Widespread disruption of host transcription termination in HSV-1 infection

Rutkowski, Andrzej J.; Erhard, Florian; L’Hernault, Anne; Bonfert, Thomas; Schilhabel, Markus; Crump, Colin; Rosenstiel, Philip; Efstathiou, Stacey; Zimmer, Ralf; Friedel, Caroline C.; Dölken, Lars

doi:10.1038/ncomms8126

Cited by 275Herpesvirus Infections and TreatmentsRNA Research and SplicingGenomics and Chromatin Dynamics

Widespread disruption of host transcription termination in HSV-1 infection

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Rutkowski, Andrzej J., Erhard, Florian, L’Hernault, Anne, Bonfert, Thomas, Schilhabel, Markus, Crump, Colin, Rosenstiel, Philip, Efstathiou, Stacey +3 more·2015·Nature Communications

DOI 10.1038/ncomms8126PMC PMC4441252

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Abstract

Herpes simplex virus 1 (HSV-1) is an important human pathogen and a paradigm for virus-induced host shut-off. Here we show that global changes in transcription and RNA processing and their impact on translation can be analysed in a single experimental setting by applying 4sU-tagging of newly transcribed RNA and ribosome profiling to lytic HSV-1 infection. Unexpectedly, we find that HSV-1 triggers the disruption of transcription termination of cellular, but not viral, genes. This results in extensive transcription for tens of thousands of nucleotides beyond poly(A) sites and into downstream genes, leading to novel intergenic splicing between exons of neighbouring cellular genes. As a consequence, hundreds of cellular genes seem to be transcriptionally induced but are not translated. In contrast to previous reports, we show that HSV-1 does not inhibit co-transcriptional splicing. Our approach thus substantially advances our understanding of HSV-1 biology and establishes HSV-1 as a model system for studying transcription termination.

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Transcriptional read-through is induced downstream of thousands of genes in response to different kinds of stresses.
“Moreover, transcriptional read‐through is induced downstream of thousands of genes in response to different kinds of stresses (Rutkowski et al, 2015; Vilborg et al, 2015; Vilborg et al, 2017; Cardiello et al, 2018; Hennig et al, 2018) and has been proposed to play an important role in the stress response by reinforcing the nuclear scaffold integrity after nuclear stress (Vilborg et al, 2015).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Rutkowski et al, 2015
The Results section (‘HSV-1 disrupts transcription termination’; page not provided) reports read-through downstream of thousands of cellular genes during HSV-1 infection: 64% of 9,690 genes had read-out exceeding 15% of the gene’s RPKM. This supports the infection example, but this paper does not establish the claim for different kinds of stresses. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Increased transcriptional read-through is known to interfere with the expression of downstream genes in other contexts such as cancer or HSV-1 infection in human cells, as well as cold acclimation in plants.
“Increased transcriptional read‐through is known to interfere with the expression of downstream genes also in other contexts such as cancer or HSV‐1 infection in human cells (Grosso et al, 2015; Rutkowski et al, 2015; Hennig et al, 2018), as well as cold acclimation in plants (Kindgren et al, 2018).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Rutkowski et al, 2015

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“…transcriptional read-through is known to interfere with the expression of downstream genes also in other contexts such as cancer or HSV-1 infection in human cells (Grosso et al , 2015; Rutkowski et al , 2015; Hennig et al , 2018), as well as cold acclimation in plants (Kindgren et al , 2018).”
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ATRX limits the accessibility of histone H3-occupied HSV genomes during lytic infection
Cabral, J. M., Cushman, C. H., Sodroski, C. N., & Knipe, D. M. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009567 · Cited by 27 · see citing works

