromatin restoration after DNA damage by focusing on the human histone chaperone complex HIRA, which is required for transcription recovery post UV. We demonstrate that HIRA is recruited to UV-damaged chromatin via the ubiquitin-dependent segregase VCP to deposit new H3.3 histones. However, this local activity of HIRA is dispensable for transcription recovery. Instead, we reveal a genome-wide function of HIRA in transcription restart that is independent of new H3.3 and not restricted to UV-damaged loci. HIRA coordinates with ASF1B to control transcription restart by two independent pathways: by stabilizing the associated subunit UBN2 and by reducing the expression of the transcription repressor ATF3. Thus, HIRA primes UV-damaged chromatin for transcription restart at least in part by relieving transcription inhibition rather than by depositing new H3.3 as an activating bookmark.

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Section: Genome-wide Impact Of Hira On Transcription Restart Post Uvmentioning

confidence: 95%

Dissecting regulatory pathways for transcription recovery following DNA damage reveals a non-canonical function of the histone chaperone HIRA

Bouvier

Chevallier

et al. 2020

Preprint

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“…In yeast, HIRA histone chaperone has been shown to be involved in transcriptional stimulation in response to osmotic and oxidative stresses (Chujo et al, 2012). Previous studies, including ours (Zhu et al, 2013;Tripathi et al, 2015), have suggested that expression of a few plant histone chaperones is perturbed during biotic and abiotic stress conditions.…”

Section: Discussionmentioning

confidence: 91%

“…Taking clues from some previous studies that have shown genome-wide transcriptional changes attributed to the nucleosome assembly/disassembly activity of histone chaperones (Zhu et al, 2006;Chujo et al, 2012), we hypothesized that manipulating the expression of OsNAPL6 may alter the expression of several genes, many of which might be associated with abiotic stress response. Consistent to our hypothesis, we observed large-scale changes in the rice transcriptome when the expression of OsNAPL6 was manipulated by overexpression or knockdown (Fig.…”

Section: Discussionmentioning

confidence: 99%

A NAP-Family Histone Chaperone Functions in Abiotic Stress Response and Adaptation

2016

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Modulation of gene expression is one of the most significant molecular mechanisms of abiotic stress response in plants. Via altering DNA accessibility, histone chaperones affect the transcriptional competence of genomic loci. However, in contrast to other factors affecting chromatin dynamics, the role of plant histone chaperones in abiotic stress response and adaptation remains elusive. Here, we studied the physiological function of a stress-responsive putative rice (Oryza sativa) histone chaperone of the NAP superfamily: OsNAPL6. We show that OsNAPL6 is a nuclear-localized H3/H4 histone chaperone capable of assembling a nucleosome-like structure. Utilizing overexpression and knockdown approaches, we found a positive correlation between OsNAPL6 expression levels and adaptation to multiple abiotic stresses. Results of comparative transcriptome profiling and promoter-recruitment studies indicate that OsNAPL6 functions during stress response via modulation of expression of various genes involved in diverse functions. For instance, we show that OsNAPL6 is recruited to OsRad51 promoter, activating its expression and leading to more efficient DNA repair and abrogation of programmed cell death under salinity and genotoxic stress conditions. These results suggest that the histone chaperone OsNAPL6 may serve a regulatory role in abiotic stress physiology possibly via modulating nucleosome dynamics at various stress-associated genomic loci. Taken together, our findings establish a hitherto unknown link between histone chaperones and abiotic stress response in plants.

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“…ChIP-seq density profiles followed by co-immunoprecipitation show that multiple subunits of the HUCA complex bind to both the initiating and elongating forms of RNAPII [74]. The importance of the interaction between HUCA and RNAPII is underscored by the fact that in yeast cells depleted of HIRA, RNAPII recruitment is impaired [75]. HIRA binds to both subunits of DSIF [76] which travels throughout the coding region along with RNAPII [77].…”

Section: Interactions Between Huca the 26s Proteasome And Rnapiimentioning

confidence: 99%

A Role for Histone Chaperones in Regulating RNA Polymerase II

Osborn¹,

Greer²

2015

ABC

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Transcription is a highly regulated cellular process in which dysfunction leads to disease. One level of regulation is chromatin structure which protects promoters from transcription factor binding. To circumvent this blockade, histone chaperones aid in displacement of nucleosomes. In particular, the histone chaperone complex HUCA, consisting of Hira, Ubn1, Cabin1, and ASF1a, replaces histone variant H3.1 with H3.3 in front of actively transcribing RNA Polymerase II (RNAPII). The 26S proteasome is a major degrader of proteins within the cell and plays both proteolytic and nonproteolytic roles in transcriptional regulation. One major role is the degradation of irreversibly arrested RNAPII. Several interactions between HUCA, the 26S proteasome, and RNAPII have been characterized individually; we now present observations from our lab and others which directly associate elongating RNAPII with the degradation machinery through observations of involvement with the HUCA complex. Our short report presents these ideas and discusses their importance in transcriptional regulation as well as implications in disease manifestation.

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HIRA, a Conserved Histone Chaperone, Plays an Essential Role in Low-dose Stress Response via Transcriptional Stimulation in Fission Yeast

Cited by 15 publications

References 62 publications

Dissecting regulatory pathways for transcription recovery following DNA damage reveals a non-canonical function of the histone chaperone HIRA

Dissecting regulatory pathways for transcription recovery following DNA damage reveals a non-canonical function of the histone chaperone HIRA

A NAP-Family Histone Chaperone Functions in Abiotic Stress Response and Adaptation

A Role for Histone Chaperones in Regulating RNA Polymerase II

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