Viral Ubiquitin Ligase Stimulates Selective Host MicroRNA Expression by Targeting ZEB Transcriptional Repressors

Infection with herpes simplex virus-1 (HSV-1) brings numerous changes in cellular gene expression. Levels of most host mRNAs are reduced, limiting synthesis of host proteins, especially those involved in antiviral defenses. The impact of HSV-1 on host microRNAs (miRNAs), an extensive network of shor...

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Published inViruses Vol. 9; no. 8; p. 210
Main Authors Lutz, Gabriel, Jurak, Igor, Kim, Eui Tae, Kim, Ju Youn, Hackenberg, Michael, Leader, Andrew, Stoller, Michelle L., Fekete, Donna M., Weitzman, Matthew D., Coen, Donald M., Wilson, Angus C.
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 07.08.2017
MDPI
Subjects
Cell Nucleus
Cells, Cultured
Crystallin
E3 ubiquitin ligase
Fibroblasts
Fibroblasts - virology
Gene expression
Gene Expression Regulation
Herpes simplex
herpes simplex virus
Herpesvirus 1, Human - enzymology
Herpesvirus 1, Human - genetics
Homeobox
host shutoff
Host-Pathogen Interactions
HSV-1
Humans
ICP0
Immediate-Early Proteins - deficiency
Immediate-Early Proteins - genetics
Kinases
microRNA
MicroRNAs - genetics
miR-182
miR-183
miR-96
miRNA
mRNA stability
Nerve Tissue Proteins - genetics
Neurons - virology
Non-coding RNA
Protein Binding
Proteolysis
Repressors
RNA-Binding Proteins - genetics
Smad protein
Transcription factors
Ubiquitin
Ubiquitin-protein ligase
Ubiquitin-Protein Ligases - deficiency
Ubiquitin-Protein Ligases - genetics
Ubiquitin-Protein Ligases - metabolism
Virus Replication
ZEB
Zinc Finger E-box-Binding Homeobox 1 - genetics
Zinc Finger E-box-Binding Homeobox 1 - metabolism
Zinc finger proteins
herpes simplex virus
HSV-1
host shutoff
ZEB
ICP0
miR-182
miR-183
miR-96
microRNA
E3 ubiquitin ligase
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Abstract Infection with herpes simplex virus-1 (HSV-1) brings numerous changes in cellular gene expression. Levels of most host mRNAs are reduced, limiting synthesis of host proteins, especially those involved in antiviral defenses. The impact of HSV-1 on host microRNAs (miRNAs), an extensive network of short non-coding RNAs that regulate mRNA stability/translation, remains largely unexplored. Here we show that transcription of the miR-183 cluster (miR-183, miR-96, and miR-182) is selectively induced by HSV-1 during productive infection of primary fibroblasts and neurons. ICP0, a viral E3 ubiquitin ligase expressed as an immediate-early protein, is both necessary and sufficient for this induction. Nuclear exclusion of ICP0 or removal of the RING (really interesting new gene) finger domain that is required for E3 ligase activity prevents induction. ICP0 promotes the degradation of numerous host proteins and for the most part, the downstream consequences are unknown. Induction of the miR-183 cluster can be mimicked by depletion of host transcriptional repressors zinc finger E-box binding homeobox 1 (ZEB1)/-crystallin enhancer binding factor 1 (δEF1) and zinc finger E-box binding homeobox 2 (ZEB2)/Smad-interacting protein 1 (SIP1), which we establish as new substrates for ICP0-mediated degradation. Thus, HSV-1 selectively stimulates expression of the miR-183 cluster by ICP0-mediated degradation of ZEB transcriptional repressors.
AbstractList Infection with herpes simplex virus-1 (HSV-1) brings numerous changes in cellular gene expression. Levels of most host mRNAs are reduced, limiting synthesis of host proteins, especially those involved in antiviral defenses. The impact of HSV-1 on host microRNAs (miRNAs), an extensive network of short non-coding RNAs that regulate mRNA stability/translation, remains largely unexplored. Here we show that transcription of the miR-183 cluster (miR-183, miR-96, and miR-182) is selectively induced by HSV-1 during productive infection of primary fibroblasts and neurons. ICP0, a viral E3 ubiquitin ligase expressed as an immediate-early protein, is both necessary and sufficient for this induction. Nuclear exclusion of ICP0 or removal of the RING (really interesting new gene) finger domain that is required for E3 ligase activity prevents induction. ICP0 promotes the degradation of numerous host proteins and for the most part, the downstream consequences are unknown. Induction of the miR-183 cluster can be mimicked by depletion of host transcriptional repressors zinc finger E-box binding homeobox 1 (ZEB1)/δ-crystallin enhancer binding factor 1 (δEF1) and zinc finger E-box binding homeobox 2 (ZEB2)/Smad-interacting protein 1 (SIP1), which we establish as new substrates for ICP0-mediated degradation. Thus, HSV-1 selectively stimulates expression of the miR-183 cluster by ICP0-mediated degradation of ZEB transcriptional repressors.
