Hu proteins regulate alternative splicing by inducing localized histone hyperacetylation in an RNA-dependent manner

Zhou, Hua-Lin; Hinman, Melissa N.; Barron, Victoria A.; Geng, Cuiyu; Zhou, Guangjin; Luo, Guangbin; Siegel, Ruth E.; Lou, Hua

doi:10.1073/pnas.1103344108

Cited by 136RNA Research and SplicingGenomics and Chromatin DynamicsRNA regulation and disease

Hu proteins regulate alternative splicing by inducing localized histone hyperacetylation in an RNA-dependent manner

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Zhou, Hua-Lin, Hinman, Melissa N., Barron, Victoria A., Geng, Cuiyu, Zhou, Guangjin, Luo, Guangbin, Siegel, Ruth E., Lou, Hua·2011·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1103344108PMC PMC3169152

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Abstract

Recent studies have provided strong evidence for a regulatory link among chromatin structure, histone modification, and splicing regulation. However, it is largely unknown how local histone modification patterns surrounding alternative exons are connected to differential alternative splicing outcomes. Here we show that splicing regulator Hu proteins can induce local histone hyperacetylation by association with their target sequences on the pre-mRNA surrounding alternative exons of two different genes. In both primary and mouse embryonic stem cell-derived neurons, histone hyperacetylation leads to an increased local transcriptional elongation rate and decreased inclusion of these exons. Furthermore, we demonstrate that Hu proteins interact with histone deacetylase 2 and inhibit its deacetylation activity. We propose that splicing regulators may actively modulate chromatin structure when recruited to their target RNA sequences cotranscriptionally. This “reaching back” interaction with chromatin provides a means to ensure accurate and efficient regulation of alternative splicing.

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By blocking HDAC2 activity, histones surrounding specific exons remain hyperacetylated, resulting in an increased RNAPII transcription rate and decreased exon inclusion at these genomic loci.
“In vitro transcription elongation assays showed that, by blocking HDAC2 activity, histones surrounding specific exons remained hyperacetylated, which resulted in an increased RNAPII transcription rate and decreased exon inclusion at these genomic loci.”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Zhou et al. 2011
The Discussion (page unavailable) proposes that Hu proteins inhibit HDAC2, sustaining local histone hyperacetylation and increasing RNAPII elongation; the elongation-rate Results report decreased Nf1 exon 23a inclusion with HuC expression. But the claim misidentifies the evidence as in vitro transcription elongation assays: the in vitro assay measured HDAC2 activity, while elongation was measured in cells. The full causal chain is presented as a proposed mechanism, not as the result of one assay. (LLM, conf=0.88)
Experimental — accuracy not yet measured
The linker region and RRM3 are necessary for nELAV regulation of alternative splicing.
“Experiments with HuB and HuC deletion mutants indicated that the linker region and RRM3 are necessary for nELAV regulation of alternative splicing (Zhu et al. 2008; Zhou et al. 2011).”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Zhou et al. 2011
The section ‘Hu Proteins Associate with Transcriptionally Active RNAPII in Neuronal’ reports that deleting RRM3 or the hinge domain reduced HuC’s interaction with RNAPII. It does not establish that these regions are necessary for nELAV regulation of alternative splicing, or report the claimed HuB and HuC deletion-mutant splicing result. No page number was available for the passage. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Hu proteins interact with RNA polymerase II and histone deacetylase 2 (HDAC2) to regulate alternative splicing.
“In addition to binding intronic sequences, co-IP assays revealed that Hu proteins interact with RNA polymerase II and histone deacetylase 2 (HDAC2) to regulate alternative splicing (Zhou et al. 2011).”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Zhou et al. 2011

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Authors: Zhou, H.-L., Hinman, M. N., Barron, V. A., Geng, C., Zhou, G., Luo, G., Siegel, R. E., & Lou, H.
Affiliations: Case Western Reserve University (US)
Case Comprehensive Cancer Center (US)
Department of Pharmacology,
ORCID: Hinman, Melissa N.
Zhou, Guangjin
Luo, Guangbin
Lou, Hua
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2011-08
Volume: 108
Issue: 36
Pages: E627-35
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1103344108
PMC: PMC3169152
OpenAlex: W2107278624
Cited by: 136
References: 67
Citations by year: 2026: 3 · 2025: 4 · 2024: 5 · 2023: 8 · 2022: 5 · 2021: 11 · 2020: 6 · 2019: 5 · 2018: 8 · 2017: 10 · 2016: 5 · 2015: 13 · 2014: 19 · 2013: 20 · 2012: 12
FWCI: 6.89
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Defense
American Heart Association
University of Otago
Universidad de Buenos Aires
National Institutes of Health
National Cancer Institute (CA112094, R01CA112094)
National Institute of General Medical Sciences (T32GM008613)
National Institute of Neurological Disorders and Stroke (R56NS049103, R01NS049103, 5R03NS59648, NS-049103, R03NS059648, F31NS064724)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD00710432, T32HD007104)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
Keywords: HU protein, alternative splicing, histone hyperacetylation, HDAC2, chromatin regulation, splicing regulation, pre-mRNA, alternative exons, transcription elongation, embryonic stem cell-derived neurons
MeSH terms: Acetylation, Animals, Cells, Cultured, Chromatin, Exons, Histones, Neurons, RNA Precursors, Transcription, Genetic, Alternative Splicing, Mice, ELAV Proteins, Histone Deacetylase 2

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Hu proteins regulate alternative splicing by inducing localized histone hyperacetylation in an RNA-dependent manner

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