Dissecting Herpes Simplex Virus 1-Induced Host Shutoff at the RNA Level
Friedel, C. C., Whisnant, A. W., Djaković, L., Rutkowski, A. J., Friedl, M.-S., Kluge, M., Williamson, J. C., Sai, S., Vidal, R. O., Sauer, S., et al. (2020) · Journal of Virology · doi:10.1128/jvi.01399-20 · Cited by 51 · see citing works
Self-citation
Nuclear-cytoplasmic compartmentalization of the herpes simplex virus 1 infected cell transcriptome is co-ordinated by the viral endoribonuclease vhs and cofactors to facilitate the translation of late proteins
Pheasant, K., Möller‐Levet, C. S., Jones, J., Depledge, D. P., Breuer, J., & Elliott, G. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007331 · Cited by 37 · see citing works
A Review of the Multipronged Attack of Herpes Simplex Virus 1 on the Host Transcriptional Machinery
Hennig, T., Djaković, L., Dölken, L., & Whisnant, A. W. (2021) · Viruses · doi:10.3390/v13091836 · Cited by 21 · see citing works
Self-citation
HSV-1-induced disruption of transcription termination resembles a cellular stress response but selectively increases chromatin accessibility downstream of genes
Hennig, T., Michalski, M., Rutkowski, A. J., Djakovic, L., Whisnant, A. W., Friedl, M.-S., Jha, B. A., Baptista, M. A. P., L’Hernault, A., Erhard, F., et al. (2018) · PLOS Pathogens · doi:10.1371/journal.ppat.1006954 · Cited by 95 · see citing works
Self-citation
Herpes Simplex Virus 1 Dramatically Alters Loading and Positioning of RNA Polymerase II on Host Genes Early in Infection
Birkenheuer, C. H., Danko, C. G., & Baines, J. D. (2018) · Journal of Virology · doi:10.1128/jvi.02184-17 · Cited by 62 · see citing works

Authors: Rutkowski, A. J., Erhard, F., L’Hernault, A., Bonfert, T., Schilhabel, M., Crump, C., Rosenstiel, P., Efstathiou, S., Zimmer, R., Friedel, C. C., & Dölken, L.
Affiliations: University of Cambridge (GB)
Ludwig-Maximilians-Universität München (DE)
Christian-Albrechts-Universität zu Kiel (DE)
Corresponding author: Friedel, Caroline C.
Dölken, Lars
ORCID: Erhard, Florian
Crump, Colin
Rosenstiel, Philip
Zimmer, Ralf
Friedel, Caroline C.
Dölken, Lars
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2015-05-20
Volume: 6
Issue: 1
Pages: 7126-7126
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/ncomms8126
PMC: PMC4441252
OpenAlex: W1519422934
Cited by: 275
References: 63
Citations by year: 2026: 14 · 2025: 21 · 2024: 23 · 2023: 26 · 2022: 29 · 2021: 37 · 2020: 35 · 2019: 20 · 2018: 28 · 2017: 14 · 2016: 23 · 2015: 3 · 2014: 1 · 2013: 1
FWCI: 19.34
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion)
Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by)
Apollo (University of Cambridge) (submittedVersion, cc-by)
Funders: NHS Blood and Transplant (WP11-05)
Deutsche Forschungsgemeinschaft (FR2938/1-2)
Medical Research Council (G1002523, MR/J002232/1)
Dalian Institute of Chemical Physics
Topics: Health Sciences › Medicine › Epidemiology › Herpesvirus Infections and Treatments
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
Keywords: herpes simplex virus type 1, transcription termination, ribosome profiling, RNA processing, co-transcriptional splicing, poly(A) site, viral infection, host-virus interaction, translation (biology)
MeSH terms: Culture Media, Exons, Fibroblasts, Genes, Viral, Herpes Simplex, Humans, Introns, Poly A, Ribosomes, RNA, RNA, Messenger, Time Factors, Transcription, Genetic, Protein Biosynthesis, Virus Replication, Gene Expression Regulation, Viral, Open Reading Frames, Genome, Viral, Alternative Splicing, Herpesvirus 1, Human, Codon, Terminator

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Widespread disruption of host transcription termination in HSV-1 infection

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