Infection with herpes simplex virus-1 (HSV-1) brings numerous changes in cellular gene expression. Levels of most host mRNAs are reduced, limiting synthesis of host proteins, especially those involved in antiviral defenses. The impact of HSV-1 on host microRNAs (miRNAs), an extensive network of short non-coding RNAs that regulate mRNA stability/translation, remains largely unexplored. Here we show that transcription of the miR-183 cluster (miR-183, miR-96, and miR-182) is selectively induced by HSV-1 during productive infection of primary fibroblasts and neurons. ICP0, a viral E3 ubiquitin ligase expressed as an immediate-early protein, is both necessary and sufficient for this induction. Nuclear exclusion of ICP0 or removal of the RING (really interesting new gene) finger domain that is required for E3 ligase activity prevents induction. ICP0 promotes the degradation of numerous host proteins and for the most part, the downstream consequences are unknown. Induction of the miR-183 cluster can be mimicked by depletion of host transcriptional repressors zinc finger E-box binding homeobox 1 (ZEB1)/-crystallin enhancer binding factor 1 (δEF1) and zinc finger E-box binding homeobox 2 (ZEB2)/Smad-interacting protein 1 (SIP1), which we establish as new substrates for ICP0-mediated degradation. Thus, HSV-1 selectively stimulates expression of the miR-183 cluster by ICP0-mediated degradation of ZEB transcriptional repressors.
Infection with herpes simplex virus-1 (HSV-1) brings numerous changes in cellular gene expression. Levels of most host mRNAs are reduced, limiting synthesis of host proteins, especially those involved in antiviral defenses. The impact of HSV-1 on host microRNAs (miRNAs), an extensive network of short non-coding RNAs that regulate mRNA stability/translation, remains largely unexplored. Here we show that transcription of the miR-183 cluster (miR-183, miR-96, and miR-182) is selectively induced by HSV-1 during productive infection of primary fibroblasts and neurons. ICP0, a viral E3 ubiquitin ligase expressed as an immediate-early protein, is both necessary and sufficient for this induction. Nuclear exclusion of ICP0 or removal of the RING (really interesting new gene) finger domain that is required for E3 ligase activity prevents induction. ICP0 promotes the degradation of numerous host proteins and for the most part, the downstream consequences are unknown. Induction of the miR-183 cluster can be mimicked by depletion of host transcriptional repressors zinc finger E-box binding homeobox 1 (ZEB1)/-crystallin enhancer binding factor 1 (δEF1) and zinc finger E-box binding homeobox 2 (ZEB2)/Smad-interacting protein 1 (SIP1), which we establish as new substrates for ICP0-mediated degradation. Thus, HSV-1 selectively stimulates expression of the miR-183 cluster by ICP0-mediated degradation of ZEB transcriptional repressors.Infection with herpes simplex virus-1 (HSV-1) brings numerous changes in cellular gene expression. Levels of most host mRNAs are reduced, limiting synthesis of host proteins, especially those involved in antiviral defenses. The impact of HSV-1 on host microRNAs (miRNAs), an extensive network of short non-coding RNAs that regulate mRNA stability/translation, remains largely unexplored. Here we show that transcription of the miR-183 cluster (miR-183, miR-96, and miR-182) is selectively induced by HSV-1 during productive infection of primary fibroblasts and neurons. ICP0, a viral E3 ubiquitin ligase expressed as an immediate-early protein, is both necessary and sufficient for this induction. Nuclear exclusion of ICP0 or removal of the RING (really interesting new gene) finger domain that is required for E3 ligase activity prevents induction. ICP0 promotes the degradation of numerous host proteins and for the most part, the downstream consequences are unknown. Induction of the miR-183 cluster can be mimicked by depletion of host transcriptional repressors zinc finger E-box binding homeobox 1 (ZEB1)/-crystallin enhancer binding factor 1 (δEF1) and zinc finger E-box binding homeobox 2 (ZEB2)/Smad-interacting protein 1 (SIP1), which we establish as new substrates for ICP0-mediated degradation. Thus, HSV-1 selectively stimulates expression of the miR-183 cluster by ICP0-mediated degradation of ZEB transcriptional repressors.
Author Hackenberg, Michael
Kim, Ju Youn
Wilson, Angus C.
Lutz, Gabriel
Weitzman, Matthew D.
Stoller, Michelle L.
