The interferon stimulated gene-encoded protein HELZ2 inhibits human LINE-1 retrotransposition and LINE-1 RNA-mediated type I interferon induction

Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles...

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Published inNature communications Vol. 14; no. 1; pp. 203 - 26
Main Authors Luqman-Fatah, Ahmad, Watanabe, Yuzo, Uno, Kazuko, Ishikawa, Fuyuki, Moran, John V., Miyoshi, Tomoichiro
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 13.01.2023
Nature Publishing Group
Nature Portfolio
Subjects
13
13/21
13/31
13/89
14/35
14/63
38/1
38/44
38/88
38/90
5' Untranslated Regions
631/208/211
631/250/262
631/337/1645
82/1
82/58
82/83
Binding
DNA helicase
Genes
Humanities and Social Sciences
Humans
Immune response
Immune system
Immunoprecipitation
Innate immunity
Interferon
Interferon Type I - genetics
Liquid chromatography
Localization
Long Interspersed Nucleotide Elements - genetics
Mass spectrometry
Mass spectroscopy
multidisciplinary
Proteins
Proteins - genetics
Proteomics
Retrotransposition
Ribonucleic acid
RNA
RNA - genetics
RNA Helicases - genetics
RNA-directed DNA polymerase
RNA-Directed DNA Polymerase - genetics
Science
Science (multidisciplinary)
Ubiquitin
Ubiquitin-protein ligase
Zinc finger proteins
α-Interferon
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-022-35757-6

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Abstract Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles. Three ISG proteins that interact with ORF1p inhibit retrotransposition: HECT and RLD domain containing E3 ubiquitin-protein ligase 5 (HERC5); 2′−5′-oligoadenylate synthetase-like (OASL); and helicase with zinc finger 2 (HELZ2). HERC5 destabilizes ORF1p, but does not affect its cellular localization. OASL impairs ORF1p cytoplasmic foci formation. HELZ2 recognizes sequences and/or structures within the L1 5′UTR to reduce L1 RNA, ORF1p, and ORF1p cytoplasmic foci levels. Overexpression of WT or reverse transcriptase-deficient L1s lead to a modest induction of IFN-α expression, which is abrogated upon HELZ2 overexpression. Notably, IFN-α expression is enhanced upon overexpression of an ORF1p RNA binding mutant, suggesting ORF1p binding might protect L1 RNA from “triggering” IFN-α induction. Thus, ISG proteins can inhibit retrotransposition by different mechanisms. Proteomic analyses revealed that a group of interferon-stimulated genes suppresses LINE-1 retrotransposon activities, including HELZ2, which reduces LINE-1 RNA and the associated innate immune response levels.
AbstractList Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles. Three ISG proteins that interact with ORF1p inhibit retrotransposition: HECT and RLD domain containing E3 ubiquitin-protein ligase 5 (HERC5); 2′−5′-oligoadenylate synthetase-like (OASL); and helicase with zinc finger 2 (HELZ2). HERC5 destabilizes ORF1p, but does not affect its cellular localization. OASL impairs ORF1p cytoplasmic foci formation. HELZ2 recognizes sequences and/or structures within the L1 5′UTR to reduce L1 RNA, ORF1p, and ORF1p cytoplasmic foci levels. Overexpression of WT or reverse transcriptase-deficient L1s lead to a modest induction of IFN-α expression, which is abrogated upon HELZ2 overexpression. Notably, IFN-α expression is enhanced upon overexpression of an ORF1p RNA binding mutant, suggesting ORF1p binding might protect L1 RNA from “triggering” IFN-α induction. Thus, ISG proteins can inhibit retrotransposition by different mechanisms. Proteomic analyses revealed that a group of interferon-stimulated genes suppresses LINE-1 retrotransposon activities, including HELZ2, which reduces LINE-1 RNA and the associated innate immune response levels.
Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles. Three ISG proteins that interact with ORF1p inhibit retrotransposition: HECT and RLD domain containing E3 ubiquitin-protein ligase 5 (HERC5); 2'-5'-oligoadenylate synthetase-like (OASL); and helicase with zinc finger 2 (HELZ2). HERC5 destabilizes ORF1p, but does not affect its cellular localization. OASL impairs ORF1p cytoplasmic foci formation. HELZ2 recognizes sequences and/or structures within the L1 5'UTR to reduce L1 RNA, ORF1p, and ORF1p cytoplasmic foci levels. Overexpression of WT or reverse transcriptase-deficient L1s lead to a modest induction of IFN-α expression, which is abrogated upon HELZ2 overexpression. Notably, IFN-α expression is enhanced upon overexpression of an ORF1p RNA binding mutant, suggesting ORF1p binding might protect L1 RNA from "triggering" IFN-α induction. Thus, ISG proteins can inhibit retrotransposition by different mechanisms.Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles. Three ISG proteins that interact with ORF1p inhibit retrotransposition: HECT and RLD domain containing E3 ubiquitin-protein ligase 5 (HERC5); 2'-5'-oligoadenylate synthetase-like (OASL); and helicase with zinc finger 2 (HELZ2). HERC5 destabilizes ORF1p, but does not affect its cellular localization. OASL impairs ORF1p cytoplasmic foci formation. HELZ2 recognizes sequences and/or structures within the L1 5'UTR to reduce L1 RNA, ORF1p, and ORF1p cytoplasmic foci levels. Overexpression of WT or reverse transcriptase-deficient L1s lead to a modest induction of IFN-α expression, which is abrogated upon HELZ2 overexpression. Notably, IFN-α expression is enhanced upon overexpression of an ORF1p RNA binding mutant, suggesting ORF1p binding might protect L1 RNA from "triggering" IFN-α induction. Thus, ISG proteins can inhibit retrotransposition by different mechanisms.
Proteomic analyses revealed that a group of interferon-stimulated genes suppresses LINE-1 retrotransposon activities, including HELZ2, which reduces LINE-1 RNA and the associated innate immune response levels.
Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles. Three ISG proteins that interact with ORF1p inhibit retrotransposition: HECT and RLD domain containing E3 ubiquitin-protein ligase 5 (HERC5); 2'-5'-oligoadenylate synthetase-like (OASL); and helicase with zinc finger 2 (HELZ2). HERC5 destabilizes ORF1p, but does not affect its cellular localization. OASL impairs ORF1p cytoplasmic foci formation. HELZ2 recognizes sequences and/or structures within the L1 5'UTR to reduce L1 RNA, ORF1p, and ORF1p cytoplasmic foci levels. Overexpression of WT or reverse transcriptase-deficient L1s lead to a modest induction of IFN-α expression, which is abrogated upon HELZ2 overexpression. Notably, IFN-α expression is enhanced upon overexpression of an ORF1p RNA binding mutant, suggesting ORF1p binding might protect L1 RNA from "triggering" IFN-α induction. Thus, ISG proteins can inhibit retrotransposition by different mechanisms.
Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles. Three ISG proteins that interact with ORF1p inhibit retrotransposition: HECT and RLD domain containing E3 ubiquitin-protein ligase 5 (HERC5); 2′−5′-oligoadenylate synthetase-like (OASL); and helicase with zinc finger 2 (HELZ2). HERC5 destabilizes ORF1p, but does not affect its cellular localization. OASL impairs ORF1p cytoplasmic foci formation. HELZ2 recognizes sequences and/or structures within the L1 5′UTR to reduce L1 RNA, ORF1p, and ORF1p cytoplasmic foci levels. Overexpression of WT or reverse transcriptase-deficient L1s lead to a modest induction of IFN-α expression, which is abrogated upon HELZ2 overexpression. Notably, IFN-α expression is enhanced upon overexpression of an ORF1p RNA binding mutant, suggesting ORF1p binding might protect L1 RNA from “triggering” IFN-α induction. Thus, ISG proteins can inhibit retrotransposition by different mechanisms.Proteomic analyses revealed that a group of interferon-stimulated genes suppresses LINE-1 retrotransposon activities, including HELZ2, which reduces LINE-1 RNA and the associated innate immune response levels.
Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid chromatography-tandem mass spectrometry to identify proteins that associate with the L1 ORF1-encoded protein (ORF1p) in ribonucleoprotein particles. Three ISG proteins that interact with ORF1p inhibit retrotransposition: HECT and RLD domain containing E3 ubiquitin-protein ligase 5 (HERC5); 2′−5′-oligoadenylate synthetase-like (OASL); and helicase with zinc finger 2 (HELZ2). HERC5 destabilizes ORF1p, but does not affect its cellular localization. OASL impairs ORF1p cytoplasmic foci formation. HELZ2 recognizes sequences and/or structures within the L1 5′UTR to reduce L1 RNA, ORF1p, and ORF1p cytoplasmic foci levels. Overexpression of WT or reverse transcriptase-deficient L1s lead to a modest induction of IFN-α expression, which is abrogated upon HELZ2 overexpression. Notably, IFN-α expression is enhanced upon overexpression of an ORF1p RNA binding mutant, suggesting ORF1p binding might protect L1 RNA from “triggering” IFN-α induction. Thus, ISG proteins can inhibit retrotransposition by different mechanisms.
ArticleNumber 203
Author Watanabe, Yuzo
Ishikawa, Fuyuki
Miyoshi, Tomoichiro
Luqman-Fatah, Ahmad
Uno, Kazuko
Moran, John V.
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  year: 2015
  ident: 35757_CR118
  publication-title: Biotechnol. J.
  doi: 10.1002/biot.201400821
– volume: 21
  start-page: 319
  year: 2017
  ident: 35757_CR80
  publication-title: Cell Stem Cell
  doi: 10.1016/j.stem.2017.07.009
– reference: 36717557 - Nat Commun. 2023 Jan 30;14(1):493
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Snippet Some interferon stimulated genes (ISGs) encode proteins that inhibit LINE-1 (L1) retrotransposition. Here, we use immunoprecipitation followed by liquid...
Proteomic analyses revealed that a group of interferon-stimulated genes suppresses LINE-1 retrotransposon activities, including HELZ2, which reduces LINE-1 RNA...
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StartPage 203
SubjectTerms 13
13/21
13/31
13/89
14/35
14/63
38/1
38/44
38/88
38/90
5' Untranslated Regions
631/208/211
631/250/262
631/337/1645
82/1
82/58
82/83
Binding
DNA helicase
Genes
Humanities and Social Sciences
Humans
Immune response
Immune system
Immunoprecipitation
Innate immunity
Interferon
Interferon Type I - genetics
Liquid chromatography
Localization
Long Interspersed Nucleotide Elements - genetics
Mass spectrometry
Mass spectroscopy
multidisciplinary
Proteins
Proteins - genetics
Proteomics
Retrotransposition
Ribonucleic acid
RNA
RNA - genetics
RNA Helicases - genetics
RNA-directed DNA polymerase
RNA-Directed DNA Polymerase - genetics
Science
Science (multidisciplinary)
Ubiquitin
Ubiquitin-protein ligase
Zinc finger proteins
α-Interferon
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Title The interferon stimulated gene-encoded protein HELZ2 inhibits human LINE-1 retrotransposition and LINE-1 RNA-mediated type I interferon induction
URI https://link.springer.com/article/10.1038/s41467-022-35757-6
https://www.ncbi.nlm.nih.gov/pubmed/36639706
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https://pubmed.ncbi.nlm.nih.gov/PMC9839780
https://doaj.org/article/1eb5dddf7a114310a23918c5a3aac13f
Volume 14
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