Cited by 923interferon and immune responsesImmune Response and InflammationCytokine Signaling Pathways and Interactions

The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index; none of the 41 sources its claims cite is checked for support yet.

Virus-Dependent Phosphorylation of the IRF-3 Transcription Factor Regulates Nuclear Translocation, Transactivation Potential, and Proteasome-Mediated Degradation

Open access
Lin, Rongtuan, Heylbroeck, Christophe, Pitha, Paula M., Hiscott, John·1998·Molecular and Cellular Biology

Abstract

The interferon regulatory factors (IRF) consist of a growing family of related transcription proteins first identified as regulators of the alpha beta interferon (IFN-alpha/beta) gene promoters, as well as the interferon-stimulated response element (ISRE) of some IFN-stimulated genes. IRF-3 was originally identified as a member of the IRF family based on homology with other IRF family members and on binding to the ISRE of the ISG15 promoter. IRF-3 is expressed constitutively in a variety of tissues, and the relative levels of IRF-3 mRNA do not change in virus-infected or IFN-treated cells. In the present study, we demonstrate that following Sendai virus infection, IRF-3 is posttranslationally modified by protein phosphorylation at multiple serine and threonine residues, which are located in the carboxy terminus of IRF-3. A combination of IRF-3 deletion and point mutations localized the inducible phosphorylation sites to the region -ISNSHPLSLTSDQ- between amino acids 395 and 407; point mutation of residues Ser-396 and Ser-398 eliminated virus-induced phosphorylation of IRF-3 protein, although residues Ser-402, Thr-404, and Ser-405 were also targets. Phosphorylation results in the cytoplasm-to-nucleus translocation of IRF-3, DNA binding, and increased transcriptional activation. Substitution of the Ser-Thr sites with the phosphomimetic Asp generated a constitutively active form of IRF-3 that functioned as a very strong activator of promoters containing PRDI-PRDIII or ISRE regulatory elements. Phosphorylation also appears to represent a signal for virus-mediated degradation, since the virus-induced turnover of IRF-3 was prevented by mutation of the IRF-3 Ser-Thr cluster or by proteasome inhibitors. Interestingly, virus infection resulted in the association of IRF-3 with the CREB binding protein (CBP) coactivator, as detected by coimmunoprecipitation with anti-CBP antibody, an interaction mediated by the C-terminal domains of both proteins. Mutation of residues Ser-396 and Ser-398 in IRF-3 abrogated its binding to CBP. These results are discussed in terms of a model in which virus-inducible, C-terminal phosphorylation of IRF-3 alters protein conformation to permit nuclear translocation, association with transcriptional partners, and primary activation of IFN- and IFN-responsive genes.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

In Sendai virus-infected cells, IRF-3 is phosphorylated at C-terminal Ser/Thr residues, which drives nuclear translocation, DNA binding/transactivation, CBP association, and subsequent proteasome-mediated degradation. Phosphomimetic IRF-3(5D) acts as a constitutive strong activator of IFN-β and ISG-15 promoters.

Key findings

  • Virus-induced phosphorylation mapped to the C-terminal region -ISNSHPLSLTSDQ- between amino acids 395 and 407; Ser-396 and Ser-398 were critical, since IRF-3(2A) and IRF-3(5A) eliminated virus-induced phosphorylation, while IRF-3(3A) was weakly phosphorylated, implicating Ser-402, Thr-404, and Ser-405 as secondary sites.
  • Phosphorylation was required for cytoplasm-to-nucleus translocation: Sendai virus induced nuclear translocation in 90 to 95% of cells within 8 h, GFP–IRF-3(5A) completely abrogated this, and GFP–IRF-3(5D) localized partly to the nucleus in uninfected cells and intensely to the nucleus after infection.
  • IRF-3(5D) alone stimulated the IFN-β promoter by 90-fold and the ISG-15 promoter by 50-fold; with RelA(p65), IRF-3(5D) produced an 80-fold stimulation of IFN-β, while IRF-3(407) stimulated IFN-β about 6-fold and ISG-15 12-fold.
  • Phosphorylation signaled proteasome-mediated degradation and CBP binding: calpain inhibitor I or MG132 blocked virus-induced IRF-3 degradation, IRF-3(5A) was resistant, and IRF-3 coimmunoprecipitated with CBP only from virus-infected cells, requiring Ser-396/Ser-398 and the C-terminal CBP-3 domain.

Methods

  • Transient transfections were performed in human embryonic kidney 293 cells, murine NIH 3T3 cells, and COS-7 cells, plus a stable rtTA-IRF-3 293 line; cells were infected with Sendai virus at 80 hemagglutinating units/ml, and IRF-3 deletion and point mutants were generated by PCR mutagenesis.
  • Analyses included Western blotting for IRF-3 mobility and degradation, phosphatase treatment with PPA or CIP, CAT reporter assays for IFN-β (SVoβ CAT) and ISG-15 promoters normalized to β-galactosidase, EMSA with PRDIII or ISRE probes, GFP–IRF-3 fluorescence microscopy, and coimmunoprecipitation with anti-CBP or anti-myc antibodies.