Jurak, Igor
Fekete, Donna M.
Coen, Donald M.
Kim, Eui Tae
Leader, Andrew
AuthorAffiliation 4 Department of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine and The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA; kime2@email.chop.edu (E.T.K.); weitzmanm@email.chop.edu (M.D.W.)
3 Department of Biotechnology, University of Rijeka, 51000 Rijeka, Croatia
5 Department of Genetics, Computational Genomics and Bioinformatics Group, University of Granada, Granada 18071, Spain; hackenberg@go.ugr.es
2 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; igor.jurak@biotech.uniri.hr (I.J.); Andrew.Leader@icahn.mssm.edu (A.L.); don_coen@hms.harvard.edu (D.M.C.)
6 Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA; mstoller2@gmail.com (M.L.S.); dfekete@purdue.edu (D.M.F.)
1 Department of Microbiology, New York University School of Medicine, New York, NY 10016, USA; Gabriel.Lutz@med.nyu.edu (G.L.); jyk294@gmail.com (J.Y.K.)
AuthorAffiliation_xml – name: 2 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; igor.jurak@biotech.uniri.hr (I.J.); Andrew.Leader@icahn.mssm.edu (A.L.); don_coen@hms.harvard.edu (D.M.C.)
– name: 4 Department of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine and The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA; kime2@email.chop.edu (E.T.K.); weitzmanm@email.chop.edu (M.D.W.)
– name: 6 Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA; mstoller2@gmail.com (M.L.S.); dfekete@purdue.edu (D.M.F.)
– name: 1 Department of Microbiology, New York University School of Medicine, New York, NY 10016, USA; Gabriel.Lutz@med.nyu.edu (G.L.); jyk294@gmail.com (J.Y.K.)
– name: 3 Department of Biotechnology, University of Rijeka, 51000 Rijeka, Croatia
– name: 5 Department of Genetics, Computational Genomics and Bioinformatics Group, University of Granada, Granada 18071, Spain; hackenberg@go.ugr.es
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  surname: Jurak
  fullname: Jurak, Igor
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  givenname: Eui Tae
  orcidid: 0000-0002-1631-3197
  surname: Kim
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  givenname: Ju Youn
  surname: Kim
  fullname: Kim, Ju Youn
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  orcidid: 0000-0003-2248-3114
  surname: Hackenberg
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  surname: Coen
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  orcidid: 0000-0002-5016-4164
  surname: Wilson
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/28783105$$D View this record in MEDLINE/PubMed
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Issue 8
Keywords herpes simplex virus
HSV-1
host shutoff
ZEB
ICP0
miR-182
miR-183
miR-96
microRNA
E3 ubiquitin ligase
Language English
License https://creativecommons.org/licenses/by/4.0
Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
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Current address: Precision Immunology Institute, Icahn School of Medicine at Mt. Sinai, New York, NY 10029, USA.
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Snippet Infection with herpes simplex virus-1 (HSV-1) brings numerous changes in cellular gene expression. Levels of most host mRNAs are reduced, limiting synthesis of...
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StartPage 210
SubjectTerms Cell Nucleus
Cells, Cultured
Crystallin
E3 ubiquitin ligase
Fibroblasts
Fibroblasts - virology
Gene expression
Gene Expression Regulation
Herpes simplex
herpes simplex virus
Herpesvirus 1, Human - enzymology
Herpesvirus 1, Human - genetics
Homeobox
host shutoff
Host-Pathogen Interactions
HSV-1
Humans
ICP0
Immediate-Early Proteins - deficiency
Immediate-Early Proteins - genetics
Kinases
microRNA
MicroRNAs - genetics
miR-182
miR-183
miR-96
miRNA
mRNA stability
Nerve Tissue Proteins - genetics
Neurons - virology
Non-coding RNA
Protein Binding
Proteolysis
Repressors
RNA-Binding Proteins - genetics
Smad protein
Transcription factors
Ubiquitin
Ubiquitin-protein ligase
Ubiquitin-Protein Ligases - deficiency
Ubiquitin-Protein Ligases - genetics
Ubiquitin-Protein Ligases - metabolism
Virus Replication
ZEB
Zinc Finger E-box-Binding Homeobox 1 - genetics
Zinc Finger E-box-Binding Homeobox 1 - metabolism
Zinc finger proteins
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Title Viral Ubiquitin Ligase Stimulates Selective Host MicroRNA Expression by Targeting ZEB Transcriptional Repressors
URI https://www.ncbi.nlm.nih.gov/pubmed/28783105
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https://pubmed.ncbi.nlm.nih.gov/PMC5580467
https://doaj.org/article/399ba1a201cf46ed98842061f1561abc
Volume 9
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