Limitations

  • The paper states that the nature of the subnuclear changes in IRF-3(NES) localization is not explained, it is unclear whether the upper virus-induced protein-DNA complex contains other proteins such as VIC or DRAF or whether the lower complex is an IRF-3 breakdown product, the functional consequences of IRF-3 interaction with CBP/p300 remain to be elucidated, and the nuclear localization sequence is unidentified.
  • Evident from the text: many experiments rely on transfected or overexpressed IRF-3 in immortalized cell lines, with endogenous IRF-3 turnover sometimes more pronounced than that of transfected protein; no in vivo animal model is presented, and some supporting observations are cited as unpublished data.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1128/mcb.18.5.2986

Cites

69 of 69 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

0 of 41 cited sources checked · 0 supported · 0 flagged

Show all 77 claims

  • It may state two separate claims as one. 23
  • Probably not a substantial claim. 21
38 of 38
  • The paper relies on this without support.

    Phosphomimetic Asp at the sites of C-terminal phosphorylation functionally mimics phosphorylation.

    “IRF-3 containing the phosphomimetic Asp at the sites of C-terminal phosphorylation”
  • The authors state this as an assumption.

    IRF-3 exists in a latent state in the cytoplasm of uninfected cells.

    “IRF-3 exists in a latent state in the cytoplasm of uninfected cells”
  • The authors state this as an assumption.

    The C terminus of IRF-3 may physically interact with the DNA binding domain to obscure both the DBD and IAD regions.

    “the C terminus may physically interact with the DNA binding domain in such a way as to obscure both the DBD and the IAD regions of the protein”
  • The authors state this as an assumption.

    The C-terminal 20 aa (407 to 427) contains an autoinhibitory domain.

    “the presence of an autoinhibitory domain within the C-terminal 20 aa (407 to 427)”
  • The authors state this as an assumption.

    Translocation of IRF-3 to the nucleus occurs via an unidentified nuclear localization sequence or in conjunction with a transcriptional partner associating through the IAD region.

    “Translocation to the nucleus, occurring via an unidentified nuclear localization sequence or in conjunction with a transcriptional partner associating through the IAD region”
  • The authors state this as an assumption.

    The presence of a NES element ultimately shuttles IRF-3 from the nucleus and terminates the initial activation of IFN-responsive promoters.

    “The presence of a NES element ultimately shuttles IRF-3 from the nucleus and terminates the initial activation of IFN-responsive promoters.”
  • The authors state this as an assumption.

    The phosphorylated form of IRF-3 exported from the nucleus may then be susceptible to proteasome-mediated degradation.

    “The phosphorylated form of IRF-3 exported from the nucleus may then be susceptible to proteasome-mediated degradation.”
7 of 7

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Figure 2B lane 6 cited for both presence and disappearance of phosphorylated IRF-3

    Minor

    Lane 6 is cited as showing the additional IRF-3 form in infected cells and also as showing its complete disappearance after phosphatase treatment.

  • Residue 404 identified as both threonine and serine

    Minor

    The mapped phosphorylation cluster identifies residue 404 as threonine, whereas the discussion calls it serine.

  • Different residues identified for the NES mutation

    Minor

    The results identify the nuclear export signal mutation as L145A-L146A, but the discussion identifies it as L144A and L145A.

3 of 3

Citations

Cites

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Show all 69 references

Research works printed but not linked: 3

  1. Crepieux P., 1994, Crit. Rev. Oncog., 5, 615
  2. Evan G. I., 1984, Mol. Cell. Biol., 4, 2843
  3. Nguyen, H., J. Hiscott, and P. M. Pitha. The growing family of IRF transcription factors. Cytokine Growth Factor Rev., in press.

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Metadata

Authors
Lin, R., Heylbroeck, C., Pitha, P. M., & Hiscott, J.
Affiliations
  • Lady Davis Institute for Medical Research (CA)
  • Johns Hopkins University (US)
Corresponding author
Lin, Rongtuan
Venue
Molecular and Cellular Biology
Published
1998-05-01
Volume
18
Issue
5
Pages
2986-2996
ISSN
  • 0270-7306 (ISSN-L)
  • 1098-5549
OpenAlex
W2130576390
Cited by
915
References
69
Citations by year
2026: 11 · 2025: 20 · 2024: 24 · 2023: 26 · 2022: 33 · 2021: 24 · 2020: 30 · 2019: 26 · 2018: 27 · 2017: 28 · 2016: 33 · 2015: 26 · 2014: 38 · 2013: 42 · 2012: 30
FWCI
10.65
Type
journal article
Language
en
Open access
Locations
  • Molecular and Cellular Biology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
  • Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
Keywords
IRF3, interferon regulatory factors, protein phosphorylation, Sendai virus, nuclear translocation, transcriptional activation, interferon-stimulated response element, proteasomal degradation, CREB-binding protein, transcriptional coactivator, post-translational modification, interferon-stimulated genes, phosphomimetic mutations
MeSH terms
Amino Acid Sequence, Animals, Biological Transport, Cell Compartmentation, Cell Nucleus, Cysteine Endopeptidases, Cytoplasm, DNA Mutational Analysis, DNA-Binding Proteins, Humans, Molecular Sequence Data, Multienzyme Complexes, Peptide Mapping, Phosphorylation, Protein Binding, Protein Processing, Post-Translational, Transcription Factors, Transcriptional Activation, Trans-Activators, Respirovirus, Proteasome Endopeptidase Complex, Interferon Regulatory Factor-3, Mice, Histone Acetyltransferases, Nuclear Receptor Coactivator 3

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